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Rate of bone loss in furcation-involved molars: a retrospective analysis

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Rate of bone loss in furcation-involved molars: a retrospective analysis

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RATE OF BONE LOSS IN FURCATION-INVOLVED MOLARS:
A RETROSPECTIVE ANALYSIS

by

Clara S. Kim

A Thesis Presented to the
FACULTY OF THE USC GRADUATE SCHOOL
UNIVERSITY OF SOUTHERN CALIFORNIA
In Partial Fulfillment of the
Requirements for the Degree
MASTER OF SCIENCE
(CRANIOFACIAL BIOLOGY)

August 2010

Copyright 2010 Clara S. Kim

ii
Dedication

This thesis is dedicated to my family and friends whom I am greatly indebted for
their love and support. A very special thank you to my mother who has been a source of
encouragement and inspiration to me throughout my life, you have actively supported me
in my determination to find and realize my potential.

iii
Acknowledgements
I would like to first thank my director, Dr. Hessam Nowzari, whose steadfast
support of this project was greatly needed and deeply appreciated. I would also like to
thank Dr. Sandra Rich; her sage advice, insightful criticisms, and patient encouragement
aided the writing of this thesis in innumerable ways. I would also like to thank Dr.
Mahvash Navazesh for providing me invaluable advice on my research.

iv
Table of Contents
Dedication ii
Acknowledgements iii
List of Tables v
List of Figures vi
Abstract vii
Chapter 1: Introduction 1
Chapter 2: Materials and Methods 8
Chapter 3: Results 16
Chapter 4: Discussion 23
Chapter 5: Conclusion 37
Bibliography 38

v
List of Tables
Table 1: Demographic Characteristics of the Study Population 17
Table 2: Tooth Characteristics of the Study Population 17
Table 3: Summary of Bone Loss according to Parameters 20

vi
List of Figures
Figure 1: Identified Anatomical Landmarks 13
Figure 2: Using ImageJ to Measure Total Root Length 14
Figure 3: Overall Bone Loss as % of Total Root Length 18
Figure 4: Annual Bone Loss as % of Total Root Length 19
Figure 5: Effect of Gender, Age, Systemic disease, Interproximal restoration 21
and Adjacency to another tooth on % Bone Loss (Total Root Length)
Figure 6: Effect of Periodontal Recall on Bone Loss 22

vii
Abstract
Background: Periodontal attachment loss around multi-rooted teeth can lead to exposure
of furcation sites and colonization of periodontopathogens. Furcation-involved teeth are
often given a poor prognosis and are considered unpredictably responsive to conventional
treatments. Objective: To determine radiographic bone loss patterns over time, testing the
hypothesis that bone loss in furcation sites is more rapid and extensive than that at
interproximal sites. Methods: Existing radiographs were analyzed to compare rate of
bone loss between furcation and interproximal sites of the same tooth. Selection criteria
included mandibular molars with furcation involvement and a minimum follow-up of 5
years. Using ImageJ software, anatomical landmarks (CEJ, furca, apex) were located and
measured corono-apically. P-values for differences between interproximal and furcation
bone loss and sub-groups associations were calculated using Wilcoxon signed-rank test.
Results: Follow-up time for 29 teeth from 19 patients ranged from 5 to 12 years (mean =
6.3 years). Bone level change over time averaged 4.22 % + 2.49 (range: 0.04 – 13.9) for
interproximal sites and 4.55% + 2.84 (range: 0.49 – 15.52) for furcation sites. Significant
bone loss (p < 0.05) was noted in furcation sites for the non-compliant sub-group. No
other sub-group variables were associated with bone loss. Conclusion: In this study, there
were no overall significant differences in bone loss over time between furcation sites and
interproximal sites of the same tooth.

1
Chapter 1: Introduction
Periodontal attachment loss around multi-rooted teeth can progressively lead to
exposure of the furcation area. The furcation-involved teeth are generally not amenable
to definitive management with conventional periodontal procedures (Kalkwarf et al. 1988,
Parashis et al. 1993). Even for the most dedicated patients and practitioners, furcation
involvement frequently perpetuates marginal inflammatory changes and can cause
continuous periodontal breakdown. Thus, the furcation area raises a considerable
challenge in treatment and in clinical management.
Historically, furcation-involved molars are reported to respond less favorably to
various alternative therapies and are at greater risk for further attachment loss compared
with singled rooted teeth (Nordland et al. 1987, Loos et al. 1989, Wang et al. 1994).
Hirschfeld & Wasserman (1978) reported that over a 22-year period there was a loss of
31.4% of molars compared to 4.9% of single-rooted teeth. Even without periodontal
surgeries, deep probing depths around the single-rooted teeth responded favorably and
predictably to gross debridement whereas molars that received additional surgical
treatments still had higher mortality rate. Wang et al. (1994) studied changes in
attachment loss on molars with furcation involvement for a period of 8 years. He found
that even with surgical procedures and a strict periodontal maintenance system, teeth with
furcation involvement were 2.5 times more like to lose attachment compared to teeth
without furcation involvement. Waerhaug (1980) reported that nonfurcation surfaces of
molars respond better to non-surgical therapy and treatment failures have been associated
with incomplete root surface debridement in furcation areas. He found marginal

