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Precision care to optimize safe return to function following surgical flexor tendon repair
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Precision care to optimize safe return to function following surgical flexor tendon repair
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Content
Copyright 2023 Sandy Chie Takata
PRECISION CARE TO OPTIMIZE SAFE RETURN TO FUNCTION
FOLLOWING SURGICAL FLEXOR TENDON REPAIR
by
Sandy Chie Takata
A Dissertation Presented to the
FACULTY OF THE USC GRADUATE SCHOOL
UNIVERSITY OF SOUTHERN CALIFORNIA
In Partial Fulfillment of the
Requirements for the Degree
DOCTOR OF PHILOSOPHY
(OCCUPATIONAL SCIENCE)
May 2023
ii
DEDICATIONS
My loving Mom and Dad,
Thank you for allowing me the freedom to be,
encouraging who I want to become,
and supporting the occupations I love to do.
For Forest, Ivy, and Bella,
Thank you for your love, trust, and warmth–
for reminding me to play at least once a day
and that sometimes life’s simpler after a little cat nap.
iii
ACKNOWLEDGEMENTS
“The most important things are the hardest to say,
because words diminish them.”
– Stephen King
First, I would like to thank my advisor, Dr. Shawn Roll, for his attentive guidance,
expertise, enthusiasm for research, and tireless devotion to mentoring me over the
years. I would also like to thank the other members of my committee, Dr. Sook-Lei Liew
and Dr. Wendy Mack for their mentorship, kind encouragement, thoughtful feedback,
and dedication to my development and training. I am so appreciative of the unique
opportunities and experiences my committee has provided to help me advance my
career and personal growth.
I would also like to thank my friends and colleagues at the Musculoskeletal
Sonography and Occupational Performance laboratory and the Department of
Occupational Science. I appreciate the warmth of your friendships, helpful collaboration,
and benevolence that motivated me and brought so much joy through this experience.
Finally, I am grateful to my loving family and dearest friends for their unwavering
support, encouragement, and dedication to keeping me mentally and physically healthy.
Thank you for providing such generous nourishment for my soul, body, and mind. My
journey has been both enriched by you and successful because of you.
iv
TABLE OF CONTENTS
Dedications ...................................................................................................................... ii
Acknowledgments ........................................................................................................... iii
List of Tables .................................................................................................................. vii
List of Figures ................................................................................................................ viii
List of Abbreviations ........................................................................................................ x
Abstract .......................................................................................................................... xii
CHAPTER 1. General Introduction ............................................................................... 1
1.1. Significance of Tendon Injuries in the Hand on Occupational Wellbeing ............ 1
1.2. Repair and Recovery Following Tendon Injury ................................................... 4
1.3. Challenges to Recovery and Return to Function................................................. 7
1.4. Sonography in Musculoskeletal Rehabilitation .................................................... 9
1.5. Application for Sonography and Precision Care in Tendon Recovery ............... 15
1.6. Dissertation Overview ....................................................................................... 18
1.7. References........................................................................................................ 21
CHAPTER 2. The Recovery Process for Surgical Flexor Tendon Repair:
A Timeline of Healing ............................................................................................ 30
2.1. Introduction ....................................................................................................... 30
2.2. Methods ............................................................................................................ 31
2.3. Results .............................................................................................................. 34
2.3.1. Factors Complicating Tendon Repair and Recovery ................................ 34
2.3.2. Physiology and Morphology of Tendon Healing After Surgical
Repair ...................................................................................................... 36
2.3.3. Timeline of Tendon Healing Progression After Surgical Repair ................ 38
2.3.4. Musculoskeletal Sonography to Evaluate Tendons .................................. 45
2.4. Discussion......................................................................................................... 50
2.5. References........................................................................................................ 54
CHAPTER 3. Establishing a Protocol to Evaluate the Flexor Digitorum
Profundus Tendon .................................................................................... 62
3.1. Introduction ....................................................................................................... 62
3.2. Research Methods ............................................................................................ 64
3.2.1. Study Design ............................................................................................ 64
3.2.2. Methods for Initial Protocol Development and Adaptation ........................ 65
3.2.3. Subjects .................................................................................................... 66
3.2.4. Equipment and Subject Positioning .......................................................... 67
3.2.5. Image Acquisition Protocol ...................................................................... 67
3.2.6. Image Analysis ......................................................................................... 70
v
3.3. Results .............................................................................................................. 71
3.3.1. Establishing Validity and Optimizing Image Quality ................................. 72
3.3.2. Refined Protocol and Best Practices ........................................................ 83
3.4. Discussion......................................................................................................... 95
3.5. Conclusions ...................................................................................................... 99
3.6. References...................................................................................................... 100
CHAPTER 4. Measuring Sonographic Biomarkers of Healing Over Time:
A Case Study of Functional Recovery After Flexor Tendon
Surgery .................................................................................................... 103
4.1. Introduction ..................................................................................................... 103
4.2. Research Methods .......................................................................................... 105
4.2.1. Study Design .......................................................................................... 105
4.2.2. Outcome Measures ................................................................................ 106
4.2.3. Equipment and Subject Positioning ........................................................ 111
4.2.4. Sonographic Image Acquisition Protocol ................................................ 112
4.2.5. Sonographic Image Analysis Protocol .................................................... 113
4.2.6. Data Analysis .......................................................................................... 117
4.3. Results ............................................................................................................ 117
4.3.1. Participant Demographics ....................................................................... 117
4.3.2. Clinical Presentation of Participant ......................................................... 118
4.3.3. Functional Outcome Measures ............................................................... 119
4.3.4. Sonographic Biomarkers ........................................................................ 120
4.3.5. Intra-rater Reliability Scores for Continuous Measures .......................... 126
4.4. Discussion....................................................................................................... 126
4.4.1. Interpretation of Case Findings ............................................................... 127
4.4.2. Additional Opportunities for MSKS in Tendon Rehabilitation .................. 131
4.4.3. Study Limitations .................................................................................... 133
4.5. References...................................................................................................... 135
CHAPTER 5. Discussion/Future Directions ............................................................ 141
5.1. Introduction ..................................................................................................... 141
5.2. Summary of Key Findings ............................................................................... 142
5.2.1. Conclusions from Chapter 2: A Literature Review on the Timeline
of Tendon Healing ................................................................................. 143
5.2.2. Conclusions from Chapter 3: A Standardized MSKS Protocol to
Evaluate Healthy Flexor Tendons .......................................................... 146
5.2.3. Conclusions from Chapter 4: A Case Study of Functional Recovery
After Tendon Surgery............................................................................. 147
5.3. Synthesis of Knowledge Gained ..................................................................... 150
5.4. Future Directions for Knowledge Application .................................................. 151
5.5. References...................................................................................................... 157
BIBLIOGRAPHY ......................................................................................................... 160
APPENDICES ............................................................................................................. 178
vi
APPENDIX A: Supplementary Material for Chapter 2 ....................................... 178
Appendix A.1. Search Strategy for Literature Review ....................................... 178
Appendix A.2. PRISMA Diagram of Articles Identified, Screened, Reviewed
and Included in the Literature Review ...................................... 179
Appendix A.3. Physiology and Morphology of Healthy Tendons ...................... 180
APPENDIX B: Supplementary Material for Chapter 3 ....................................... 183
Appendix B.1. Serial Images of Healthy Flexor Tendons of Included
Participants Using Sonography Protocol .................................. 183
Figure B.1. Serial Images of Participant One .............................................. 184
Figure B.2. Serial Images of Participant Two .............................................. 185
Figure B.3. Serial Images of Participant Three ............................................ 186
Figure B.4. Serial Images of Participant Four.............................................. 187
Figure B.5. Serial Images of Participant Five .............................................. 188
Figure B.6. Serial Images of Participant Six ................................................ 189
Figure B.7. Serial Images of Participant Seven ........................................... 190
Figure B.8. Serial Images of Participant Eight ............................................. 191
Figure B.9. Serial Images of Participant Nine.............................................. 192
Figure B.10. Serial Images of Participant Ten ............................................. 193
Figure B.11. Serial Images of Participant Eleven ........................................ 194
Figure B.12. Serial Images of Participant Twelve ........................................ 195
Figure B.13. Serial Images of Participant Thirteen ...................................... 196
Figure B.14. Serial Images of Participant Fourteen ..................................... 197
Figure B.15. Serial Images of Participant Fifteen ........................................ 198
vii
LIST OF TABLES
Chapter 3
Table 3.1. Demographic of Healthy Participants (N=15) ............................................... 66
Table 3.2. Finalized Sonography Protocol and Recommendations for Image
Organization ................................................................................................ 88
Chapter 4
Table 4.1. Summary of Reliability, Validity, and Clinical Interpretations of
Functional Outcome Measures .................................................................. 107
Table 4.2. Schedule of Data Collection and Visits with Functional Measures ............. 118
Table 4.3. Total Active Range of Motion of Injured Upper-Extremity and
9-Hole Peg Test Scores Obtained at Visits 3 and 4 ................................... 120
Table 4.4. Comparison Of FDP CSA Measures at Specified Locations in the
Healthy and Injured Hands Over Time ....................................................... 122
Table 4.5. Comparison Of Localized Edema CSA Measures at Specified
Locations in the Healthy and Injured Hands Over Time ............................. 123
Table 4.6. Overall and Location-Specific Interclass Correlation Coefficients
for FDP and Localized Edema CSA Measures in the Injured Hand ........... 126
viii
LIST OF FIGURES
Chapter 1
Figure 1.1. Longitudinal View of a Healthy Flexor Digitorum Profundus Tendon .......... 10
Figure 1.2. Sonographic Images of Surgically Repaired Flexor Tendon ....................... 17
Chapter 2
Figure 2.1. Timeline of Tendon Healing Progression .................................................... 40
Chapter 3
Figure 3.1. Long-Axis Views of Healthy Flexor Tendons at Two Different
Depths ........................................................................................................ 73
Figure 3.2. Short-Axis Views of Typical and Atypical Flexor Tendon
Presentations ............................................................................................. 75
Figure 3.3. Typical Long-Axis View of Flexor Digitorum Profundus Tendon
over the Volar Plate at the Proximal Interphalangeal Joint ......................... 76
Figure 3.4. Short-Axis View of an Early Bifurcation of the Flexor Digitorum
Superficialis Tendon over the Proximal Phalanx ........................................ 77
Figure 3.5. Typical Long-Axis View of Flexor Digitorum Profundus Tendon
Over the Volar Plate at the Proximal Interphalangeal Joint ........................ 78
Figure 3.6. Short-Axis Presentations of the Flexor Tendons over the Volar
Plate at the Proximal Phalanx .................................................................... 80
Figure 3.7. Typical Short-Axis View of Flexor Digitorum Profundus Tendon
over the Distal Interphalangeal Joint .......................................................... 81
ix
Figure 3.8. Typical and Atypical Presentations of the Flexor Digitorum
Profundus Tendon in Short-Axis over the Volar Plate at the
Middle Phalanx ........................................................................................... 83
Chapter 4
Figure 4.1. Patient Positioning for Sonography Acquisition Protocol Using
Hockey Stick Transducer to Obtain Images of the Small Finger
Flexor Tendon After Surgical Repair ........................................................ 112
Figure 4.2. Example Images of the Direct Tracing Method Used to Measure
the Cross-Sectional Area of Anatomic Structures in Short-Axis of
the Tendon for the Calculation of Localized Edema ................................. 115
Figure 4.3. Image of Vascular Activity of Surgically Repaired Flexor Digitorum
Profundus Tendon in Long-Axis Captured Using Doppler
Ultrasound ................................................................................................ 116
Figure 4.4. Scatterplot of the Flexor Digitorum Profundus Cross-Sectional Area
Measured at Four Locations of the Hand Over Time ................................ 121
Figure 4.5. Scatterplot of the Localized Edema Cross-Sectional Area Measured
at Three Locations of the Hand Over Time ............................................... 123
Figure 4.6. Image Series of Vascularity Identified at the Repair Site Over Time
Using Doppler Ultrasound ........................................................................ 125
x
LIST OF ABBREVIATIONS
9HPT – 9-Hole Peg Test
AROM – Active Range of Motion
BMI – Body Mass Index
CI – Confidence Interval
CSA – Cross-Sectional Area
DASH – Disabilities of the Arm, Shoulder and Hand questionnaire
DIP – Distal Interphalangeal Joint
DP – Distal Phalanx
FDP – Flexor Digitorum Profundus
FDS – Flexor Digitorum Profundus
MCH – Metacarpal head
ICC – Interclass Correlation Coefficient
IF – Index Finger
MCP – Metacarpophalangeal Joint
MF – Middle Finger
MP – Middle Phalanx
MRI – Magnetic Resonance Imaging
MSKS – Musculoskeletal Sonographic Ultrasound
PIP – Proximal Interphalangeal Joint
PP – Proximal Phalanx
RF – Ring Finger
SD – Standard Deviation
xi
SEM – Standard Error Measurement
SF – Small Finger
SS – Suture Site
TAM – Total Active Range of Motion
VBP – Vinculum Brevis Profundus
VBS – Vinculum Brevis Superficialis
VLP – Vinculum Longus Profundus
VLS – Vinculum Longus Superficialis
VP – Volar Plate
κ – Kappa Score
xii
ABSTRACT
From birth, our hands help us interact with other people and our environment,
supporting mental and physical development throughout our lives. Hand function allows
us opportunities to engage in meaningful occupations, shape our surroundings, and
communicate and express our thoughts and ideas, facilitating our health, identity, and
wellbeing. Because of the vital importance of our hands, the work presented in this
dissertation was inspired by patients and loved ones who have lost or limited use of
their hands with the aspiration that they may experience a safe and efficient return to
function. More specifically, this work explores how the clinical use of musculoskeletal
sonography (MSKS) can facilitate a more precise method of individualized care and
improve outcomes for patients with tendon injuries.
The research conducted in this dissertation focused on three aims: 1) conduct a
systematic literature review to describe the morphologic and physiologic changes of
healing tissue over time after a surgical tendon repair, 2) establish a sonographic image
acquisition and analysis protocol to evaluate healing and recovery following flexor
tendon repair, and 3) identify sonographic biomarkers that predict functional recovery
and most easily distinguish patterns of healing following tendon repair. As a first step,
an extensive literature review was conducted to help elucidate the physiologic and
morphologic processes that occur in healing tissues after surgical tendon repair and the
timing for when these processes take place. This literature review was also used to
identify factors that may influence the healing process as well as distinguish MSKS
biomarkers of recovery that may be indicative of the healing status of the repair.
Second, as there is no standardized MSKS protocol to evaluate flexor tendons in
xiii
the upper extremity, the following cohort study focused on developing and refining a
protocol to obtain sonographic images of the flexor tendons in the hand with a sample of
15 healthy individuals. This research helped establish the feasibility of deploying a
standardized MSKS protocol to examine healthy flexor tendons as well as elucidated
anatomic anomalies in flexor tendons that may frequently occur in the healthy
population. Moreover, the results of this study and the information garnered from the
literature review served as a template to guide the development of a second MSKS
protocol to assess surgically repaired flexor tendons.
In the final case study, an MSKS protocol was developed and deployed in an
individual with a zone II flexor tendon laceration and surgical repair during the third to
twelfth weeks of his recovery. This research helped establish the feasibility of using
MSKS to evaluate surgically repaired flexor tendons and the surrounding tissues during
the early weeks of healing. Furthermore, the study findings also helped to establish
good to excellent reliability for selected sonographic biomarkers of healing that were
identified from the literature review (Chapter 2). Together, this work demonstrates
promise for the future integration of MSKS into rehabilitation, displaying the potential to
improve patient outcomes as well as create avenues for clinicians to provide more
holistic care.
1
CHAPTER 1. General Introduction
1.1. Significance of Tendon Injuries in the Hand on Occupational Wellbeing
“Man, through the use of his hands, as they are energized by
mind and will can influence the state of his own health… and can
creatively deploy his thinking, feelings, and purpose to make
himself at home in the world and to make the world his home”
(Reilly, 1963).
As occupational engagement provides meaningfulness (Clark, 1993; Wilcock,
1999), participation in preferred occupations is a necessary element to one’s health and
wellbeing (Christiansen, 1999). Participation in occupations like exercise can promote
wellbeing by being healthful. Even more importantly, participation in elected occupations
can help define or shape one’s identity and by extension, one’s society (Wilcock, 1999).
For example, a woman named Susan enjoys sewing and finds quilting to be a
meaningful occupation. Her satisfaction from quilting is further enhanced whenever she
wraps a newly sewn quilt around her daughter or gifts one to a beloved niece or
nephew. By sewing these quilts, she expresses her love by providing warmth and
comfort. As such, the occupation of quilting helps Susan self-identity as a loving
caregiver for her family, thus enhancing her enjoyment of quilting while supporting her
physical and mental wellbeing.
In addition to supporting Susan’s role as a caregiver, quilting also provides
2
opportunities to participate in shared social activities that are centered around this
occupation. At least once a month, Susan invites her quilting circle of friends to her
home to share crafting ideas, exchange fabrics, create new patterns, and enjoy each
other’s company. Another important social event centered around her occupation of
quilting is the local arts and crafts show held annually in her hometown. Accompanied
by friends and family, Susan excitedly attends this social outing to meet other quilters,
be inspired by new quilting ideas, and purchase beautiful, unique fabrics to sew more
quilts and help support other crafters. Through the shared occupation of quilting, Susan
is provided with many opportunities to socialize with her friends and her community. By
participating in these activities, Susan adds pleasure and finds meaningfulness to her
life, thereby making the occupation of quilting an important aspect of her health and
wellbeing.
For many others, such as Susan, participation in some of the most meaningful
occupations is dependent on the ability to use our hands. One crucial element of hand
function is the hands’ flexor tendons. In particular, the flexor digitorum superficialis
(FDS) and the flexor digitorum profundus (FDP) play an essential role in finger motion
and dexterity. These tendons are necessary for occupations that involve the use of our
fingers, as they control finger flexion; the FDS flexes the proximal interphalangeal joint,
and similarly, the FDP flexes the distal interphalangeal joint. Activities that require
gripping, pinching, and lifting objects engage the FDS and FDP tendons. In our
example, Susan needs her flexor tendons for quilting and uses them whenever she
sketches quilt patterns, threads a needle, or cuts fabric with her scissors, as these
activities require precision, prehension, and grip strength.
3
Similar to providing meaningfulness, discontinuing or losing the ability to
participate in preferred occupations can be a powerful detriment to wellbeing (Wilcock,
1999). An injury to the hand that limits participation in elected occupations can
negatively influence the state of one’s health, especially when coupled with trauma.
Activities that were once completed with ease may now be challenging or even
impossible to perform. This functional loss disrupts many previously established
occupational habits, roles, and routines that are often taken for granted.
A hand injury may also limit participation in shared social activities, particularly if
those activities require the use of the upper extremity. This social isolation can have a
heightened negative affect on recovery and create additional barriers to engaging in
occupations by restricting access to social support systems. Consequently,
experiencing an injury to the upper extremity can be emotionally challenging.
Unaddressed psychological factors, such as stress and anxiety, can lead to poor
recovery (Keijsers et al., 2010). Moreover, these factors can have a negative influence
on patient health, work status, and overall satisfaction with recovery as much as 12
months post-injury (Michaels et al., 2000).
Unfortunately, tendon lacerations are extremely common, costly, and result in
functional limitations. Over 300,000 tendon repair procedures are performed annually in
the United States alone, and acute traumatic tendon injuries in the hand occur in
roughly 100,000 people (de Jong et al., 2014; Mehrzad et al., 2019). Flexor tendon
laceration injuries incur an estimated annual cost of between $240.8 and $409.1 million
to the American medical system; estimates of total direct cost is $13,725, with indirect
costs ranging from $60,786 to $112,888 for each injury (Mehrzad et al., 2019). An injury
4
to one or both tendons can significantly reduce hand function and, as tendons are
mostly avascular, take at least four months to heal.
1.2. Repair and Recovery Following Tendon Injury
Typically, partial tendon tears greater than 50% of the tendon and complete
tendon lacerations necessitate surgical repair to regain function (Klifto et al., 2018).
Although the most effective surgical methods are still being researched, surgeons often
use a four- or six-strand core suture configuration to stitch the tendon ends in
combination with an epitendinous suture to prevent gapping at the repair site (Klifto et
al., 2018; Myer & Fowler, 2016; Tang, 2019). Although added sutures typically
strengthen the repair, each additional suture increases its bulkiness, which can have
negative effects. As the number of strands increases, the friction and pressure within
the synovial sheath increase along with it–adding more resistance during tendon glide
and increasing the risk of tendon gapping or rupture (Singh et al., 2015).
Following surgical repair, recovery is a long process that typically requires at
least 3-4 months and involves follow-through in a physical rehabilitation setting.
Immediately after surgery, all patients initially wear an orthotic that restricts motion at
the fingers and wrist to protect the healing tendon. Meanwhile, the patient must strictly
follow movement restrictions as well as adhere to therapist recommendations, such as
diligent completion of their daily home exercise programs; both of which can be
challenging yet necessary for optimal recovery. For much of this time, patients also
have extremely limited use of their injured wrist and hand, which reduces their ability to
independently complete many daily activities. To successfully heal, tendons require
5
adequate tensile strength, coaptation (i.e., joining of the tendon ends), and unimpeded
gliding for hand and finger movement.
Currently, there are several therapeutic approaches following surgical repair. Full
immobilization throughout the healing process is often used with children to enforce
movement restrictions and has mostly positive outcomes for this young population
(Sikora et al., 2013). In contrast to the immobilization approach, three movement
approaches are typically used with adults: controlled passive mobilization, place-and-
hold regimens, and early active motion (Peters et al., 2021). Controlled passive
protocols (e.g., Kleinert, Duran) only allow for passive flexion of the finger through
external force, delaying active movement to reduce strain on the healing tendon (Cetin
et al., 2001; Starr et al., 2013). In place-and-hold regimens, the injured digit is passively
moved into a partially flexed position and the patient uses active muscle contraction to
hold the flexed position. This approach places mild stress on the tendon to facilitate
healing while restoring the tendon’s tensile strength (Singh et al., 2015). Early active
motion protocols are the most aggressive, encouraging active finger flexion exercises
as soon as 3-5 days post-surgery (Higgins & Lalonde, 2016; Lalonde & Higgins, 2016).
Across all therapeutic protocols, evidence for positive outcomes and negative
complications is equivocal, (Bigorre et al., 2018; Khanna et al., 2009; Starr et al., 2013)
leading to significant variation in practice, with no consensus on the most effective
therapeutic approach (Bigorre et al., 2018; Peters et al., 2021; Powell & von der Heyde,
2014). Despite decades of research on surgical and rehabilitation interventions focused
on optimizing outcomes for individuals with flexor tendon lacerations, the likelihood of
successful recovery without residual complications has remained relatively unchanged.
6
Moreover, the generalization of research findings is challenging (Gibson et al., 2017;
Kannas et al., 2015; Neiduski & Powell, 2019; Peters et al., 2021; Starr et al., 2013).
Roughly 30% of this population continue to have residual impairments, such as joint
contractures, dense adhesions, tenosynovitis, or trigger finger (Kilic et al., 2015; Lilly &
Messer, 2006; Rrecaj et al., 2014). Up to 20% of patients require tenolysis or tendon
graft surgeries to salvage tendon gliding in cases of severe contracture (Bigorre et al.,
2018; Griffin et al., 2012). Even more disconcerting, over 10% of these individuals
experience a tendon repair rupture, which requires a second surgery to regain function
(Ibrahim et al., 2014; Johnson et al., 2020). Patients undergoing follow-up surgery,
either to repair a ruptured tendon or to release a severely adhered tendon, have more
complications and worse long-term outcomes than those who have only had primary
repairs (Elliot & Giesen, 2013; Ibrahim et al., 2014; Johnson et al., 2020).
