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3D volumetric analysis of post extraction maxillary sinus floor changes: a retrospective CBCT analysis

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3D volumetric analysis of post extraction maxillary sinus floor changes: a retrospective CBCT analysis

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Content 1

3D VOLUMETRIC ANALYSIS OF POST EXTRACTION MAXILLARY SINUS FLOOR
CHANGES:

A RETROSPECTIVE CBCT ANALYSIS

Thesis Presented to the Graduate
School of the University of Southern California
In Partial Fulfillment of the Requirements for the degree of
MASTER OF SCIENCE IN CRANIOFACIAL BIOLOGY BY
SARA ElHUSSEINI AHMED
DEGREE CONFERRAL DATE: AUGUST 2019

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Table of Contents

AUTHORS AND AFFILIATIONS ................................................................................................................................. 3
DEDICATION ............................................................................................................................................................ 4
ACKNOWLEDGMENTS .............................................................................................................................................. 5
FIGURE LEGENDS AND TABLES LIST ....................................................................................................................... 6
ABSTRACT…………………………………………………………………………………………………………………………………………………………..9
1. INTRODUCTION .............................................................................................................................................. 11
2. MATERIALS AND METHODS ............................................................................................................................ 14
3. RESULTS ......................................................................................................................................................... 21
4. DISCUSSION ................................................................................................................................................... 24
5. CONCLUSIONS ................................................................................................................................................ 32
6. FIGURE LEGENDS AND TABLES ........................................................................................................................ 33
7. REFERENCES ................................................................................................................................................... 50

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Authors and Affiliations
Sara Elhusseini BDS,
Graduate student, Candidate for Master of Science in Craniofacial Biology (CBY).
Division of Periodontology, Diagnostic Sciences and Dental Hygiene.
Herman Ostrow School of Dentistry, University of Southern California (USC).
925 W 34th St Room 4278 Los Angeles CA 90089.

Correspondence: Selhusse@usc.edu

Committee members:
Chair: Dr. Kian Kar, DDS, MS
Dr. Casey Chen DDS, PhD
Dr. Parish Sedghizadeh DDS, MS

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Dedication

To my beloved husband, Dr. Ahmed Sharaf for his infinite love and support.

To my dear father, Dr. Safeyeldin Elhusseini and treasured mother Dr. Inas Rashed for their unconditional love and support.

To my precious mother in law, Mrs. Lobna Saleh for her tremendous support during my program.

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Acknowledgments
My sincere gratefulness goes to the following incredible individuals without whom this project would have not been started and
completed.
Dr. Homayoun Zadeh, DDs, PhD, for designing the project and for his tremendous mentorship.
Dr. Kian Kar DDS, MS, for his mentorship in this project and for serving as the chair of my thesis committee.
Dr. Michael Paine BDS, PhD, for accepting me into the master’s program.
Dr. Mahvash Navazesh, BS, DMD, DMD, for helping me to get accepted into the master’s program.
Dr. Casey Chen, DDS, PhD, for being on my thesis committee.
Dr. Parish Sedghizadeh, DDS, MS, for being on my thesis committee.
Dr. Neema Bakhshalian, DDS, PhD, for helping with the usage of the software used in this project.
Dr. Jassem Alsharah, BDS, for participating in this study and for his remarkable help on this project.
Dr. Diana Sedler DDS, MS, for useful discussions about the software used in this project and help during application process.
Dr. Alex Kiss, PhD, for assistance with the statistical analysis.
Dr. Andres Stucky, PhD, for assistance with the statistical analysis.

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Figure Legends and tables list:
Tables
Table 1. Clinical characteristics of study patients and sites.
Table 2. Mean alveolar bone heights pre and post extraction MB, DB and Palatal roots and all
roots collectively measured at buccal, center and palatal positions.
Table 3. Mean changes alveolar bone height at MB, DB and Palatal roots and all roots
collectively measured at buccal, center and palatal positions (from crest to the lowest point of the
sinus).
Table 4. Mean alveolar bone width pre and post extraction at MB, DB and Palatal roots and all
roots collectively measured at 1,2,3 and 5 mm from the crest.
Table 5. Mean changes in alveolar bone width at MB, DB and Palatal roots and all roots
collectively measured at 1,2,3 and 5 mm from the crest.
Table 6. Mean apex to sinus distances (pre) and mean reference line to sinus at MB, DB and
Palatal roots and all roots collectively measured from apex/reference line to shortest distance to
the sinus.
Table 7. Mean Changes in the sinus floor position at MB, DB and palatal roots and all roots
collectively.
Figures
Figure 1. Screen shots from Amira (AMIRA, version 6.5, thermo Fisher Scientific, USA
showing axial view of pre-volume (post untoggled) (A), post-volume (pre-untoggled) (B), both
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volumes toggled before superimposition (C), pre and post volumes superimposed (D).
Figure 2. Screenshots from Amira software showing ( A ) Sagittal view of Pre volume with
ortho-slice bisecting the MB root (post-volume toggled off) , (B) Sagittal view of post volume
with ortho-slice bisecting the crest at the same exact position pre-extraction (pre-volume toggled
off ), ( C) Pre and post extraction volumes superimposed ortho slice bisecting both in same exact
slice number, (D) Ortho-slice MB root, (E) ortho slice post-operative (same slice number and
orientation) and (F) coronal cross section showing both pre and post-operative ortho-slices.

Figure 3. Screenshots from Amira software showing alveolar bone dimensions measured in pre-
and post-extraction CBCTs. (A) Measurements of pre and post-extraction alveolar bone height,
measured at buccal, central and palatal location from the crest to the lowest point of the sinus,
(B) Measurements of pre- and post-extraction alveolar bone width, measured at 1, 2, 3 and 5mm
locations relative to the alveolar crest, (C) Pre-operative apex to sinus distance (post-operative
toggled off) and (D) Post-operative apex reference line (root apex) to post-operative sinus
position. Note: The same exact same slice showing both pre and post-operative volumes.

