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High-resolution ultrasonography of periodontium for periodontal diagnosis in healthy and diseased subjects

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High-resolution ultrasonography of periodontium for periodontal diagnosis in healthy and diseased subjects

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High-resolution ultrasonography of periodontium for periodontal diagnosis in healthy and
diseased subjects

by

Jane Law, D.D.S., MS

A Thesis Presented to the
FACULTY OF THE USC HERMAN OSTROW SCHOOL OF DENTISTRY
UNIVERSITY OF SOUTHERN CALIFORNIA
In Partial Fulfullment of the
Requirements for the Degree
MASTER OF SCIENCE
(BIOMEDICAL IMPLANTS AND TISSUE ENGINEERING)

August 2022

Copyright 2022 Jane Law
ii
ACKNOWLEDGEMENTS

The authors acknowledge NIH. funding under R21 DE029025, R21 DE029917, and UL
TR001442. This publication was supported in part by the National Science Foundation Graduate
Research Fellowship Program under Grant No. DGE-1650112. C.M. graciously acknowledges
support from the ARCS Foundation. Panels A, C, and D of Figure 1 were created in part with
BioRender. Jane Law, Colman A. Moore, Christopher T. Pham, Kai Chiao J. Chang, and Casey
Chen report no conflicts of interest related to this study. Jesse V. Jokerst is a co-founder of
StyloSonics, L.L.

iii
Table of Contents

Acknowledgements……………………………………………………………….…………ii

List of Tables………………………………………………………………………..……….iv

List of Figures…………………………………………………………………….….………v

Abstract…………………………………………………………………………..….……….vi

Introduction…………..………..……………………………………………….….………….1

Chapter 1: Materials and Methods……………………………………………………………2

Chapter 2: Results………...………………..……………...………………………….…….…5

Chapter 3: Discussion…..…………………...…………………………..…………….………8

Chapter 4: Conclusion……………...………..…………………………………….…………11

References………………….………..…………………………………………….…………12

Tables………………….…………………..…………………………………………………17

Figures……………….…..………………………………………………………...…………19

iv
List of Tables

Table 1: Image quality metrics, clinical measurements, and imaging measurements of human
subjects

Table 2: Image quality metrics, clinical measurements, and imaging measurements of swine
mandibles.

v
List of Figures

Figure 1. Overview of periodontal ultrasound imaging.

Figure. 2. Comparison of ultrasound to physical examination for an extracted swine mandible
following gum flap resection and periodontal measurement with physical probing.

Figure 3. B-mode image depicting ultrasound image-based measurements in a) extracted swine
mandible and b) human subject

Figure 4. Ultrasound for diagnostic measurements and interrater variability for ultrasound
image-based measurements of pocket depth (iPD) and clinical attachment level (iCAL).

Figure 5. Comparison between ultrasound image-based measurements (iGH, iABL) and clinical
probing measurements (PPD, CAL) for individual teeth (n = 66) of patients with healthy or
diseased clinical diagnoses.

Figure 6. Comparison between clinically assigned biotype and U.S. image-based measurements
of gingival thickness (iGT).

Figure 7 B-mode images in six subjects demonstrating ultrasound monitoring of gingival
recession via periodontal landmarks.

vi
ABSTRACT

Periodontal examination via physical probing provides critical metrics such as pocket depth,
clinical attachment level, and gingival recession; however, this practice is time-consuming,
variable, and often causes discomfort. Ultrasonography is painless, non-ionizing, and can
simultaneously resolve hard and soft tissues. In this study, 16 subjects were identified from patients
scheduled to receive dental care and clinically classified as periodontally healthy (n = 10) or
diseased (n = 6). A 40-MHz ultrasound system was used to measure gingival recession, gingival
height, alveolar bone level, and gingival thickness from 66 teeth to compare probing measurements
of pocket depth and clinical attachment level. Gingival recession and its risk in non-recessed
patients were assessed via ultrasonographic measurement of the supra- and subgingival
cementoenamel junction relative to the gingival margin. Inter-examiner bias for ultrasound image
analysis was negligible (<0.1 mm) for gingival height measurements and 0.45 mm for alveolar
bone level measurements. Ultrasound measurements of gingival height and alveolar bone level
were equivalent to periodontal probing depth and clinical attachment level for disease
classification (1.57-mm and 0.25-mm bias, respectively). Overall, ultrasonography possessed
equivalent diagnostic capacity as gold-standard probing for periodontal metrics while resolving
the subgingival anatomy.
1
INTRODUCTION
Periodontitis is one of the most common infectious diseases
1
and a leading cause of tooth loss.
2, 3