Unfortunately, there is no universal consensus on optimal treatment for people
who have had a flexor tendon laceration and undergone a primary surgical tendon
repair (Abate, 2014; Ibrahim et al., 2014; Peters et al., 2021; Sandrey, 2003;
Silfverskiold et al., 1993; Skirven et al., 2011; Wu & Tang, 2013). With mixed evidence
of the effectiveness for different rehabilitation protocols and numerous factors that
influence successful recovery, (Abate, 2014; Ibrahim et al., 2014; Sandrey, 2003;
Silfverskiold et al., 1993; Skirven et al., 2011; Wu & Tang, 2013) the decision of when to
start active motion depends heavily on surgeon recommendation and therapist
experience. As a result, it is not clear that patients are receiving the most effective care,
and clinicians are often placing patients at risk for complications, such as ruptures or
severe adhesions.
7
1.3. Challenges to Recovery and Return to Function
The location of the tendon injury is a key factor affecting recovery following
tendon repair. Flexor tendon repair in zone II has been known to be particularly
challenging, (Bigorre et al., 2018; Chesney et al. 2011; Kotwal & Ansari, 2012; Peters et
al., 2021) gaining the name of “no man’s land” (Kotwal & Ansari, 2012). This zone
extends from the proximal border of the A1 pulley (below the distal crease of the palm)
to the insertion point of the FDS (around the central middle phalanx). Although the most
frequently injured area of flexor tendons in the hand, zone II injuries have the poorest
prognosis and are particularly complex due to the proximity of several small anatomic
structures (Bekhet et al., 2021).
Zone II tendon lacerations are primarily challenging because the FDS bifurcates
in this region, diving around the FDP and inserting on the lateral and medial aspect of
the middle phalanx. In addition to the FDS bifurcation, the proximity of these two
tendons tightly surrounded by annular pulleys while encased by a synovial sheath
introduce numerous biomechanical, physiological, and kinematic factors; each of which
is susceptible to injury and make repair, healing, and recovery in zone II more
challenging (Kotwal & Ansari, 2012). As a result, recovery in this region requires
restoration of tendon gliding within a tight fibro-osseous sheath with little room for
adhesions, swelling, or other complications in surrounding tissues (Dy & Daluiski, 2014).
In addition to the injury location, recovery is further affected by individual patient
factors (Karen Pettengill & Strien, 2011) as well as factors external to the patient
(Ibrahim et al., 2014). When tailoring treatment plans for individuals in this population,
many risk factors that elevate the risk of tendon injury or that often influence the process
8
of tendon healing need consideration. For instance, intrinsic factors such as the
individual’s sex, age (Gross & Hoffmann, 2013), and existing comorbidities (e.g., type 2
diabetes mellitus or obesity) affect the process of tendon healing (Nichols et al., 2019;
Nourissat et al., 2015; Rigo & Røkkum, 2016). In addition to intrinsic factors, many
extrinsic factors (e.g., the timing of surgery after the initial injury, surgical repair
technique, zone of injury, non-dominant hand injury, or smoking habits) can also
significantly influence the healing process; together, these factors affect overall recovery
and functional outcomes (Ibrahim et al., 2014; Nichols et al., 2019; Reito et al., 2019;
Rigo & Røkkum, 2016).
Although there are numerous factors affecting recovery outcomes, the most
critical factor following tendon repair is the timing of active movement following surgery.
In the past, protective protocols were predominantly used as they minimize the risk of
rupturing the tendon repair. To avoid tendon defect or rupture, these protocols
prohibited the movement of the repaired tendon before coaptation occurred. However,
delaying motion to protect the repair can promote dense adhesion formation between
the tendon and its surrounding tissues (Starr et al., 2013), which can decrease hand
mobility and cause joint contractures (Kilic et al., 2015; Rrecaj et al., 2014).
With these risks in mind, early tendon glide is frequently implemented as part of
rehabilitation to deter detrimental adhesion development. However, any motion of the
tendon before the repair has fully coapted is risky, as the strength of the repair heavily
relies on the surgical sutures and immature, newly forming tissues. Consequently, if
tendon movement begins too early, the repair may gap (i.e., tendon defect) or, in worse
situations, may even rupture. Despite this, early tendon gliding is highly recommended
9
for optimal outcomes. For example, moving the tendon as it heals can promote tendon
strength, mass, and mechanical properties that are all necessary for proper hand
function (Killian et al., 2012; Kjaer et al., 2009; Thomopoulos et al., 2015; Titan et al.,
2019). Due to this delicate balance, identifying the appropriate time to initiate active
tendon motion is critical for optimal recovery.
There is a dire need to support the decision-making process following surgical
tendon repair to promote an efficient return to function with lower rates of complications.
A primary impediment to identifying the optimal interventions for this population is the
lack of precise measures or evaluative methods to guide informed decisions regarding
individualized rehabilitation protocols for tendon repair. A precision medicine approach
to tendon rehabilitation requires acknowledgment that a multitude of individual intrinsic
and extrinsic factors can influence recovery and an understanding that interventions
must be individualized. As such, a method to directly assess and measure the healing
status for each tendon repair throughout the recovery process is urgently needed to
provide precision care and ensure the most optimal treatment. Furthermore, developing
a precise method to evaluate flexor tendon healing and successful coaptation can
potentially help elucidate the association of individual factors with successful outcomes
as well as compare the effectiveness of different interventions.
1.4. Sonography in Musculoskeletal Rehabilitation
Given the multitude of challenges and the dire need for a precise evaluative
method to care for this population, the research conducted in this dissertation posits that
integrating musculoskeletal sonography (MSKS) into clinical rehabilitation will enhance
10
precision medicine approaches to recovery following a surgical tendon repair.
Sonography is an inexpensive, widely available, non-invasive, and pain-free imaging
modality that presents real-time images of anatomical structures under the skin. In
addition, MSKS provides static and dynamic views of anatomic structures and
surrounding tissues at rest and during active motion in real-time (Lee et al., 2016).
Recent technological advances in MSKS, including smaller and lighter portable devices,
cross-compatibility of software for more commonly used platforms (e.g., Android
TM
or
iOS
TM
devices), and significantly reduced costs, have increased the availability of
sonography and enhanced its utility for clinicians as an ideal imaging tool. One of the
most significant technological advances is high-frequency transducers and image
processing. This technology allows for the effective use of MSKS for examining very
small superficial musculoskeletal structures (Figure 1.1) (Lee et al., 2000).
Although the potential utility of MSKS may seem endless, there are some key
limitations to be considered when using MSKS within rehabilitation. A primary
disadvantage is the operator-dependent nature of imaging acquisition. Attaining clear
images with sonography is highly dependent on the skill of the individual conducting the
examination. The examiner must be trained in MSKS and have prior experience
11
replicating images of the anatomical structures under interrogation with healthy
individuals before examining patients. Given the dependency on operator skill level,
many studies using MSKS to investigate tendon injury often report the examiner’s
certifications or years of experience. In addition, studies also typically report the inter-
and intra-rater reliabilities of the examiners who acquire the sonographic images and, if
different, who interpret or measure the images.
One common pitfall of MSKS imaging is anisotropy, meaning that the properties
of the structure under examination are highly dependent on the angle of the structure
relative to the reflected sound waves returning to the transducer. To produce clear and
accurate images, the soundwaves must be uniformly sent from the transducer and then,
received in the same manner. If the soundwaves reflect off the interrogated structure
and are angled elsewhere, away from the transducer, the examiner may falsely
determine that the structure is missing, injured, or elsewhere.
A popular example of anisotropy occurs during the examination of the long bicep
tendon as it inserts onto the radial tuberosity at the elbow. As this tendon helps with
forearm supination and pronation, it changes angularity as it wraps around the radius.
This angularity produces an anisotropic effect by deviating the soundwaves away from
the transducer and can lead to misdiagnosis, typically a false positive tendon tear.
However, adjusting the transducer to the appropriate angle can often “fix” anisotropy
and help the examiner visualize the “missing” part of the structure. In contrast to novice
users, experienced sonographers are trained to be cautious when examining areas of
the body where anisotropy is common. Furthermore, skillful use of anisotropy can even
help sonographers identify or measure anatomic structures that are unable to be viewed
12
under conventional examination approaches.
Given the few limitations of MSKS, particularly when investigating specific types
of structures or tissues (e.g., ligaments surrounded by bone), magnetic resonance
imaging (MRI) is often used as a comparator (Jacobson, 2005). In contrast to MRI, the
constraints of MSKS include a small field of view, limited visualization of deep joints and
cartilage, and the ability to evaluate only the cortical surface of bones. Other
considerations when using MSKS include the use of a medium with open wounds (e.g.,
sterile gel) and imaging around sutures or Steri-Strip™, which can increase the risk of
infection and could generate artifacts in the images.
Despite these limitations, musculoskeletal rehabilitation research has leveraged
many advantages of MSKS, supporting its utility within clinical practice to evaluate
musculoskeletal structures (Docking et al., 2015; Hodgson et al., 2012; Nwawka, 2016;
Robinson, 2009). The most prominent advantages of MSKS include its cost-
effectiveness, portability, high spatial resolution, dynamic assessment potential, real-
time visualization, non-invasiveness, and ability to rapidly assess musculoskeletal
tissues, foreign bodies, or tissues adjacent to metal hardware (Jacobson, 2005; Lee et
al., 2016; Lee et al., 2013). Research applications of MSKS have primarily focused on
the evaluation of peripheral nerves and neurological disorders, the diagnosis of
arthropathy and inflammatory conditions, and the examination of muscles and tendons
(Nwawka, 2016).
Regarding the peripheral nerves, several studies demonstrate that sonography
has a high sensitivity for diagnosing various pathologies, with dynamic imaging
particularly useful when assessing nerve entrapment disorders. Even more auspicious,
13
the diagnoses made with sonography correlate well with other frequently used
evaluative methods, such as MRI and electromyography (Domkundwar et al., 2017;
Zaidman et al., 2013). Moreover, scientists have explored using MSKS to evaluate
complex nervous disorders and for some, have been able to detect potential causes.
For example, MSKS can be used to evaluate post-traumatic brachial plexopathy and
can help pinpoint and identify causations, such as nerve root avulsion,
pseudomeningocele, and traction neuroma (Chen et al., 2011; Gunes et al., 2018;
Haber et al., 2006).
Regarding arthropathies and inflammatory conditions, sonography can readily
reveal proliferative bone formation, osseous erosion, and bursitis (Grassi et al., 2004;
Iagnocco et al., 2011). Much of the literature that uses MSKS to evaluate these types of
disorders is primarily focused on assessing rheumatoid arthritis, (Kang et al., 2012) joint
synovitis, and tenosynovitis (Nwawka, 2016). Applications of sonography to evaluate
individuals with rheumatoid arthritis have been especially useful as this disease
operates on a continuum. Multiple studies have demonstrated sonography’s potential to
help predict the progression of this disease for individuals who are at risk, confirm an
early diagnosis, consider differential diagnoses, monitor the disease, and detect disease
remission (Di Matteo et al., 2020). Furthermore, given sonography can allow for direct
visualization of anatomic structures and tissues, it can also be used as an assessment
tool for individuals with inflammatory arthritis to detect subclinical synovitis,
asymptomatic enthesis inflammation, bone erosions, and crystal deposits; all of which
may be otherwise missed during routine physical examinations (Kaeley et al., 2020).
Another one of the most common uses of MSKS has been for the examination of
14
muscles and tendons. Within muscles, MSKS has been used to evaluate post-traumatic
muscle tissue for myofascial tears, intramuscular hematoma, fatty atrophy, and fibrosis
(Nwawka, 2016). Sonography can help researchers distinguish morphological
differences in muscle abnormalities as well as help determine specific causes by
differentiating myopathy versus neuropathy (Maurits et al., 2003). Although not yet
clinically validated, newer research has explored using MSKS to assess glycogen
storage and muscle fasciculations, which can aid in the diagnosis of neuromuscular
disorders (Nwawka, 2016). Furthermore, and more relevant to the focus of this
dissertation, recent research has supported the use of MSKS for evaluating
tendinopathies, tendon tears, and ligament injuries (Docking et al., 2015; Hodgson et
al., 2012; Nwawka, 2016; Robinson, 2009).
In addition to the aforementioned applications of sonography, MSKS can also be
used for the dynamic assessment of anatomic structures and tissues in real-time.
Dynamic evaluation allows for the collection and evaluation of cinematic videos that are
obtained while the underlying structures are in motion. This type of dynamic video can
help visualize the architecture of a specific structure or tissues during movement in vivo.
Even more importantly, dynamic sonography can help visualize the relationships
between different structures while in motion, such as during muscle contraction. Another
important use of dynamic sonography is deciphering the location and potential cause of
symptoms that an individual experiences with motion. These dynamic assessments are
especially useful when symptoms can only be elicited during motion. For example,
when recreating symptoms of pain, MSKS can be used to detect atypical movement
patterns of the relevant anatomic structures, which can lead to the identification and
15
localization of the pain source. This dynamic capability has led to the primary use of
sonography by clinicians as a biofeedback tool (Giggins et al., 2013; Gray et al., 2017;
Roll et al., 2016; Roll et al., 2015).
Another pertinent use of MSKS is Doppler ultrasound, which can be used to
identify and measure the velocity of moving tissues, such as blood flow. This
sonographic technique is frequently implemented in research studies on rheumatoid
arthritis and other inflammatory arthropathies to evaluate the status of disease
progression and aid diagnosis. Other uses of Doppler are to differentiate active synovitis
and inactive synovial thickening, characterize the pattern of soft tissue masses, and
indicate the vascularity of repaired rotator cuff tendons (Adler et al., 2011; Nwawka,
2016). Although these techniques still need more research, these novel applications of
MSKS demonstrate its increasing utility and potential to advance the diagnosis and
evaluation of a multitude of upper extremity injuries and disorders.
1.5. Application for Sonography and Precision Care in Tendon Recovery
In clinical practice, MSKS is increasingly used to rapidly evaluate small structures
of the hand and fingers. For example, clinicians use MSKS to investigate or diagnose
pathologies, such as sagittal band injuries (e.g., Boxer’s knuckle), extensor and flexor
tendon tears, ligament tears, fractures and dislocations, nerve and vessel injuries, finger
deformities (e.g., Boutonnière deformity), trigger finger, volar plate injuries,
tenosynovitis, Dupuytren’s disease, masses, and finger lesions (Bianchi & Martinoli,
2007; Lee et al., 2016). In addition to diagnosis, MSKS has been used in direct
intervention as a tool for needle guidance (e.g., injection), delivery of pharmacologic
16
therapy, biofeedback, and patient education (Roll et al., 2016). Other uses of MSKS in
rehabilitation include evaluating tissue response to intervention, guiding clinical
reasoning for managing care, and evaluating the progression of healing tissues, such as
surgical tendon repair (Giggins et al., 2013; Roll et al., 2016).
MSKS is arguably the ideal tool for rapid point-of-care assessment of healing
flexor tendons in the hand following surgical repair. Sonography can detect morphologic
changes within tendons and is primarily used to diagnose acute injuries (Furrer et al.,
2009; Lee et al., 2000; Wang et al., 2017; Wu et al., 2012). However, MSKS can also be
used post-surgically to assess the integrity of the tendon and sutures (Figure 1.2) and
identify signs of recovery (Bianchi et al., 2007; Cohen, 2011; Corduff et al., 1994;
Jeyapalan et al., 2008; Marlborough et al., 2015; Nugent et al., 2012; Puippe et al.,
2011; Reissner et al., 2018). The sonographic appearance of successful tendon
healing, or coaptation, includes thickening at the repair site (Reissner et al., 2018),
minimal fluid collection, and a lack of scar adhesions surrounding the tendon (Cohen,
2011; Jeyapalan et al., 2008). Before coaptation, neovascularization or disorganized
and interrupted tendon fibers within a hypoechoic space at the suture site are both
positive signs of healing (Cohen, 2011; Puippe et al., 2011).
17
In contrast, MSKS can also help identify signs of poor healing or pathology within
the post-surgical tendon. Common signs of poor healing include tendon thinning or
gapping (Griffin et al., 2012), persistent fluid collection (e.g., edema) within the tendon
sheath, intra-tendinous calcifications, or severe adhesions (Cohen, 2011; Jeyapalan et
al., 2008; Varghese & Bianchi, 2014). Furthermore, capturing real-time, dynamic
movement of anatomical structures with sonography is particularly useful for evaluating
tendon recovery. For example, severe adhesions to surrounding tissue become
apparent during disrupted tendon motion that occurs when actively or passively moving
the tendon. Finally, dynamic MSKS is an excellent way to evaluate for suspected
rupture of a healing tendon (Yasrebi et al., 2015; Zhang et al., 2012).
Multiple sonographic biomarkers correlate with immediate and long-term
outcomes following tendon repair. Adhesions, edema, and calcification are associated
with decreased range of motion (Cohen, 2011; Puippe et al., 2011; Reissner et al.,
2018), and macro-morphologic biomarkers of tendon length, cross-sectional area
(CSA), and excursion are predictive of functional outcomes 3-6 months post-surgery
(Puippe et al., 2011; Zellers et al., 2018). Similarly, micro-morphologic biomarkers
18
quantified using spatial frequency analysis are related to general tendon health
(Bashford et al., 2008; Kulig et al., 2016; Kulig et al., 2013; Pearson et al., 2017).
Among the micro-morphologic biomarkers, peak spatial frequency radius and dominant
frequency bandwidth appear most useful for evaluating tendon health (Bashford et al.,
2008; Kulig et al., 2016; Kulig et al., 2013). Furthermore, a tendon’s peak spatial
frequency radius can help determine the tensile strength of the tendon during recovery
by evaluating acute alterations in micromorphology between rest and isometric
contractions (Pearson et al., 2017).
Unfortunately, a translational model for implementing sonography in clinical
rehabilitation for tendon repair has yet to be developed. There is limited research
focused on using MSKS to evaluate surgically repaired tendons during the acute
healing phases, and there appears to be no evidence documenting the appearance of
repaired tendons with MSKS across the entire process of post-surgical healing;
specifically, sonographic biomarkers of tendon healing after surgical repair have yet to
be extensively assessed in rehabilitation settings and throughout the recovery process.
Moreover, a standardized protocol to evaluate flexor tendons does not exist. Given the
potential for sonography to inform clinical decisions by evaluating early and ongoing
signs of progressive healing or pathology following tendon repair, this dissertation aims
to establish a foundation upon which a translational model for clinical implementation
can be built.
1.6. Dissertation Overview
The long-term goal of this research is to develop a precision medicine approach
19
for the rehabilitation of individuals who have had surgically repaired flexor tendon
lacerations using MSKS. Sonography has been increasingly used to evaluate acute
tendon injuries (Furrer et al., 2009; Lee et al., 2000; Wang et al., 2017; Wu et al., 2012)
as well as for the investigation of post-surgical outcomes following tendon repair
(Yasrebi et al., 2015; Zhang et al., 2012). This growing evidence indicates that
sonography may be useful in evaluating morphologic changes of tendons during the
acute stages of healing, which is the most critical time for therapeutic intervention
(Puippe et al., 2011; Reissner et al., 2018).
As a crucial step, the goal of this dissertation is to provide foundational
information to optimize the use of sonography for assessing the status of a healing
flexor tendon after surgical repair. The following aims will be achieved by systematically
reviewing the literature to elucidate the progression of tendon healing, establishing a
standardized image acquisition and analysis protocol to evaluate healthy flexor tendons,
and applying an adapted version of this image acquisition and analysis protocol to
demonstrate its feasibility in the patient population and document the progression of
healing tendons after surgical repair:
Aim 1: Conduct a systematic review to describe the morphologic and physiologic
changes of healing tissue over time after a surgical tendon repair, including evidence
of MSKS biomarkers associated with healing progression or development of
complications.
20
Aim 2: Establish a sonographic image acquisition and analysis protocol to evaluate
healing and recovery following flexor tendon repair.
Aim 3: Identify sonographic biomarkers that predict functional recovery and most
easily distinguish patterns of healing following tendon repair.
21
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CHAPTER 2. The Recovery Process for Surgical Flexor Tendon Repair:
A Timeline of Healing
2.1. Introduction
Despite decades of research, the functional outcomes for people who have had a
surgically repaired flexor tendon have remained relatively unchanged and are
unsatisfactory. With roughly 30% of individuals having residual impairments, up to 20%
requiring tenolysis, and 10% experiencing tendon rupture, there is a dire need for
methods to improve functional outcomes following tendon repair surgery (Bigorre et al.,
2018; Griffin et al., 2012; Ibrahim et al., 2014; Johnson et al., 2020; Kilic et al., 2015;
Lilly & Messer, 2006; Rrecaj et al., 2014).
Rehabilitation is critical to successful recovery, and one of the most important
aspects of therapeutic intervention for this population is appropriately timing the
initiation of active motion of the repaired tendon. Clinicians must make key decisions to
estimate proper timing given the tendon’s current healing status and progress therapy
accordingly; these decisions can either significantly enhance or impede recovery. If
movement is initiated too late, more adhesions will form around the tendon, inhibiting
tendon glide and limiting the strength of the repair (Aufwerber et al., 2020; Nourissat et
al., 2015). If initiated too early, the repair site will form a gap and may even rupture
(Renfree et al., 2021; Singh et al., 2015). Severe tendon gapping can also intensify
adhesion development, negatively affecting function.
Although these clinical decisions are critical to successful healing and efficient
return to function, there is no universal consensus on the optimal rehabilitative approach
31
for treating individuals with surgically repaired tendons (Bigorre et al., 2018; Peters et
al., 2021; Powell & von der Heyde, 2014). Initiating motion early, before the repair is
fully healed, is necessary for optimal recovery; however, there is no standardized
assessment to immediately and directly examine the status of the healing repair to
ensure patients recover safely, avoiding the risk of a tendon rupture. Consequently,
therapists must rely heavily on their clinical knowledge, previous experience, and
intuition to determine the appropriate progression of therapy and initiation of active
tendon movement. These clinical decisions not only put patients at risk for developing
complications but also lead to suboptimal outcomes for many individuals. In the worst
cases, patients require secondary surgery to successfully return to function.
To address these problems, an extensive literature review was conducted to
elucidate the physiologic and morphologic processes involved during tendon healing
and identify when these changes typically occur. Using the literature included in this
review, this study aimed to develop a timeline of healing for lacerated flexor tendons in
the hand after surgical repair that can be used to enhance the precision of treatment
and patients’ safe, efficient return to function. Furthermore, given that MSKS allows
clinicians to view the status of a healing repair rapidly, directly, and in real-time,
sonographic biomarkers indicative of successful tendon healing or potential
complications are also identified in this review.
2.2 Methods
The data included in this review were extracted from published literature that
discussed the physiologic or morphologic processes of tendon healing after a primary
32
surgical tendon repair following acute trauma, immediately after surgery to the end of
the maturation phase of healing (i.e., 1-2 years). Two constructs were examined in this
review: 1) the physiologic and morphologic processes of tendon healing, including
surrounding tissues, and 2) the assessment of morphologic biomarkers associated with
tendon healing or functional recovery following acute tendon injury or surgical tendon
repair. For the examination of morphologic biomarkers, the review focused primarily on
the use of sonographic imaging as a potential clinical tool.