Figure 4. Bar plot showing mean values for pre- and post-extraction alveolar bone height,
measured at buccal, central and palatal location, as well as percentage change from pre- to post-
extraction.
Figure 5. Bar plot showing the mean values for pre- and post-extraction alveolar bone width,
measured at 1, 2, 3 and 5 mm locations relative to the alveolar crest, as well as percentage
change from pre- to post-extraction.

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Figure 6. Box plots representing alveolar bone and sinus floor dimensions and changes. (A)
Mean values for pre- and post-extraction alveolar bone width and height, as well as sinus floor
positions. (B) Changes from pre- to post-extraction measured for alveolar bone (width and
height), and sinus floor positions.

Figure 7. Scatter plots showing correlation between sinus floor position change and distance
between each root apex to the sinus floor (A) and post-extraction healing time (B).

Figure 8. Scatter plots showing correlation between alveolar bone height change and post-
extraction healing time (A) and age (B).

Figure 9. Scatter plots showing correlation between alveolar width change at all levels from the
crest (1,2,3 and 5mm) and age(A) and post-extraction healing time (B).

Figure 10. Scatter plot showing correlation between sinus floor position change and alveolar
height change.

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Abstract:
Aims:
Dimensional changes of the alveolar ridge crest following tooth extraction has been extensively
studied. However, there is insufficient information in literature about post extraction changes in
the maxillary sinus floor. The aim of the present retrospective study was to evaluate maxillary
sinus floor and alveolar crest dimensional changes, following single maxillary molar extraction
and unassisted socket healing using 3D cone beam computed tomography (CBCT) analysis.
Materials and Methods:
20 Pre- and post-operative CBCTs of 20 individuals, who had maxillary molar tooth extraction
were included. The pre- and post-operative CBCTS were imported to an imaging software
(AMIRA, version 6.5, thermo Fisher Scientific, USA) to construct 3D volumes. The pre and post
3D volumes were superimposed. Coronal sections were made in the center of each root for linear
measurements. The pre-extraction and post-extraction measurements were compared using
paired-sample t-tests. Pearson’s correlation was used to assess the association between the
parameters and the outcome measures. Results were reported as means and standard deviations.
Significance was sought at the p = 0.05 level.
Results:
Linear measurements made at same locations of pre- and post-extraction CBCT images revealed
minute (mean 0.04+ 0.16 mm) and non-significant (p=0.23) differences between the positions of
the maxillary sinus floor at the two time points. In contrast, extensive post-extraction alterations
of the alveolar bone height (3.03+1.45 mm; p=0.000000002) and width (5.89 mm+2.48 mm;
p=0.0000000002) were noted.

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Conclusions:
Within the limitations of the current study, it was concluded that, while alveolar crest underwent
extensive post-extraction dimensional changes, the maxillary sinus floor was remarkably
unchanged. Post-extraction position of the sinus floor was not correlated to patient factors (age,
post-extraction healing time), anatomic factors (proximity of maxillary molar) or to and alveolar
bone dimensional changes.

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1. Introduction

Dimensional changes occurring after extraction of teeth has been widely investigated in
human (Pietrokovski and Massler, 1967), (Schropp et al., 2003), (Chappuis et al., 2013; Van der
Weijden et al., 2009) and animal studies (Araujo and Lindhe, 2005, 2009; Cardaropoli et al.,
2003). A great deal of information has been gained, demonstrating dimensional changes to the
alveolar bone in both horizontal and vertical direction. However, relatively less information is
available on post-extraction healing of molars, in particular maxillary molars, since most
investigators have excluded molars from their analysis.

The posterior maxilla has unique anatomical feature, most prominently, the proximity to the
maxillary sinus. It has been widely believed that maxillary molar tooth extraction is followed by
significant pneumatization of the maxillary sinus floor (Harorh and Bocutoglu, 1995; Ohba et al.,
2001; Rosen and Sarnat, 1955; Wehrbein and Diedrich, 1992). However, most of these studies
have not directly compared the same extraction sites over time. Moreover, whether the changes
in the alveolar bone correlates with any potential alterations to sinus floor position has not been
well studied. Some of the available evidence comes from cross-sectional studies comparing
dentate to edentulous sites (Cavalcanti et al., 2018; Farina et al., 2011; Pramstraller et al., 2011;
Sharan and Madjar, 2008) and others are performed on different populations comparing dentate
to edentulous patients (Wagner et al., 2017). Only in a few studies the same sites were evaluated
to investigate the magnitude of sinus pneumatization after maxillary molar extraction over time
with the use of 3D imaging CBCTs (Lombardi et al., 2018) (Hameed et.al, in press).

In a recent study from our research group alveolar bony changes after extraction of maxillary
12
molars were examined using CBCT images taken at pre- and post-extraction of single maxillary
molars (Hameed et al.2017, in press). The investigators made linear measurements in 2D
sections made from the 3D imaging, using fixed reference points. They reported 3.07±2.5 mm of
alveolar crest loss (p<0.05) and 0.47±0.3 mm of change in sinus floor position in coronal
direction after tooth extraction (p<0.05). In another recent study compared CBCTs taken
immediately after extraction of maxillary molar and 6 months post- operatively. They reported
that the sinus floor moved 1.04±0.67 mm more coronal following unassisted socket healing.
However, these investigators focused on comparison of ridge preservation to spontaneous
healing and did not report on statistical significance of the changes in sinus floor position from
pre extraction- to post extraction in each group. Therefore, the aim of this study was to evaluate
maxillary sinus floor and alveolar crest dimensional changes, following single maxillary molar
extraction, and unassisted socket healing. To achieve that, we used a more refined technique of
superimposing pre- and post-extraction CBCT’s of same sites to investigate alterations of both
sinus floor and alveolar crest formulating the following hypothesis and null hypothesis.

Hypothesis:
Hypothesis 1: Maxillary sinus floor pneumatizes after single maxillary molar extraction.
Hypothesis 2: The proximity of the root apices to the sinus floor correlates to the magnitude of
sinus pneumatization after extraction.