Preliminary evidence has suggested associations between periodontitis and systemic effects like
cardiovascular disease.
8
The disease and its sequelae reduce the quality of life and incur significant
time and costs for affected individuals.
4-7
Periodontal diagnosis is performed routinely in dental
offices. However, tools to diagnose/monitor periodontitis have major limitations. Clinical
periodontal examination and radiography are currently the standard of care but are time-consuming
for the clinician, uncomfortable for the patient, and subject to large errors. The inter-operator
variation in probing can be >40%.
9
Moreover, clinical assessment and radiographic examination
may not capture all clinical information (e.g., gingival thickness and inflammation). It is perhaps
not surprising that periodontal examination was not performed in 50-90% of the audited dental
records.
10-12
There is an urgent need to develop a novel tool for periodontal examination and
diagnosis.
Locating the cementoenamel junction (CEJ) is important for determining metrics of
periodontal health such as gingival recession and clinical attachment loss (CAL). The CEJ is
typically covered by the gingiva; its exact location is difficult to determine via physical probing
and can be subject to significant error: In mid-buccal sites, Vandana et al. reported over- or under-
estimation of the CEJ by trained periodontists for 74% (34/46) of measured teeth.
15

Ultrasound imaging has emerged as a potential tool for periodontal examination. It has the
benefits of being a portable and low-cost alternative to radiography that is noninvasive and free of
ionizing radiation.
14
Ultrasound imaging has been used to resolve dental and periodontal
structures—especially for alveolar bone and the cementoenamel junction
16-23
, anatomic landmarks
that are critical in periodontal examination. Recent studies showed the validity and reliability of
2
ultrasonography in measuring gingival thickness and other periodontal structures that cannot be
assessed through inspection and palpation. Ultrasound imaging has also been used for imaging
dental implants, the topography of edentulous crestal bone, and the bone-implant interface.
24-27

Studies that evaluated ultrasound imaging via ex vivo models and human case studies were
reported. However, higher-powered studies in human subjects using healthy and diseased cohorts
are relatively rare.
28-30
While existing work has evaluated ultrasound accuracy for imaging
periodontal structures, integrating these markers into diagnostic measurements and their
performance for staging disease is relatively unexplored.
Here, we extend this concept via 40-MHz ultrasound to locate the CEJ in relation to other
anatomical markers for image-based calculation of periodontal metrics that could serve as
surrogate measurements for physical probing. The study objective was to evaluate high-frequency
ultrasound in clinical periodontology for potential replacement of probing by comparing the
performance of the two techniques in healthy and diseased subjects. This goal was achieved by
identifying and evaluating imaging markers and comparing these markers to established clinical
metrics of periodontal health.