2
gingivitis and amount of subgingival plaque to be greater on surfaces facing furcation
than outside surfaces. Even following debridement procedures, furcation sites showed
less reduction of bacterial counts compared with nonfurcation sites. The reduced success
rate of nonsurgical and surgical treatment of furcation is proposed to be related to
constrictive anatomical characteristics of the furcation area interfering with adequate
debridement along with many other factors. Thereby, the exposed furcation area
continues to accumulate plaque and calculus and provides a challenging surface for long
term management (Everett et al. 1958, Bower 1979, Svardstrom & Wennstrom 1988).
Additionally, studies have found plaque retentive features (Lang et al. 1973, Fleisher et al.
1989, Waerhaug 1980, Kornman 1987), variation on anatomy (Al-Shammari et al. 2001),
and higher number of bacteria associated with inflammation in the furcation area. Leon
et al. (1987) evaluated responses of 33 furcated molars after scaling using gingival
crevicular fluid flow and dark-field microscopy. Less severe class I furcations were
evaluated as having significantly more coccoids and motile rods, whereas more
spirochetes and total motiles were found in deeper class III furcations. When teeth were
hand-scaled, class I furcations achieved normal healthy flora at 2 and 4 weeks, but class
II and III furcations had a significantly higher number of total motiles, which are
associated with inflammation. Limited hygienic accessibility on these furcation-involved
molars may predispose teeth for vulnerability to a high caries rate as well as result in
subsequent release of inflammatory mediators that may facilitate periodontal breakdown
and attachment loss. Therefore, it has been reasonably inferred that there is commonly

3
more periodontal destruction in the furcation sites than on the interproximal sites of
molar teeth.
When treatment planning with periodontally-involved molars, a poor or
compromised prognosis is routinely given (McGuire & Nunn 1996, Kwok & Caton 2007).
The prognosis and treatment of these teeth is often based on the severity of the furcation
involvement and its classification (Carnevale et al. 1997, Hamp et al. 1989) along with
other factors such as mobility, tooth position, and further restorative needs (Svardstrom &
Wennstrom 2000). With recent studies reporting that periodontal diseases have an
impact on overall health (Kinane & Bouchard 2008), the treatment paradigm has shifted
its focus from “dental conservation to health preservation” (Popelut et al. 2009). The
degree of furcation involvement often serves as a prognostic factor and influences
selection of a definitive plan (Svardstrom & Wennstrom 2000). Without adequate
diagnostic tools, furcation-involved teeth may be lead to diagnosis of advanced
periodontitis and potentially lead to irreversible treatment such as extraction.
Some authors believe that the furcation-involved tooth should be extracted and
others believe that under favorable circumstances the condition will improve
considerably with treatment and that the tooth can be retained and will function well for a
significant period of time (Nabers & O’Leary 1968). Hischfield & Wasserman (1978)
discuss the possibility of more aggressive surgical treatment or extraction rather than
maintaining the furcation-involved molars because of reported higher mortality rate.
Becker (1984) suggested that if there is class III furcation involvement and evidence of
horizontal bone loss, then a tooth is hopeless and further treatment is futile. Ammons and

4
Harrington (2001) recommended that once a furcation is grade III or IV, or if there is
advanced bone loss in a grade II lesion, the clinician must consider extraction and use of
a dental implant to replace teeth. However, it has been argued that furcation
classification does not accurately reflect disease status. Consequently, the clinical value
of furcation status in formulating a prognosis has limitations with regard to predicting the
treatment outcomes (Kornman 1987). Using the current classification system, several
studies suggested that teeth with short root trunks may be classified into the advanced
disease category of a relatively early stage of periodontitis. According to Rosenberg
(1988), the buccal and lingual furcation entrances in the mandibular first molars are
located an average of 3 mm and 4 mm apical to cementoenamel junction. Gher et al.
(1980) reported that an attachment loss of 6 mm would probably result to in a through-
and-through furcation involvement (grade III or IV). However, other studies have
concluded that molars with furcation involvement survive in function for many years and
that furcation involvement classification, by itself, should not condemn a tooth to an
unfavorable prognosis (Nabers & O’Leary 1968).
The anatomical barriers and difficulties in treating furcation-involved teeth led to
the idea of removing roots in attempt to eliminate plaque-retentive areas in the exposed
furcation. Root resection can improve debridement access and make the area more
accessible for daily maintenance by patients. However, the efficacy of resecting roots
has been debated over many years, and the literature differs as to the success of root
amputations or hemi-sections (Hamp et al. 1989, Carnevale et al. 1997, Langer et al.
1973). Various therapies were developed to prevent more loss or even to regenerate

5
some of the attachment. However, regenerative therapies, including bone grafting, have
not completely provided full regenerative outcomes and have reported limited successes.
Even with mandibular class II defects, which are thought to have more predictable results
than maxillary molars, strong histological evidence of new attachment formation is not
available (Pepelassi et al. 1991). The variation of results and conclusions among authors
raises the possibility of the technique sensitiveness of the recommended procedures and
the importance of strict maintenance care afterwards. Patients may feel that retaining
their teeth will require multiple and complex treatments and this may discourage them
from wanting to maintain their teeth and cause them to opt to extract instead. In this era
of dental implants with their easy availability, extraction often leads to a decision for
implant placement as an ideal replacement to natural teeth. With increasing popularity of
dental implants and their reported high success rate, clinical dilemmas arise during
decision-making process.
There are numerous studies that focus on comparison of survival, longevity or
treatment outcome between the furcation-involved multi-rooted teeth and single-rooted
teeth. However, there is a paucity of literature focusing on the differences between the
attachment in the furcation site and the non-furcation, i.e. interproximal sites, of a same
tooth. Kornman (1987) argued periodontal lesions in the furcation represent propensity
for progressive bone loss and will exhibit a mostly irreversible pattern of the loss.
Kalkwarf et al (1988) reported that even with periodontal maintenance, periodontitis in
furcation sites progressed at a different rate from other tooth surfaces and that they tended
to lose clinical attachment level regardless of therapy provided. Waerhaug et al. (1980)