Null hypothesis 1: Maxillary sinus floor position does not change following extraction of single
maxillary molars.
Null hypothesis 2: The proximity of the root apices to the sinus floor is not correlated to post-
13
extraction changes in the sinus floor position.

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2. Materials and Methods

The Institutional Review Board (IRB) of the University of Southern California (USC) approved
this study. The clinical records and CBCT scans of dental patients from Herman Ostrow school
of Dentistry of USC and a private practice were searched. The electronic patient records were
searched to identify patients undergoing maxillary molar tooth extraction and multiple CBCT’s
from March 2009 to December 2017. From 5000 records quarried, those who had undergone
extraction of a maxillary first or second molar, with available pre and post-extraction CBCT
scans were identified.
Study Population and baseline data:
Among over 5000 patient records quarried, 20 patients (9 male and 11 females) met the inclusion
and exclusion criteria. Each patient contributed one tooth extraction site and patient was
considered the unit of analysis. The clinical characteristics of included patients are listed in Table
1. The mean age of the patients was 69.5 + 11.8 years. Thirteen of the sites analyzed were
maxillary first molar (6 right, 7 left), while seven were maxillary second molar (4 right, 3 left).
The mean healing time was 14.8 +16.6 months (range from 2 to 51 months). The reasons for
extraction included caries (N=6), endodontic failure (N=2), advanced periodontitis (N=5),
fracture (N=3), malposition (N=2), external root resorption (N=1) and unknown (N=1). The
medical conditions of the patients are also listed in Table 1. Though smoking was not an
exclusion criterion, none of the patients were smokers. Patient ages, gender, medical history, site
of extraction, reason of extraction are included in table.1.

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Inclusion criteria:
• Single extraction of Maxillary first or second molar at a time.
• Adult patients aged 18-90 years old.
• Single maxillary first or second molar extraction without any ridge preservation or
augmentation procedures.
• Availability of pre- and post-extraction CBCT images.

Exclusion criteria:
• Multiple adjacent simultaneous maxillary molar extractions.
• Socket grafting or augmentation of the extraction site.
• History of sinus or other dento-alveolar surgery.

Medical history, including smoking, was not an exclusion criterion. After inclusion and
exclusion criteria were met, twenty patients (nineteen from USC school of dentistry and one
patient from a private practice) were included. Each patient contributed only one tooth extraction
socket and the patient was considered as the unit of analysis. When patients had two sites on
opposite sides that were eligible for the study, to avoid any bias, a coin was flipped to allocate
the site that would be included in the study. DICOM files acquired during imaging were
imported into AMIRA (version 6.5, thermo Fisher Scientific, USA) for analysis. 3D volumes
were rendered from pre- and post-extraction CBCT data. To facilitate data manipulation, the
volumes were cropped to generate regions of interest (ROI) in specific planes. The boundaries of
the ROI used for cropping of 3D volumes included, the midline of the nasal septum, the superior
roof of the sinus, the zygoma, the occlusal plane of maxillary teeth and the maxillary tuberosity.
16
The pre- and post-operative volumes were each assigned different colors to help to distinguish
these volumes once they were superimposed. The volumes were oriented so that the occlusal
table of the tooth of interest was made parallel to the horizontal plane to facilitate making
orthogonal slices. The two volumes were digitally superimposed using fixed reference points
unaffected by the extraction, such as adjacent teeth, lateral and medial maxillary sinus walls,
palatine process, the floor of the nose and the zygoma. Following manual superimposition to get
the landmarks as close as possible, automatic registration was made, using the “Register Images”
tool of the Amira software (Figure.1 and 2).
An orthogonal slice of the superimposed volumes was created for each of the volumes in the
coronal plane so that the slices used were in the exact same locations of the serial images. The
two separate slices were then connected so that they both act as one slice that allowed navigation
through both CBCTs at the same exact cut, in addition both pre and post cuts could be displayed
at the same time using a single orthogonal slice. This feature also allowed the linear
measurements on the pre-extraction CBCT scan to act as a reference for measuring the post-
extraction changes since now the same exact slice is used for pre and post extraction
measurements (Figure.2 A-C.). Subsequently the following linear measurements were repeated
on all three roots of each tooth; i.e. mesio-buccal (MB), disto-buccal (DB), and palatal (P) at pre
and post-extration time points, using the highest point of the apex of each root as a reference
(Figure.3):
1. Pre-operative vertical alveolar height: Measured from alveolar crest to the lowest point of
the sinus floor at buccal, palatal and center (exactly midway between buccal and palatal
measurements), repeated at each root (Figure 3.A, measurements in black).
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2. Post-operative vertical alveolar height (using pre-operative measurements as reference
lines): Measured from alveolar crest to the lowest point of the sinus floor at buccal,
palatal and center (exactly midway between buccal and palatal measurements), repeated
at each root. (Figure 3.A, measurements in white).
3. Pre-operative horizontal alveolar width: Measured at 1, 2, 3 and 5 mm from the alveolar
crest, repeated for each root. (Figure 3.B, measurements in black).
4. Post-operative horizontal alveolar width (using pre-operative measurements as reference
lines): Measured at 1, 2, 3 and 5 mm from the alveolar crest, repeated for each root.
(Figure 3.B, measurements in white).
5. Pre- operative Apex to sinus (SF-1): the shortest distance from the apex to sinus floor).
(Figure 3.C).
6. Post-operative reference line to sinus (SF-2): the reference line represents the pre-
operative apex position. (Figure 3.D).
The following linear changes were calculated from the pre- and post-extraction distances for
all three roots (all measurements made on coronal sections) (Figure 3.):

Statistical analysis
Descriptive statistics were calculated for all variables of interest. Continuous measures such as
age were summarized using means and standard deviations whereas categorical measures were
summarized using counts and percentages. Correlations between variables of interest (correlation
of sinus floor position change to alveolar dimensional changes, age and healing time, in addition
to correlation of dimensional changes to age and healing time) were run using Pearson
18
correlation coefficients. Results were reported as correlation coefficients and their associated p-
values. Changes over time in variables of interest (Sinus position, alveolar ridge height and
alveolar ridge width) were assessed using paired t-tests and their associated p-values. All
analyses were run using SAS Version 9.4 (SAS Institute, Cary, NC, USA).