The literature search was conducted in the PubMed database on May 31, 2021,
using a combination of three sets of search terms. All search sets used a combination of
MeSH terms (when available) and keywords, and results were limited to articles
published in English. The first set included the concepts of tendons, flexor tendons,
tendon injuries, or finger tendons, combined with healing, scarring, or regeneration in
articles published after May 31, 1980. As knowledge of the typical progression of tendon
healing has remained relatively unchanged in recent decades, the publication date
restriction for this first search was used to reduce the otherwise large number of articles
and consider studies that used more recent research technologies. Second, the
concepts of regeneration and assessment or evaluation were searched without date
restriction. Finally, the concepts of tendon and surgery or disorder were combined with
assessment, sonography, or ultrasound imaging in articles published after January 1
st
,
2010. The date restriction of this third search was applied given more recent
technological advances for assessing musculoskeletal tissues, particularly small
musculoskeletal structures (e.g., flexor tendons), which have become significantly more
sensitive and reliable over the past two decades. The full search strategy is included in
33
the Appendices (Appendix A.1).
After duplicate articles were removed, all study titles and abstracts were
screened for eligibility. Studies were considered for inclusion if they focused on healing
after an acute tendon injury or surgical repair and included at least one of the following:
1) physiology related to tendon healing, 2) morphology related to tendon healing, 3)
clinical assessment or evaluation of tendon healing or functional recovery, or 4)
sonographic biomarkers related to tendon healing or functional recovery. Subsequently,
studies that met these criteria progressed to a full-text review.
Priority for final eligibility was given to publications that focused on healing
following a primary surgical repair of a flexor tendon in the upper extremity or
sonographic parameters associated with tendon healing or functional recovery. There
were no restrictions on study design or level of evidence for an article to be included.
Furthermore, as a large portion of literature regarding tendon laceration and healing
uses animal subjects, the articles that studied animal tendons, even those without
human subjects, were included. Articles that identified morphologic biomarkers that are
typically observed during healing or that may be indicative of adverse outcomes were
also included.
Given the scope of this review, study quality was not evaluated, nor were any
data extraction processes conducted for quantitative synthesis. Instead, a qualitative
synthesis was conducted using an inductive approach to organize the information
provided in the included studies across four main themes:
1) anatomical, morphological, or physiological factors that may impact tendon
healing
34
2) morphology of tendons and surrounding tissue following tendon laceration and
surgical repair
3) physiology of tendon healing and surrounding tissues following tendon laceration
and surgical repair
4) measures of healing or functional recovery following tendon laceration and
surgical repair.
Throughout the document review process, any information on the timing of the
morphologic or physiologic changes that occur across recovery was noted to support
the development of a comprehensive healing timeline. In addition, any assessments
used to evaluate tendon healing, including the use of MSKS biomarkers, were included
in the timeline.
2.3. Results
After conducting the search in PubMed and removing all duplicate articles, a total
of 12,710 articles were identified for this literature review. The title and abstracts of
these articles were screened, and 216 full-text articles were reviewed for potential
inclusion. After review, a total of 64 articles were included in this literature review
(Appendix A.2). The findings of the iterative qualitative synthesis within each of the four
primary themes follow.
2.3.1. Factors Complicating Tendon Repair and Recovery
The anatomy and physiology of the healthy flexor tendons in the hand are
illustrated in the literature with excellent detail; a summary of which is provided in an
35
educational supplement piece (Appendix A.3). Despite a common anatomical
foundation, it is important to note that there is considerable heterogeneity of flexor
tendons in the healthy population, which may influence healing. The most prominent
variability is the wide range of flexor tendon sizes within and between healthy
individuals. A study by Boyer et al. (2001) observed a 38% difference in the mean
values of flexor tendon height between the largest (i.e., middle finger) and smallest (i.e.,
small finger) digits and a 42% difference in tendon cross-sectional area (CSA)
(calculated with ellipses method); in fact, height and CSA of middle finger flexor tendons
were both significantly greater than the other digits.
Furthermore, a variety of anatomic anomalies exist for flexor tendons in a large
percentage of the healthy population. Notable anomalies of flexor tendons in just the
small finger include an absence of the flexor digitorum superficialis (FDS) for 15.7% of
the population (Baker et al., 1981), aplasia of the flexor digitorum profundus (FDP), an
accessory FDS (Yilmaz et al., 2009), doubling of the FDS, attachments to other
superficialis tendons or the FDP, varying FDS insertion points, and additional muscle
bellies from the ring finger FDS to the small finger FDS (Yilmaz et al., 2009). Additional
deviations from typical hand anatomy include the pattern and arrangement of crucial
and annular ligaments, which can also vary greatly among healthy individuals (Schöffl et
al., 2012).
A final consideration is that the fibrous tissues that compose each tendon have
different properties based on their location within each tendon. Specifically, the tissue
from the dorsal aspect of the tendon has greater strength, less collagen crosslinking,
and a larger single bundle CSA than the palmar tissue (Soejima et al., 2003).
36
Appreciating the unique qualities of tendon tissues, including their distinctive, non-linear
response to mechanical loading and the heterogeneity in their composition and
morphology, can help clinicians and researchers better understand and overcome the
challenges associated with recovery following a tendon injury.
2.3.2. Physiology and Morphology of Tendon Healing After Surgical Repair
For flexor tendons to heal successfully, tendons must heal intrinsically versus
extrinsically, such that healing occurs with cell proliferation originating from intrinsic cell
components rather than from the migration of extrinsic cells. In contrast to intrinsic
healing which results in fewer complications and superior biomechanics, extrinsic
healing is aversive and leads to the formation of peritendinous adhesions that cause
joint stiffness and functional impairment (Gougoulias & Maffulli, 2011; Klifto et al., 2018;
Voleti et al., 2012). The relative balance between extrinsic and intrinsic healing is
determined by several factors, including the location of tendon laceration, the extent or
complexity of trauma, and postoperative motion (Voleti et al., 2012). To promote
successful healing, tendon gliding or scrubbing of the tendon along the tendon sheath
can mitigate extrinsic cells from forming adhesions, while pumping nutrition from
synovial fluid to tenocytes (Schöffl et al., 2012; Singh et al., 2015).
During this healing process, there is an interplay between mechanical signaling
and biochemical changes in the tendon matrix. As the repaired tendon heals, it
responds to mechanical signals, such as stress, which produce chemical changes in the
cellular environment. These chemical changes stimulate adaptations in the morphology,
structure, and material properties of the tendon that affect healing, potentially promoting
37
functional recovery (Killian et al., 2012; Kjaer et al., 2009; Titan et al., 2019). One such
example of this is muscle loading. While the tendon is healing, muscle loading facilitates
the preservation of tendon mass and facilitates the mechanical properties of the tendon
(Thomopoulos et al., 2015). Appropriate mechanical loading of the healing tendon
stimulates collagen synthesis, proper alignment of the collagen fibers, and tensile
strength. In addition to these benefits, mechanical loading also helps mitigate the
development and severity of extrinsic adhesions. When extrinsic adhesions are
extensive, patients often have poorer outcomes, including limited motion and joint
contracture (Aufwerber et al., 2020; Nourissat et al., 2015). Given this significance,
repaired tendons need to receive the appropriate level of mechanical stimuli that is
concurrent with the healing status of the repair to facilitate a successful recovery.
Generally, if the repair is more proximal (e.g., at the proximal phalanx) rather
than distal (e.g., at the distal phalanx), then differential gliding between the FDS and
FDP tendons is more limited. Ultimately, proximal tendon repairs often lead to restricted
DIP motion during composite flexion, as the adhered flexor tendons are conjoined and
functionally act as the FDS (Chinchalkar et al., 2016). This is particularly problematic for
recovery within zone II of the hand (i.e., the area between the proximal border of the A1
pulley and the insertion points of the FDS tendon). For zone II tendon repairs, the
density of adhesions will be most prominent in areas where the FDS and FDP tendons
have the least amount of differential motion during flexion. For injuries in this area of the
hand, the bulk of adhesions at the repair site is typically inhibited by the finger’s A2 and
A3 pulleys which limit the motion of the PIP and DIP joints.
Although there is much research regarding the use of biological, pharmaceutical,
38
and physical agent interventions to improve outcomes related to tendon laceration and
surgical repair, healed tendons do not obtain the same chemical and mechanical
properties after recovery compared to a native uninjured tendon due to scar formation
and inferior, non-native tissue regeneration (Gross & Hoffmann, 2013). As such,
repaired tendons are typically one-third of the tensile strength of intact tendons
(Nourissat et al., 2015) and approximately 40-70% of their original strength once fully
healed (Titan et al., 2019).
Despite recent and ongoing advancements in surgical and rehabilitation
interventions for injured flexor tendons, the biomechanical properties of a normal,
healthy tendon cannot be recreated (Myer & Fowler, 2016). For one, the type I collagen
content and tendon cells differ in cellular and molecular composition along the length of
the tendon. For example, the tendon enthesis where the tendon is attached to the bone
through fibrocartilaginous tissue has a higher amount of type I collagen cells in
comparison to the mid aspect of the tendon (Nourissat et al., 2015). This heterogeneity
across the length of the tendon leads to different responses to mechanical loading and
likely contributes to tendons having a stress-strain curve that is not linear in nature
(Myer & Fowler, 2016; Nourissat et al., 2015).
2.3.3. Timeline of Tendon Healing Progression After Surgical Repair
Through the qualitative synthesis and document review, the process of tendon
healing was outlined and a weekly timeline describing the cellular, tissue, and functional
changes that typically occur over time was developed (Figure 2.1). There are three
stages of tendon healing: inflammatory, proliferative, and remodeling. These stages
39
overlap, as the next stage of healing begins before the prior phase ends. Although the
exact timing of each phase is subject to many factors (e.g., complexity of injury, time
between injury and surgical repair, comorbidities), each phase has distinct cellular
characteristics and processes that set them apart from each other (Leong et al., 2020).
Across these three stages of healing, two critical time windows related to morphologic
and physiologic changes of the tendon were identified, and biomarkers associated with
either typical healing success or potential functional limitations were noted.
40
Figure 2.1. Timeline of Tendon Healing Progression
41
Inflammatory stage. Immediately after surgery, the inflammatory stage of healing
begins and is marked by the presence of red blood cells, white blood cells, and platelets
equipped with growth factors and endothelial chemoattractants (Voleti et al., 2012). This
initial stage of healing typically lasts for two to three days; however, in some cases, it
may last up to seven days. Generally, the longer the inflammatory phase continues, the
higher the risk of developing complications in healing and recovery (Schöffl et al., 2012).
During the inflammatory phase, the strength of the tendon is almost entirely reliant on
the surgical suture and the blood clot forming between the surgically repaired tendon
ends (Chang et al., 2000; Titan et al., 2019). As edema develops during this phase, the
tendon requires more energy to move as the severity of edema increases resistance to
tendon movement by 2-fold or 3-fold (Cao & Tang, 2006; Wu & Tang, 2013).
Fortunately, the level of edema typically decreases significantly three to seven days
after surgery. After which, any edematous tissue remaining at the site of injury begins to
harden and increase in severity (Wu & Tang, 2013). Although a pro-inflammatory
response enhances cell regeneration (Galatz et al., 2015), this increases resistance to
tendon glide and adds further risk to the repair rupturing. As such, the inflammatory
stage is when the tendon repair is weakest and most likely to rupture post-operatively
(Klifto et al., 2018; Titan et al., 2019).
Proliferative stage. As the inflammation subsides, the proliferative stage of
healing begins (around three days after surgery) and continues over the next four to five
weeks (Garner et al., 1989). This stage of healing is characterized by increased
cellularity directed by macrophages and tenocytes, as different cells are recruited to the
42
site of injury. These cells deposit a temporary, mechanically inferior matrix primarily
composed of type III collagen (Leong et al., 2020; Voleti et al., 2012). Fibroblasts or
connective tissue progenitors migrate to the repair site and proliferate to unite the
tendon ends (Garner et al., 1989; Jones et al., 2003; Leong et al., 2020; McDowell et
al., 2002). Cells that migrate away from the tendon and toward the tendon sheath
proliferate and form adhesions that can restrict tendon glide, which frequently occurs as
the relatively ischemic tendon is surrounded by more vascularized tissue (Singh et al.,
2015; Tang, 2019). Though the origin of these cells is still debated, fibroblasts and
intrinsic cells of the endotenon and epitenon begin synthesizing type III collagen,
proteoglycans, and other components of the extracellular matrix (Garner et al., 1989;
Leong et al., 2020). Unlike the type I collagen of healthy tendons, these inferior type III
cells have fewer crosslinks, decreased tensile strength, and poorer mechanical
properties (Leong et al., 2020; Voleti et al., 2012). As the repair heals, cell proliferation
continues along with the production of growth factors. This cellular activity spikes from
one to two weeks after surgery (Galatz et al., 2015).
About two to three weeks after surgery, tenocytes start producing type I collagen
cells, and the collagen fibers begin to reorganize (Garner et al., 1989; Jaibaji, 2000;
Leong et al., 2020). Because tenocytes become active later, it is believed that the
process of extrinsic healing from migrating fibroblasts begins before the process of
intrinsic healing (Myer & Fowler, 2016; Schöffl et al., 2012). As tenocytes are
responsible for synthesizing mature collagen, the strength of the tendon repair does not
improve until a few weeks after surgery, once the tenocytes become active (Myer &
Fowler, 2016). However, the healing tendon will continue to have significantly
43
decreased strength for some time after the repair. Tenocyte proliferation continues until
it drastically declines four weeks after surgery (Wu & Tang, 2013).
During the proliferative stage, adhesions continue to form until they are at their
strongest and able to withstand higher forces which typically occurs around 4 weeks
post-surgery (Voleti et al., 2012; Wu & Tang, 2013). During this time, the tendon will
also have less mobility and decreased elasticity (Gitto et al., 2016). Once the
development of adhesions peaks, the final remodeling stage of healing begins around
six weeks post-surgery (Gross & Hoffmann, 2013). It is not until type I collagen fibers
are longitudinally reoriented in alignment with the long axis of the tendon and the
collagen fibrils begin crosslinking that the strength of the tendon repair begins to
increase; a process that occurs six to eight weeks post-surgery (Myer & Fowler, 2016).
Following eight weeks after surgery, adhesions become more elastic, less dense, and
easier to break (Wu & Tang, 2013); and until that time, the tendon will have decreased
mobility and elasticity (Gitto et al., 2016). Normally, repaired tendons need to heal for 12
weeks before gaining the ability to withstand loading capacities associated with daily
activities (Schöffl et al., 2012).
Remodeling stage. The final stage of healing, remodeling, can last over a year,
with unique healing elements still present in scarred tissue years after injury (Voleti et
al., 2012). This final stage can be divided into two stages, a consolidation phase
followed by a maturation phase. The consolidation phase of healing consists of type I
collagen synthesis and alignment of the extracellular matrix, where tenocytes and the
tendon’s collagen fibers become aligned in the direction of stress (Leong et al., 2020;
44
Voleti et al., 2012). During the maturation phase, the newly deposited fibrous tissue
gradually changes to scar tissue, and the tendon’s collagen bundles increase in
thickness; tenocyte metabolism also decreases along with intra-tendinous vascularity
(Voleti et al., 2012).
Critical therapeutic windows. Two critical therapeutic windows that occur during
the first few months of healing were identified. The first therapeutic window begins two
weeks post-surgery, with the development of adhesions and the initial production of
collagen via tenocyte activity. As the tendon begins to heal intrinsically, tendon gliding
must be initiated to limit adhesions from forming between the tendon and the
surrounding tissues. Although tendon glide is needed to promote function and healing,
the repair must be protected during any motion to limit gapping at the repair site, as this
may lead to tendon rupture or complications. Interventions that focus on limiting edema
and extrinsic scar tissue during weeks four to eight are worth exploring, as this is
typically when adhesions peak.
Immediately after the first therapeutic time window, a second window occurs.
During the initial phase of this second window, adhesions become more elastic and
easier to break. Concurrent with adhesions becoming more pliable, the tendon also
becomes more mobile and the repair decreases in density. As such, the tendon may
glide more freely within the tendon sheath, giving the fingers a greater range of motion
at this time. However, this window quickly closes three months after surgery, as the
tendon’s mobility and density gradually become more static over the remaining year
following surgery. Therefore, interventions must be appropriately adapted to match the
45
progression of tendon healing, ensuring that the repair is strong, and the fingers can
easily move so that patients may achieve functional return safely and efficiently.
2.3.4. Musculoskeletal Sonography to Evaluate Tendons
Given recent advances in technology, musculoskeletal sonographic imaging is
increasingly used to assess tendon injury, evaluate outcomes, and inform intervention
for optimal recovery. Gitto, A. Draghi, and F. Draghi (Gitto et al., 2018) provide a
comprehensive overview of the appearance of healthy tendons when using sonography;
a brief overview is provided here. In long-axis, healthy tendons typically appear as a
hyperechoic (i.e., brighter and whiter), fibrillar pattern of parallel lines within a
hypoechoic (i.e., darker and blacker) matrix, as they mostly consist of longitudinally
oriented bundles of type I collagen fibers. When viewed in short-axis, tendons appear
as tight bundles of multiple hyperechoic dots surrounded by a thin hyperechoic
boundary of connective tissue. Synovial sheaths in the hand appear as thin echogenic
(i.e., solid color) or anechoic (i.e., black) fluid-containing structures that surround the
flexor tendons. Ligaments such as annular pulleys are best visualized in their short-axis
and appear as hypoechoic bands superficial to the flexor tendons.
Several studies support the use of high-resolution ultrasound for pre-operative
diagnosis of tendon injuries (Bekhet et al., 2021; Furrer et al., 2009; Hillman et al., 2019;
Lee et al., 2000; Wang et al., 2017; Wu et al., 2012). In a recent study, sonography with
a 10-15 MHz linear transducer was used to preoperatively diagnose full-thickness tears
and the presence of tenosynovitis in 50 injured flexor tendons with 100.0% accuracy,
sensitivity, and specificity; partial thickness tears were diagnosed with 98.0% accuracy,
46
100.0% sensitivity, and 97.4% specificity (Bekhet et al., 2021). As technology continues
to advance, point-of-care ultrasound may be the ideal method for diagnosing tendon
tears, given its portability, relatively inexpensive cost, and ability to dynamically assess
injuries in real-time.
Perhaps even more useful than for preoperative diagnosis, sonography has been
used to evaluate repaired tendons after surgery. These evaluations include the
investigation of suspected tendon ruptures, the integrity of the sutures, tendon gapping,
and biomarkers related to recovery (Bianchi et al., 2007; Cohen, 2012; Corduff et al.,
1994; Jeyapalan et al., 2008; Marlborough et al., 2015; Nugent et al., 2012; Puippe et
al., 2011; Reissner et al., 2018; Wang et al., 1999; Yasrebi et al., 2015; Zellers et al.,
2019; Zhang et al., 2012). Several studies have also suggested that sonography may
be an invaluable tool to assess the quality of tendon healing, especially for the clinical
evaluation of repaired flexor tendons in the hand (Budovec et al., 2006; Bűhler et al.,
2015; Corduff et al., 1994; Puippe et al., 2011; Sügün et al., 2010). As such,
sonography is a promising tool to assess post-surgical healing, and ultimately, may
facilitate better clinical outcomes that are much needed by this population.
Tendon enlargement. Immediately after surgical repair, the suture material is
distinctly visible in the operated tendon. The tendon’s hyperechoic fibrillar pattern
becomes disorganized and heterogenous at the repair site because small hypoechoic
areas or small calcareous deposits can develop around the hyperechoic sutures
(Créteur et al., 2019). Approximately three to six months after surgery, a successfully
repaired tendon will appear enlarged compared to native tendons and, though its
47
thickness may change during the first few months of recovery, its CSA will remain
thicker than the healthy, contralateral tendon (Cohen, 2012; Créteur et al., 2019; Puippe
et al., 2011; Reissner et al., 2018). Repaired tendons will also be longer than the
contralateral tendons by four weeks after surgery and will remain longer over time; this
lengthening slowly continues until it eventually tapers off after several months (Zellers et
al., 2019). Current research on Achilles tendons suggests that the lengthening of flexor
tendons may negatively affect functional outcomes (Zellers et al., 2019).
Tendon gapping. In addition to tendon thickening and lengthening, MSKS can
also be used to identify gapping. This is useful as tendon gapping has detrimental
effects on functional recovery if the gap is too wide. The formation of a gap signifies
dehiscence of the repair, which will almost always occur before the repair ruptures. A
gap formation greater than 3mm is typically associated with poor outcomes (Gelberman
et al., 1999). When assessing zone II tendon repairs, a gap of 5mm or larger is
indicative of tendon repair failure in about 80% of cases (Renfree et al., 2021). In
contrast, a gap formation of less than 3mm is common for repaired tendons. In the
majority of cases, a gap that is equal to or less than 3mm will not increase adhesion
development or stiffness, and can even result in greater tendon strength (Singh et al.,
2015).
Edema. In addition to these biomarkers, sonography can also identify localized
and intra-tendinous edema that develops around and within the tendon sheath (Lee et
al., 2016). Edema, given that it is primarily fluid, is observed as a nonmoving
48
hypoechoic or anechoic space surrounding the tendon (van Doesburg et al., 2012). In a
previous study by Puippe et al. (2011), MSKS was able to measure inflammation and
edema of surgically repaired flexor tendons during the acute phases of healing (i.e., 1-3
days after surgery) and throughout the following 12 weeks.
Vascularity. A final use of imaging that holds promise for assessing post-surgical
tendons is the examination of blood flow. Specifically, Doppler ultrasound can be used
to visualize and estimate the velocity of blood flow in real-time. Current evidence
supports the use of Doppler ultrasound to assess healing tendon repairs; applications of
this technology include measuring blood flow in large tendons (e.g., Achilles) as well as
very small tendons (e.g., flexor tendons in the hand) (Divani et al., 2010; Hackett et al.,
2016; Puippe et al., 2011; Sengkerij et al., 2009; Yang et al., 2012). By identifying blood
flow, Doppler has been used to detect the presence and number of blood vessels in the
area of interrogation and can even determine whether the vessels are peri- versus intra-
tendinous (Klauser et al., 2010).
Although the exact timing of when intra-tendinous vascularity begins is unknown,
no Doppler signal can be detected during the immediate postoperative period (Gitto et
al., 2016; Gitto et al., 2018). However, signs of neovascularization are typically present
two weeks after surgery. Vascularity steadily increases over the next 3 months,
stabilizes, and finally regresses within 6 months after surgical repair (Bűhler et al., 2015;
Gitto et al., 2018). Unlike repaired tendons, intra-tendinous vascularity is typically not
detected in uninjured FDP tendons (Bűhler et al., 2015).
49
Recovery complications. In addition to providing clinicians with the ability to
directly monitor the trajectory of tendon healing, sonography can also elucidate potential
complications that sometimes occur during the healing process. The detectable
sonographic biomarkers often indicative of worse healing outcomes include adhesive
scarring, synovial sheath thickening, and tendon rupture with as much as 96% accuracy
(Budovec et al., 2006). Sonography has also been used to quantify flexor tendon defect
or gapping at the repair site, which may help patients avoid tendon rupture (Renfree et
al., 2021; Singh et al., 2015). Furthermore, sonography can be used to examine tendon
excursion after surgery with dynamic imaging techniques as well as Doppler ultrasound.
Other uses of Doppler ultrasound include the detection of the level of vascularity within
and around the tendon (Bűhler et al., 2015; Cohen, 2012; Gitto et al., 2018; Puippe et
al., 2011).