Chapter 1: Materials & Methords
Materials: A high-frequency, commercially available imaging ultrasound system (Vevo L.A.Z.R.,
Visualsonics, Toronto, CA) was employed with a 40-MHz linear array transducer (LZ-550).
Disposable Tegaderm films were used as sterile transducer sleeves (3M, Minnesota, U.S.A.).
Periodontal probing measurements were conducted with a Williams and Marquis probe. Extracted
swine jaws were provided by Sierra for Medical Science, Inc. Whittier, CA.
3
Subject recruitment and clinical examination: The study protocol was approved by the USC and
UCSD Institutional Review Boards and in accordance with STROBE and the ethical guidelines
for human subjects research established by the Helsinki Declaration of 1975. The study subjects
were identified from patients seeking dental care at the Herman Ostrow School of Dentistry. As
part of the clinical protocol, the patients received extra- and intra-oral examinations, medical and
dental history review, a set of full-mouth radiographs, periodontal examination, periodontal
diagnosis, and treatment planning. Eligible subjects were healthy adults who weighed at least 110
pounds with one quadrant with at least upper and lower anterior teeth. Subjects were excluded if
they had bloodborne pathogen infections, bleeding disorders, acute oral infections, or were
pregnant or lactating women. Two subject groups were recruited based on the periodontal
diagnosis described in the 2017 World Workshop on the Classification of Periodontal and Peri-
implant Diseases and Conditions.
31
The first group (n = 10) comprised subjects with the following
diagnosis: periodontal health in intact or reduced periodontium in stable periodontitis patients, or
dental biofilm-induced gingivitis in the intact or reduced periodontium. The second group (n = 6)
comprised subjects diagnosed with periodontitis (Stage II-IV and Grade B or C) with localized or
generalized involvement.
The periodontal diagnosis was given by a board-certified periodontist faculty (K.C.J.C.)
and a resident (J.L.). Six maxillary or mandibular anterior teeth were then selected for the study.
We could not access molars because of the size of the transducer. Periodontal probing depth was
determined with a Williams and Marquis probe at six sites per tooth (mesio-labial, mid-labial,
disto-labial, mesio-lingual, mid-lingual, and disto-lingual). Tooth mobility was determined as
Class 1: mobility of up to 1 mm in an axial direction, Class 2: mobility of greater than 1 mm in an
axial direction, and Class 3: mobility in an apico-coronal direction (depressible tooth). Bleeding
4
on probing (BOP) provoked by applying a probe to the bottom of a sulcus/pocket was recorded.
Gingival recession was recorded by measuring the distance between the CEJ to the top of the
gingival margin in the mid-labial aspect of the tooth with a periodontal probe. Clinical attachment
level (CAL) was determined from CEJ to the bottom of the pocket. The gingival phenotype was
determined by inserting the periodontal probe into the mid-labial surface of the tooth. A thin
gingival phenotype was assigned if the probe was visible through the gingival tissue.
Periodontal ultrasound imaging: Subjects were seated supine in the dental chair and imaged with
a handheld, linear array transducer by a clinician. A disposable transparent sleeve was used to
wrap the transducer in addition to sterile ultrasound coupling gel. Imaging was performed
manually by positioning the transducer parallel to the long axis of the tooth along the buccal
midline. A layer of ultrasound coupling gel ~5 mm thick was placed between the contact areas and
the transducer to achieve good coupling and optimum resolution. Freehand scans of each tooth
were exported as a video file consisting of at least 1,000 frames.
Image analysis: All images had to meet specific quality criteria before measurement. These were:
1) clear resolution of the GM, (2) clear resolution of the ABC, and (3) a lack of interfering artifacts
coincident with the relevant anatomy. If these conditions were met, further image analysis was
performed (Table 1, 2). All imaging measurements were performed in duplicate by two individuals
blinded to data collection. These raters assessed human variation in the identification of anatomical
markers. The first was a clinician with no ultrasound experience (Analyst 1), while the second was
an ultrasound researcher with no clinical expertise (Analyst 2). Imaging measurements were
performed digitally in the VisualSonics software and ImageJ.
30, 32.
The distance from the gingival
margin (GM) to the alveolar bone crest (ABC) was defined as the image-based gingival height
(iGH). Similarly, the distance from the CEJ to the ABC was defined as the image-based alveolar
5
bone level (iABL). The image-based gingival thickness (iGT) was measured at the midpoint of the
ABC and GM.
Statistical analysis: The suitability of sample size for determining measurement differences
between teeth grouped as periodontally healthy or diseased was estimated via power analysis for
a two-tailed significance test with 95% significance (α = 0.05), 80% power (β = 0.20), variance =
0.3 mm2, and minimum differences of 0.4, 0.5, or 1.0 mm (Supplementary Appendix Figure 1).
Bland-Altman analysis was performed to quantify differences (bias, limits of agreement)
between image examiners and between physical probing and imaging measurements. Box-and-
whisker plots were combined with unpaired, two-tailed significance testing (α = 0.05) to
compare healthy and diseased groups of measured/imaged teeth. Analysis was performed with
GraphPad Prism 9 (San Diego, CA) and Microsoft Excel (Redmond, Washington).