6
reported that of loss of attachment and marginal gingivitis on the surfaces facing the
furcations was greater than outer surfaces. The average loss of attachment was reported
to be 62.8% in the furcation surfaces and 47% in the interproximal surfaces of the same
tooth. He concluded that more attachment was likely to be lost in the furcation sites than
on the outer interproximal sites of a same tooth. However, the Waerhaug study has
limitations in methodology as it was a case report and also showed that treatment failure
was linked to incomplete root surface preparation. His results do not reflect amount of
bone destruction, but only roughly estimate clinical attachment loss based on staining
methods used on extracted teeth. Currently, there is no research available that
investigates the pattern of bone loss in the furcation site and examines if bone loss in the
furcation site progresses faster over time than the interproximal site of the same tooth.
Periodontal attachment loss, including clinical and radiographic loss, is vital in
monitoring the progress of the periodontal disease and in giving patients a complete
diagnosis and accurate prognosis as a prerequisite for appropriate therapy. However,
information solely based on clinical examination is not complete without knowledge of
average progression of bone loss and an understanding the association between clinical
aspects and underlying bony changes.
The objective of the study was to determine whether teeth with furcation
involvement lose significantly more bone in furcation sites over time than the
interproximal sites of the same tooth. A further objective was to determine if gender,
age, interproximal restorations, systemic disease, adjacent tooth or periodontal recall
schedule has an affect on the bone loss. The research hypothesis is that mandibular

7
molars with Glickman grade III or IV furcation involvement will lose significantly more
bone in the furcation sites over time than the interproximal sites of the same tooth. The
null hypothesis is that there is no statistically significant difference in bone loss over time
between the furcation sites of mandibular molars with Class III or IV furcation
involvement and the interproximal sites of the same tooth.
This study will help to elucidate the complexities of furcation involvement and
examine the accepted conventional idea of furcation therapies by retrospectively studying
radiographic patterns. Understanding the difference of underlying bony changes over the
furcation sites and the interproximal sites can provide a vital tool for improving the
predictive value of the clinical evaluation of furcation-involved teeth.

8
Chapter 2: Materials and Methods
This is a retrospective study utilizing existing, sequential, non-standardized
radiographs and the variable tested is bone loss as a percentage of total root length in the
interproximal and furcation sites.
Patient selection was completed by reviewing all available paper charts and
radiographs at the University of Southern California, School of Dentistry. Charts were
considered for inclusion if basic patient identification information, past medical and
dental history, and periapical radiographs of mandibular molars from the initial baseline
examination to minimum of 5-year follow up were present. Many authors have reported
that the best radiographs for visualizing and measuring the alveolar crest are
interproximal radiographs or bitewings (Hausmann et al. 1989). This is because bitewing
radiographs minimize the vertical angulation and, thereby, the resultant distortion.
However, because of the inherent nature of retrospective studies, interproximal
radiographs or previously standardized radiographs with positioning devices were not
available prior to measuring and comparing the bone loss. Consequently, periapical
radiographs were used to measure bone loss in percentage of maximum bone height or
the entire root length rather than measuring in millimeters (Schei et al. 1959, Bjorn &
Holmberg 1966, Williams et al. 1979; Lavstedt et al. 1975). Although this method does
not provide the bone loss in absolute number, the technique is sufficiently reliable when
comparing bone level in the same tooth in sequential radiographs. The influence of
methodical and elongation errors will be introduced into all sample results, and
accordingly to Jeffcoat et al. (1984) error in this technique was

9
reported to be as small as 2%. Also the influence of methodical and elongation errors
will be basically the same for all teeth and introduced into all sample results, thereby,
achieving acceptable measurement overall.
Only mandibular molars with furcation involvement were used in this study
because a furcal lesion in maxillary molars present within buccal and/or lingual bone
plate and overlapped roots may actually obscure furcal lesion on radiographs (Gurgan et
al. 1994). Molars with radiographic furcation involvement and evident bone loss
(Glickman grade III or IV) apical to the furcation fornix were included in the study.
Mandibular third molars were excluded, since they exhibit large variation in anatomy,
including high frequency of fused roots. Furthermore, a wide range of bone loss for the
buccal surface of third molars is reported compared to that of the mandibular first and
second molars (Theilade 1960).
All radiographs used in this study were taken and developed using standardized
equipment. After sample selection, all radiographs were digitized and transferred to a
computer. Digital manipulations and measurement of linear distances were recorded
using ImageJ for Windows. Image J is a public domain Java image processing program,
based on NIH Image, which calculates area and pixel value statistics for user-defined
selections (Rasband 2009, Abramoff 2004). All radiographs were evaluated and
measured by one examiner (CK). Inter-observer variation in locating anatomical
references such as CEJ, alveolar crest, and root apex has been documented (Gürgan et al.
1994). Variations in measurements have been affected by how clearly radiographs and
images are projected and how easy it is to identify these references by examiners.