Beyond the initial rehabilitation and recovery phase, sonography may also be
useful in assessing long-term prognosis. After six months of healing, the appearance of
tendon thinning, fluid in or around the tendon that is more than 50% thickness of the
tendon, an intra-tendinous doppler signal, persistent hypervascularization, or extensive
calcifications has been associated with poor functional outcomes and postsurgical
complications, such as tendon re-rupture and lengthening of the tendon callus (Cohen,
2012; Gitto et al., 2016; Gitto et al., 2018). After flexor tendons are repaired, the volar
plate changes in appearance, with the body of the plate having a marked wavelike or
sigmoid deformity (Saito & Suzuki, 2011).
50
2.4. Discussion
This literature review was conducted to illuminate the morphologic and
physiologic processes of flexor tendons as they heal over time after surgical repair. A
timeline was developed to detail the progression of tendon healing after surgery and
identify potential sonographic biomarkers that may elucidate the quality of tendon
healing and function. After a review of the structural architecture and physiology of
healthy tendons, the weekly progression of physiologic and morphologic changes that
occur after a surgical tendon repair was described, and two critical therapeutic windows
were identified; the recovering tendon and surrounding anatomic tissues were included
in this description. This information may be used to assess tendon healing as well as
enhance the effectiveness of interventions; subsequently, improving individualized care
and functional outcomes for this population.
Clinicians must be mindful of the architecture, anatomy, and biology of the flexor
tendons and surrounding structures to appreciate how these factors affect the gliding
surface of healing flexor tendons, especially given that these tendons are adapted with
an intrasynovial system unique to tendons in the hand. For example, vincula, which are
essential to supplying the FDS and FDP with vascular nutrition, are located within the
tendon sheath and may create a higher frictional force when passing under the pulley
system during finger flexion (Myer & Fowler, 2016). Clinicians should keep in mind the
mechanical forces involved with tendon glide as they can inhibit successful tendon
coaptation. Some considerations are 1) the friction of the gliding surfaces, such as the
added resistance of surgical sutures joining the healing tendon ends; 2) the amount of
loading on the tendon, particularly during motion or activity; and 3) the angle of the
51
tendon to the pulley system, as a greater angle increases the frictional force (Amadio,
2013).
Multiple sonographic biomarkers that can help monitor and assess the status of
healing tendons after surgical repair were identified. Sonographic measures such as
tendon CSA, length, thickness, and height can indicate how well the tendon repair is
healing. Another advantage of using these biomarkers is that they can be compared to
a patient’s uninjured, contralateral anatomy. Given that healthy flexor tendons can have
significant variability, research investigating the comparison between the healthy
contralateral and injured anatomy as the tendon heals is especially useful, and more on
this topic is needed (Cohen, 2012; Créteur et al., 2019; Puippe et al., 2011; Reissner et
al., 2018).
Of similar significance, the sonographic biomarkers identified in this review can
also be indicative of potential complications that many patients experience during
recovery. For example, hypervascularity, especially when intra-tendinous, may be
indicative of increased pain (Divani et al., 2010; Yang et al., 2012) and is correlated with
negative biomechanical outcomes related to function, including gait asymmetry and
decreased heel-rise test height (Hackett et al., 2016; Zellers et al., 2019). Sonography
can also be used to help detect causes of suboptimal recovery. With direct visualization
of the internal structures, examination under sonography can help differentiate whether
any limited range of motion is due to persistent edematous tissue, tendon gapping,
significant adhesive scarring, or in the worst case, a ruptured repair (Budovec et al.,
2006; Matthews et al., 2018; Schöffl et al., 2012; Wang et al., 1999; Yassin et al., 2020).
Knowledge of the typical process of tendon healing post-surgical repair is
52
necessary for clinicians to appropriately select the most effective and safest
interventions throughout each stage of healing. Understanding how and when the
morphology and physiology of repaired tendons and surrounding tissues change during
recovery is a critical aspect of treatment planning. In addition, sonography can help
elucidate typical versus atypical biomarkers related to functional outcomes and is an
ideal tool to facilitate precision care for rehabilitation. To illustrate, in cases of tendon
rupture, patients will have extremely diminished benefits from outpatient therapy and
instead, will require a secondary surgery to re-repair the tendon and achieve motion. By
monitoring these biomarkers, clinicians may be able to track atypical healing patterns as
they occur and make informed decisions about the best course of treatment. In doing
so, sonography may help support clinical decisions to individualize each plan of care
and may have the potential to help assess whether patients are responding positively or
negatively to interventions.
Overall, there was general agreement across most of the literature regarding the
data collected (e.g., overlapping stages of healing, the architectural structure of
tendons, estimated length of the inflammatory phase) for this review. However, there
was significant heterogeneity in the type of studies included. Many longitudinal studies
had large variability in the follow-up times for repeated measures (e.g., days, weeks,
years). This variability likely suggests that some biological processes and the timing of
tendon healing are often affected by numerous factors, such as the anatomic location of
the injured tendon or the way the injury was sustained.
This review mainly focused on the morphologic and physiologic factors related to
tendon healing after a primary surgical repair. To this end, the review aimed to include
53
as much information as possible while maintaining consistency of data across included
studies. The findings gathered from this review have many implications for clinical
practice and future research. More literature is required to better understand the exact
physiological and morphological processes that occur during typical and atypical healing
patterns over time following surgical flexor tendon repairs.
54
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CHAPTER 3. Establishing a Protocol to Evaluate
the Flexor Digitorum Profundus Tendon
3.1. Introduction
Musculoskeletal sonography (MSKS) is becoming more routinely used to
evaluate the small, superficial anatomic structures of the hand, and its usage for point-
of-care applications by physicians, therapists, and other professionals is rapidly
increasing. The initial focus of point-of-care applications of MSKS has primarily been on
diagnosis; however, more recent publications have expanded on the utility of point-of-
care MSKS and are investigating its applications as an adjunct to clinical interventions.
For example, in rehabilitation settings worldwide, clinicians are successfully
incorporating MSKS in therapy as a biofeedback tool, assisting patients with functional
activities that include muscle activation, postural control, and pain management
(Giggins et al., 2013; Roll et al., 2016; Roll et al., 2020; Shaikh et al., 2020; Takata et
al., 2020). Rehabilitation professionals have also effectively applied sonographic
imaging as a tool for outcomes measurement by using it to monitor healing progression
and to ascertain any morphologic responses of tissues to intervention (Roll et al., 2016).
Given its utility for point-of-care applications, sonography may be useful for
clinicians treating individuals in hand therapy (Roll et al., 2015). Particularly, clinicians
can use MSKS when treating tendon injuries, a prevalent condition that hand therapists
have identified as a research priority (MacDermid et al., 2002; Takata et al., 2018).
Previous studies using sonography for flexor tendon evaluation have primarily focused
on the diagnosis of tendon injuries, predominantly for acute tendon traumas (Furrer et
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al., 2009; Lee et al., 2000; Wang et al., 2017; Wu et al., 2012). However, there is limited
literature in this area, and a dearth of information exists on the sonographic
investigation and appearance of healthy tendons in the hand.
Previous studies of flexor tendon anatomy have established that flexor tendons
have a wide range of sizes within and across healthy individuals (Boyer et al., 2001).
Furthermore, flexor tendons have numerous anatomic anomalies. For example, some
anatomic anomalies in the small finger alone include an absence of the flexor digitorum
superficialis tendon (FDS), aplasia of the flexor digitorum profundus tendon (FDP), a
supplementary FDS, varying attachments and insertion points of the FDS, and
accessory muscle bellies from the ring finger FDS (Baker et al., 1981; Yilmaz et al.,
2009). Given the significant variance of flexor tendon morphology in healthy individuals,
knowledge of variability in sonographic appearance would be useful.
A standardized protocol to assess these structures is essential for identifying
both health and pathologic tendons. Although it is common practice to use standardized
protocols to evaluate musculoskeletal anatomy, the protocols that currently exist are
either focused on assessing global areas of the body (i.e., shoulder) or diagnosing
specific disorders or injuries. For example, previously established protocols published
by The European Society of Musculoskeletal Radiology have focused on the global
examination of joints, which include the shoulder, elbow, wrist, hip, knee, and ankle
(Martinoli, 2010). For more detailed assessments, adaptations of these global protocols
have been published to assist with the confirmation of existing injuries or for differential
diagnoses (Jacobson & Jacobson, 2018). Despite numerous existing protocols, there is
no established standardized protocol to examine flexor tendons in the distal hand.
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There is an urgent need for a standardized protocol to support clinicians and
researchers in the evaluation of flexor tendons with MSKS. As such, the aim of this
research was to 1) establish an image acquisition protocol to standardize assessment
and 2) elucidate the typical variation in morphology of flexor tendons in healthy
individuals. By evaluating flexor tendons in healthy individuals, we can establish the
typical morphologic appearances and anatomic anomalies that can occur without
dysfunction. Furthermore, by standardizing images, we can establish measurable
sonographic parameters that can be reliably replicated across individuals when
evaluating these structures.
3.2. Research Methods
3.2.1. Study Design
This feasibility study was completed to develop a standardized protocol for image
acquisition and analysis to evaluate flexor tendons in the distal upper extremity for
research and clinical use. Participants were individually scanned to optimize the
sonographic equipment and to standardize image acquisition techniques for the most
accurate portrayal of the FDP tendon in the right index finger. As this application of
sonography is relatively novel and the research on this topic is still emergent, an initial
image acquisition protocol was developed and deployed over two data collection
sessions with one healthy participant. Multiple meetings were held to refine the protocol,
and after revisions were agreed upon, a revised protocol was carried out with a series of
healthy volunteers. The images acquired from these participants were qualitatively
analyzed to 1) elucidate the appearance of the flexor tendons in the finger, 2) identify
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anatomical variants that may exist in the healthy population, and 3) create a list of
suggestions and considerations to optimize data collected using the finalized protocol.
This study was approved by the university’s institutional review board, and all
participants provided informed consent before enrollment and data collection.
3.2.2. Methods for Initial Protocol Development and Adaptation
Using an iterative process, informed by existing literature and the researchers’
combined knowledge and experience, an initial sonography protocol was developed to
interrogate the morphology of the flexor tendons, using static and dynamic sonographic
techniques. This initial protocol was conducted with a 32-year-old healthy white male
with no history of trauma to the right hand. Data were collected over two sessions that
were two weeks apart. The first session was slightly more than one hour, and the
second was two hours. All images and cine clips were collected by an occupational
therapist with over three years of musculoskeletal sonography training and experience.
The data from this participant were examined, and the protocol was refined
through an iterative process of discussion between the occupational therapist collecting
the data and another researcher certified in musculoskeletal sonography with over a
decade of experience. Multiple discussions were held between the two researchers to
refine the protocol. The first discussion took place after the first data collection, and any
suggestions from the discussion were implemented during the second data collection.
During the second session of data collection, both researchers engaged in conversation
to ensure that machine settings and imaging techniques were optimal for the final
protocol. Once all data from the first participant were collected and reviewed, additional
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meetings were held between the two researchers to make final adjustments to the
protocol. Across these discussions, topics included the ideal transducer placement,
anatomic landmarks, considerations for imaging long- and short-axes of the tendon, and
optimization of equipment software (e.g., depth, gain, focus number and position) to
improve the quality of the data.
3.2.3. Subjects
A total of 15 healthy volunteers were scanned using the refined protocol
developed for this feasibility study (Table 3.1). Participants were a convenience sample
of students and faculty who were recruited from research labs at the university.
Participants were included in the study if they reported being healthy and had a right
upper extremity. Participants were excluded from the study if they had a history of
trauma of the right wrist or hand that affected the health or morphology of their flexor
tendons, previous surgery of the right hand, or known history of other conditions that
might significantly affect the morphology of their tendons (e.g., flexor tendon synovitis).
Table 3.1. Demographic of Healthy Participants (N=15)
Mean (SD) /
Frequency (%)
Range
Gender, female 8 (53.33) NA
Race
Asian 10 (66.67) NA
White 3 (20.00) NA
Black or African American 1 (6.67) NA
Mixed Race 1 (6.67) NA
Ethnicity, non-Hispanic 13 (86.67) NA
Age, years 35.80 (12.53) 20-70
Handedness, right 13 (86.67) NA
Notes: SD = Standard Deviation; Handedness = Hand-dominance
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3.2.4. Equipment and Subject Positioning
Sonography was completed with a LOGIQ-e portable ultrasound machine with a
15-18 MHz linear array, hockey stick transducer (GE Healthcare, Milwaukee,
Wisconsin). Spatial compounding (i.e., crossbeam technology) was used, and gain was
adjusted for optimal resolution of the FDP and surrounding tissues based on the
echogenicity and depth of the participant’s finger, ensuring the cortical surface of the
metacarpal and phalanges were included throughout the interrogation of the FDP.
During scanning, subject variability required slight adjustments to gain controls and
depth. To enhance images, two focal points were typically used at the depths of 0.2 cm
and 0.6 cm, and when the total field of view was less than 1cm, one focal point was
used at the depth of 0.4 cm; additional adjustments to the focal point depths were also
made when necessary.
Identical positioning was used to scan all participants included in the study. Each
subject was seated at a table across from the sonographer with the forearm and hand
supinated resting on a flat surface. The wrist, hand, and fingers were relaxed in a
neutral position (i.e., slightly flexed) and placed upon a thin towel so that the
participant’s hand felt comfortable. Throughout the exam, the index finger was held in
full extension by the sonographer.
3.2.5. Image Acquisition Protocol
Imaging was conducted on the right index finger of each participant. Because of
the uneven surface anatomy of the fingers, especially at the metacarpophalangeal
(MCP), proximal interphalangeal (PIP), and distal interphalangeal (DIP) joints, a surplus
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of gel was used to minimize anisotropy and ensure optimization of the tendon in the
images and cine clips. Minimal transducer pressure was applied to ensure that the
vasculature and other small soft tissue structures were not falsely deformed.
At the beginning of each exam, an initial sweep was performed over the entire
area of interest, with the transducer held in short-axis of the FDP to gain familiarity with
each person’s unique anatomy. This initial scan was started at the mid-palm
immediately proximal to the MCP joint and the head of the second metacarpal over the
distal shaft of the bone. The transducer was moved distally to just beyond the point of
FDP insertion at the distal phalanx. Once familiar with the individual anatomy, two cine
clips and six images were obtained with each participant. Each step was then repeated
to collect a second set of imaging data for each participant.
The first data point was a cine clip surveying the length of the FDP in short-axis
(cine 1). Beginning over the second metacarpal, the transducer was placed in short-axis
of the FDP just proximal to the metacarpal head at the distal aspect of the metacarpal
shaft. The transducer was then moved distally while maintaining the FDP and
phalanges in the central field of view, and the cine clip was ended once the transducer
was beyond the FDP insertion point onto the distal phalanx. Special attention was given
to optimizing the appearance of the FDP and minimizing anisotropy throughout the clip,
particularly when scanning over articular surfaces. This step was then replicated to
examine the FDP in long-axis (cine 2). Similarly, the transducer was placed in the
longitudinal plane over the second metacarpal with the proximal edge of the metacarpal
appearing on the distal aspect of the image. The transducer was moved distally while
keeping the FDP in focus and centered in the image. The cine clip continued until the
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center transducer was distal to the FDP insertion point on the distal phalanx.
Next, long- and short-axis images of the FDP were taken at each of the three
phalangeal joints of the index finger–the MCP, PIP, and DIP–providing a series of six
images. In other words, three images of the FDP were in long-axis at the MCP (image
1), the PIP (image 3), and the DIP (image 5); and three images of the FDP were in
short-axis at the MCP (image 2), the PIP (image 4), and the DIP (image 6).
First, the transducer was placed in long-axis over the MCP with the joint space
centered in the image and with the FDP in focus (image 1). Then, after turning 90 in
short-axis of the FDP, the transducer was slid proximally until the head of the
metacarpal appeared on the image and when the FDP was observed with the least
amount of anisotropy (image 2). These two steps were then repeated at the PIP and
DIP. Again, the transducer was placed in long-axis over the PIP with the joint space
centered in the image and with the FDP in focus (image 3). Then, in short-axis of the
FDP, the transducer was slid proximally until the head of the proximal phalanx appeared
on the image and when the FDP was observed with the least amount of anisotropy
(image 4). To obtain the final two images in this series, the same steps were repeated
at the DIP. After the transducer was placed in long-axis of the FDP, the image was
taken while centered over the DIP joint space and with the FDP in focus (image 5).
Then, the transducer was placed in short-axis of the FDP and slid proximally until the
head of the middle phalanx appeared on the image and when the FDP was observed
with the least amount of anisotropy (image 6).
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3.2.6. Image Analysis
All images and cine clips from each case were reviewed using an iterative
process. Multiple discussions were held between the two researchers and were
primarily focused on the proper identification of anatomic landmarks and the
surrounding structures across all data. The process for image analysis and final
consensus between authors is described. First, data from the first five participants were
reviewed, one participant at a time, by both researchers together in the same room.
After these images were analyzed, the primary researcher continued data analysis for
the remaining participants. Once completed, the primary researcher presented the
findings to the second researcher. The images from each participant were reviewed
over several discussions until a consensus was reached on the identification of
anatomic structures across the within-participant data.
Given that at least two data points were collected at each location, the clearest
image or cine clip among the data points collected was chosen for analysis. These
selected images and clips were compiled across all participants by each sonographic
unit of analysis (e.g., cine 1, cine 2, image 1). The primary author then conducted
between-participant analysis for each unit using the selected data. A descriptive
analysis of the data was documented, noting any similarities and differences in tendon
morphology among the participants at each location. Patterns among the participants
were characterized and unique anatomic structures were identified. This analysis was
presented to the secondary author until a consensus was reached regarding the
interpretation of data. Any disagreements were resolved by referencing the participant’s
cine clip data, which helped provide a more holistic view of the flexor tendons and
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surrounding structures along the length of the finger.
Finally, potential threats to image validity were noted via discrepancies between
the tendon’s morphologic appearance among the different units of analysis, and the
quality of images at each location was considered. To do this, the primary researcher
analyzed the content, quality, and utility of each unit of analysis. Any challenges
interpreting imaging data were also noted. Together, the authors reviewed this data and
the overall process for image collection and analysis. Discussions focused on
enhancing imaging techniques when interrogating the FDP to support future studies.
Conversations regarding the sonographic presentation of the FDS were primarily
focused on developing methods to distinguish the flexor tendons and confirm that the
FDP was properly identified across the data.
3.3. Results
Findings from this feasibility and protocol development study are presented in
two sections. First, a summary characterizing the anatomic patterns and unique
presentations of the flexor tendons across the participants is provided. Second, based
on the perceived utility and quality of the images obtained across the participants, a
detailed description of a recommended protocol with best practices to maximize image
quality for systematic evaluation of the flexor tendons is provided. Throughout the
results, representative images are provided as examples, and full image galleries can
be found in Appendix B.
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3.3.1. Establishing Validity and Optimizing Image Quality
Among the 15 participants, the sonographic appearance of both the FDS and
FDP were similar across all image 1 data. An example of the sonographic appearance
of the flexor tendons in longitudinal view at the MCP is provided in Figure 3.1. The MCP
joint space created by the head of the second metacarpal and the base of the proximal
phalanx is centered on the image. The cortical surfaces of the metacarpal head and the
base of the proximal phalanx appear as hyperechoic curvatures near the bottom of the
image. Both flexor tendons are housed within a hyperechoic tendon sheath, with the
FDS superficial to the FDP. The fibrils of both the FDP and FDS appear as organized
hyperechoic striations that run longitudinally within each of the tendons. Superficial to
the cortical surfaces of the bones, the volar plate appears as an archway that spans
over the MCP joint space, protecting the MCP from injurious movements. Unlike the
fibrillar pattern of the flexor tendons, the volar plate can be easily differentiated by its
homogenous echogenic appearance throughout its structure.
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Just proximal to the MCP joint space, the flexor tendons were viewed cross-
sectionally in image 2. In this image, the cortical surface of the metacarpal head is the
deepest structure, appearing hyperechoic and convex beneath the flexor tendons. The
flexor tendons in the near field of view are typically close together with the FDS
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superficial to the FDP. Each tendon can be visualized as an ovoid structure surrounded
by a thin layer of anechoic synovial fluid within a hyperechoic sheath. This thin layer of
synovial fluid may appear more pronounced at the radial and ulnar aspects of the
tendon sheath. Within each of the tendons, the multiple fascicular bundles may be
discernable from each other, with each bundle surrounded by the endotenon.
Although the tendons were similar in appearance across all participants in image
2, important morphologic differences were noted when comparing the images. In a third
of the participants (n=5), there were distinct hypoechoic muscle bellies located on both
radial and ulnar aspects of the flexor tendons near the edges of the image. For most
participants (n=10), the hyperechoic tendons of the intrinsic muscles rather than their
muscle bellies appeared on the lateral aspects of the flexor tendons when at this distal
level in the hand. Examples of the two different presentations of tendon or muscle belly
at this level of the hand are provided in Figure 3.2.
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Moving distally, image 3 provides a long-axis view of the FDP over the PIP joint
(Figure 3.3). In this view, the hyperechoic appearances of the head of the proximal
phalanx and the base of the middle phalanx create the PIP joint space, which can be
identified in the far field at the center of the image. At this level of the finger, the
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appearance of the interphalangeal joint can be differentiated from that of the MCP joint,
as the head of the proximal phalanx and the base of the middle phalanx appear almost
circular with more apparent overlap at the joint space. This difference in appearance is
due to the PIP being a hinge joint with fewer degrees of motion (i.e., flexion and
extension) compared to the condyloid surfaces of the MCP that allow for more range of
motion and appear as gradually descending slopes.
The long-axis appearance of the FDP was similar across all participants as it
arched above the PIP joint in image 3. The hyperechoic sheath of the FDP outlines the
tendon, and the fibrils within the tendon appear as longitudinal, organized hyperechoic
striations. The FDP can be visualized throughout the entirety of the image, including
both proximal and distal aspects, and is verified by the continuity of the superficial and
deep boundaries of its hyperechoic sheath. The volar plate can once more be seen
77
arching across the PIP, connecting the cortical surfaces of the phalanges and
recognizable by the homogenous echogenicity within the structure.
Although the FDP had a similar appearance for all participants in image 3, the
presence and appearance of the FDS were inconsistent across participants when
viewed in long-axis at this location. The presentation of the FDS in image 3 data likely
varied due to differences in the location of FDS tendon bifurcation. After reviewing the
short-axis cine clips (cine 1) and comparing them across all 15 participants, it was noted
that the bifurcation of the FDS typically occurred somewhere over the shaft of the
proximal phalanx (n=13). However, in two participants, the FDS bifurcation occurred at
the base of the proximal phalanx, which was much earlier than in the other participants.
Figure 3.4 shows the short-axis appearance of early FDS bifurcation at the base
proximal phalanx near the MCP joint.
78
When the FDS was present in image 3, the tendon only appeared on the
proximal aspect of the image before falling out of view. In these cases, the location of
the FDS appeared as a curved hyperechoic line (i.e., the FDS tendon sheath) falling
deep to the FDP as it traveled laterally toward its insertion point on the middle phalanx
(Figure 3.5). In other cases, the FDS could not be easily viewed as the bifurcated slips
separated and fell deep around the FDP at a much earlier point before reaching the
PIP.
The short-axis view in image 4 provides a visualization of the flexor tendon(s)
over the head of the proximal phalanx, just proximal to the PIP joint. The cortical surface
of the proximal phalanx head appears as two hyperechoic “mounds” or “hills” in the
deep field. Just superficial to the cortical surface of the proximal phalanx rests the volar
plate, recognizable by the homogenous echogenicity throughout its structure. In the
near field, the flexor tendon(s) can be seen, often as multiple distinct bundles, or slips,
79
that are somewhat similar and symmetrical in appearance. Across all participants, the
slips of the FDP were separated by a thin layer of hypoechoic space, which became
more pronounced at the center of the tendon.