Chapter 2: Results
A high-frequency, commercially available imaging system was used for chairside imaging
of subjects (Fig. 1A). The handheld linear array transducer (40 MHz, Fig. 1B) permitted access to
the maxillary/mandibular incisors and cuspids (teeth 6-11 and 22-27, Fig. 1C). B-mode images
(2D ultrasound cross-sectional images) were collected in the sagittal plane at the mid-buccal site
of each tooth. The anatomy of the imaged region is depicted in (Fig. 1D) for comparison to a
representative B-mode image in (Fig. 1E). In general, six anatomical markers were consistently
identified and used to orient the imaging operator/analyst: alveolar bone, alveolar bone crest
(ABC), gingiva, gingival margin (GM), CEJ, and the tooth surface (Fig. 1D-E).
First, we confirmed that our ultrasound system could resolve the CEJ in cadaver swine
jaws (Fig. 2). This was achieved by imaging each tooth (Fig. 2A), measuring the CEJ with image
6
analysis (Fig. 2B-E), and comparing the values to tactile probing measurements following gum
flap resection (Fig. 2F-G) and measurement by a clinician (Fig. 2H). These measurements are
restricted to integers but represent the gold standard and showed good agreement with imaging
(<1.0 mm difference between GM-CEJ values and <0.5 mm difference between GM-ABC values)
(Fig. 2I).
79 B-mode images were acquired in humans from 16 subjects comprising 43 teeth
clinically diagnosed as healthy and 36 diagnosed with periodontal disease via physical
measurements and examination. Of these images, 66 (84%) met quality criteria and were used for
analysis. All image quality metrics, image measurements, and clinical measurements are included
in (Table 1). All image-based measurements including iGH (GM to ABC), iABL (CEJ to ABC),
iGR (image-based gingival recession), and iGT (image-based gingival thickness) are depicted for
a representative tooth site in (Fig. 3). The same image-based measurements were used on the
extracted swine mandibles and human subjects.
To determine the iGH and iABL values in this study, two blinded analysts (one clinician
and one researcher) independently measured each frame, and their values were averaged. Bias
between raters was < 0.1 mm for iGH (Fig. 4A) and 0.45 mm for iABL (Fig. 4B). The increased
variance for iABL reflected differences between the raters in assigning the CEJ, which can be a
less obvious feature than the ABC or GM.
The average iGH and iABL values for teeth from healthy/diseased subjects were compared
to clinical PPD and CAL measurements, respectively (Fig. 5). Without the aid of a contrast agent
in the gingival sulcus, we were unable to determine the image-determined probing depth.
However, we hypothesized that iGH correlates with the clinical PPD. The average PPD
measurements were 1.68 mm for healthy subjects and 2.25 mm for diseased subjects (Fig. 5A). A
7
similar increase was observed for iGH measurements: 3.19 mm for healthy subjects and 3.67 mm
for diseased subjects (Fig. 5A). In both cases, measurements in diseased subjects were
significantly higher than in healthy subjects (unpaired, two-tailed t-test, p = 0.0142 for PPD, p =
0.0286 for iGH). Expectedly, iGH values were larger than PPD values (1.57 mm Bland-Altman
bias, on average) because the iGH measurements terminated at the ABC rather than the gingival
sulcus (Fig. 5B). As with the PPD measurements, CAL measurements were significantly higher
for diseased than healthy subjects: 1.68 mm in the healthy group and 2.56 mm in the diseased
group (unpaired, two-tailed t-test, p = 0.0003, Fig. 5C). For iABL, the healthy average was 1.80
mm, and the diseased average was 2.74 mm—this difference between groups was even more
significant than the CAL measurements (p < 0.0001, Fig. 5C). Bland-Altman analysis revealed a
minor 0.25-mm magnitude bias toward the iABL measurements (Fig. 5D). Lastly, iGT was
compared to gingival biotype: 93.5% of the associated gingiva for measured teeth possessed a
thick biotype, and there was no correlation to disease status (Fig. 6A). Accordingly, the iGT
measurements (from the midpoint of the ABC and GM) were not significantly different for healthy
versus diseased patients (Fig. 6B).
One simple periodontal measurement is the distance between the CEJ and GM: This was
used to track gingival migration (recession or overgrowth) and demonstrate varying positions of
the CEJ relative to the GM for six different subjects (Fig. 7). The CEJ has an angled disruption in
the echogenicity of the tooth surface between the GM and ABC For subjects in (Fig. 7A-C), the
CEJ is apical to the GM (i.e., no gingival recession) showing subgingival CEJ-GM distances of -
4.0 mm, -1.3 mm, and -0.6 mm. The CEJ and GM were at the same location in (Fig. 7D). The last
two cases have gingival recession (Fig. 7E-F), where the GM is apical to the CEJ (0.6 mm and 1.1
mm respectively).
8