10
It was concluded that the wide discrepancy in the ability of the examiners to locate the
bifurcation could largely be attributed to individual variation. Even with calibrated tools
and methods, difference between different examiners’ judgment and opinions pose
problems in epidemiologic surveys and longitudinal studies. Employing the same
examiner through all studies has been found to avoid study errors, promote consistent
uniformity and maximize the sensitivity for detecting changes (Theilade 1960, Hausmann
et al. 1989). Thus, a single examiner was used in this study to detect the radiographic
landmarks and complete the measurements.
Anatomical landmarks, identified on the radiographs, included CEJ or restorative
margin, alveolar crest, furcation fornix, and apex of the root. Baseline radiographs and
the follow-up radiographs were digitized and saved on the computer. Linear
measurements between the fixed reference points (Hausmann et al. 1992) were
determined and bone loss was expressed as a percentage of tooth root length.
The study was approved by the Institutional Review Board for exempt studies of
the University of Southern California (approval # UP-08-00149). An estimated 7000
patients’ charts were reviewed and searched for samples that met all inclusion criteria.
Periapical radiographs of mandibular first and second molars with radiographic furcation
involvement were selected. A molar with restorations covering the CEJ were only
included if the same restorations were present for the follow-up radiograph. Only
samples with follow-up radiographs of a minimum of 5-years’ time period were selected.
Therefore, from each individual, a series of two periapical radiographs were obtained.
Patient charts were reviewed for complete information on age, gender, presence or

11
absence of a medical condition such as diabetes or medication such as, phenytoin known
to negatively affect the periodontium, smoking status, compliance and frequency with
treatment recommendations. Exclusion criteria were minimal bone loss from the fornix
to the alveolar crest in the furcation area, diagnostically unacceptable or unclear
anatomical landmarks, excessive image distortion with obvious over- or under-estimation
of the amount of bone loss, presence of infrabony defects, and presence of root resorption
or periapical lesions in either baseline or follow-up radiographs. If the patient had a
history of periodontal surgical treatment, including osseous surgery, root resection, or
tunneling procedures in the selected tooth within the studied period of time, the chart was
also excluded. All patients were on a periodontal maintenance schedule including oral
hygiene instruction and professional tooth cleaning either at the USC School of Dentistry
Predoctoral clinic or dental hygiene clinic. The periodontal maintenance regime over
study period was recorded according to patient’s individual periodontal status. A patient,
who complied with at least one periodontal maintenance visit per year, was classified to
be compliant with their regular recall. Since this study is done on patients receiving
dental care at a teaching university setting, some patients likely had some recall visits in
private dental clinics and no effort could be made to differentiate the location of
periodontal treatment by their dentists during the study period.
All radiographs used in this study were #2 size intra-oral films and were at USC.
All radiographs were scanned using a flat bed scanner (Epson Expression 10000XL-
Graphic Arts Scanner, Epson America Inc., Long Beach, CA, USA) to a 500 x 400 dpi
resolution, 10-bit grey values and then transferred to a computer (IBM-PC, Lenovo, New

12
York, USA) PC: 1.83 GHz. Digital manipulations were performed and recorded using
image analysis software for Windows (Image J 1.32j, National Institutes of Health). The
contrast of the images was enhanced by using background subtraction tool. All
radiographs were evaluated under 10-fold magnification.
Landmarks identified on the radiographs are described below and illustrated in
Figure 1. This set of anatomical landmarks was chosen since the represented attributes
do not vary substantially over time. All radiographic assessment by computer was
performed by one examiner (CK) and the same rules were used to identify landmarks on
both initial baseline and follow-up images.
Cemento-enamel junction (CEJ): The most apical extent of enamel
inteproximally which can be identified by a change in radiographic density
(Hausmann et al. 1989). If the CEJ was covered by same interproximal
restoration that existed in the baseline and follow-up radiographs, the margin of
the restoration was used as a reference. If CEJ (margin of restoration) or alveolar
crest was not identified in one or both of the consecutive radiographs, the sample
was excluded.
Alveolar crest (AC): Most coronal point whereby the periodontal ligament space
retained its normal and continuous width. If no periodontal ligament space could
be identified, the point where the projection of the AC crossed the root surface
was taken as the landmark (Benn 1992, Bjorn et al. 1969). If several bony
contours could be identified mesial or distal of the tooth, possibly due to
infrabony defect or crater, these radiographs were excluded.

13
Furcation fornix (Fx): The most apical portion of the root trunk that mesial and
distal roots begin to bifurcate.
Root apex (Ax): The point where the root canal meets the most apical end of the
root.

Figure 1: Identified Anatomical Landmarks

a) b)

a) At baseline: CEJ, fornix, apex.(yellow). Alveolar crest (AC) level was marked (red)
b) At follow- up: Alveolar crest level was marked (blue)

After the landmarks were identified on the baseline radiograph, the measurements
were performed using the method described by Hausmann et al. (1992). Linear
measurements between the fixed reference point (CEJ or restoration margin) and
radiographic apex were made along the root surfaces on both mesial and distal roots
using ImageJ (Benn 1990, Figure 2).

14
Figure 2: Using ImageJ to Measure Total Root Length

The program set the linear distance from CEJ or restoration to the radiographic
apex as 100% which denotes the total root length. The linear distance between apex and
AC, as well as fornix and AC were assessed and recorded for each root. Every time a
different root or radiograph was chosen, root length was re-measured and set as 100%.
The same measurement was repeated on the follow-up radiographic image and recorded.
All radiographic bone loss measurements were expressed as a percentage of total root
length. For each sample tooth, linear distances were measured along the mesial and distal
root of the tooth. The mesial and distal root measurements were not averaged and used in
the calculation separately from each other. Radiographs were further reviewed to record
presence or absence of an adjacent tooth. The condition of having a tooth adjacent to the
test tooth surface is furthermore referred to as “adjacency” in this paper.