For nearly all participants (n=13), the slips of the FDS typically bifurcated as they
passed over the shaft of the proximal phalanx. For most participants, the FDS tendon
slips either fell laterally out of view soon after the point of bifurcation or were difficult to
image clearly due to anisotropy, as the transducer was positioned to prioritize
optimization of the FDP. As such, the superficial tendon was not visible in image 4 for
about half of the participants (n=8). In the other seven participants, at least part of the
FDS was visible in image 4. In these participants, the FDS had multiple presentations
with slips of the FDS appearing in-line with the FDP, directly below the FDP, or as a
combination of those positions (e.g., beside and wrapped underneath the FDP). The
varied presentations of the FDP and FDS in short-axis just proximal to the PIP are
demonstrated in Figure 3.6.
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81
Across all 15 participants, the FDP presented very similarly when viewed
longitudinally over the DIP in image 5 (Figure 3.7). At this location, the head of the
middle phalanx and the base of the distal phalanx met to create the joint space of the
DIP centered in the image. The distal phalanx may appear to slightly overlap with the
head of the middle phalanx as this joint space is the smallest of the three imaged.
Superficial to the bones, the volar plate appeared as an archway bridging the phalanges
of the DIP. The hyperechoic border of the FDP epitenon appeared on the proximal
aspect of the image, and the tendon became thinner as it crossed over the DIP and
inserted the distal phalanx. Organized collagen fibrils appeared as hyperechoic
striations within the FDP and seemed to lessen in density once distal to the DIP,
causing the tendon to appear more hypoechoic as it inserted the distal phalanx.
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Short-axis views of the FDP and other anatomical structures over the DIP in
image 6 were similar in appearance described over the PIP (i.e., image 4), just smaller
and more superficial. The head of the middle phalanx appeared deep as two
hyperechoic “mounds,” the volar plate appeared superficial to the cortical surface, and
the slips of the FDP were viewed superficially. Apart from three individuals, the FDP
typically appeared with two or more distinct slips that sat closely together, separated by
a circular hypoechoic space or line at the center where the slips met (Figure 3.8).
Depending on the size of the individual’s finger, these tendons either appeared as
circular structures or as thin flat ovoid structures.
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3.3.2. Refined protocol and best practices
Given the presentation patterns and variations of tendon morphology that were
observed across the participants (described in section 3.3.1), further adaptations to
optimize the sonography protocol are suggested. A detailed description of the steps for
image acquisition in the final protocol and recommendations for best practices are
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included in Table 3.2.
As part of the protocol, we emphasize the importance of the initial long- and
short-axis dynamic scans to gain familiarity with each person’s anatomy before
acquiring any imaging data. During these scans, careful attention should be given to the
positioning of the flexor tendons, particularly the positioning of the FDS as it changes
along the length of the finger in relation to the FDP. Other important factors that should
be considered include the accurate identification of the flexor tendons throughout the
length of the finger, the point that the FDS bifurcates, and the location of the FDS slips
as they travel dorsally in the finger and around the FDP.
In addition to this step, a key finding of this study is the invaluable nature of the
cine clips (i.e., cine 1 and cine 2) when interrogating the flexor tendons, expressly the
short-axis cine of the flexor tendons throughout the length of the finger (i.e., cine 1).
During post-exam image analysis, these cine clips were essential for the accurate
identification of each flexor tendon and helped to illuminate the location of each tendon
at various levels of the finger. This is especially useful as the data from this study
indicate that the positioning of the flexor tendons, particularly the FDS, varies among
healthy individuals. As such, observing and comparing these cine clips with each other
along with the images collected from a participant is necessary to confidently interpret
the imaging data.
Furthermore, given the necessity of comparing cine clips within participants, we
recommend that each cine clip begins at the same level of the hand, proximal to the
head of the second metacarpal (i.e., at the level of the mid-palm). When all cine clips
begin at the same level of the hand, the images are easier to interpret when identifying
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the flexor tendons, as the FDP and FDS are more distinguished from one another.
Moreover, due to the varied levels of FDS bifurcation and differences in the location of
the FDS slips observed among participants, we stress that these cine clips should begin
proximal to the MCP, as the FDS and FDP are more easily discernible at more proximal
levels in the hand.
The longitudinal cine clip (i.e., cine 2) is particularly useful for following the length
of the flexor tendons to their insertion points, as it confirms the accurate identification of
each tendon and each tendon’s relative positioning along the finger to its insertion point.
We suggest adding two longitudinal cine clips to the protocol (i.e., cine 3 and 4). These
cine clips should follow the same steps as cine 2, but rather than focusing on the FDP,
each additional cine should focus on the FDS. Two separate cine clips are required as
the FDS has two slips of insertion, on the lateral and medial aspects of the middle
phalanx. The first cine clip should begin at the mid-palm and follow the FDS as it inserts
on the lateral aspect of the middle phalanx. The second cine clip should begin the same
way and follow the FDS as it inserts on the medial aspect of the middle phalanx. These
additional cine clips will help to confirm the proper identification and location of each
tendon as their positioning varies along the length of the finger and across individuals.
Although the longitudinal view of the flexor tendons is useful for identification,
these cine clips may be difficult to replicate. Moreover, the flexor tendons may be
challenging to reliably measure when viewing its longitudinal axis. After data analysis, it
was evident that each flexor tendon is comprised of multiple fascicular bundles that
appeared in different shapes (e.g., crescentic, ovular) and sizes, which often changed
and became smaller more distally. When scanning a flexor tendon in long-axis, it may
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be useful to specify whether the transducer is centered over the medial or lateral aspect
of the tendon. For example, when interrogating the FDS at the level of the proximal
phalanx, the FDS will bifurcate, and depending on which part of the FDS is in focus, the
FDS will travel to the lateral or medial aspect of the middle phalanx.
Furthermore, the fascicular bundles within the FDS and FDP are often separated
by hypoechoic or anechoic space. This separation varies among individuals and may be
more distinct in others, particularly when distal in the finger. As such, if the transducer is
directly over the center of a tendon, it may miss the tendon entirely or only capture a
partial view of the edge of a tendon slip. Given these aspects of flexor tendon
morphology, many factors need consideration when replicating scans and developing
methods for measuring flexor tendons. For example, the height of a flexor tendon may
be highly dependent upon which fascicular bundle of the tendon is in the image. Despite
these possible limitations, the longitudinal cine clips are critical for the proper
identification and differentiation of anatomic structures and are particularly useful for
interpreting other images that were collected within the same participant.
When analyzing the short-axis cine clip, it is necessary to begin analysis at the
start of the cine clip where the FDS and FDP can be easily differentiated. After
identifying the FDP, one should follow the flexor tendon as its bundles separate and fan
outwards along the length of the finger until its point of insertion. Similarly, the FDS
should also be identified at the start of the cine clip and followed along the length of the
finger until its tendon slips fall deep out of view. When observing the FDS, the location
where the tendon begins to bifurcate should be noted along with anatomical landmarks,
and careful attention should be given to each tendon slip as they separate and move
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towards the lateral aspects of the FDP. Closely monitoring each flexor tendon from the
start of the cine, where they are easiest to differentiate, along the length of the finger
ensures that the tendons are accurately identified throughout the cine clip and not
mislabeled as other structures or tissues. Another way to potentially differentiate the
flexor tendons is by viewing the cine clip in reverse, starting at the FDP insertion point
where only one tendon is present. This can help confirm the identification of the FDP
and differentiate it from other anatomic structures throughout the short-axis cine.
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Table 3.2. Finalized Sonography Protocol and Recommendations for Image Optimization
Best Practice Suggestions
• The transducer should be moved slowly, particularly
when passing over the uneven cortical surfaces of
each joint, as the tendons are subject to anisotropy in
these areas.
• The transducer should be carefully tilted when
passing over bony structures, and these small
adjustments must be made throughout the cine-clip.
This will help ensure the transducer is continuously
perpendicular to the tendon under interrogation and
that anisotropy is minimized.
• Losing visualization of the tendons due to anisotropy
may lead to misidentification of the tendon, and the
cine clip should be reattempted. One or two additional
recordings may be added if minimizing anisotropy
throughout the entirety of the cine clip is challenging,
as these may be useful for cross-referencing data
points.
• For ease of comparison, all cine clips should begin at
the same anatomic location throughout the protocol.
• For analysis, care should be taken to focus on one
fascicular bundle at a time when reviewing the cine
clip.
Process for Image Acquisition
Place the transducer in cross-section of the FDP
directly over the second metacarpal. The
transducer should be proximal to the metacarpal
head with the cine clip beginning at the distal end
of the metacarpal shaft. Slowly move the
transducer distally, keeping the FDP center of
the image with minimal anisotropy. End the cine
clip once the transducer passes over the FDP
insertion point onto the distal phalanx.
Media
1 Cine
89
• The transducer should be moved slowly, particularly
when passing over the uneven cortical surfaces of
each joint, as the tendons are subject to anisotropy in
these areas.
• The FDP is comprised of multiple fascicular bundles
that appear separated by anechoic space. As such, if
the transducer is placed directly over the center of the
FDP throughout the length of the finger, the image is
subject to anisotropy whenever directly over these
anechoic areas. To prevent this, the transducer
should be placed directly over one of the fascicular
bundles of the FDP throughout the entirety of the cine
clip, carefully avoiding the hypoechoic spaces
between the tendon bundles.
• Shifting the transducer laterally or medially may alter
which fascicular bundle of the FDP is in focus, so
careful attention must be paid during the scan to
ensure the continuity of the tendon from the proximal
to the distal aspects of the image.
• Once the transducer is over the shaft of the
proximal phalanx, the FDS will bifurcate and fall out
of view across the image. Careful attention must be
made to keep the transducer focused on the FDP to
avoid following one of the FDS tendon slips.
Place the transducer in long-axis of the FDP over
the second metacarpal and with the proximal
edge of the second metacarpal head in view on
the distal aspect of the image. Slowly move the
transducer distally, keeping the FDP in focus with
minimal anisotropy. End the cine clip once the
center of the image moves beyond the FDP
insertion point onto the distal phalanx.
2 Cine
90
• The transducer should be moved slowly, particularly
when passing over the uneven cortical surfaces of
each joint, as the tendons are subject to anisotropy
in these areas.
• The FDS is comprised of multiple fascicular bundles
that appear separated by anechoic space. As such,
if the transducer is placed directly over the center of
the FDS, the image is subject to anisotropy
whenever directly over these anechoic areas. To
prevent this, the transducer should be placed
directly over one of the fascicular bundles of the
FDS throughout the entirety of the cine clip,
carefully avoiding the hypoechoic spaces between
the tendon bundles.
• Shifting the transducer laterally or medially may
alter which fascicular bundle of the FDS is in focus,
so careful attention must be paid during the scan to
ensure the continuity of the tendon from the
proximal to the distal aspects of the image.
• Once the transducer is over the shaft of the
proximal phalanx, the FDS will bifurcate, and the
tendon slip on the lateral aspect of the finger must
be followed. Careful attention must be made to keep
the transducer focused on the FDS to avoid
following a different tendon.
Place the transducer in long-axis of the lateral
aspect of the FDS over the second metacarpal
and with the proximal edge of the second
metacarpal head in view on the distal aspect of
the image. Slowly move the transducer distally,
keeping the FDS in focus with minimal
anisotropy. End the cine clip once the center of
the image moves beyond the FDS insertion point
onto the lateral aspect of the middle phalanx.
3 Cine
91
• The transducer should be moved slowly, particularly
when passing over the uneven cortical surfaces of
each joint, as the tendons are subject to anisotropy in
these areas.
• The FDS is comprised of multiple fascicular bundles
that appear separated by anechoic space. As such, if
the transducer is placed directly over the center of the
FDS, the image is subject to anisotropy whenever
directly over these anechoic areas. To prevent this,
the transducer should be placed directly over one of
the fascicular bundles of the FDS throughout the
entirety of the cine clip, carefully avoiding the
hypoechoic spaces between the tendon bundles.
• Shifting the transducer laterally or medially may alter
which fascicular bundle of the FDS is in focus, so
careful attention must be paid during the scan to
ensure the continuity of the tendon from the proximal
to the distal aspects of the image.
• Once the transducer is over the shaft of the proximal
phalanx, the FDS will bifurcate, and the tendon slip on
the medial aspect of the finger must be followed.
Careful attention must be made to keep the
transducer focused on the FDS to avoid following a
different tendon.
Place the transducer in long-axis of the medial
aspect of the FDS over the second metacarpal
and with the proximal edge of the second
metacarpal head in view on the distal aspect of
the image. Slowly move the transducer distally,
keeping the FDS in focus with minimal
anisotropy. End the cine clip once the center of
the image moves beyond the FDS insertion point
onto the medial aspect of the middle phalanx.
4 Cine
92
• Small adjustments often need to be made to keep
the FDP in view throughout the proximal and distal
aspects of the image.
• Both tendons should appear in this image, and the
FDS should be superficial to the FDP.
• Ensure that the cortical surface is parallel to the
bottom of the image, reducing the anisotropy
caused by the potential overlap of nearby tendon
bundles.
• For analysis, confirmation of the identity of each
fascicular bundle should be made by cross-
referencing the short-axis cine 1, following the
pathways of each fascicular bundle, and comparing
each of their locations when at the level of image 2.
• Small adjustments often need to be made to keep
the FDP in view throughout the proximal and distal
aspects of the image.
• Care must be taken to ensure that the FDS is not
mistaken for the FDP. The FDS will fall out of view
as it bifurcates around the FDP, whereas the
superficial and deep edges of the FDP should
appear throughout the image.
Place the transducer in long-axis of the FDP
between the metacarpal head and the base of
the proximal phalanx. The MCP joint space
should be centered in the image, and the FDP
should be in focus throughout the image. This
includes providing a clear view of the superior
and inferior aspects of the FDP hyperechoic
sheath at both the proximal and distal edges of
the image.
After placing the transducer in long-axis over the
MCP with the joint space centered in the image,
rotate the transducer 90 in short-axis of the
FDP. Slide the transducer proximally until the
base of the proximal phalanx appears on the
image, keeping the FDP in focus with the least
amount of anisotropy.
Place the transducer in long-axis of the FDP
between the head of the proximal phalanx and
the base of the middle phalanx. The PIP joint
space should be centered in the image, and the
FDP should be in focus throughout the image.
This includes providing a clear view of the
superior and inferior aspects of the FDP
hyperechoic sheath at both the proximal and
distal edges of the image.
1
2
3
Image
Image
Image
93
• Increasing the gain may enhance the appearance of
the FDP, as it curves over the PIP joint, making
anisotropy more likely at the proximal and distal
edges of the image.
• Scanning the FDP using a longitudinal view will
likely produce different images when scanning
between different fascicular bundles of the tendon.
• Ensure that the cortical surface is parallel to the
bottom of the image, reducing the anisotropy caused
by the potential overlap of nearby tendon bundles.
• The FDS bifurcates and either remains present in this
image or falls deep to the FDP and out of view
proximal to this level of the finger.
• Careful attention should be made to ensure that the
fascicular bundles of the FDP are optimized and that
the tendons are not misidentified.
• For analysis, confirmation of the identity of each
fascicular bundle should be made by cross-
referencing the short-axis cine 1, following the
pathways of each fascicular bundle, and comparing
each of their locations when at the level of image 4.
After placing the transducer in long-axis over the
MCP with the joint space centered in the image,
rotate the transducer 90 in short-axis of the
FDP. Slide the transducer proximally until the
base of the proximal phalanx appears on the
image, keeping the FDP in focus with the least
amount of anisotropy.
4
Image
94
• An anechoic or hypoechoic gap or linear separation
often appears between the fascicular bundles of the
FDP at this level of the hand. As such, if the
transducer is placed directly over the center of the
FDP, the image is subject to anisotropy whenever
directly over these anechoic areas.
• The transducer should be placed directly over one of
the fascicular bundles of the FDP to ensure that it is
present throughout the image, including the proximal
to the distal aspects of the image.
• It should be noted that scanning the FDP using a
longitudinal view may produce different images if
the transducer is placed over different fascicular
bundles of the tendon.
• Ensure that the cortical surface is parallel to the
bottom of the image, reducing the anisotropy
caused by the potential overlap of nearby tendon
bundles.
Place the transducer in long-axis of the FDP
between the head of the middle phalanx and the
base of the distal phalanx. The DIP joint space
should be centered in the image, and the FDP
should be in focus throughout the image. This
includes providing a clear view of the superior
and inferior aspects of the FDP hyperechoic
sheath at both the proximal and distal edges of
the image.
After placing the transducer in long-axis over the
DIP with the joint space centered in the image,
rotate the transducer 90 in short-axis of the
FDP. Slide the transducer proximally until the
base of the distal phalanx appears on the image,
keeping the FDP in focus with the least amount
of anisotropy.
5
6
Image
Image
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3.4. Discussion
Acute tendon injuries are common, and when in the volar aspect of the hand,
they are difficult to treat successfully as evidenced by the high percentage of suboptimal
outcomes; roughly three out of ten patients are expected to have residual impairments
(Kilic et al., 2015; Lilly & Messer, 2006; Rrecaj et al., 2014). The results of this study
have demonstrated that it is feasible to use MSKS to image the FDS and FDP tendons
in the distal upper extremity at the level of the palm and fingers. Once the equipment
was optimized and the approaches for image acquisition were standardized,
sonographic images of the FDP were successfully acquired and analyzed. The process
of developing these imaging techniques along with the finalized imaging protocol can
help elucidate the normative morphology of the flexor tendons and may potentially
inform future research studies of this nature. Standardizing the process of image
acquisition and establishing anatomical landmarks with this study protocol are the first
steps toward understanding typical tendon morphology and reliable measurement
parameters.
This study suggests there are many differences in tendon morphology that exist
in the healthy population. Observing the common variations of flexor tendon morphology
and positioning in the hand across this small sample of healthy volunteers demonstrates
the need for careful evaluation of all structures within the finger. Deploying this
standardized protocol in future research with larger and more heterogenous samples
can lead to a better understanding of the typical and atypical morphologies of flexor
tendons. Furthermore, this information may help elucidate differences in tendon
morphology that exist within and between both healthy and unhealthy populations,
96
which may be exceptionally useful for evaluating or assessing pathologies.
As this protocol was successfully deployed to gather data from healthy
volunteers in a lab setting, future applications of this protocol may be feasible in a
clinical setting, which can be particularly useful for assessing tendon pathologies.
Previous studies have indicated MSKS can be used to readily diagnose tendinopathies,
tenosynovitis, tendon tears, and ligament injuries (Docking et al., 2015; Hodgson et al.,
2012; Nwawka, 2016; Robinson, 2009). In addition to being useful for diagnoses, MSKS
has also been used to evaluate flexor tendon repairs during the acute stages of healing
(Puippe et al., 2011) as well as inform clinical interventions for patients with tendon
repairs who have been unresponsive to therapy (Marlborough et al., 2015; Reissner et
al., 2018). Moreover, MSKS can help clinicians detect signs of complications related to
healing after surgery, such as tendon gapping, persistent edema, intra-tendinous
calcifications, and severe adhesions (Cohen, 2011; Griffin et al., 2012; Jeyapalan et al.,
2008; Varghese & Bianchi, 2014). As such, the use of MSKS may be invaluable if
integrated as an adjunct tool for the clinical assessment of healing progression to inform
and evaluate targeted therapies.
Given this protocol can standardize the process for image acquisition, it is
potentially feasible to develop standardized measures of the flexor tendons, such as
cross-sectional area, length, and height. Developing reliable measures of tendons may
be valuable for future research and in clinical settings where patients with tendon
injuries are frequently treated. However, the results of this study also suggest that there
may be potential challenges that need to be considered when establishing standardized
measures using these image acquisition techniques, specifically when using images in
97
the long-axis of the tendon. While tendon length shows promise as a reliable measure,
the structure of the tendon may limit the reliability of other measures derived from
images acquired in the tendon’s longitudinal view.
Despite being able to clearly differentiate and repeatedly image the flexor
tendons in the long-axis, obtaining reliable measures across multiple images of the
same tendon may be challenging, particularly if the specific region of the tendon in the
image is not identified. As each tendon is composed of multiple fascicular bundles that
often vary in size and shape, each tendon may vary in its appearance depending on
which part of the tendon (i.e., which fascicular bundle) is in the image. Without
specifying the tendon region, reliably measuring images of flexor tendons when in the
longitudinal view may be challenging and will likely result in measurement error for
tendon height. For measurement consistency, the specification of which fascicular
bundle of the tendon is in the image is needed when establishing quantitative measures
or analytic techniques. Any measurements rendered from the data should specify which
aspect of the tendon was in the image to increase reliability.
The findings from this research suggest that establishing measures using
imaging data acquired in the short-axis of the tendon may improve reliability and
reproducibility, and consequently, may be more appropriate for clinical and research
settings. For example, short-axis images of the tendon can be referenced to measure its
cross-sectional area. Furthermore, measures of the tendon’s cross-sectional area will
be more consistent and informative of the tendon’s morphology in comparison to
measures of tendon height or width. Moreover, in future studies, measures of tendon
width should be provided in addition to height. The reliability of tendon height measures
98
between images in the short-axis compared to the long-axis of the tendon should also
be explored.
Given that research regarding MSKS of the flexor tendons in the hand is
relatively scant, the protocol developed in this study should be implemented and further
evaluated in a larger sample of the healthy population. Deploying this protocol in a
larger number of healthy individuals may reinforce the presentation patterns of the flexor
tendons that were identified in this study as well as elucidate other patterns or variations
in tendon morphology that typically exist. Beyond using this protocol for image
acquisition, another necessary step to advance the utility of this protocol is developing
reliable measures to analyze these standardized images. These measures may help
researchers and clinicians identify reference values for flexor tendons within
participants, which may be useful for screening or diagnostic purposes.
Although the protocol was successfully deployed and the process of image
acquisition was standardized, several limitations of this study need to be considered.
This protocol was carried out by one person with a small sample of healthy individuals.
Furthermore, grey-scale MSKS was used to obtain all data for this study, and other
techniques, such as Doppler ultrasound, were not explored. Lastly, although this
protocol appears to be generalizable to other settings, adaptations to the protocol need
to be considered when applying it to unhealthy populations, being mindful of any
structural or tissue changes (e.g., arthritic joints, edema, scar adhesions) that may only
exist in patient populations.
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3.5. Conclusions
Researchers and clinicians can successfully use MSKS as a tool to obtain and
analyze images of the flexor tendons in the distal upper extremity. Although the
techniques used to collect the data presented in this study require further validation, it is
feasible to interrogate the small structures of the hand with sonography, and numerous
applications of high-frequency sonographic imaging for research and clinical practice
are not only possible but potentially necessary for optimal patient outcomes.
100
3.6. References
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5023(81)80047-0
Boyer, M. I., Meunier, M. J., Lescheid, J., Burns, M. E., Gelberman, R. H., & Silva, M. J.
(2001). The influence of cross-sectional area on the tensile properties of flexor
tendons. J Hand Surg Am, 26(5), 828-832.
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Cohen, M. (2011). US imaging in operated tendons. Journal of Ultrasound, 15(1), 69-75.