Chapter 3: Discussion
We compared iGH to PPD and iABL to CAL because these measurements are physically
equivalent except for their termini—that is, the iGH and iABL terminate at the ABC while the
PPD and CAL terminate at the depth of the gingival sulcus. This difference, the distance between
the ABC and the terminus of the gingival sulcus (corresponding to connective tissue and junctional
epithelium), has been described as the biologic width.
36
Therefore, if known, the biologic width
should be subtracted as a correction factor to calculate an image-based pocket depth (iPD) from
the iGH as well as an image-based clinical attachment level (iCAL) from the iABL. Thus, iPD
should approximate PPD and correlate with iGH. This correction factor is useful to help correlate
these novel imaging markers to conventional metrics of periodontal health; however, it is possible
to imagine these novel imaging markers being used to stratify oral health independent of
conventional probing depths.
The average difference between iGH and PPD measurements in this dataset was 1.57 mm
(Fig. 5B). If this value is defined as the average biologic width and subtracted from each iGH
measurement, then we obtain a set of iPD values after rounding to the nearest integer similar to
rounding done when measuring the PPD. Likewise, we obtained a set of iCAL values after
performing the same subtraction from the iABL data. This analysis suggested 83% agreement
between iPD and PPD values, and 49% agreement between iCAL and CAL values, where the
agreement was defined as ≤ 1 mm difference between paired measurements. While our measured
estimate for the biologic width falls within the range of mean values reported in a systematic meta-
analysis (between 1.15- 3.95 mm), disease state, tooth type, probing depth, and attachment loss
can all affect the biological width.
33
The combination of these variables and the lack of precision
9
in locating the subgingival CEJ with a periodontal probe are likely reasons for the relatively low
agreement between iCAL and CAL values. Indeed, this limitation of physical probing for CEJ
identification reduces the value of this comparison. Given the higher accuracy of physical probing
for PPD measurements, the comparison between iPD and PPD is both more reliable and promising.
Notably, while recapitulating the PPD values via imaging has value, the iGH is simpler
and more straightforward to measure (noninvasive). It also does not require a prior knowledge of
the biological width. More importantly, we show here that iGH correlates to disease as well as if
not better than PPD, and thus we suggest that it could be a standalone metric of periodontal health.
Of course, the true value will need to be validated with larger cohorts, including molars that could
not be accessed here due to the large size of the transducer.
The CEJ and the GM are two of the most prominent features in ultrasound images at mid-
buccal sites. These can be used to precisely measure the extent of gingival recession and its future
risk (Fig. 7). Though useful for longitudinal monitoring, the position of the CEJ in relation to the
GM (gingival recession) at any single time point is insufficient for diagnosing periodontal health
because gingival recession is often multifactorial in origin (Fig. 5).
34, 35
Therefore, we evaluated
the diagnostic value of measurements derived from the ABC, CEJ, and GM. Specifically, we
measured image-based alveolar bone level (iABL) and image-based gingival height (iGH) for each
tooth site and compared them to clinically measured PPD and CAL values. We also compared the
magnitudes of these values after classifying patient images into healthy or diseased groups
corresponding to their clinical diagnosis.
Ultrasound can also measure gingival thickness with a high degree of precision and
accuracy—while iGT alone does not reflect periodontal health, it is an important metric in the
context of operations such as mucogingival and periodontal surgeries. Currently, biotype is a
10
binary evaluation performed by inserting the periodontal probe into the gingival sulcus and
assessing probe visibility. A visible probe corresponds to a “thin” biotype and an invisible probe
corresponds to a “thick” biotype. Actual values for thin and thick biotypes have been proposed as
< 1.0 mm GT and > 1.0 mm GT, respectively.
37
We did not observe a statistical difference between
GT or iGT measurements in healthy and diseased patients (Fig. 6). Though imaging is significantly
more precise than the probe visibility method, this comparison served as assurance that iGT
measurements were not biased by the health status of the patient.
Our technique does have some limitations. Many images possessed reflection artifacts
generated by the ultrasound sleeve. These artifacts are caused by the specific geometry of the
transducer, i.e., the ~ 0.5-mm gap between the transducer elements and the subject/imaging target.
Most transducers do not have this gap. Another limitation of the transducer was its size. This
restricted imaging to the buccal surfaces of teeth 6-11 and 22-27. The ideal transducer could access
the buccal and lingual surfaces of the full dentition. The practical clinical deployment will also
need to integrate computational techniques to automatically extract imaging markers.
16, 22, 38, 39

Nevertheless, ultrasound may have significant clinical value for longitudinal monitoring of
periodontal health. Unlike other oral imaging modalities, ultrasonography offers details of both
hard and soft tissues, thus facilitating the measurement of periodontal metrics that require the
resolution of both hard (ABC, CEJ) and soft (GM, GT) features. It is non-ionizing, painless, and
can be operated chairside with minimal training.

Chapter 4: Conclusions
We investigated the use of high-frequency ultrasound in 10 healthy subjects (34 teeth) and
six subjects with periodontal disease (32 teeth) for measuring critical metrics of periodontal health,
11
including probing pocket depth, clinical attachment level, gingival recession, and gingival
thickness at mid-buccal sites. Image-based measurements of gingival height extended from the
gingival margin to the alveolar bone crest. They were comparable to probing pocket depth (1.57-
mm magnitude bias) with functional equivalence for assessing disease status. Identification of the
cementoenamel junction by human operators also allowed image-based measurement of alveolar
bone level and gingival recession. Inter-operator bias was negligible (<0.1 mm) for gingival height
and 0.45 mm for alveolar bone level measurements. Image-based alveolar bone level
measurements were equivalent to clinical attachment level for staging disease (0.25-mm
magnitude bias). Overall, ultrasonographic metrics in this patient group had at least an equivalent
diagnostic capacity as gold-standard physical probing while offering more detailed anatomical
information and painless operation. We anticipate that advances in the form factor of ultrasound
hardware will facilitate the further translation of this technology into the dental clinic.
The periodontal examination provides critical information such as probing pocket depth
(PPD; current periodontal health) and clinical attachment level (CAL; cumulative destruction).
13

PPD, CAL, and other clinical parameters form the basis of periodontal diagnosis. Radiography
offers excellent sensitivity to hard tissue (bone, enamel, etc.) but cannot discriminate between
healthy and diseased gingiva or map disease within soft tissue; it also has a small but non-
negligible dose of ionizing radiation.