Statistical analysis was done to compare the following parameters:
1. Mean pre-extraction sinus floor position of all three roots together versus mean post
extraction sinus floor position of all three roots collectively.
2. Mean pre-extraction vertical height of all roots versus mean post-extraction vertical height of
all roots at all sites combined (Buccal, Palatal, central).
3. Mean pre-extraction vertical buccal measurement of all roots versus mean post-extraction
vertical buccal measurement of all roots.
4. Mean pre-extraction vertical central measurement of all roots versus mean post-extraction
central measurement of all roots.
5. Mean pre-extraction vertical palatal measurement of all roots versus mean post-extraction
vertical palatal measurement of all roots.
6. Mean pre-extraction horizontal ridge width of all roots versus mean post- extraction
horizontal ridge width of all roots, at all levels from the crest combined (1 mm,2 mm,3 mm
& 5 mm)
7. Mean pre-extraction horizontal ridge width at 1mm measurement from crest of all roots
versus mean post- extraction horizontal ridge width at 1 mm measurement of all roots.
8. Mean pre-extraction horizontal ridge width at 2 mm measurement from crest of all roots
versus mean post- extraction horizontal ridge width at 2 mm measurement of all roots.
19
9. Mean pre-extraction horizontal ridge width at 3 mm measurement from crest of all roots
versus mean post- extraction horizontal ridge width at 3 mm measurement of all roots.
10. Mean pre-extraction horizontal ridge width at 5 mm measurement from crest of all roots
versus mean post- extraction horizontal ridge width at 5 mm measurement of all roots.
11. Comparing pre and post extraction changes between MB versus DB versus P roots:
a) Mean height change (buccal, center, palatal collectively), comparing all three roots to
each other.
b) Mean pre and post extraction height change at buccal crest, comparing all three roots
to one another.
c) Mean pre and post extraction height change at the palatal crest, comparing all three
roots to one another.
d) Mean pre and post extraction width change (1,2,3 and 5 mm collectively), comparing
all three roots to one another.
12. Change in height of MB root (pre versus post extraction), DB root (pre versus post
extraction) and Palatal (pre versus post extraction).
13. Change in width of MB (pre versus post extraction), DB (Pre versus post extraction) and
palatal (pre versus post extraction).
14. Change in sinus floor position of MB (pre versus post extraction), DB (Pre versus post
extraction) and palatal (pre versus post).
15. Correlation between healing time and sinus changes.
16. Correlation between age and sinus changes.
17. Correlation between apex to sinus distance and sinus changes
18. Correlation between healing time and height changes.
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19. Correlation between age and height changes.
20. Correlation between height changes and sinus changes.
21. Correlation between healing time and width changes.
22. Correlation between age and width changes.

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3. Results

Following superimposition of the pre- and post-extraction CBCT’s, alveolar bone dimensional
changes, as well as sinus floor position changes were measured relative to each of the 3 roots.
The mean alveolar height changes of all roots measured at 3 different locations, i.e. buccal,
center and palatal positions was 3.03+1.45 mm and was statistically significant
(p=0.000000002). No statistically significant differences were found between the MB, DB and P
roots in regard to the amount of vertical height loss, however the change at each root was
statistically significant (Table.3). The mean alveolar bone height pre-extraction of all roots
collectively, measured at buccal, central and palatal locations were 10.59±4.44 mm (buccal)
10.59±4.37 mm (center) and 10.52±4.43 mm (palatal). After extraction the corresponding values
were 5.51±4.96 mm (buccal), 9.08±4.51 mm (center) and 8.09±4.25 mm (palatal) (Table 2.). The
mean percentage change of all roots collectively at buccal 47.96 %, center 14.74% and palatal
23.09% measurements of all roots (Figure 4.). The mean change of vertical height at buccal,
central and palatal measurement were all statistically significant, 5.08±3.40 mm (p=0.0000002),
1.57±1.08 mm (p=0.0000003), 2.43±1.57 mm (p=0.0000001) (Figure 4.).

When buccal measurement height changes were separately compared between roots the MB root
(6.74±5.65 mm change) lost more height than DB root (4.85±3.70 mm change) (p=0.03) and
palatal root (3.66±2.82 mm change) (p=0.03) but no differences was found between DB and P
roots (p=0.12). When height changes at the palatal measurement were separately compared
between different roots the only statistical difference was found between MB (1.71±1.47 mm
change) and palatal (3.04±2.09 mm change) (p=0.02) with more bone loss on palatal root. The
DB palatal measurement was not statistically different when compared to the same palatal
22
measurement of the other two roots (2.55±2.21 mm change).

Horizontal width changes were measured at each root at 1, 2, 3 and 5 mm levels from the
alveolar crest. The mean horizontal width changes of all levels from crest (5.89±2.48 mm) were
statistically significant (p=0.0000000002) (Table 5.). The width changes of the Mesio-buccal
root (5.08±2.26 mm) was statistically significant (p=0.03) compared to the disto-buccal
(6.69±3.39 mm). The width change at the palatal root was 5.9±3.11mm and was not statistically
different from MB root (p=0.23) or DB root (p=0.29). The horizontal mean values for pre-
extraction alveolar bone width at 1mm distance from the crest was 11.74±1.39 mm, 12.63±1.10
mm at 2 mm from crest, 13.44±1.26 mm at 3 mm from crest and 14.29±1.31 at 5 mm from crest.
After extraction the corresponding values were 2.29+2.26 mm at 1mm from crest, 5.48±3.32 mm
at 2 mm, 8.64±3.47 mm at 3 mm and 11.51±2.35 mm at 5mm (Figure 5.). The mean percentage
change of width at the same locations were 75.12% at 1 mm, 56.61 % at 2 mm, 35.71% at 3 mm
and 19.45% at 5 mm from alveolar crest. (Figure 5.). The mean change of horizontal width in
millimeters at 1,2,3 and 5 mm were all found to be statistically significant at all levels from the
crest, 8.82±2.46 mm at 1mm (p=0.0000000000001), 7.15±3.40 mm at 2 mm (p=0.000000001),
4.8±3.24 mm at 3mm (p=0.0000002), 2.78±2.01 mm at 5mm (p=0.0000005) (Figure 5.).