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Docking, S. I., Ooi, C. C., & Connell, D. (2015). Tendinopathy: Is Imaging Telling Us the
Entire Story? Journal of Orthopaedic & Sports Physical Therapy, 45(11), 842-
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Furrer, M., Schweizer, A., Rufibach, K., & Meuli-Simmen, C. (2009). The Value of
Ultrasonography in Hand Surgery. Hand (N Y), 4(4), 385-390.
https://doi.org/10.1007/s11552-009-9188-5
Giggins, O. M., Persson, U. M., & Caulfield, B. (2013). Biofeedback in rehabilitation. J
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CHAPTER 4. Measuring Sonographic Biomarkers of Healing Over Time:
A Case Study of Functional Recovery After Flexor Tendon Surgery
4.1. Introduction
One of the most highly prioritized (MacDermid et al., 2002) and frequently
researched topics in hand therapy (Takata et al., 2018) is flexor tendon injuries in the
upper extremity. Notwithstanding the decades of published research on this topic, many
individuals who have had a flexor tendon laceration that resulted in a surgical tendon
repair suffer suboptimal outcomes (Bigorre et al., 2018; Griffin et al., 2012; Ibrahim et
al., 2014; Johnson et al., 2020; Kilic et al., 2015; Lilly & Messer, 2006; Rrecaj et al.,
2014). Even though a wide variety of treatment approaches have been explored,
including biological, surgical, and clinical interventions, the main limitation to functional
return is adhesion formation that impedes hand range of motion.
Current research, regardless of the specific intervention under study, is aimed at
reducing the formation of extrinsic adhesions around the healing tendon while protecting
the repaired tendon from a rupture. Encouraging tendon glide helps reduce extrinsic
adhesion development; however, any active motion that is applied too forcefully or too
early will weaken the repair and may lead to a ruptured tendon. As such, the early
months following a surgical tendon repair is a critical time of recovery. During this time,
adhesion development peaks while the tendon has the highest risk of rupturing as the
repair requires time to strengthen and heal.
The culmination of these issues leads to one question: when is it safe to actively
move? Without the direct and real-time evaluation of the repair, clinicians must rely on
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external cues to determine the healing status of the tendon and estimate the strength of
the repair. As a result, clinicians are unable to securely pinpoint the moment when a
patient is ready to actively move their injured hand. Furthermore, if there is a problem
during recovery, clinicians must wait until the issue manifests externally as well as infer
the causing factor(s) and the most appropriate intervention. Consequently, many
clinicians are forced to implement global approaches to care and wait for external cues
before responding to any complications that develop.
This study’s proposed solution to help more patients safely and efficiently return
to function is the use of musculoskeletal sonographic imaging during rehabilitation.
Musculoskeletal sonographic ultrasound (MSKS) is a well-established, non-invasive,
pain-free method for examining soft tissue structures, including very small superficial
structures of the finger (Lee et al., 2016). MSKS has been used to evaluate post-
surgical flexor tendon repairs in patients with zone I and zone II injuries (Cohen, 2012;
Jeyapalan et al., 2008; Marlborough et al., 2015; Nugent et al., 2012; Puippe et al.,
2011; Reissner et al., 2018), where tendon lacerations in the hand most commonly
occur.
Using the information obtained through a rigorous literature review (Chapter 2), a
timeline of typical tendon healing following surgery was developed, and several
sonographic biomarkers related to healing were identified. This feasibility study was
conducted as a first attempt to map the course of healing for an individual with a flexor
tendon laceration and surgical repair using MSKS. This longitudinal case study aimed to
1) determine the feasibility of obtaining and measuring images of the flexor digitorum
profundus tendon (FDP) and surrounding anatomical structures of the distal hand
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following a tendon laceration and surgical repair, 2) refine sonographic imaging
techniques (see Chapter 3) for acquiring standardized images and cine clips in this
region in patients receiving rehabilitation, and 3) identify potential sonographic
biomarkers that may indicate healing status of the tendon and surrounding tissues
across time.
4.2. Research Methods
4.2.1. Study Design
Because of the preliminary and novel nature of this investigation, a longitudinal,
single-subject design was used to establish feasibility and refine an imaging protocol
before initiating larger trials. One participant was scanned using an adapted version of a
previously developed protocol (Chapter 3) to optimize the sonographic equipment
settings, refine image acquisition techniques for grey-scale and Doppler ultrasound, and
explore reliability for measures of sonographic biomarkers potentially indicative of
healing status. The sonography protocol was deployed to interrogate the morphology of
a surgically repaired FDP tendon and surrounding musculoskeletal tissues, and the
protocol was also carried out on the participant’s uninjured contralateral hand for
comparison. General descriptive information and functional outcomes were collected at
multiple time points. The university’s institutional review board approved this research
study, and the research participant gave informed, written consent before enrolling in
the study.
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4.2.2. Outcome Measures
Three categories of data were obtained, including demographic information,
functional outcomes, and measurement of sonographic biomarkers. Demographic
information included participant age, gender, ethnicity, handedness, race, height,
weight, body mass index (BMI), and comorbidities (e.g., diabetes, hypertension,
depression). Injury-related information included the location of the tendon laceration,
date of injury, date of surgery, and the rehabilitation protocol used for hand therapy. The
participant’s level of function was measured in three ways: patient self-report,
biomechanical, and objective rater-observed. Key reliability, validity, and clinical
interpretation for the three functional outcome measures are included in Table 4.1, and
a detailed description with additional metrics for each variable follows. For each session
of data collection, the primary researcher also made brief clinical notations regarding
any relevant information the patient disclosed. This included topics such as the
participant’s report of pain, the level of pain when reported, and a description of the
external appearance of the tendon repair. The level of pain was reported on a scale of
0-10, with 0 being no pain, and 10 being extreme pain.
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Table 4.1. Summary of Reliability, Validity, and Clinical Interpretations of Functional Outcome Measures.
Minimal detectable
change or minimal clinical
important difference
values, and reference
Minimal Clinically Important
Difference: 10.83 points
Minimum Detectable Change:
10.81 points
Citation: (Franchignoni et
al., 2014)
Minimal Detectable Change:
[11.8 - 14.4] degrees
Citation: (de Kraker et al.,
2009)
Minimal Detectable Change:
1.3-2.6 seconds
Citation: (Earhart et al.,
2011)
Note: ICC = Interclass correlation coefficient
Validity values, population, gold
standard comparator, and
reference
Construct Validity: r >0.7
Population: Patients with either wrist,
hand, or shoulder problems.
Comparator: the Brigham
Questionnaire, the Shoulder Pain and
Disability Index, and other markers of
pain and function
Citation: (Beaton et al., 2016)
Concurrent Validity: 0.85 (kappa)
Population: Patients with surgically
repaired flexor tendons of the hand
Comparison: Original Strickland test
Citation: (Libberecht et al., 2006)
Concurrent Validity: (p=-0.74 to -0.75);
(p=-0.87 to -0.89)
Population: Healthy adults
Comparator: Purdue Pegboard test;
Bruininks-Oseretsky Test of Motor
Proficiency
Citation: (Wang et al., 2011)
Reliability values, population
studied, and reference
Test-retest: 0.96 (ICC)
Population: Patients with wrist,
hand, or shoulder diagnoses
Citation: (Beaton et al., 2001)
Intra-rater: 0.98-0.99 (ICC)
Inter-rater: 0.83-0.99 (ICC)
Population: Healthy and patients
Citation: (Norkin, 2016)
Test-retest: 0.85 (ICC)
Intra-rater reliability: (r = 0.68 to
0.99)
Inter-rater reliability: (r = 0.75 to
0.99)
Population: Patients with stroke
Citation: (Chen et al., 2009;
Heller et al., 1987)
Outcome
Measure
Disabilities
of the Arm,
Shoulder,
and Hand
(DASH)
Total active
motion
(TAM)
9-Hole Peg
Test (9HPT)
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Self-reported function was measured using the Disabilities of the Arm, Shoulder
and Hand (DASH). This 30-item questionnaire uses a 5-point Likert scale to assess the
ability of patients with upper extremity musculoskeletal disorders to perform activities.
The DASH has good internal consistency for measuring disability (alpha = .90)
(Gummesson et al., 2003) with final scores ranging from 0 (no disability) to 100 (most
severe disability) (Beaton et al., 2016; Beaton et al., 2001). The DASH detects small
and large changes in function over time in patients with upper extremity disorders who
have undergone surgery (Gummesson et al., 2003) and has successfully measured the
functional ability of patients with surgically repaired zone II flexor tendons (Kitis et al.,
2009; Peters et al., 2021). The DASH is also recommended for use over other
functional measures when multiple joints are affected, as it can reflect very small
changes to a patient’s altered condition (Changulani et al., 2008).
Considered one of the gold standards to measure function in this population, the
participant’s biomechanical level of function was measured using total active motion
(TAM). Active range of motion (AROM) was selected as it more accurately represents
the participant’s ability to move without assistance, which is required for independent
function. AROM was measured using a small goniometer designed for the hand, as
soon as the participant was cleared for active motion by their medical provider (i.e.,
before visit 3). TAM was calculated as the total arc of the active range of motion (Peters
et al., 2021), which is described by the American Society for Surgery of the Hand as the
sum of active metacarpophalangeal (MCP), proximal interphalangeal (PIP), and distal
interphalangeal (DIP) motion (in degrees) within each digit (Casanova, 1992). The total
arc of finger motion is typically compared to the normative digit arc of 260 degrees.
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Wrist mobility was also examined as it is a significant aspect of function that can be
impaired following tendon repair surgery. Wrist motion was compared to normative
values of 73 degrees of flexion and 71 degrees of extension (Kim et al., 2014).
Finally, the 9-Hole Peg Test (9HPT) was obtained as an objective rater-observed
measure of finger dexterity (Mathiowetz et al., 1985). This test is administered by asking
the participant to individually take nine pegs from a container using one hand and place
them one at a time into nine holes on the board as quickly as possible. The participant
must then individually remove the pegs from the holes and place them back into the
container, one at a time. Scores are based on the time taken to complete the test
activity, recorded in seconds. The 9HPT has moderate to excellent intra-rater reliability
(r = 0.68 to 0.99) and good to excellent inter-rater reliability (r = 0.75 to 0.99) (Heller et
al., 1987). It has been validated through high correlation with other tests of dexterity,
including the Purdue Pegboard test (p = -0.74 to -0.75) and the Bruininks-Oseretsky
Test of Motor Proficiency (Wang et al., 2011). Additionally, the 9HPT has a minimal
detectable change of 2.6 seconds for the dominant hand and 1.3 seconds for the non-
dominant hand (Earhart et al., 2011).
A set of candidate sonography biomarkers were identified from the existing
literature as described in Chapter 2. A review of these measures using clinical expertise
in flexor tendon healing and an examination of viable imaging techniques for the flexor
tendon (Chapter 3) resulted in the final selection of three primary sonographic
biomarkers: 1) FDP tendon cross-sectional area (CSA), 2) localized edema (Lee et al.,
2016), and 3) intra-tendinous vascularity in the area of the repair site (Cohen, 2012;
Pearson et al., 2017; Puippe et al., 2011; Reissner et al., 2018).
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Tendon CSA was selected as the primary sonographic biomarker since
successfully healed tendons are thicker at the site of surgical repair when compared to
the healthy contralateral hand. During the first 12 weeks following surgery, properly
healing tendons will have minimal tendon thinning and maintain tendon thickness (i.e.,
tendon CSA) for several weeks at the repair site following surgery (Puippe et al., 2011).
In this study, intra-tendinous edema that surrounds the tendon within the
subsynovial connective tissue will also be referred to as localized edema and is
recognized as a nonmoving hypoechoic layer surrounding the tendon and will be
referred to interchangeably as intra-tendinous (van Doesburg et al., 2012). This
definition of edema does not include general edema, which can be found outside of the
subsynovial sheath, surrounding the tendon in other areas of the hand. Edema is
expected to be highest during the earliest stage of healing (i.e., the inflammatory
phase), decreasing significantly thereafter. Over time, edematous tissue remaining in
the area gradually hardens, contributing to adhesion formation that peaks four to eight
weeks after surgery (Wu & Tang, 2013).
Finally, flexor tendons are mostly avascular; therefore, intra-tendinous blood flow
is typically not present in healthy flexor tendons. As such, neovascularization or intra-
tendinous vascularization that gradually develops during the first three months following
surgery typically indicates cellular proliferation and tendon healing. After three months
following surgery, intra-tendinous vascularization is expected to stabilize and eventually
regress within six months (Bűhler et al., 2015; Gitto et al., 2018). Any persistent
vascularity that continues beyond six months is usually indicative of pathology.
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4.2.3. Equipment and Subject Positioning
Sonography was completed with a LOGIQ-e portable ultrasound machine using a
15-18 MHz linear array, hockey stick transducer (GE Healthcare, Milwaukee,
Wisconsin). Spatial compounding (i.e., cross-beam technology) was used, and gain was
adjusted for optimal resolution of the FDP and surrounding tissues based on the
echogenicity and depth of the participant’s finger, ensuring the cortical surfaces of the
metacarpal and phalanges were included throughout the interrogation of the FDP. To
enhance images, two focal points were typically used at depths of 0.2 cm and 0.6 cm.
When the total field of view was less than 1cm, one focal point was used at the depth of
0.4 cm. Additional adjustments to the focal point depths were also made when
necessary.
During the initial two research visits, the participant’s hand was imaged while
resting in a dorsal-blocking orthosis that was fabricated by his hand therapist. The
orthosis was adjusted between visits one and two per the treating hand therapist’s
discretion, gradually allowing for more finger extension. Once the participant was
cleared for full AROM (i.e., research visits 3-5), the patient no longer wore a splint
during image acquisition, and the same positioning was used for all remaining visits.
Across all visits, the participant was seated at a table across from the sonographer with
his supinated forearm resting on a flat surface, and hand resting in either the dorsal
blocking splint or on the table surface in compliance with any existing movement
restrictions. Throughout the exam, the injured finger was held in a comfortable end-
range extension by the sonographer, with the finger held either against the splint or on
the flat table surface.
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4.2.4. Sonographic Image Acquisition Protocol
Sonographic images were
acquired of the injured finger with the
surgical tendon repair at each
research visit and of the unaffected,
contralateral finger at baseline
(Figure 4.1). Throughout the protocol,
minimal transducer pressure was
applied to ensure that vasculature
and small structures of the hand were
not falsely deformed. Each step was repeated to obtain a duplicate data point (e.g., cine
clip, image) to increase the precision of the anatomic structures’ portrayal.
The protocol developed and described in Chapter 3 served as the foundation for
the collection of gray-scale images. First, a cine clip was obtained to examine the entire
length of the tendon in the short-axis, beginning proximal to the MCP joint, sliding
distally, and ending once distal to the insertion point of the FDP onto the distal phalanx
of the finger (cine 1). To obtain cine 2, this step was repeated in long-axis of the FDP,
beginning proximal to the MCP joint, and ending once distal the tendon’s insertion point
onto the distal phalanx. Following the cine clips, a total of eight images of the FDP were
obtained representing short-axis and long-axis views at each of four locations: over the
MCP in short-axis (image 1) and long-axis (image 2), over the PIP in short-axis (image
3) and long-axis (image 4), over the DIP in short-axis (image 5) and long-axis (image 6),
and over the suture site in short-axis (image 7) and long-axis (image 8).
Figure 4.1. Subject positioning for
sonographic imaging protocol using a
linear hockey stick transducer with a
copious amount of sterile gel.
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Power Doppler ultrasound was used to examine vascularity in the FDP over the
site of surgical repair. The transducer was placed directly over the FDP in long-axis so
that the surgical site was centered on the screen, and a power Doppler region of
interest was placed over the length of the tendon. A previously established preset (from
Chapter 3) was used to detect movement at a pulse repetition frequency of 0.8 kHz with
a wall filter of 123 Hz. Power Doppler gain was increased until noise artifacts were
present throughout the image; then, the gain was slowly decreased until noise artifacts
were minimized, or vasculature activity was detected (approximately 10.0 MHz).
Vasculature was identified as a consistent or rhythmic pulsatile Doppler signal that was
present within the same location. When vascularity was observed using Doppler, a 5-
second cine-clip was obtained to capture the location and intensity of blood flow. If no
vascularity was present in the region of interest, a static image was taken to document
that no evidence of blood flow was observed. This process was conducted with the
transducer centered over the FDP tendon at the suture site (Doppler 1) and then
repeated at the lateral (ulnar) edge (Doppler 2) and medial (radial) edge of the FDP
(Doppler 3) in the same location.
4.2.5. Sonographic Image Analysis Protocol
All images, cine clips, and Doppler ultrasound data were reviewed. Given that at
least two data points were collected at each location, the clearest image or cine clip was
chosen for analysis. To promote the reliability of measures, all image acquisition,
processing, and measurements were completed by one individual. Across the selected
data, the sonographic biomarkers of 1) tendon CSA, 2) localized edema, and 3)
114
hypervascularization were each measured three times to increase reliability. A detailed
description of each measure is provided below.
CSA of the FDP and localized edema were measured using the short-axis
images that were obtained at each level of the hand (i.e., image 1, image 3, image 5,
and image 7) across the study period were analyzed. First, the tendon’s CSA was
measured in mm
2
using a continuous trace around the outer hyperechoic border of the
tendon sheath. Next, the continuous trace method was used to measure three separate
CSAs: (a) just outside of the hyperechoic borders of the hyperechoic synovial sheath
including all anatomic structures present in the image, (b) flexor tendons in the region
(i.e., FDP and or flexor digitorum superficialis [FDS]), and (c) the volar plate; see Figure
4.2. Localized edema was derived by calculating the difference between the total CSA
of subsynovial space and the total CSAs of the other anatomic structures within that
space as seen in equation (1).
localized edema = a – (b+c) (1)
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As a point of comparison for the CSA and localized edema measures, the
location of the suture site was estimated on the healthy, contralateral finger. To
accomplish this, the short-axis cine clip (i.e., cine 1) of the participant’s uninjured finger
was reviewed, and a snapshot was obtained at the estimated equivalent location. While
reviewing the cine, anatomic landmarks such as bony prominences were used as a
general guide and the distance distal to the PIP was approximated to best match the
location of the surgery site on the healthy tendon.
Hypervascularization was analyzed by reviewing the Doppler ultrasound data
Figure 4.2. Example of sonography images measured using a direct trace method to
calculate localized edema CSA (mm
2
). The CSA of the tendon sheath (A) was measured
first, and then the total sum of the FDP CSA (B1), FDS CSA (B2), and volar plate CSA
(C) was then subtracted to calculate localized edema.
A B1
B2 C
116
across the study period. Based on previous studies using power Doppler to measure
vascularity in the distal upper extremity, a four-level rating system was used to evaluate
the presence of vascularity around the suture site (Borire et al., 2020; Dejaco et al.,
2013; El Miedany et al., 2015; Gonzalez-Suarez et al., 2019). Power Doppler data were
rated on a scale of 0-3, where 0 indicated no signals, 1 represented a single vessel, 2
represented two or three signals or two confluent vessels, and 3 indicated more than
three signals or more than two confluent vessels in the flexor tendon. Figure 4.3
provides a sample rating of hypervascularity.
Figure 4.3. Image of FDP over the middle phalanx viewed with Doppler ultrasound to
identify blood flow within a region of interest (yellow rectangle). Vascular activity is present
in the image and identified as three bright signals, indicating an intra-tendinous vascularity
score of 2.
117
4.2.6. Data Analysis
Demographic and injury data were aggregated to describe the participant
examined in this case study. Functional measures of DASH, TAM, and 9HPT were
calculated and compared across time; these values were compared against normative
measures. Averages were calculated among the three repeated measures obtained
from each image for FDP CSA and localized edema. These measures were
descriptively compared across time points, and CSA values were plotted by the number
of days following surgery. Vascularity categories were examined for change (i.e.,
increasing or decreasing) across time. Intra-rater reliabilities for the sonographic
biomarkers with continuous measures (i.e., tendon CSA, localized edema) were
analyzed using IBM SPSS Statistics for Windows, Version 28.0.0.0 software. Intraclass
correlation coefficients were calculated by visit using the three repeated measures for
each level of the finger and the overall finger as a whole. A two-way mixed-effects
model was used to evaluate the absolute agreement of repeated single-rater measures
(Koo & Li, 2016).
4.3. Results
4.3.1. Participant Demographics
The participant was a 41-year-old, white, non-Hispanic or Latino male with a
zone II FDP tendon laceration of the left ring finger in his non-dominant hand. Other
than being overweight with a BMI of 28.2, he had no other medical concerns or
preexisting conditions. His FDP was surgically repaired four days after the injury, with
the location of the suture site over the middle phalanx. Although he was working full-
118
time as an electrician, he was on a temporary leave of absence during the first several
weeks of the study due to his injury. The participant visited the research lab for a total of
five visits starting 26 days after surgery and ending on the 83
rd
day after surgery, that is,
data were collected within the window of approximately 4 weeks to 12 weeks post-
surgery. Sonographic data were collected during each of the five visits, and patient-
reported function was obtained at baseline and approximately 3-week follow-up
intervals (i.e., research visits 3 and 4) along with the other functional measures (Table
4.2).
Table 4.2. Schedule of Data Collection and Visits with Functional Measures.
Visit Number 1 2 3 4 5
Days (weeks) 26 (3.7) 33 (4.7) 47 (6.7) 72 (10.3) 83 (11.9)
Functional Outcome
DASH X X X
TAM X X
9HPT X X
Notes: Days = Number of days following surgery; DASH = Disabilities of the Arm,
Shoulder and Hand questionnaire; TAM = Total active motion; 9HPT = 9-Hole Peg
Test.
4.3.2. Clinical Presentation of Participant
The participant arrived at the first data collection session wearing a dorsal-
blocking splint. The external sutures had already been removed, and the hand was
lightly bandaged over the site of surgery. The bandages were clean, and the wound
appeared to be fully closed and healing well, with no drainage or signs of infection. The
hand appeared to have general, moderate swelling.
The participant’s hand appeared to be healing well by the second session, and
the participant continued wearing the dorsal blocking splint as instructed by his
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therapist. However, the participant reported that he had started driving, using his injured
hand to lightly assist the steering wheel. The participant also admitted to reflexively
grabbing a drink that fell over with his injured hand. Though he had been wearing the
dorsal blocking splint, he stated that he still managed to grasp the drink using active
finger flexion. Despite being noncompliant with early active motion, the participant
stated that there were no apparent repercussions or complaints of pain. There were
minimal changes to edema, with moderate swelling of the fingers.
The participant arrived at the third session wearing a flexion-blocking splint on his
injured ring finger to promote PIP and DIP extension. There was mild hypertrophic
scarring of the surgical incision on the volar aspect of his palm and ring finger. Swelling
appeared to have localized nearer to the injury and was present at the PIP and DIP
joints.
By the fourth visit, the participant reported he had returned to work as an
electrician and was using his hand more often. He reported an increase in pain that
began with stiffness in the morning. This pain progressed throughout the day, averaging
a score of 2 when the hand was at rest, and 4 during finger motion (out of 10). The
participant’s hand pain appeared to have worsened over time, as he complained of a
level 4 soreness by the last visit. The pain was more localized to his injury near the
middle phalanx of the ring finger, radiating from the dorsal aspect of the PIP to the mid
palm and the thumb thenar eminence.
4.3.3. Functional Outcome Measures
The participant reported a gradual increase in his ability to perform daily activities
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that required the use of his injured upper extremity across the study period. At the initial
visit, the participant reported the highest level of upper extremity dysfunction with a
DASH score of 74.2, which decreased to 65.0 and 46.67 roughly 7 and 10 weeks after
surgery, respectively. TAM measures obtained at research visits 3 and 4 were
compared to the normative finger and wrist arc of AROM (i.e., 260 degrees and 144
degrees respectively). Between the two visits, which were a little more than three weeks
apart, the AROM improved in the wrist and each of the four fingers (Table 4.3). At both
time points, the participant performed the 9HPT within the 95
th
percentile relative to
normative values for males his age, and the difference within and between the hands
was not greater than the minimally detectible difference at either time (Oxford Grice et
al., 2003).