12
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34. Bahal P, Malhi M, Shah S, Ide M. Managing the consequences of periodontal
diseases/treatment: gingival recession. Dental Update 2019;46:966-977.
35. Tugnait A, Clerehugh V. Gingival recession—its significance and management. Journal
of dentistry 2001;29:381-394.
36. Nugala B, Kumar BS, Sahitya S, Krishna PM. Biologic width and its importance in
periodontal and restorative dentistry. Journal of conservative dentistry: J.C.D. 2012;15:12.
16
37. Alves PHM, Alves TCLP, Pegoraro TA, Costa YM, Bonfante EA, de Almeida ALPF.
Measurement properties of gingival biotype evaluation methods. Clinical Implant
Dentistry and Related Research 2018;20:280-284.
38. Ilhan B, Guneri P, Wilder-Smith P. The contribution of artificial intelligence to reducing
the diagnostic delay in oral cancer. Oral Oncology 2021;116:105254.
39. Daniels K, Gummadi S, Zhu Z, et al. Machine Learning by Ultrasonography for Genetic
Risk Stratification of Thyroid Nodules. JAMA Otolaryngology–Head & Neck Surgery
2020;146:36-41.

17
Table 1: Image quality metrics, clinical measurements, and imaging measurements of
human subjects.

18
Table 2: Image quality metrics, clinical measurements, and imaging measurements of
swine mandibles.

19

Figure 1. Overview of periodontal ultrasound imaging. (A) Schematic of chairside ultrasound
imaging during routine dental examination. (B) Photograph of the commercial 40-MHz transducer
with coupling gel and sterile sleeve used for subject imaging. (B) Dental chart with teeth
highlighted (6-11, 22-27) that could be physically accessed by the ultrasound transducer. (C)
Diagram of the periodontal anatomy surrounding the gingival sulcus with magnification of the
sagittal plane. Roman numerals denote the I: alveolar bone, II: gingiva, III: alveolar bone crest
(ABC), IV: gingival margin (GM), V: cementoenamel (CEJ), VI: tooth surface. (D) B-mode
ultrasound image of the region in (C) for the central mandibular incisor (#25) of a patient with
anatomical markers labeled.

(D)
(E)
II
I III
IV
VI
I. Alveolar bone
II. Gingiva
III. Alveolar bone crest (ABC)
IV. Gingival margin (GM)
V. Cementoenamel junction (CEJ)
VI. Tooth surface
II
I
III
V
IV
1 mm
6
7
8 9
10
11
27
26
25 24
23
22
Imaging
accessible
(C) (A)
Figure 1. Overview of periodontal ultrasound imaging. (A) Schematic of chairside
ultrasound imaging during routine dental examination. (B) Photograph of the
commercial 40-MHz transducer with coupling gel and sterile sleeve used for
subject imaging. (B) Dental chart with teeth highlighted (6-11, 22-27) that could
be physically accessed by the US transducer. (C) Diagram of the periodontal
anatomy surrounding the gingival sulcus with magnification of the sagittal plane.
Roman numerals denote the I: alveolar bone, II: gingiva, III: alveolar bone crest
(ABC), IV: gingival margin (GM), V: cementoenamel (CEJ), VI: tooth surface. (D) B-
mode ultrasound image of the region in (C) for the central mandibular incisor
(#25) of a patient with anatomicalmarkers labeled.
VI
V
(B)
Disposable
cover
US gel
1. Clinical dental exam
2. Ultrasound imaging
20

Figure. 2. Comparison of ultrasound to physical examination for an extracted swine
mandible following gum flap resection and periodontal measurement with physical probing.
(A) Photograph of the 2
nd
molar (M2), 1
st
molar (M1), 2
nd
premolar (PM2), 1
st
premolar (PM1),
and the imaging plane for each tooth (white dashed lines). (B-E) Visualization of the
cementoenamel junction (CEJ) relative to the alveolar bone crest (ABC) and gingival margin (GM)
for the (B) 2
nd
molar, (C) 1
st
molar, (D) 2
nd
premolar, and (E) first premolar. The CEJ is
consistently resolvable as a disruption in the echogenicity of the tooth surface between the GM
and the ABC. The image-based measurements of the GM to CEJ (yellow lines) were M2 = 2.53,
M1 =1.88, PM2 = 1.39 mm, PM1 = 1.60 mm. The corresponding GM to AC measurements (red
lines) were M2 = 4.19 mm, M1 = 6.30 mm, PM2 = 4.95 mm, PM1 = 4.59 mm. (F) Following
imaging, the GM was traced along the teeth with a marker. (G) The gingiva (gum flap) was
resected to reveal the roots of the teeth. (H) The distances from GM to CEJ and GM to ABC were
measured by a clinician using physical probing. (I) These values were plotted and compared to the
image-based measurements. All resection + probe values were restricted to integers.