Sinus floor position pre- extraction was measured from the highest point of the apex to closest
distance to the sinus floor; post extraction the reference of the apex position was used to measure
the position changes of the maxillary sinus floor. The mean sinus floor changes (0.04±0.16 mm)
were not statistically significant (p=0.23) (Table 7.). No changes in the sinus floor position were
found in 85% of the evaluated teeth (Figure 6.). The changes occurred in three instances and 2 of
23
which the sinus moved in an apical position after peri-apical infection and membrane thickening
resolved as a result of extraction of the teeth.

The results from Pearson’s correlation tests revealed that age, healing time (figure 7A.) and apex
to sinus distance (figure 7B.) and the magnitude of dimensional changes (vertical) of the crest
were not correlated with sinus floor position changes (Figure 10). Moreover, age and healing
time were also not correlated to the magnitude of dimensional changes that took place (vertical
and horizontal) of the alveolar crest (Figure 8 and 9).

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4. Discussion

It has long been an accepted view that the maxillary sinus undergoes significant pneumatization
following maxillary molar extraction; though the evidence is often weak or indirect (Harorh and
Bocutoglu, 1995; Ohba et al., 2001; Rosen and Sarnat, 1955; Wehrbein and Diedrich, 1992).
Some of the limitations of the published reports on post-extraction sinus floor changes include:
1) Using two-dimensional methodology to study the position of the maxillary sinus (Crespi et al.,
2009; Lang et al., 1994; Levi et al., 2017; Moya-Villaescusa and Sanchez-Perez, 2010; Schropp
et al., 2003)
2) Comparing different patient populations in cross-sectional manner to conclude sinus floor
changes (Wagner et al. 2017)
3) Comparing edentulous sites to contra-lateral dentate sites (Cavalcanti et al., 2018; Farina et
al., 2011; Pramstraller et al., 2011; Sharan and Madjar, 2008). Only few studies have utilized 3D
imaging to compare pre- and post-extraction CBCT’s of the same maxillary molar site
(Lombardi et al., 2018) (Hameed,et al. in press) .

Often, alveolar crestal resorption, which also limits the availability of vertical bone volume in
posterior maxilla is managed with sinus augmentation. Some studies have reported that the need
for sinus augmentation after ridge preservation was reduced (Rasperini et al., 2010). However,
these studies have not directly measure sinus floor position changes. Therefore, the question of
post-extraction maxillary sinus pneumatization and the effect of alveolar ridge preservation, if
any, remain unanswered. The question thereafter is what is the magnitude of the changes that
occur in the sinus floor post extraction, how much these changes affect the available bone after
extraction, and if there is a way to reduce these changes.
25

In a recent study on unassisted healing of extraction socket, Hameed, et al. (in press) have
reported that only minimal (0.47mm±0.32), though statistically significant, maxillary sinus floor
changes occurred following maxillary molar extraction. In contrast, relatively large vertical
alveolar crest changes (3.07 mm±2.53) were observed. A limitation of this study was that linear
measurements were made relative to reference points on the pre- and post-operative CBCT
images. To overcome this limitation, the present study superimposed the CBCTs taken at two
different time points so that measurements were made at exact locations. The results of the
present study showed extremely small changes to the sinus floor position (0.04±0.16mm;p=0.23)
following single maxillary molar extraction, a change that was not statistically significant. We
also observed relatively large and statistically significant changes to the alveolar bone height
(3.03 +1.45mm; p=0.000000002) and width (5.89 +2.48mm; p=0.0000000002).

In a recent prospective randomized controlled clinical trial, the effect of alveolar ridge
preservation on sinus floor pneumatization and alveolar bone changes was tested (Lombardi et
al., 2018). Unlike in our study where the CBCT’s were taken before extraction and the post-
extraction at different timelines representing different healing periods, in Lombardi study the
baseline CBCT’s were preformed immediately after extraction and post extraction CBCT’s were
taken after 6 months healing. In our study we superimposed pre and post CBCT’s as one unit, a
technique that was found to be accurate and reproducible by Koerich (Koerich et al., 2016).
Even though their CBCTs were superimposed, using the same software used in our study
(Amira, Thermo Fisher Scientific, USA) the superimposed images were then imported to Fiji
software (Schindelin et al., 2012) for linear measurements. In our current study, however, both
26
superimposition and linear measurements were done on the same 3D (Amira, Thermo Fisher
Scientific, USA). In Lombardi study it was reported that maxillary sinus floor expansion in
coronal direction after extraction to be 0.69±0.48 mm in the ridge preservation group and
1.04±0.67 mm in the unassisted healing group with no statistical significance found (p=0.15) and
a difference between groups being only 0.35±0.19mm. The same group found that vertical and
horizonal changes are not statistically significant between the two groups, with difference
between groups 0.34 ±0.35 for vertical change and 0.9±0.56mm horizontal width change.
Albeit no statistical significance was achieved between any of the parameters, the authors
concluded that alveolar ridge preservation performed after maxillary molar extraction may
reduce the entity of sinus pneumatization and alveolar bone resorption, compared to unassisted
socket healing and that this technique could decrease the necessity of advanced regenerative
procedures prior to dental implant placement in posterior maxilla. It is also surprising that
statistical analysis between pre and post treatment outcomes of each group separately was not
included in their study.

In our study however, pre and post extraction measurements of the sinus floor position after
unassisted healing was compared and it was found that the mean changes were negligible with
no statistical significance (mean=0.04±0.16, p=0.23). Furthermore, it was observed that sinus
floor position does not always move in a coronal direction, in two out of the twenty cases, the
sinus position moved in an apical direction after extraction. Both cases had periapical lesions and
the resolution of that following post-extraction healing was accompanied by bone gain in apical
region.