Table 4.3. Total Active Range of Motion of Injured Upper-Extremity and 9-Hole Peg
Test Scores Obtained at Visits 3 and 4.
Visit Number 3 4
Days (weeks) 47 (6.7) 72 (10.3)
TAM at Location (degrees)
Wrist 104 110
IF 164 228
MF 165 237
RF 141 183
SF 143 239
9HPT (seconds)
Dominant Hand 18.43 19.22
Non-Dominant Hand 20.70 21.45
Notes: TAM = Total active range of motion (extension to flexion arc); IF = Index finger;
MF = Middle finger; RF = Ring finger; SF = Small finger; 9HPT = 9-Hole Peg Test.
4.3.4. Sonographic Biomarkers
Generally, the CSA of the tendon gradually increased over time across all
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measurement locations Figure 4.4. With exception of the first visit, measures of the FDP
CSA over the three finger joints were similar at each time point, being nearly identical at
the last visit. The FDP was significantly larger at the site of surgery than at the other
locations where the FDP was measured for the entirety of the study period. Compared
to the participant’s contralateral healthy ring finger, the injured FDP was consistently
larger at all locations (Table 4.4). The FDP CSA at the surgery site was the largest of all
the locations measured, despite being the smallest CSA on the contralateral, healthy
hand.
Figure 4.4. Scatterplot of the FDP CSA (mm
2
) measured at different locations in the
injured finger across the study period marked by the number of days following the
surgical repair of the tendon. Notes: FDP = Flexor digitorum profundus; CSA =
Cross-sectional area; MCP = Metacarpophalangeal joint; PIP = Proximal
interphalangeal joint; DIP = Distal interphalangeal joint; Surgery site = Location of
Surgical Repair.
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Table 4.4. Comparison Of FDP CSA Measures at Specified Locations in the Healthy
and Injured Hands Over Time.
Injured FDP CSA
Healthy
FDP CSA
Visit Number 1 2 3 4 5
Days (weeks) 26 (3.7) 33 (4.7) 47 (6.7) 72 (10.3) 83 (11.9)
Location
MCP 17.40 9.24 12.09 15.69 16.69 N/A*
PIP 11.27 9.90 15.45 11.99 16.78 12.73
DIP 12.77 10.99 12.67 18.40 17.35 9.27
Surgery 19.46 22.50 26.80 26.06 29.02 6.63
Notes: FDP = Flexor digitorum profundus; CSA = Cross-sectional area (mm
2
); PIP =
Proximal interphalangeal joint; DIP = Distal interphalangeal joint; Surgery = Location
of tendon repair; *Missing data.
Similar to the patterns that were observed for FDP CSA, localized edema was
also largest at the site of surgery compared to the other locations where edema was
measured (i.e., PIP, DIP) at each time point (Figure 4.5). There was also a general
increase in edematous tissue area over time at the PIP and the surgery site. However,
localized edema at the DIP joint was relatively unchanged over the study period. Table
4.5 reports edema measures between the subsynovial tissue of the healthy and injured
fingers. The largest contralateral differences were noted over the middle phalanx (i.e.,
site of surgery), with the amount of localized edema in the injured finger being nearly
four times larger than the healthy side. There was minimal difference in edema between
the healthy and injured hands at the level of the DIP, and measures over the PIP were
nearly the same or only moderately increased in the injured finger.
123
Table 4.5. Comparison Of Localized Edema CSA Measures at Specified Locations in
the Healthy and Injured Hands Over Time.
Localized Edema CSA in Injured Hand
Edema CSA
in Healthy
Hand
Visit Number 1 2 3 4 5
Days (weeks) 26 (3.7) 33 (4.7) 47 (6.7) 72 (10.3) 83 (11.9)
Location*
PIP 7.34 12.98 9.13 14.91 25.28 9.19
DIP 9.00 5.08 8.30 11.43 7.78 7.03
Surgery 24.38 21.15 13.64 25.23 41.87 11.04
Notes: CSA = Cross-sectional area (mm
2
); PIP = Proximal interphalangeal joint; DIP =
Distal interphalangeal joint; Surgery = Location of tendon repair; *Localized edema
was not measured at the metacarpophalangeal joint.
Figure 4.5. Scatterplot of the localized edema CSA (mm
2
) measured at different
locations in the injured finger across the study period marked by the number of days
following the surgical repair of the tendon. Notes: CSA = Cross-sectional area; PIP =
Proximal interphalangeal joint; DIP = Distal interphalangeal joint; Surgery site =
Location of surgical repair.
124
Intra-tendinous vascularity fluctuated over time. At the initial visit, four signals
were present at the proximal tendon end (i.e., proximal to the site of surgery) near the
PIP, indicating a vascularity score of 3 (Figure 4.6.a). By the second visit, a new blood
vessel and an additional signal appeared proximal to the surgery site, decreasing the
vascularity score to 2. The new blood vessel appeared dorsal to the FDP over the
middle phalanx, and a signal was identified nearby, distal to the vessel (Figure 4.6.b).
These signals persisted in the same area for the rest of the study period, and the
vascularity score remained unchanged at 2 through the fourth visit. At the final visit (i.e.,
83 days post-surgery), an additional confluent blood vessel that traversed from the
superficial to the dorsal aspect of the tendon was identified, appearing distal to the PIP,
above the base of the middle phalanx (Figure 4.6.c); thereby increasing the vascularity
score to 3.
125
126
4.3.5. Intra-rater Reliability Scores for Continuous Measures
Table 4.6 provides the intraclass correlation coefficients for the intra-rater
reliability calculations for FDP CSA and edema CSA. The overall intra-rater reliability for
measurement of the FDP CSA and localized edema were both excellent (ICC=0.97,
p<0.001). Most of the FDP and edema measures at each site were within the excellent
range [0.90 – 0.97]. Reliability for measurement of the FDP CSA over the surgery site
(0.88) and edema over the DIP (0.71) was slightly lower but still considered good.
Table 4.6. Overall and Location-Specific Intraclass Correlation Coefficients for FDP
and Localized Edema CSA Measures in the Injured Hand
Sonographic Biomarker ICC 95% CI Significance
FDP CSA (mm
2
)
Overall (N=20) 0.972 0.942-0.988 <0.001
MCP (N=5) 0.967 0.858-0.996 <0.001
PIP (N=5) 0.945 0.776-0.994 <0.001
DIP (N=5) 0.907 0.646-0.989 <0.001
Suture Site (N=5) 0.881 0.583-0.985 <0.001
Localized Edema CSA (mm
2
)
Overall (N=15) 0.965 0.920-0.987 <0.001
PIP 0.968 0.864-0.996 <0.001
DIP 0.712 0.157-.962 0.009
Suture Site 0.935 0.747-0.992 <0.001
Notes: FDP = Flexor digitorum profundus tendon; CSA = Cross-sectional area; MCP
= Metacarpophalangeal joint; PIP = Proximal interphalangeal joint; DIP = Distal
interphalangeal joint; Suture Site = Location of surgical repair; ICC = Intraclass
correlation coefficient; CI = Confidence interval.
4.4. Discussion
This study demonstrated that it is feasible to carry out this study protocol for
people with flexor tendon repairs in the distal upper extremity, such that MSKS can be
used to assess the healing status of flexor tendon repairs in the hand and observe
127
changes in the affected tissues and anatomic structures over time. Several sonographic
biomarkers of interest were obtained and analyzed using MSKS, with measures having
good to excellent reliability. The protocol deployed in this study can be applied in clinical
and research settings and may be useful to evaluate the progression of tendon healing
after surgical repair.
4.4.1. Interpretation of Case Findings
Combining the patient-reported DASH and objective measures of function aimed
to convey a comprehensive picture of a patient’s level of function following a flexor
tendon repair (Magnani et al., 2012). Each of the three functional measures elucidated
various aspects of the participant’s functional performance. The change in DASH scores
from baseline was not clinically significant until visit four, which was a little over ten
weeks after surgery. Although the DASH questionnaire does not correlate scores with
specific levels of disability, a score that ranges from 0 to 29 (out of 100) typically occurs
when patients consider their upper-limb disorder no longer a problem (Williams, 2014).
Applying this interpretation of the DASH, the participant likely experienced functional
deficits throughout the ten weeks following surgery and was not fully recovered by that
time point.
Like the DASH, the biomechanical functional measure using TAM also increased
between time points 3 and 4. Although there were improvements across each area
measured, the participant continued to have a limited AROM in all four fingers and wrist
at day 72, with the highest movement restriction apparent in the injured finger. Lastly,
there were no clinically meaningful differences in the 9HPT scores between the injured
128
and non-injured hand. This may be because the participant’s injury was the FDP in the
ring finger, which did not have a noticeable effect on his ability to grasp pegs using his
thumb and index fingers. Future studies conducted with a larger sample of individuals
are needed to understand if and how these functional measures correlate with
sonographic biomarkers of healing and changes in the healing tissues over time.
For this case study, the CSA of the FDP was the largest at the surgery site
compared to the other locations in the hand where the tendon was measured. Increased
tendon CSA at the repair site is consistent with previous studies in this area, and for
successfully repaired tendons, the repaired tendon is expected to remain enlarged in
comparison to the healthy contralateral tendon (Cohen, 2012; Creteur et al., 2019;
Puippe et al., 2011; Reissner et al., 2018). Despite the scarcity of research on the
reliability of measures for tendons in the hand, this study’s findings are consistent with
previous publications in this area that have indicated excellent reliability for MSKS
biomarkers like CSA (Mc Auliffe et al., 2017). Moreover, a recent study using MSKS to
evaluate surgically repaired Achilles tendons established excellent reliability for
measuring the tendon’s CSA at the site of rupture [ICC=0.985, standard error
measurement (SEM)=0.02cm
2
, minimal detectable change at group level=0.01cm
2
]
(Zellers et al., 2019). However, more research focused on using MSKS to assess flexor
tendons in the upper extremity and more specifically, after a laceration and surgical
repair, is needed to investigate the generalizability of this study’s reliability measures.
Another important finding from this case study is the technique used to measure
localized edema with good to excellent intra-rater reliability. Despite being a biomarker
of interest in previous research, a standardized methodology to calculate tendon edema
129
has yet to be established. Generally, after the inflammatory phase of healing (i.e., after
1 week), edematous tissue remaining in the area begins to harden and contributes to
extrinsic adhesion development, limiting finger motion. Consequently, efforts should be
made to minimize edema, particularly between four to eight weeks after surgery when
adhesions peak (Chapter 2).
For the participant in this study, localized edema around the tendon repair site
was the largest and fluctuated the most compared to the other areas measured.
Although this participant initially demonstrated a decreasing trend in edema around the
surgical site, this trend reversed between visits three and five. During this time, the
edema around the repair appeared to increase from six weeks to twelve weeks after
surgery, measuring the largest at the last visit (i.e., 41.87 mm
2
). Given the time that
edema CSA increased, the participant’s return to work as an electrician which resulted
in heavy use of his injured hand may have caused more swelling. These findings may
also suggest a relationship between edema and pain, as edema CSA appeared to
increase in conjunction with the levels of pain; the patient reported his highest level of
pain (i.e., 4 out of 10) at the last session when edema CSA was largest, and the second
highest level of pain was reported the session prior when edema CSA was the second
largest. According to the literature, persistent edema that reaches more than 50% of the
operated tendon beyond six months after surgery often indicates poor healing and
possible tendon rupture (Cohen, 2012). Consequently, the study participant may be at
risk for poor healing if his edema continues to increase or remains relatively unchanged
around the tendon repair after six months.
As with sonographic measures of localized edema, previous studies have
130
identified intra-tendinous vascularity as an important biomarker of tendon healing
(Puippe et al., 2011). In this study, intra-tendinous vascularity fluctuated but generally
appeared to gradually increase over the study period. When viewed with Doppler
ultrasound, the initial, weak signals matured over time to form blood vessels with more
apparent blood flow. These changes in vascularity were apparent and could be
described qualitatively, yet the categorical rating used in this study was unable to reflect
those changes. Persisting and increased power Doppler signals during early recovery
may indicate that the participant will likely have significantly better TAM and tendon
excursion three months after surgery (Puippe et al., 2011). Additional studies with
longer follow-ups are needed to explore how changes in vascularity correlate with other
healing biomarkers and functional outcomes.
Although feasibility has been established in this study, the reliability of intra-
tendinous vascularity measures has yet to be determined in this specific population.
Power Doppler has been used in similar populations to measure peri- and intra-
tendinous vessels more proximally in the wrist, such as for patients with tenosynovitis,
and has demonstrated excellent inter-rater reliability (κ = 0.806-0.942) (Klauser et al.,
2010). Similarly of note, excellent inter-rater reliability has been established to measure
hypervascularization in other areas of the body, such as the Achilles tendon (i.e., ICC =
0.85) (Sengkerij et al., 2009). Future studies regarding vascularity measures may also
want to consider using power Doppler or imaging software to estimate blood flow for a
continuous and perhaps more accurate measure of vascular activity.
131
4.4.2. Additional Opportunities for MSKS in Tendon Rehabilitation
In addition to quantitatively measuring the morphology of repaired tendons (i.e.,
CSA), it may be prudent to qualitatively assess a tendon’s appearance. A previous
study using MSKS to observe surgically repaired FDP tendons over time indicated that
repaired tendons with an early appearance of spindle-shaped fibers tended to heal
faster than tendon ends with other shapes (Puippe et al., 2011). This may be because
tenoblasts or immature tendon cells are spindle-shaped and elongate as they transform
into tenocytes (Gross & Hoffmann, 2013). As such, these spindle-like fibers may be
indicative of increased tenoblast and tenocyte activity or maturation, which may be
linked to faster healing and return to function.
Dynamic imaging may also be useful for observing the tendon in the rehabilitation
and recovery process. As an important factor for functional performance, tendon
excursion may be a salient biomarker to determine healing status related to functional
activities. Increased tendon excursion allows for an increased range of motion, an
essential component for activities that require gripping or fine motor dexterity (Puippe et
al., 2011). Furthermore, previous studies have examined tendon excursion in the hand
using dynamic ultrasound (Corduff et al., 1994; Kelly et al., 2019; Korstanje et al., 2010;
Puippe et al., 2011; Reissner et al., 2018; Soeters et al., 2004). One study reported
excellent reliability at 10 days and 3 months following surgery [ICC = 0.88 and 0.94
respectively], with a minimum detectable difference of 3.3mm when measuring tendon
excursion in patients with tendon repairs (Soeters et al., 2004). In a more recent study
of healthy individuals, tendon excursion has been reported to have excellent within-
session reliability (i.e., ICC = 0.87) and acceptable between-session reliability (i.e., ICC
132
= 0.76), with a minimal detectable change that ranged from 0.58 mm to 0.179 mm (Kelly
et al., 2019). Further research is needed to elucidate sonographic measures of tendon
excursion related to functional outcomes.
Another significant sonographic biomarker for this population is tendon gapping,
which occurs when the tendon ends separate or thin at the repair site. Historically,
several research studies focused on surgically repaired tendons have successfully
evaluated tendon gapping using MSKS (Corduff et al., 1994; Reissner et al., 2018;
Zellers et al., 2019). Currently, high-frequency ultrasound is typically used diagnostically
to assess tendon injuries preoperatively, with examinations yielding excellent diagnostic
accuracy for zone II flexor tendon injuries. Moreover, diagnostic details can also specify
the type of tendon rupture (i.e., complete or partial), as well as provide the location of
the severed tendon ends (Zhang et al., 2012).
Although reliability for these measures has not been formally established in
patients with surgically repaired flexor tendons, previous studies have demonstrated
that sonography can detect tendon gapping via dynamic imaging (Corduff et al., 1994;
Reissner et al., 2018), where the tendon can be viewed while the extremity is in motion.
When present, tendon gapping appears as either 1) hypoechoic space between the
proximal and distal tendon ends that increases with dynamic motion or 2) apparent lag
between the two ends during motion (Zellers et al., 2019). This is a significant biomarker
as ruptured tendon repairs rarely occur without the prior presence of tendon gapping.
More importantly, a tendon gap greater than 3 mm is associated with poor outcomes
(Gelberman et al., 1999), and a gap that is 5 mm or greater leads to a failed tendon
repair in roughly 80% of cases (Renfree et al., 2021). As such, more studies measuring
133
tendon gapping with MSKS are clinically relevant and needed.
4.4.3. Study Limitations
There were several limitations in this case study. Firstly, to comply with movement
restrictions, the participant was scanned while his hand was placed in a dorsal blocking
splint for the initial two visits. Consequently, while wearing the dorsal blocking splint, the
participant’s fingers and tendons were not in full extension, which may have falsely
deformed the flexor tendons. Different amounts of deformation of the tendon and
surrounding tissues at each time point could account for some of the differences noted
between time points and when comparing measures to the contralateral side. Given that
flexor tendons will typically not be fully extended during the first 4 to 6 weeks of
rehabilitation, there is a need to better understand how this sub-maximal lengthening or
decreased tension affects the morphology and measurement of the tendon. Conducting
additional normative studies in healthy individuals with their fingers held at various
degrees of flexion may be useful for understanding the relative changes in tendon
morphology one should expect to see when the tendon is flexed.
Another limitation of potential consequence was not using anatomic landmarks to
designate the exact location of the surgery. This area of the tendon was a few
millimeters in length over the middle phalanx, and although the same area of the hand
was repeatedly scanned, there may be variability in the locations imaged, specifically
among the short-axis images of the surgical site. Next, though the intra-rater reliabilities
of the continuous sonographic biomarkers were good to excellent, they are not yet
generalizable due to data being obtained in only one individual and measures being
134
conducted by one rater. Lastly, data were collected beginning at nearly 4 weeks post-
surgery and 2-3 week intervals, limiting any ability to determine early post-surgical
changes and requiring extrapolation between follow-up times. Although attempts were
made to enroll the participant as early as possible, the participant was unavailable for
recruitment immediately after surgery.
135
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CHAPTER 5. Discussion and Synthesis
5.1. Introduction
Our hands provide a means to engage in occupations and experience the world
around us. The significance of our hands can be evidenced by our palmar grasp reflex
present in newborns, an involuntary response where a stimulus to the palm elicits finger
closure and clinging (Anekar & Bordoni, 2022). As babies grow, they develop fine motor
skills, using their hands to interact with their environment through grasping, crawling,
and pointing. During the sensorimotor stage, hand usage is thought to influence the
structure and function of brain development. For example, different developmental
trajectories of hand preference may be predictive of developmental differences in
language, object manipulation, and tool usage, all of which are important cognitive skills
(Michel et al., 2016).
Given the significant implications associated with hand use and the magnitude of
consequences we experience when we lose hand function, this dissertation focused on
one of the most critical areas in upper-extremity research and therapy: surgical flexor
tendon repair. As many individuals who experience a traumatic tendon injury and
undergo surgical repair suffer from suboptimal outcomes, the purpose of this work was
to support this population’s efficient return to functional recovery. Using musculoskeletal
sonography as a part of rehabilitation can help clinicians directly assess the healing
status and quality of the tendon repair as well as evaluate surrounding tissues. This
information can support the early identification of potential complications as well as help
elucidate the best course of treatment for patients. As such, the research studies
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conducted for this project had three aims:
Aim 1: Conduct a systematic literature review to describe the morphologic and
physiologic changes of healing tissue over time after a surgical tendon repair,
including evidence of MSKS biomarkers associated with healing progression or
development of complications.
Aim 2: Establish a sonographic image acquisition and analysis protocol to evaluate
healing and recovery following flexor tendon repair.
Aim 3: Identify sonographic biomarkers that predict functional recovery and most
easily distinguish patterns of healing following tendon repair.
5.2. Summary of Key Findings
The information gleaned from the extensive literature review (Chapter 2)
elucidated the physiologic and morphologic processes involved in healing and the
timing for which these occur after tendon laceration and surgical repair. Results of the
literature review also revealed factors that may affect the healing processes of the
tendon and surrounding tissues as well as identified potential biomarkers of recovery
that could be identified and measured using MSKS. These findings were the impetus to
develop a standardized protocol to examine flexor tendons in the hand using MSKS
(Chapter 3). Furthermore, deploying this protocol in a healthy population established the
feasibility of examining the small structures of the distal upper extremity with MSKS and
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more importantly, illuminated the typical tendon morphology and common anatomic
anomalies in the healthy population. After the sonography protocol was established to
visualize healthy flexor tendons, it was adapted to standardize the assessment of
surgically repaired flexor tendons. Together, the findings from the first two studies
served as the foundation to conduct a case study (Chapter 4). In this case study, a
participant with a flexor tendon injury and repair was evaluated using MSKS, starting
roughly four weeks after surgery and continuing every three weeks until about 12 weeks
after surgery. This last study helped determine the feasibility of using MSKS to evaluate
the healing status of a repaired tendon and the surrounding tissues as well as establish
methods to reliably measure biomarkers associated with healing over time. Key findings
and implications from each study chapter are described in the sections below.
5.2.1. Conclusions from Chapter 2: A Literature Review on the Timeline of Tendon
Healing
• Numerous Individualized Factors Influence the Process of Tendon Healing.
There is much variability in the flexor tendons of healthy individuals, including a
wide range of tendon sizes within and across individuals. In addition to size
heterogeneity, anatomic anomalies of the small structures in the distal hand are
diverse and relatively common in the healthy population; this includes common
anomalies in flexor tendon morphology. To add further complexity, the
collagenous fibers that compose the flexor tendons have non-linear responses to
mechanical loading, and the mechanical properties of the fibers can differ based
on their location within a tendon (i.e., volar versus dorsal). Hence, the dorsal
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aspect of a tendon is typically larger in cross-sectional area (CSA) and therefore
stronger than the palmar-sided tissue.
o Implications: The uniqueness of tendons across individuals amplifies the
complexity of the tendon healing process after an injury and surgical
repair. Appreciating this uniqueness can help us better understand how
these factors affect healing and elucidate potential causes of suboptimal
outcomes. Development of such understanding can strengthen avenues
for informed and individualized approaches to recovery.
• Paradoxes of Tendon Healing Influence Treatment. Successful recovery often
requires balance. On one hand, the tendon should heal quickly so that the repair
is strong and able to withstand forces that occur with movement or tendon glide.
However, ideal healing is intrinsic, between the tendon ends; whereas, extrinsic
healing typically leads to the development of peritendinous adhesions. If
extensive or left untreated, these adhesions impede tendon glide, which can
cause joint stiffness and functional impairment. Thusly, during recovery, intrinsic
healing is encouraged while extrinsic healing may lead to complications. Even
more tenuous, to prevent these adhesions and encourage intrinsic healing, the
tendon must move. Mechanical stress should be applied to the tendon soon after
surgery, while the repair is still healing and not at its full strength.
o Implications: The paradoxical conditions of a successful healing
environment create a tenuous situation for therapists and patients. Without
careful management, a repaired tendon is susceptible to complications,
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including a ruptured repair. The balance necessary to support ideal
recovery and optimal outcomes is multifaceted and requires precision.
• Two Critical Therapeutic Windows Exist in the Timeline of Tendon Healing. Many
processes rapidly occur as soon as a tendon is surgically repaired. Given the
specific timing and respective changes in the healing tissues, there are two
critical therapeutic windows during the first three months after surgery. The first
of which occurs two through eight weeks after surgery, when both intrinsic and
extrinsic healing occur simultaneously, collagen and tenocytes are rapidly
proliferating, and the repair is beginning to gain its strength. The second critical
window begins immediately after the first, two through three months after
surgery. At this time, the repair should be more mobile and decrease in density,
while adhesions become more elastic and easier to break.
o Implications: Given the description of the healing processes occurring in
the initial time window, the focus of therapy should be around protecting
the repair, reducing remaining edema, and limiting the development of
extrinsic adhesions. During the second time window, the focus of therapy
should change. Interventions may be more effective if directed towards
tendon mobility, increased range of motion of the injured upper extremity,
and disrupting extrinsic adhesions to promote optimal functional return.