21

Figure 3. B-mode image depicting ultrasound image based measurements in a) extracted
swine mandible and b) human subject. B-mode image with manual annotations showing the
extraction of iGH (teal), iABL (white), iGR (yellow), and iGT (red). iABL: CEJ to ABC for
assessing bone height; GH: GM to ABC for the calculation of the probing depth; GR: GM to CEJ
for assessing gingival recession; iGT: gingival thickness for gingival phenotyping.

22

Figure 4. Ultrasound for diagnostic measurements and interrater variability for ultrasound
image-based measurements of pocket depth (iPD) and clinical attachment level (iCAL
(A, B) Bland-Altman plots comparing the iGH and iABL measurements from two blinded image
analysts for the same image set (n = 66 teeth). The increased variance (bias) between analysts for
iABL (0.45 ± 0.96 mm) relative to iGH (0.06 ± 0.61 mm) was due to differences in identification
of the CEJ between the two image analysts.

23

Figure 5. Comparison between ultrasound image-based measurements (iGH, iABL) and
clinical probing measurements (PPD, CAL) for individual teeth (n = 66) of patients with
healthy or diseased clinical diagnoses. (A) Box-and-whisker plots for PPD and iGH both indicate
significantly higher measurements in the diseased group (n = 32) than the healthy group (n = 34);
PPD values are limited to integers. Pairwise comparison values are p-values (unpaired, two-tailed
t-test). (B) Bland-Altman analysis between the measurement methods shows a 1.57 ± 0.95 mm
bias toward iGH measurements averaged from all teeth– these values are larger because—while
both measurements begin at the GM—the iGH is measured to the ABC rather than the terminus of
the gingival sulcus. This difference, due to the connective tissue and junctional epithelium between
the ABC and gingival sulcus, has been described as the “biological width”
30
. (C) Box-and-whisker
plots for iABL and CAL indicate significantly higher values for teeth in the diseased group than
the healthy group. CAL values are limited to integers. Pairwise comparison values are p-values
(unpaired, two-tailed t-test). (D) Bland-Altman analysis between the iABL/CAL measurement
methods reveal a 0.25 ± 0.98 mm bias toward the iABL measurements indicating a minimal
difference between the two methods.

0 1 2 3 4 5 6 7
-4
-2
0
2
4
Average of methods (mm)
PPD - iGH (mm)
+ 0.29 mm
- 3.42 mm
Bias
- 1.57 mm
(A)
(C)
Figure 4. Comparison between US image-based measurements
(iGH, iABL) and clinical probing measurements (PPD, CAL) for
individual teeth (n = 66) of patients with healthy or diseased
clinical diagnoses. (A) Box-and-whisker plots for PPD and iGH
both indicate significantly higher measurements in the diseased
group (n = 32) than the healthy group (n = 34). PPD values are
limited to integers. Pairwise comparison values are p-values
(unpaired t-test). (B) Bland-Altman analysis between the
measurement methods reveal a 1.57 ± 0.95 mm bias toward iGH
measurements averaged from all teeth– these values are larger
because though both measurements begin at the GM, the iGH is
measured to the ABC rather than the terminus of the gingival
sulcus. This difference, due to the connective tissue and
junctional epithelium between the ABC and gingival sulcus, is
referred to as the biological width. (C) Box-and-whisker plots for
iABL and CAL indicate significantly higher values for teeth in the
diseased group than the healthy group.CAL values are limited to
integers. Pairwise comparison values are p-values (unpaired t-
test). (D) Bland-Altman analysis between the iABL/CAL
measurement methods reveal a 0.25 ± 0.98 mm bias toward the
iABL measurements, indicating a minimal difference between
the two methods.
(B)
(D)
0 1 2 3 4 5 6 7
-4
-2
0
2
4
Average of methods (mm)
CAL - iABL (mm)
+ 1.67 mm
- 2.17 mm
Bias
- 0.25 mm
0
2
4
6
8
10
Measurement (mm)
CAL iABL
<0.0001
Healthy
Diseased
0.0003
0
2
4
6
8
10
Measurement (mm)
PPD iGH
0.0286
0.0142
Healthy
Diseased
24

Figure 6. Comparison between clinically assigned biotype and US image-based
measurements of gingival thickness (iGT). (A) Teeth from healthy (n = 30) and diseased (n =
32) groups were classified as a thick or thin biotype according to the conventional probe-visibility
method. Photographic inset: example of a thick biotype. (B) The imaged gingival thickness (iGT)
can provide significantly more quantitative assessment (< 0.1 mm precision over the full cross-
sectional area) than probe-based biotyping. As expected, no significant difference was observed
between iGT for the healthy and diseased groups. Here, the iGT was measured from the midpoint
between the ABC and CEJ.