27
The superimposition of CBCT scans using different imaging applications has been used to
assess orthopedic and surgical outcomes (Cevidanes et al., 2005; Claus et al., 2019; De
Clerck et al., 2012; de Paula et al., 2013; Ryckman et al., 2010). Koerich et al (Koerich et al.,
2016) tested the validity and reproducibility of superimposing CBCT’s scans. In this study, the
accuracy and reproducibility of the superimpositions were assessed using the repeated closest
point technique to measure the root mean square (RMS) distance between the images. An RMS
more than or equal to 0.25 was considered successful. Intra-class correlation coefficient (ICC)
were used to compare the intra-observer measurement reproducibility. The ICC was ³ 0.980 for
all of the variables and the highest RMS found was 0.241. The inter-observer reproducibility of
each case was assessed and was perfect (RMS 0) for 68% (23 out of 34) of the superimpositions
done and not clinically significant (RMS £ 0.25) for the other 32%. The authors concluded, that
superimposition of CBCT’s is an accurate and reproducible method.

In another study the bone changes were evaluated three-dimensionally following ridge
preservation procedures (RPP) using computed tomography (CT) (Clozza et al., 2012). A total of
32 alveolar sites were analyzed where several patients contributed with more than one socket of
single rooted teeth maxillary and mandibular teeth (mean of 2.33 sockets per patient) and each
patient was defined as the statistical unit. In this study the CT scans were obtained at 1 week
(initial) and 3 months (final) after ridge preservation with Bio-active glass.

The initial and final
CT scans were superimposed according to the method previously described by Ryckman et al
(Ryckman et al., 2010)
.
The authors stated the software allowed them to make linear
measurements directly from the 3D models however, detailed explanation of whether the single
rooted teeth analyzed were incisors, cuspid or bicuspids and where the measurements were
28
exactly done was not reported. Their results showed that alveolar sites treated with RPP
demonstrated a preservation of about 77% of the original width dimensions, with a mean loss of
1.8 ± 1.1 mm in width. Moreover, it was observed that the vertical loss of buccal bone was 2.7 ±
1.1 mm, while the loss of lingual bone was 1.9 ± 1.2 mm. The lack of control in the study was
considered as one of its limitations mentioned by the authors. Additionally, the use of CT scans
might be considered inappropriate due to the accumulative radiation dose to the head and neck
area, and its financial cost. Albeit the design of this study is difficult to reproduce, it provides
evidence of feasibility and applicability of superimposing CT scans of the same region of interest
from two separate time points which could improve the accuracy of the assessment of our dental
treatment outcomes utilizing CBCT’s.

In a systematic review on the alveolar bone dimensional changes of post-extraction sockets in
humans (Tan et al., 2012), only six studies out of 20 included molars in their analysis. The meta-
analysis was conducted only for 6 re-entry studies and non-of which included molars. The results
showed dimensional changes in a horizontal (3.79 ± 0.23 mm) direction were more than vertical
(1.24 ± 0.11 mm on buccal, 0.84 ± 0.62 mm on mesial and 0.80 ± 0.71 mm on distal sites) at 6
months. The percentage of vertical and horizontal dimensional change after 6 months was 11–
22% and 29–63% respectively. A few studies in literature have looked at the dimensional
changes of the same sites after molar teeth extraction, four of which used periapical radiographs
to measure vertical height changes (Crespi et al., 2009; Lang et al., 1994; Moya-Villaescusa and
Sanchez-Perez, 2010; Schropp et al., 2003), one used stents (Rasperini et al., 2010) and three
used CBCT’s (Kerr et al., 2008; Lombardi et al., 2018) (Hameed et.al 2019, in press) to assess
the magnitude of alveolar dimensional changes. In the study by Kerr et al., however, multiple
29
tooth types were included to evaluate the effect of ultrasound on the dimensional changes post
extraction and were pooled together for the analysis: three pairs of incisors, one pair of canines,
three pairs of premolars, and five pairs of molars. Moreover, it was not clear if the molars
included were maxillary or mandibular and there was no information about sinus floor changes
post extraction of maxillary molars. Therefore, there is scarcity in literature about the magnitude
of dimensional changes of bone in posterior maxilla utilizing three-dimensional analysis.

Our current study is challenged with several limitations, including the retrospective study design,
which precluded a pre-determined study protocol, with respect to patient population, extraction
technique, and healing time. The status of the remaining alveolar bone post-extraction such as
partial or total loss of buccal bone, dehiscence’s and remaining bone thickness is not known..
Secondly, the number of included cases was relatively small, which might have contributed to
the lack of correlation between all parameters. However, CBCTs are not routinely taken prior to
tooth extraction, over 5000 records had to be examined to identify 20 cases. Thirdly, since the
CBCT was taken prior to tooth extraction, any bone loss that could have occurred during
extraction cannot be distinguished from post-extraction dimensional alterations. These potential
confounding effects are likely to have affected the crestal changes and not sinus floor position
changes. Another limitation of the study is that some of the single extraction sites were bound by
the presence of the mesial and distal adjacent teeth and some patients had one adjacent tooth
missing next to the extraction site. Moreover, on some patients first molar sites were evaluated
and in others second molar sites were evaluated. The anatomical variation between first and
second molars can influence the alveolar bone remodeling considering variability in length of the
root trunk, divergence of the roots, presence, absence, or the volume of the furcation bone.
30
Evaluating the correlation of these factors to the post extraction bone remodeling would be an
interesting topic for future studies.