15
The means of the radiographic measurement were compared using the statistical
tests. For the total and for the periodontal recall, gender, age group and systemic disease
subgroups, analyses first calculated mean bone loss per patient and then in total or by
subgroup. One patient, however, may have different values for interproximal restoration
or adjacency for different teeth or tooth sections. Therefore, for these analyses, the first
set of values for each patient was used. All p-values were calculated using non-
parametric tests. The Wilcoxon signed-rank test was used for differences between
interproximal and furcation bone loss. The Wilcoxon rank-sum test was used for
differences between subgroups. A p-value of less than .05 was considered statistically
significant.

16
Chapter 3: Results
Twenty-six sets of periapical radiographs were obtained of mandibular first and
second molars (20 first molars, 6 second molars) with radiographic furcation involvement
in all 18 patients (Table 1). Four patients contributed two teeth, two patients contributed
three, and twelve patients contributed one each. Mesial and distal roots were measured
separately and were analyzed individually as sites (total = 56 sites). The average age of
the patients at the baseline radiograph was 61 + 9.8 years (range: 41 to 81 years).
Patients were arbitrarily divided into 2 groups, younger than age 60 and older than 60 (n
= 10, age < 60; n = 8, age > 60). Eleven patients reported medical conditions
(hypertension, diabetes, thyroid disease, hypercholestremia, or arthritis). One patient
reported an active smoking history. All patients had received nonsurgical periodontal
maintenance therapy; however, the periodontal recall schedule varied from patient to
patient (intervals of 4 to 24 months). If their periodontal recall was within every 12
months, they were considered to be in the compliant group. After the study follow-up
period, sample teeth in 14 patients were still intact, whereas those in 4 patients were
extracted. The follow-up time ranged from 5 to 12 years (mean = 6.3 years).

17
Table 1: Demographic Characteristics of the Study Population
Patient (n = 18) Tooth (n = 26)
Patient characteristic:
Age (years; mean + SD
(range))
61 + 9.8 (41-81)
< 60 y.o. 10 12
> 60 y.o. 8 14
Gender: male 11 18
female 7 8
Systemic disease: present 11 13
absent 7 13
Periodontal recall:
compliant
14 14
non-compliant 4 12
Follow-up time (years):
Mean + SD 6.31 + 2.4
Range 5 - 12

Table 2: Tooth Characteristics of the Study Population
Tooth (n = 26) Site (n = 52)
Tooth characteristic:
Interproximal restoration:
present 17 30
absent 9 22
Adjacent to tooth 37
edentulous area 15
Type of tooth
1st molar 20
2nd molar 6

Presence or absence of an adjacent tooth and of any interproximal restorations
was noted on individual interproximal sites on the radiographs. There were 17 teeth that
had either full coverage restorations or interproximal restorations on one surface (mesial
or distal), leading to total of 30 sites. There were 37 interproximal sites that were by an
adjacent tooth and 15 sites that were by an edentulous area.

18
The bone loss was compared between interproximal and the furcation sites within
the same tooth. No significant differences were found between mesial and distal sites of
the same tooth, therefore no attempt was made to differentiate them further. In
comparing baseline and follow-up periapical radiographs of furcation-involved teeth, the
average bone loss over time was 4.22 % + 2.4 for the interproximal (I) sites and 4.55% +
2.8 for the furcation (F) sites (Figure 3, table 3). The average annual bone level change
was 0.90 % + 1.0 for (I) sites and 0.74% + .79 for (F) sites (Figure 4, table 3). No
significant differences in overall or annual bone loss over time were found between the
interproximal sites and the furcation sites.

Figure 3: Overall Bone loss as % of Total Root Length
3
3.2
3.4
3.6
3.8
4
4.2
4.4
4.6
4.8
5
Interproximal site Furcation site
% Bone Loss

19
Figure 4: Annual Bone Loss as % of Total Root Length
0.5
0.7
0.9
1.1
Interproximal site Furcation site
% Bone Loss

Table 3 summarizes the overall and annual bone loss between interproximal site
and furcation site according to age, gender, periodontal recall, systemic disease,
interproximal restoration, and adjacency.

20
Table 3: Summary of Bone Loss according to Parameters
Overall Annual

Interproximal
site
Furcation
site
p-
value
Interproximal
site
Furcation
site
p-
value
Total 4.22 (2.49) 4.55 (2.84) 0.87 0.88 (0.61) 0.96 (0.74) 0.87
Periodontal recall w/i 12 mo:
Yes 3.47 (2.41) 3.76 (2.82) 0.97 0.67 (0.40) 0.73 (0.55) 0.83
No 5.40 (2.29) 5.79 (2.57) 0.94 1.22 (0.74) 1.32 (0.90) 0.81
p-value 0.07 0.04 0.15 0.06
Gender:
Male 3.96 (2.41) 4.20 (2.76) 0.7 0.89 (0.57) 0.97 (0.85) 0.76
female 4.63 (2.76) 5.10 (3.09) 1 0.87 (0.70) 0.93 (0.60) 0.94
p-value 0.47 0.59 0.72 0.86
Presence of interproximal restoration:
Yes 4.45 (4.00) 4.45 (3.22) 0.83 0.88 (0.95) 0.82 (0.60) 0.9
No 4.64 (2.06) 4.25 (2.59) 0.58 1.09 (0.65) 1.07 (0.98) 0.69
p-value 0.32 0.86 0.2 0.72
Age:
<60 4.82 (2.10) 5.08 (3.48) 0.92 0.99 (0.67) 1.01 (0.89) 0.85
>60 3.47 (2.87) 3.89 (1.75) 0.55 0.75 (0.53) 0.89 (0.55) 0.55
p-value 0.12 0.76 0.76 0.76
Systemic disease:
Yes 3.90 (2.44) 3.56 (2.22) 0.74 0.89 (0.56) 0.89 (0.87) 0.74
No 4.62 (2.67) 5.79 (3.17) 1 0.88 (0.70) 1.05 (0.59) 1
p-value 0.45 0.07 0.45 0.23
Adjacency:
Yes 3.52 (2.42) 4.19 (3.39) 0.71 0.74 (0.66) 0.86 (0.84) 0.86
No 6.98 (3.24) 3.40 (0.62) 0.5 1.55 (0.01) 0.86 (0.84) 0.5
p-value 0.14 0.62 0.11 0.62
* p-value < 0.05 for statistical significance