25

Figure 7. B-mode images in six subjects demonstrating ultrasound monitoring of gingival
recession via periodontal landmarks. Clinically, the distance between the CEJ and GM defines
the extent of gingival recession and is used to determine CAL. Panels A-F show teeth from subjects
with increasing levels of gingival recession. (A-C) Images from subjects with the CEJ apical to
the GM (i.e., non-recessed). These measurements are represented as negative values (green). (D)
Image from a subject where the GM is coincident with the CEJ (i.e., PPD = CAL). (E-F) Images
from subjects with the GM apical to the CEJ (i.e., recessed). Recessed measurements are
represented as positive values (red).

A B C D E F
-2
0
2
4
6
Subject
CEJ to GM (mm)
US
Tactile probing
GM CEJ ABC
GM
CEJ
ABC
GM
CEJ
ABC
GM = CEJ
ABC
ABC GM
CEJ
A
B
C
D
ABC
GM CEJ
F
E
- 4.0 mm
- 1.3 mm
- 0.6 mm
0 mm
+ 0.6 mm
+1.1 mm
Figure 2. B-mode images in six subjects demonstrating US monitoring of gingival recession via
periodontal landmarks. Clinically, the distance between the CEJ and GM defines the extent of gingival
recession and is used with PD to determine CAL. Panels A-F show teeth from subjects with increasing
levels of gingival recession. (A-C) Images from subjects with the CEJ apical to the GM (i.e., non-recessed).
These measurements are represented as positive values (green). (D) Image from a subject where the GM
is coincident with the CEJ (i.e., PD = CAL). (E-F) Images from subjects with the CEJ coronal to the GM (i.e.,
recessed). Recessed measurements are represented as negative values (red). (G) Comparison between
US measurements and physical (tactile) probing measurements by a periodontist.
Non-recessed
(Healthy)
At risk
Gingival
recession

Abstract (if available)

Abstract Periodontal examination via physical probing provides critical metrics such as pocket depth, clinical attachment level, and gingival recession; however, this practice is time-consuming, variable, and often causes discomfort. Ultrasonography is painless, non-ionizing, and can simultaneously resolve hard and soft tissues. In this study, 16 subjects were identified from patients scheduled to receive dental care and clinically classified as periodontally healthy (n = 10) or diseased (n = 6). A 40-MHz ultrasound system was used to measure gingival recession, gingival height, alveolar bone level, and gingival thickness from 66 teeth to compare probing measurements of pocket depth and clinical attachment level. Gingival recession and its risk in non-recessed patients were assessed via ultrasonographic measurement of the supra- and subgingival cementoenamel junction relative to the gingival margin. Inter-examiner bias for ultrasound image analysis was negligible (<0.1 mm) for gingival height measurements and 0.45 mm for alveolar bone level measurements. Ultrasound measurements of gingival height and alveolar bone level were equivalent to periodontal probing depth and clinical attachment level for disease classification (1.57-mm and 0.25-mm bias, respectively). Overall, ultrasonography possessed equivalent diagnostic capacity as gold-standard probing for periodontal metrics while resolving the subgingival anatomy.

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Asset Metadata

Creator Law, Jane Kimberly (author)

Core Title High-resolution ultrasonography of periodontium for periodontal diagnosis in healthy and diseased subjects

School School of Dentistry

Degree Master of Science

Degree Program Medical Implants and Tissue Engineering

Degree Conferral Date 2022-08

Publication Date 07/27/2022

Defense Date 05/18/2022

Publisher University of Southern California (original), University of Southern California. Libraries (digital)

Tag 40 MHz,alveolar bone crest,alveolar bone level,B-mode,cementoenamel junction,clinical attachment level,clinical measurements,disease,gingival margin.,gingival phenotype,gingival thickness,high-resolution ultrasound,OAI-PMH Harvest,periodontal health,periodontology,probing depths,ultrasonography,ultrasound

Format application/pdf (imt)

Language English

Contributor Electronically uploaded by the author (provenance)

Advisor Chen, Casey (committee chair), Kar, Kian (committee member), Paine, Michael (committee member)

Creator Email janelaw@usc.edu,janelaw75@gmail.com

Permanent Link (DOI) https://doi.org/10.25549/usctheses-oUC111375361

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