Clinicians usually request CBCT’s of their patients after extraction for the purpose of replacing the
missing teeth with implants, a time point at which the vertical height from the crest to the sinus floor
had already reduced due to crestal resorption and subsequently assume that the sinus had
pneumatized. The results of the current study demonstrate that the position of the sinus floor
remained unchanged in 85% of the cases and the changes that took place were not clinically and
statistically significant. Within the limitations of this study, the first null hypothesis could not be
rejected. If the sinus floor is at close proximity to the crest of the ridge before extraction and if
the sinus floor does not change post-extraction, the need for sinus lifting may be inevitable even
after attempting ridge preservation since the grafting in these instances is limited to the available
height of the socket wall coronally and the sinus floor position apically.

To date there is limited evidence to support or refute the use of alveolar ridge preservation for
maxillary molars and if its use reduces the need for further sinus augmentation. Most of the
available literature and systematic reviews comparing alveolar ridge preservation to unassisted
socket healing is mainly on anterior maxilla (Avila-Ortiz et al., 2019; Avila-Ortiz et al., 2014;
Mardas et al., 2015; Troiano et al., 2018). The articles that include molars in analysis do not
distinguish if the included molars were maxillary or mandibular. Additionally they do not report on
the effect of alveolar ridge preservation on sinus pneumatization and finally do not utilize 3D
analysis (Alissa et al., 2010; Barone et al., 2013; Barone et al., 2017a; Barone et al., 2017b;
Cardaropoli et al., 2014, 2015; Cardaropoli et al., 2012; Guarnieri et al., 2017; Iorio-Siciliano et al.,
31
2017; Schropp et al., 2003). The only randomized controlled clinical trial on maxillary molars solely
comparing socket grafting to spontaneous healing using CBCT’s found there was no statistically
significant differences between groups in regard to sinus changes and dimensional changes of the
crest (Lombardi et al., 2018). More randomized controlled clinical trials utilizing 3D analysis to
compare the outcomes of ridge preservation to unassisted healing of maxillary molars are needed.

32
5. Conclusions

Within the limitations of the current study, it is concluded that, while alveolar crest underwent
extensive post-extraction dimensional changes, the maxillary sinus floor was remarkably stable.
Post-extraction position of the sinus floor was not apparently correlated to patient’s age, post-
extraction healing time, proximity of maxillary molar or to alveolar bone dimensional changes.
33

6. Figure legends and Tables

Table.1 Clinical characteristics of the study patients and sites

Parameter Value
Subjects (n) 20 (9 male, 11 female)
Teeth (n) 20 (13 first, 7 second)
Age (years) Mean 69.4 + 11.8 SD
Max first molar N= 13 (6 right, 7 left)
Max second molar N= 7 (4 right, 3 left)
Healing time (months) Mean 14.82 +16.56 SD
(range 2 to 51 months)

Reason for extraction

Caries (N=6)
Endodontic lesion (N=2)
Advanced periodontitis (N=5)
Fracture (N=3)
Malposition (N=2)
External root resorption (N=1)
Unknown (N=1)

Medical History
Smoking (N=0)
Hypothyroidism (N=1)
Asthma (N=3)
Anxiety and depression (N=2)
Hypertension (N=11)
Cardiovascular disease (N=5)
Allergy (Penicillin, codeine,
betadine, latex) (N=3)
Arthritis (Rheumatoid arthritis, osteoarthritis) (N=3)
Diabetes mellitus II (N=2)
34

Table 2. Mean alveolar bone heights pre and post extraction MB, DB and Palatal roots and all roots
collectively measured at buccal, center and palatal positions.

Roots
Pre-extraction alveolar bone Height Post-extraction alveolar bone Height
Mean Median Min Max SD Mean Median Min Max SD

MB
Buccal 10.86 9.75 5.56 17.89 4.53 4.12 0 0 17.70 5.80
Central 10.98 9.92 3.73 17.89 4.68 9.71 9.13 1.95 17.89 4.70
Palatal 11.15 10.79 4.12 18.86 4.72 9.45 9.61 2.73 18.86 4.93
Mean of
3 positions
11.00 10.09 4.47 18.21 4.57 7.76 6.88 1.56 17.32 4.27

DB
Buccal 9.92 9.34 3.25 18.96 4.90 5.07 4.20 0 18.96 5.01
Central 10.45 8.85 4.43 19.03 4.30 8.67 7.07 2.69 18.40 4.55
Palatal 10.21 8.95 3.93 18.83 4.51 7.67 6.40 3.20 16.78 4.11
Mean of
3 positions
10.19 8.61 4.24 18.79 4.45 7.14 5.44 3.67 18.05 4.10

Palatal
Buccal 11 9.48 5.07 21.27 4.67 7.34 6.70 0 21.27 5.90
Central 10.53 9.54 3.14 20.81 4.87 8.84 7.43 2.24 20.81 4.81
Palatal 10.20 9.56 4.94 20.34 4.69 7.16 6.11 2.48 19.42 4.43
Mean of
3 positions
10.57 9.43 4.38 20.81 4.62 7.79 6.28 2.44 20.50 4.76

All
Roots
Buccal 10.59 9.72 5.36 19.31 4.44 5.51 4.19 0 19.31 4.96
Central 10.59 9.29 3.79 18.88 4.37 9.08 7.65 3.73 18.88 4.51
Palatal 10.52 9.51 4.72 19.21 4.43 8.09 6.87 3.21 17.68 4.25
Mean of
3 roots
10.59 9.57 4.62 19.13 4.32 7.56 6.09 2.78 18.62 4.20
Measured from alveolar crest of each root to the sinus floor in the coronal orthogonal sections.
35

Table 3. Mean changes alveolar bone height at MB, DB and Palatal roots and all roots
collectively measured at buccal, center and palatal positions (from crest to the lowest point of the
sinus).

Item Total alveolar bone height change
Roots Mean Median Min Max SD P-Value
MB 3.24 2.97 0 6.76 1.97 0.00000006
DB 3.06 2.80 0.55 5.92 1.70 0.00000001
Palatal 2.79 2.91 0.31 5.16 1.40 0.000000003
Mean of 3 roots 3.03 3.23 0.51 5.41 1.45 0.000000002
36

Table 4. Mean alveolar bone width pre and post extraction at MB, DB and Palatal roots and all
roots collectively measured at 1,2,3 and 5 mm from the crest.