Different parameters were reviewed to see the possible association between bone
loss including age, gender, presence of systemic disease, interproximal restoration,
adjacency, and compliance to periodontal recall within 12 months. Other than
compliance with periodontal recall schedule, no other parameters were statistically
associated with bone loss between the interproximal and furcation sites (Figure 5). That
is, teeth in the complaint group demonstrated a smaller overall bone loss in the furcation

21
site than the interproximal site. There appeared to be greater bone loss in sites adjacent
to an edentulous area than in sites adjacent to another tooth; however, the difference was
not statistically significant. None of the findings for other variables were significant.
Interproximal sites adjacent to edentulous sites showed a trend of losing more bone than
furcation sites.

Figure 5: Effect of Gender, Age, Systemic disease, Interproximal restoration and
Adjacency to another tooth on % Bone Loss (Total Root Length)
0
1
2
3
4
5
6
7
Male
Female
Age < 60
Age 60+
Systemic Dx
No Systemic Dx
Restoration
No restoration
Adjacent tooth
No Adjacent tooth
% Bone loss
Inteproximal site
Furcation site

Additionally, Patients with a more regular recall schedule had statistically less
bone loss over the furcation site than patients with erratic periodontal recall p ≤.05

22
(Figure 6). The interproximal sites showed no statistical differences in relation to
compliance.

Figure 6: Effect of Periodontal Recall on Bone Loss
0
1
2
3
4
5
6
7
8
9
Interproximal Site Furcation site
% Bone loss
No Recall
Recall

* p-value < 0.05 for statistical significance

All p-values were calculated using non-parametric tests. Wilcoxon signed rank
test was used for differences between interproximal and furcation sites. No significant
differences were detected.

*

23
Chapter 4: Discussion
The exclusion criteria for this retrospective study, using radiographs to measure
and compare bone loss between tooth sites, eliminated the possible confounder of
surgical treatment. Therefore, the studied teeth essentially exhibited a natural
progression of inflammatory periodontal disease without intervention. Results showed
that with nonsurgical maintenance only, there was continual progression of bone loss in
both furcation sites and interproximal sites. However, bone loss change between sites
was not statistically different. Based on the results of this study, a research hypothesis
that over time furcation sites lose more bone than other sites is not supported.
Findings from the previous studies (Waerhaug 1980, Kornman 1987, Kalkwarf et
al. 1988) that reported more attachment loss on furcation sites than nonfurcation sites are
contradictory to our findings. A potential reason may be due the difference between
clinical and radiographic studies. Some authors reported that clinical measurements and
radiographic bone level reflect different features of periodontal destruction and
periodontal healing (Cury et al. 2004). Although clinically evident inflammatory changes
of the gingiva are considered a precursor of periodontal destruction, the disease may not
necessarily evolve and lead to bone loss. At least part of reason for the differing result in
the current study can possibly be attributed to using radiographs as the basis for analysis,
instead of clinical parameters. Radiographic studies may show less attachment loss than
the clinical studies because of difficulties and inaccuracies related to identifying the
alveolar bone crest projected over the tooth and detecting bone level changes. Therefore,
the rate of bone loss found in the present research may reflect conservative changes and

24
reveal a different component of periodontal disease. Likewise, the previously
mentioned studies focused on the clinical parameters utilizing periodontal probes. In
diagnosing periodontal disease and estimating severity of inflammation and response to
treatment, the probe is used commonly (Garnick et al. 2000). However, the periodontal
probe is known to gain entry into the long junctional epithelium attachment easily if the
site is inflamed (Listgarten 1980). Inflamed tissue allows greater tissue penetration and
probe displacement (Van del Velden et al. 1981). Studies (Leon et al. 1987) have
reported that furcation sites often exhibit more inflammation than the interproximal sites.
Thus, in case of untreated chronic periodontitis patients, clinical parameters estimated by
clinical attachment loss, probing depth measurement, and bleeding on probing in
furcations may be analyzed as more advanced than that of the other nonfurcation sites.
This may lead to unfavorable outcome being reported in the clinical studies when
comparing furcation sites to nonfurcation sites.
Another reason for the differences in our results and those found in clinical
studies cited above may be the specific inclusion criteria used in the present study. While
most clinical studies on furcations tend to use teeth with Glickman grade I and II
furcation involvement, our study used only teeth with radiographic furcation involvement
(Glickman grade III and IV). This could allow for the analysis of interproximal and
furcation sites without the potential dilution of the overlapped tooth images that are
present on radiographs. As bone moves corono-apically from the CEJ, incipient to mild
furcation lesions may exhibit a different pattern of disease progression against a root
trunk versus the interradicular area.