• MSKS has Utility for Monitoring the Healing of Surgically Repaired Tendons.
Multiple biomarkers were identified that are associated with healing that can be
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observed and measured using MSKS, including tendon enlargement, tendon
gapping, localized edema, vascularity, and potential identifiers of healing
complications. These biomarkers can indicate the appropriate, positive healing
status of a repaired tendon, identify potential complications or barriers to
recovery, determine the potential causes of poor outcomes, and alert a provider
to signs of improper healing.
o Implications: Given the utility of MSKS to directly evaluate the healing
status of the tendon and biomarkers indicative of poor outcomes, MSKS
may be useful as an imaging tool to evaluate tendons as they heal over
time. Identifying these biomarkers and understanding how they relate to
the healing status of tendons or complication development may support
the utility of MSKS as an imaging tool both in surgical follow-up and in
monitoring recovery over time during rehabilitation.
5.2.2. Conclusions from Chapter 3: A Standardized MSKS Protocol to Evaluate
Healthy Flexor Tendons
• It is Feasible to Acquire MSKS Images for the Evaluation of Flexor Tendons. A
standardized MSKS protocol was developed, and feasibility was established to
evaluate healthy flexor tendons in the distal hand. Deploying this protocol in a
healthy sample elucidated similarities and a few relatively common anomalies of
flexor tendon morphology, such as differences in tendon bifurcation location.
o Implications: A standardized MSKS protocol for evaluating flexor tendons
in the distal upper extremity is available for use in future research or
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clinical practice, which creates opportunities for developing standardized
and reliable measures of flexor tendons.
• Multiple Best Practice Suggestions Emerged for Imaging Flexor Tendons. While
developing the MSKS protocol, multiple considerations were identified that could
potentially influence the quality of the image obtained. These suggestions were
compiled, and a table with best practice suggestions was created, detailing the
optimal approaches to refine the protocol for image acquisition of flexor tendons.
o Implications: Although MSKS may be highly useful for evaluating flexor
tendons, there are many considerations necessary to optimize the validity
and accuracy of the images obtained. Without using the proper scanning
method, it is possible to obtain invalid measures or misrepresent flexor
tendon morphology.
5.2.3. Conclusions from Chapter 4: A Case Study of Functional Recovery After
Tendon Surgery
• It is Feasible to Conduct MSKS Evaluation of Flexor Tendons During the Early
Stages of Healing Post-Surgery. An MSKS image acquisition and measurement
protocol was deployed in a patient with an FDP laceration and tendon repair.
This protocol was feasibly implemented beginning at 4 weeks after the patient
had surgery through to 12 weeks of recovery. Throughout the study period, the
FDP was able to be imaged consistently across time, including at the site of
surgical repair.
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o Implications: MSKS can be used to directly observe the flexor tendons
after surgery during the early phases of healing while keeping a patient
adherent to any movement restrictions. Using MSKS can support the
evaluation of repaired tendons soon after surgery, providing a direct view
of the condition of the surgical repair and healing tissues.
• Measurements of Sonographic Biomarkers Can Be Obtained Reliably in a
Patient Recovering from Flexor Tendon Repair Surgery. Measurement
techniques were established to evaluate multiple sonographic biomarkers of
interest, including tendon CSA, localized edema CSA, and intra-tendinous
vascularity. Good to excellent reliability was established for continuous measures
of CSA values. However, intra-tendinous vascularity was measured on a scale
that appeared to misrepresent the level of vascular activity in the surgery area.
Although measures were good to reliable, there was a difference in subject
positioning, while the participant was wearing a dorsal blocking splint to comply
with safety and movement restrictions that may have deformed the tendon
leading to a misrepresentation of CSA measures or the appearance of other
tissues.
o Implications: Obtaining reliable measures for MSKS biomarkers is a first
step towards standardizing image analytic techniques, supporting
sonography’s utility as an evaluative tool. Furthermore, establishing
reliable measures can enhance the precision of assessing the healing
status and integrity of surgically repaired tendons over time and potentially
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across people. Although this preliminary evidence only supports the
reliability of one therapist evaluating a patient using CSA measures, there
are two key implications from reliability testing that require further
investigation. First, there is scant literature on how this positioning could
falsely deform the tendons, which creates a need for more research to
understand the impact of various degrees of flexion on the measurement
of tendons. Secondly, the scale used to evaluate intra-tendinous
vascularity appeared to conflict with the amount of blood flow around the
surgical site, which seemed to steadily increase over time. Other
measures of intra-tendinous vascularity need to be evaluated for validity
and reliability. Future work should consider the use of continuous
measures and may incorporate the rate or quantity of blood flow using
Power Doppler ultrasound.
• Variability Between MSKS Biomarkers Could be Identified at Different Locations
and Over Time. Using the MSKS protocol, changes in all three biomarkers of
interest could be observed over time. Furthermore, biomarker measures of CSA
differed between the imaged locations as well as the contra-lateral uninjured
hand. Measures of FDP and localized edema CSAs were the largest at the site of
surgery at all time points. Lastly, intra-tendinous vascularity appeared to steadily
increase over time.
o Implications: Observing changes in sonographic biomarkers throughout
the study period in this patient's case provide proof of concept that
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repeated assessment of the repaired flexor tendon using MSKS may be
beneficial for monitoring recovery during rehabilitation. Additional
information is necessary to explore the generalization of the MSKS
protocol to other individuals with flexor tendon repairs in the distal hand.
Furthermore, applying this protocol to a wider sample may help explicate
any relationships between sonographic biomarkers and functional
outcomes.
5.3. Synthesis of Knowledge Gained
The key findings and implications described above are synthesized here to
explicate the opportunities for future research that can support both clinical practice and
further understanding of the occupational foundation underlying rehabilitation for both
individuals with flexor tendon injuries and the therapists supporting their recovery. A
noteworthy implication of this dissertation is that it is feasible and may be beneficial to
use MSKS as an imaging tool to evaluate individuals with flexor tendon injuries and
surgical repairs. At present, there is a lack of precise measures that can readily and
directly assess the healing status of a surgically repaired flexor tendon. This work has
established a standardized protocol for sonographic image acquisition and analysis of
healthy flexor tendons and more importantly, for individuals with surgical tendon repairs.
The study results demonstrate how MSKS may serve as an invaluable tool, providing
clinicians with critical information unavailable to the naked eye that can then be used to
improve individualized interventions and patient care. The application of MSKS as an
assessment tool can allow clinicians to directly view surgically repaired tendons and
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surrounding tissues as they heal over time. Applying the protocol developed in this
study may support safe and efficient rehabilitation processes that could lead to
improved functional outcomes for these individuals.
Safe and efficient rehabilitation requires therapists to understand the progression
of tendon healing, as described in Chapter 2. After a successful surgical intervention,
the path of recovery is most volatile in the initial weeks following surgery. As a result,
early interventions are likely to be the most influential during this time. Being mindful of
the physiologic and morphologic processes that typically occur in healing tissues
described in this dissertation can help clinicians decide upon the most appropriate
interventions and when to apply them most effectively.
Clinicians can be assisted in this effort by MSKS. To further guide treatment
plans using MSKS, this work also helped to identify, longitudinally observe, and
measure biomarkers of healing in a patient recovering after a zone II FDP laceration
and surgical repair in his left ring finger. When monitored over two months, sonographic
biomarkers appeared to change over time, and each continuous measure (i.e., tendon
CSA and localized edema CSA) was able to be obtained reliably. Establishing reliability
with this initial work serves as a first step towards generalizing the use of MSKS and
expanding these findings through future research or clinical evidence. Additionally,
establishing reliability for these biomarkers can inform techniques for other sonographic
biomarkers that may be related to healing, such as scar adhesion and tendon length.
5.4. Future Directions for Knowledge Application
The primary future direction suggested by these dissertation findings is focused
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on advancing patient outcomes through the integration of MSKS into clinical practice.
Additional knowledge generation to support the advancement of MSKS in this way fall
into three categories: 1) replication of preliminary findings in larger studies, 2)
identification and validation of additional MSKS biomarkers, and 3) exploration of the
impact of MSKS on patient engagement and the occupation of recovery. A discussion of
these three opportunities follows in the paragraphs below.
Replication studies can further validate the limited and preliminary nature of the
findings in this work. The sample size is a significant limitation of this dissertation, both
in the healthy participant and patient components. To build upon this work, studies with
larger samples of healthy individuals can help elucidate the numerous anomalies of
flexor tendon morphology that are relatively common in the healthy population.
Understanding these anomalies can help further refine a sonographic protocol for
increased generalizability to capture the differences among healthy individuals.
Establishing normative measures of flexor tendon morphology can also help us better
compare healthy versus unhealthy tendons for clinical evaluation or screening of
conditions. These measures may be especially useful as substantial variation in the
cross-sectional area of flexor tendons exist within and across healthy individuals (Boyer
et al., 2001).
Even more importantly, although the single-subject case study provides proof of
concept, it is necessary to deploy this sonography protocol in a large, heterogeneous
patient sample. These studies would further support the clinical utility of MSKS to
evaluate injured flexor tendons, serving to refine and establish a standardized
sonographic protocol that is accurate and reliable. Such studies would support a better
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understanding of tendon healing following surgery and allow for comparisons of healing
patterns and variations among patients. This research could also support the accuracy
and reliability of sonographic biomarkers that could reflect patient healing status or
indicate complications related to recovery. Additionally, this information could help
ascertain the frequency for when MSKS should be used to evaluate patients and
identify the time when patients need close monitoring.
A second limitation of this dissertation was that only one individual obtained and
measured all sonographic images. Image acquisition and analysis techniques should be
validated in additional sonographers with MSKS training to make these findings more
generalizable. Several factors that need examination include protocol fidelity; the
accuracy of acquired images across different individuals, settings, and equipment; and
an estimation of the amount of training required to deploy the protocol. For images
obtained using this protocol, the quality of images across individuals should be reviewed
to ensure the accurate portrayal of tendon morphology across a heterogenous patient
sample. Moreover, further validation of inter-rater reliability for each biomarker that is
measured will be necessary to accurately evaluate images, establish typical healing
patterns, and identify the most salient biomarkers associated with healing and function.
Once successfully validated across multiple sonographers, a final refined protocol can
then be used to help elucidate the influence of injury, patient, and lifestyle factors on
tendon healing as well as determine the effectiveness of various surgical procedures
and post-surgical rehabilitation protocols.
In addition to replication studies, the second area of opportunity is to explore
additional sonographic techniques for use in post-surgical tendon rehabilitation.
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Dynamic imaging is one such technique that would support the evaluation of additional
sonographic biomarkers identified in the literature review. In this imaging technique, the
transducer is typically held in place, and the participant is asked to move; this way, the
anatomic structures in focus can be observed during movement in real-time. Some
healing biomarkers that can be assessed with this technique include tendon excursion
and tendon gapping, which are more evident while the tendon is in motion and under
tension provoked by the activated muscle. Tendon excursion is of importance as its
quality is typically related to hand motion, with more tendon excursion associated with
more range of motion (Yoshii et al., 2011). Sonography can also help identify causes of
limited tendon excursion, which can guide future interventions, such as the need for
secondary surgery. Similarly, measuring tendon gapping can help limit tendon ruptures,
as gapping is often a precursor to rupture and should be avoided (Singh et al., 2015).
Finally, there are indirect implications for this research relative to enhancing
clinical rehabilitation and supporting patients in their recovery. Specifically, there are
other promising applications of MSKS that could be easily integrated into the evaluation
protocol, which have been shown to improve patient engagement and ownership of the
recovery process. Of leading interest is using MSKS in rehabilitation to facilitate holistic
care – an enduring priority for hand therapists (McColl, 2016; Winthrop Rose et al.,
2011). More explicitly, given its unique utility, MSKS can support mind-body
interventions for patients with upper extremity disorders. Although numerous holistic
uses for rehabilitation have been discussed in the literature, sonography has been
primarily implemented as a mind-body intervention by clinicians as a biofeedback tool
(Gray et al., 2017; Roll et al., 2015), particularly for muscle retraining (Chipchase et al.,
155
2009; Giggins et al., 2013).
When using sonography for biofeedback, patients can directly view the anatomic
structures of their upper extremities, and observe how the dynamic movement of these
structures corresponds to their muscle contractions in real-time. This helps patients gain
knowledge and increased conscious awareness of their bodies to facilitate deeper
insight into the affected versus non-affected anatomic structures when performing
functional activities. Sonography biofeedback has been demonstrated to improve
function in individuals with severe gait disorders (Hamacher et al., 2012) and enhance
the quality of exercise performance to reduce low back pain (Wand et al., 2012).
Integrating musculoskeletal sonography as a biofeedback tool into clinical rehabilitation
can support a holistic approach to patient recovery following hand surgery, helping
patients gain insight into their bodies, relax, and feel more in control of their recovery
(Takata et al., 2020).
Lastly, using MSKS in rehabilitation can help facilitate a partnership between
patient and provider and promote engagement in the occupation of recovery, thereby
improving healthcare outcomes (Dugdale et al., 1999; Noseworthy, 2019). For example,
MSKS can assist as a tool for patient education and allow patients to directly observe
their injury, while their therapist serves as their guide. This transparency can support
patients’ understanding of their bodies and appreciation of a targeted intervention that
was individualized by their therapist. Using MSKS as an engagement tool can help
clinicians build a mental model that is accurately shared by both patient and provider,
reinforcing motivation and engagement (Rizzo, 2015; Wright et al., 2014).
In summary, the efforts of this dissertation culminate to achieve one goal: to promote
156
health through the occupation of one’s hands. From infancy, hand use affects
occupational participation and engagement, which in turn influence the sense of self,
meaning, and overall well-being (Christiansen, 1999; Clark, 1993; Wilcock, 2002;
Wilcock, 2007). The achievement of this work is a humble attempt to restore
occupational performance to those in need.
157
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APPENDICES
APPENDIX A: Supplementary Material for Chapter 2
Appendix A.1. Search Strategy for Literature Review
Database Name: PubMed
Database Vender: National Library of Medicine: National Center for Biotechnical
Date Last Searched: May 31, 2021
(Tendon injuries or tendons or tendinopathy) and (wound healing or inflammation or
stress or repair) and ((flexor tendon or finger tendon) or "Tendon
Injuries/therapy"[Mesh]) or (tendon scar and regeneration) AND ((fft[Filter]) AND
(1980/5/31:2021/5/31[pdat]) AND english[Filter]))
OR
flexor tendon AND (assessment OR clinical assessment) AND evaluation AND
((fft[Filter]) AND (english[Filter]))
OR
tendon and (clinical assessment or sonography or ultrasound imaging) and (surgery or
disorder) AND ((fft[Filter]) AND (2010/1/1:2021/5/31[pdat]) AND english[Filter]))
Limiters: English, Full-text
179
Appendix A.2. PRISMA Diagram of Articles Identified, Screened, Reviewed and
Included in the Literature Review
180
Appendix A.3. Physiology and Morphology of Healthy Tendons
Healthy tendon is mostly composed of spatially organized type I collagen fibers.
Tropocollagen, the smallest structural unit within a tendon, aggregates to form
microfibrils. The microfibrils aggregate into fibrils, fibrils into fibers, fibers into fiber
bundles, and fiber bundles into fasciculi, which combine to form the tendon proper. The
fiber bundles and fasciculi are each surrounded by a loose connective tissue called the
endotenon, which allows for independent sliding of fasciculi and fibrils. The endotenon
also provides paths for blood vessels and nerves to supply nutrition and innervation to
the tissue. The epitenon, a fibrous layer continuous with the epitenon, binds groups of
fasciculi together to form the tendon proper. This structure is then surrounded by a
secondary layer of connective tissue, the paratenon. Together, the epitenon and
paratenon external sheaths compose the peritenon. Unique to other areas of the body,
the flexor tendons of the hand are encased in a synovial tendon sheath. This synovial
sheath provides the flexor tendons with lubrication to facilitate tendon glide between
tight anatomic gaps in the distal upper extremity and over bony prominences that would
otherwise damage the tendon. As flexor tendons have a very limited blood supply, they
are considered avascular and are supplied with nutrition via diffusion of substances
through synovial fluid (Myer & Fowler, 2016; Nichols et al., 2019; Nourissat et al., 2015;
Tadros et al., 2018).
Functionally, the endotenon and epitenon connective tissues that surround the
tendon fiber bundles, fasciculi, and tendon proper are mostly composed of type III
collagen. Within tendons, tenocytes are the predominant cell type and are primarily
responsible for creating and secreting collagen. Once secreted, the collagen fibers
181
arrange into triple helices and cross-link to increase their strength and stability. These
collagen fibers are surrounded within an extracellular matrix, which supports gliding
between the fibrils and provides functional stability. Lymphatic, vascular, and neural
elements are present within the endotenon; blood vessels and tracts for the lymphatics
and nerves are present within the epitenon. The paratenon and, exclusively for flexor
tendons, the synovial sheath, provide protection and pathways for blood vessels and
nerves to supply nutrition to and innervate tendons respectively (Myer & Fowler, 2016;
Nichols et al., 2019).
The flexor digitorum profundus (FDP) and flexor digitorum profundus (FDS)
tendons receive nutritional supply from both vascular perfusion and synovial diffusion.
Vascularization for each FDP and FDS tendon is received through two vincula, a longus
and a brevis. Each FDS tendon is vascularized by the vinculum longus superficialis
(VLS) and the vinculum brevis superficialis (VBS) from proximal to distal. Each FDP
tendon is similarly supplied from proximal to distal by the vinculum longus profundus
(VLP) and the vinculum brevis profundus (VBP). These vincula enter from the dorsal
aspects of each FDP and FDS tendon. The most proximal vinculum, the VLS, arises
from the floor of the digital sheath of the proximal phalanx and enters the FDS just
proximal to the tendon’s bifurcation. The VLP supplying the FDP arises from the FDS at
the level of the proximal interphalangeal joint. Both the VBS and the VBP vincula enter
their respective FDS and FDP tendons near the tendon’s point of insertion. Because
these flexor tendons are vascularized dorsally, there is a richer blood supply on the
dorsal side of the tendons (Myer & Fowler, 2016).
As the flexor tendons pass through the carpal tunnel and into the fingers, they
182
enter a series of pulleys that create the flexor tendon sheath in the digits. For each
finger, there are five annular pulleys (A1-A5) and three cruciate pulleys (C1-C3). The
stronger, stiffer, and thicker annular pulleys hold the tendon close to the phalanges,
while the collapsible, flexible cruciate pulleys allow for stable mobility of the sheath
during flexion. The A1, A3, and A5 pulleys arise from the volar plates of the MCP, PIP,
and DIP joints respectively. The A2 and the A4 pulleys stabilize the tendon over the
proximal and middle phalanges respectively. Of the five annular pulleys, the A2 pulley is
the largest and strongest followed by the A4 pulley, and both are the narrowest and
most constricting to the flexor tendons. Maintaining these pulleys during surgical repair
helps give the tendons mechanical advantage during flexion, with pulley injury leading
to potential bowstringing of the tendon. However, fully intact pulleys may add
compression and friction to the repaired tendon, especially during the inflammatory
period due to post-operative swelling. To protect the repair and promote easier tendon
glide, judicious venting of critical pulleys is currently recommended during surgery (Klifto
et al., 2018; Myer & Fowler, 2016; Tang, 2019).
183
APPENDIX B: Supplementary Material for Chapter 3
Appendix B.1. Serial Images of Healthy Flexor Tendons of Included Participants
Using Sonography Protocol
The following serial images of healthy flexor tendons were selected for analysis
in Chapter 3 using the sonography protocol. Images 1-6 of the flexor tendons are
ordered from left to right, top to bottom. The first two images are over the
metacarpophalangeal joint in long- and short-axis, the second two are over the proximal
interphalangeal joint in long- and short-axis, and the last two are over the distal
interphalangeal joint in long- and short-axis.
184
Figure B.1. Serial Images of Participant One
185
Figure B.2. Serial Images of Participant Two
186
Figure B.3. Serial Images of Participant Three
187
Figure B.4. Serial Images of Participant Four
188
Figure B.5. Serial Images of Participant Five
189
Figure B.6. Serial Images of Participant Six
190
Figure B.7. Serial Images of Participant Seven
191
Figure B.8. Serial Images of Participant Eight
192
Figure B.9. Serial Images of Participant Nine
193
Figure B.10. Serial Images of Participant Ten
194
Figure B.11. Serial Images of Participant Eleven
195
Figure B.12. Serial Images of Participant Twelve
196
Figure B.13. Serial Images of Participant Thirteen
197
Figure B.14. Serial Images of Participant Fourteen
198
Figure B.15. Serial Images of Participant Fifteen
Abstract (if available)
Abstract
From birth, our hands help us interact with other people and our environment, supporting mental and physical development throughout our lives. Hand function allows us opportunities to engage in meaningful occupations, shape our surroundings, and communicate and express our thoughts and ideas, facilitating our health, identity, and wellbeing. Because of the vital importance of our hands, the work presented in this dissertation was inspired by patients and loved ones who have lost or limited use of their hands with the aspiration that they may experience a safe and efficient return to function. More specifically, this work explores how the clinical use of musculoskeletal sonography (MSKS) can facilitate a more precise method of individualized care and improve outcomes for patients with tendon injuries.
The research conducted in this dissertation focused on three aims: 1) conduct a systematic literature review to describe the morphologic and physiologic changes of healing tissue over time after a surgical tendon repair, 2) establish a sonographic image acquisition and analysis protocol to evaluate healing and recovery following flexor tendon repair, and 3) identify sonographic biomarkers that predict functional recovery and most easily distinguish patterns of healing following tendon repair. As a first step, an extensive literature review was conducted to help elucidate the physiologic and morphologic processes that occur in healing tissues after surgical tendon repair and the timing for when these processes take place. This literature review was also used to identify factors that may influence the healing process as well as distinguish MSKS biomarkers of recovery that may be indicative of the healing status of the repair.
Second, as there is no standardized MSKS protocol to evaluate flexor tendons in the upper extremity, the following cohort study focused on developing and refining a protocol to obtain sonographic images of the flexor tendons in the hand with a sample of 15 healthy individuals. This research helped establish the feasibility of deploying a standardized MSKS protocol to examine healthy flexor tendons as well as elucidated anatomic anomalies in flexor tendons that may frequently occur in the healthy population. Moreover, the results of this study and the information garnered from the literature review served as a template to guide the development of a second MSKS protocol to assess surgically repaired flexor tendons.
In the final case study, an MSKS protocol was developed and deployed in an individual with a zone II flexor tendon laceration and surgical repair during the third to twelfth weeks of his recovery. This research helped establish the feasibility of using MSKS to evaluate surgically repaired flexor tendons and the surrounding tissues during the early weeks of healing. Furthermore, the study findings also helped to establish good to excellent reliability for selected sonographic biomarkers of healing that were identified from the literature review (Chapter 2). Together, this work demonstrates promise for the future integration of MSKS into rehabilitation, displaying the potential to improve patient outcomes as well as create avenues for clinicians to provide more holistic care.
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Takata, Sandy Chie (author)
Core Title
Precision care to optimize safe return to function following surgical flexor tendon repair
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School of Dentistry
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Doctor of Philosophy
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Occupational Science
Degree Conferral Date
2023-05
Publication Date
04/25/2024
Defense Date
11/17/2022
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