Roots
Pre-extraction alveolar crest width Post-extraction alveolar Crest width
Mean Median Min Max SD Mean Median Min Max SD

MB
1mm 11.28 11.01 8.02 13.86 1.58 3.99 3.35 0 12.83 3.86
2mm 11.98 11.93 9.11 14.18 1.52 5.70 5.63 0 10.81 3.38
3mm 12.71 12.40 10.14 15.73 1.49 8.67 8.59 0 14.52 3.05
5mm 13.55 13.22 11.40 17.19 1.58 10.83 10.97 4.98 16.58 2.62
MB Mean of all levels 12.38 12.32 9.78 14.03 1.36 7.30 7.49 2.21 11.19 2.32

DB
1mm 12.15 12.23 7.30 15.58 1.72 2.24 0 0 10.39 3.24
2mm 13.11 12.82 11.09 16.61 1.34 5.28 6.61 0 12.18 4.54
3mm 13.81 13.73 11.77 16.27 1.27 7.90 8.93 0 13.81 4.72
5mm 14.55 14.58 11.97 16.97 1.41 11.45 10.91 6.36 15.83 2.83
DB Mean of all levels 13.40 13.20 10.55 16.05 1.31 6.72 7.36 1.59 12.33 3.48

Palatal
1mm 11.80 11.92 5.97 14.91 1.92 2.53 0 0 8.71 3.25
2mm 12.82 12.92 8.68 14.92 1.53 5.45 6.61 0 12.04 4.54
3mm 13.79 13.62 11.30 17.26 1.73 9.35 10.39 0 14.62 4.25
5mm 14.79 14.52 12.24 17.52 1.49 12.25 11.66 6.98 17.58 2.60
Palatal Mean of all levels 13.30 13.22 10.05 15.76 1.44 7.40 7.55 1.75 12.10 3.14
Mean
width
of all
roots
1mm 11.74 11.57 8.89 14.28 1.39 2.92 2.97 0 6.32 2.26
2mm 12.63 12.50 10.80 15.05 1.10 5.48 4.49 0.85 11.13 3.32
3mm 13.44 13.21 11.41 16.42 1.26 8.64 9.49 2.37 14.32 3.47
5mm 14.29 14.37 11.93 17.23 1.31 11.51 10.90 7.61 16.66 2.35

37

Table 5. Mean changes in alveolar bone width at MB, DB and Palatal roots and all roots
collectively measured at 1,2,3 and 5 mm from the crest.

Item Alveolar bone width Change
Roots Mean Median Min Max SD P-Value
MB 5.08 4.67 1.39 9.45 2.26 0.0000000005
DB 6.69 6.17 1.55 12.81 3.39 0.000000004
Palatal 5.9 5.26 2.23 11.59 3.11 0.000000007
Mean of 3 roots 5.89 5.66 2.78 10.37 2.48 0.0000000002
38

Table 6. Mean apex to sinus distances (pre) and mean reference line to sinus at MB, DB and
Palatal roots and all roots collectively measured from apex/reference line to shortest distance to
the sinus.

Item Distance from Apex to sinus pre = SF1 Distance from reference line to sinus post=SF2
Roots Mean Median Min Max SD
Mean Median Min Max SD
MB 4.66 3.95 0 11.18 3.52
4.66 3.95 0 11.18 3.52
DB 4.23 3.77 0 13.17 3.53
4.21 3.77 0 13.17 3.53
Palatal 2.72 1.83 0 10.74 3.16
2.87 1.94 0 10.74 3.06
Mean
of all Roots
3.87 3.66 0 11.02 3.17
3.91 3.66 0.22 11.02 3.13
39

Table 7. Mean Changes in the sinus floor position at MB, DB and palatal roots and all roots
collectively.

Item Sinus Floor position Change
Roots Mean Median Min Max SD P-Value
MB 0 0 0 0 0 0.0
DB -0.01 0 -0.25 0 0.06 0.32
Palatal 0.15 0 0 2 0.48 0.19
Mean of 3 roots 0.04 0 -0.08 0.67 0.16 0.236
40

Figure 1.

41

Figure 2.

42

Figure 3.

43

Figure 4.

44

Figure 5.

45

Figure 6.

46

Figure 7.

47

Figure 8.

48

Figure 9.

49

Figure 10.

50

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Abstract (if available)

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University of Southern California Dissertations and Theses

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Asset Metadata

Creator Elhusseini Ahmed, Sara Safeyeldin (author)

Core Title 3D volumetric analysis of post extraction maxillary sinus floor changes: a retrospective CBCT analysis

School School of Dentistry

Degree Master of Science

Degree Program Craniofacial Biology

Publication Date 08/14/2019

Defense Date 05/22/2019

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

Tag alveolar bone,alveolar bone changes,cone beam computer tomography,maxillary sinus,OAI-PMH Harvest,sinus pneumatization,tooth extraction

Format application/pdf (imt)

Language English

Contributor Electronically uploaded by the author (provenance)

Advisor kar, kian (committee chair)

Creator Email sarasafeyeldin@gmail.com,selhusse@usc.edu

Permanent Link (DOI) https://doi.org/10.25549/usctheses-c89-212619

Unique identifier UC11663130

Identifier etd-Elhusseini-7777.pdf (filename),usctheses-c89-212619 (legacy record id)

Legacy Identifier etd-Elhusseini-7777.pdf

Dmrecord 212619

Document Type Thesis

Format application/pdf (imt)

Rights Elhusseini Ahmed, Sara Safeyeldin

Type texts

Source University of Southern California (contributing entity), University of Southern California Dissertations and Theses (collection)

Access Conditions The author retains rights to his/her dissertation, thesis or other graduate work according to U.S. copyright law. Electronic access is being provided by the USC Libraries in agreement with the a...

Repository Name University of Southern California Digital Library

Repository Location USC Digital Library, University of Southern California, University Park Campus MC 2810, 3434 South Grand Avenue, 2nd Floor, Los Angeles, California 90089-2810, USA