25
Results from this study challenge the generally accepted idea that over time
disease progression in furcation sites is more rapid than in interproximal sites. This
raises a question about validity of current understanding of furcation diagnosis and
treatment. Little et al. (1995) examined stability of the treatment outcome in furcation-
involved teeth after tunneling procedures. They did not find crestal bone loss in the
furcation or interproximal sites in treated teeth in 5.8 years or difference between sites.
The results reported in this study may be interpreted as a finding that shows what is
optimally achievable for controlling active periodontal disease with a surgical approach.
However, results from our study, with no surgical intervention, also found that for
furcation-involved teeth with crestal bone level past the fornix, there is no difference
between bone level changes between furcation sites and the interproximal sites. In order
to be of value in periodontitis cases, clinical assessment and diagnosis must clearly relate
to disease stability or progression of bone loss. Predictive value and significance of
clinical evaluations in furcation defects would only be improved with more studies and
evidence based understanding.
The amount of bone loss reported in this study is expressed as a percentage of the
total root length. Our findings have clinical implications when these numbers are
compared to the average root length and translated into numbers. Papapanou et al. (1988)
measured the mean root length on periapical radiographs and compared with the data
reported by Wheeler (1966) on extracted teeth. Both values show similar root length
with small differences. They reported that the mesial root of mandibular first molar is
15mm + 0.17 and distal root is 13.8 mm + 0.18. The second molar is reported to have

26
14.6mm +0.15 for mesial root and 13.3mm + 0.14 for distal root. Our study did not find
significant differences in bone loss between the mesial and distal roots or between first
and second molars. Therefore, 4.22% bone loss found in the interproximal site can be
translated in the range of 0.56 - 0.63 mm over the study period (average 6.3 years). For
the teeth in this study, this assessment translates into an estimate of an annual
interproximal bone loss of 0.09 – 0.1mm. This annual rate of bone loss, although an
estimate, is similar to the reported average annual bone loss in chronic inflammatory
periodontitis patients. The rate and the average loss of attachment in periodontal disease
have been studied extensively in clinical trials and radiographic studies. In a clinical
study using a periodontal probe, loss of attachment level has been reported an annual
average in the range of 0.08 -0.3mm. (Suomi et al. 1971, Axelsson & Lindhe 1972,
Waerhaug 1977, Loe et al. 1978, Haffajee et al. 1983, Lindhe et al. 1983). In a study by
Albandar et al (1986), when the initial level of bone loss was held constant, rate of bone
loss in the age group 58-68 was 0.135mm in 2 years. Studies utilizing radiographs
showed annual alveolar bone loss of 0.07mm (Suomi 1971, Rohner et al. 1983).
Svardstrom & Wennstrom (2000) monitored the proximal radiographic bone level
changes over 10 years and reported minimal bone loss of 0.1 to 0.6mm. Therefore our
finding of 0.09 – 0.1mm for annual bone loss mandibular molars with periodontal
involvement is in agreement with previously reported estimates of annual bone loss found
in chronic periodontitis patients. However, there is no study available that specifically
analyzes rate of bone loss in the furcation site versus interproximal sites to compare with

27
finding of our study. But, based on our results, it is likely that bone loss in the furcation
site also occurs at a similar rate.
Our study did not find significant influence of gender, age, presence of the
interproximal restorations, chronic systemic diseases, or adjacent tooth or edentulous area
have on bone loss. Historically, many epidemiologic studies have suspected age-
dependent periodontal breakdown. Ainamo (1983) reported that destructive periodontal
disease affects all subjects after the age of 40. Papapanou et al (1988) also reported that
with increasing age, the marginal bone loss increased. Albandar et al. (1986) reported
that the rate of bone loss increased linearly and rapidly between ages 33 and 56 and that
the rate reaches its peak through age of 56 years. The strength of the relationship is
weaker for the age interval 58-68 years. They concluded that there is interaction between
initial bone loss, age and longitudinal bone loss. Hence, the prevalence and severity of
periodontitis in a population are reported to increase with age. However, bone loss with
increasing age compared to younger age may be due to the fact that susceptible teeth are
already lost in old age and a small percentage of diseased teeth account for majority of
periodontally affected sites in cross sectional studies. Therefore, attachment loss and
periodontal destruction seen in older ages can be attributed to chronic disease
accumulation rather than “age-specific condition” (Burt et al. 2005). This explains why
age was not significantly associated with bone loss in this study. Age was randomly
divided into two groups, < 60 y.o. and > 60.y.o. Both groups exhibited similar bone loss
in interproximal and furcation sites.

28
Gender differences in clinical attachment loss were consistently reported in many
national surveys (Burt et al. 2005). Papapanou et al (1988) reported in their study that
after the age of 35, the mean alveolar bone loss for men was higher than for women and
concluded that men had more marginal bone loss than women. Various reasons are
thought to be related to the gender difference including poor oral hygiene and other
behavioral traits. Our study had more female subjects (18 female, 8 male) than male
patients and the gender difference did not reach significant difference in bone loss.
The presence of interproximal restorations was reviewed for their association with
bone loss and possible plaque retaining feature. The results show that presence of
restorations did not influence the rate of bone loss on either furcation sites or the
interproximal sites. Any restoration with obvious defective margins was excluded from
the study population to rule out the reported association between overhanging dental
restoration and the periodontal conditions (Lang et al. 1988). However, this does not
eliminate the possibility that subgingival margins were present. Schätzle et al. (2001)
confirmed the long-held concept that having subgingival restoration margins was
associated with attachment loss and detrimental to periodontal health in a long-term study.
Other studies have reported shifts in microbial environment with overhanging and
defective restorations (Lang et al. 1983). No difference found in this study may be
simply due to the fact that most of restorations were not subgingival, or they were present
before study was conducted. Schartzle et al. (2001) reported that attachment loss occurs
within the first three years of placement and that periodontal indices improve as

29
restoration margins become supragingival over time. Our study period was more than 5
years; therefore, the effect of subgingival margins on bone loss was likely minimized.
Systemic diseases including diabetes, cardiovascular disease and inflammatory
disease have been associated with periodontal disease. More than half of the current
study population had systemic disease including cardiovascular disease and diabetes.
Presence of systemic disease; however, was not found to influence the bone loss in either
site. The small sample size can possibly explain why there was no statistical significant
influence from presence of systemic disease in the present study. This also may be the
reason that interproximal sites adjacent to an edentulous ridge or another tooth surface
did not influence the bone level changes. It is known that alveolar bone resorbs after
tooth extraction. The suspected reasons for resorption include disuse atrophy, decreased
blood supply, localized inflammation or unfavorable prosthesis pressure (MacKay et al.
1979, Ashman 2000). Although it did not reach statistical significance, there was a
definite trend toward more bone loss on interproximal sites adjacent to an edentulous
ridge than on the furcation site or interproximal sites adjacent to another tooth surface.
During the entire observation period, none of the edentulous sites in this study were
replaced with dental implants. Therefore, the alveolar ridge was continually resorbed
while it can be assumed that the bone in between roots of mandibular molars, i.e.
furcation site, had bone loss due to an inflammatory process. A larger sample size may
be able to elucidate further whether alveolar bone loss, in a similarly designed study, is
due to ridge resorption or an inflammatory process in any different rates or patterns.

30
The results from this study indicate that destruction of alveolar bone in furcation
sites was significantly greater among the noncompliant group than the compliant group.
This finding is similar to previous studies in regard to the progression of periodontal
destruction in noncompliant groups, and emphasizes the importance of continuous
periodontal maintenance program in controlling the disease. Historically, studies have
found a relationship between oral hygiene practices, periodontal recall visits and loss of
periodontal attachment. Bjorn & Hjort (1982) studied bone loss of furcated mandibular
molars radiographically and reported the frequency of sites with bone loss in the
furcation regions increased from 18% to 32% over 13 years in a population not
participating in any periodontal recall program. Hischfield & Wasserman (1978) also
found that in well maintained group, 80% of teeth lost over 22 year period had been
marked questionable. While most of the molars lost in the well-maintained group had
furcation involvements initially, only 19.3% of these same molars were lost. Other
studies confirmed this finding and reported that patients who comply with regular
supportive periodontal therapy are less likely to have attachment loss and able to keep
their teeth longer. The regular periodontal recall and patients’ compliance in this study
was defined as at least one documented recall visit per year, which is a “low threshold”
(Nickles et al. 2009). This may not be an ideal interval for this moderate to severe
chronic periodontitis population when many authors advocate periodontal maintenance
interval to be every 3 -6 months (Ramfjord 1987). This result shows that even
compliance with a low threshold periodontal maintenance can influence bone loss and,
thus, periodontal health. Wilson et al. (1987) also reported a finding that erratic

31
compliers retain tenfold more teeth than non-compliers. Whether the compliant group
did better because of beneficial effect of maintenance or because there is some beneficial
behavioral characteristic of this group, regular and frequent periodontal recall evidently
serves as a tool for better longevity of teeth and positive outcome of periodontal
treatment.
It is interesting to note that bone loss in the furcation site shows a difference
between compliers and noncompliers, whereas the interproximal sites did not show any
difference related to compliance. A potential reason for this may be due to poor
accessibility in furcation areas for personal plaque removal during their daily hygiene.
Close approximation of roots in the furcation entrance even make the area inaccessible
for thorough mechanical debridement. Especially with the grade III and IV furcation
involvement, soft tissue may occlude the furcation opening and favor the retention of
bacterial deposits, making daily oral hygiene difficult. The present results indicate that
professionals, through regular periodontal maintenance, may be able to achieve
substantially better debridement with visual and mechanical access in the furcation area
than patients with their daily oral hygiene. Previously, Bower (1979) compared
furcation entrance diameter of first permanent mandibular molar teeth to width of
commonly used periodontal curettes. He found that 50% of mandibular molars had
diameter of .75mm or less and the standard size for a curettes range from 0.7 mm to
1.1mm, suggesting that in 50% of furcation area cannot be properly debrided. He
concluded that standard curettes when used alone may not be suitable for proper
instrumentation. However, with introduction of power-driven ultrasonic scalers and

32
smaller size mini-scalers, more recent studies found the access in the furcation area is
easier with professional instrumentation (Leon & Vogel 1987). Therefore, results from
this study suggest that professional debridement in the furcation site during regular
periodontal visits is able to keep away from localized environment of inflammation and
prevent further destruction. When discussing the prognosis, treatment, and outcome of
furcation-involved molars, it should be emphasized that regular and frequent recall is part
of the therapy and successful outcome is expected only when patient is compliant with
the daily oral hygiene and professional treatment schedules.
This was a retrospective study, a limitation is that radiographs alone were used to
determine bone loss. Clearly, there are inherent difficulties and limitations to using
radiographs to measure the bone loss. Standard radiographs are two-dimensional
representation of a three-dimensional structure and do not incorporate the areas of bone
surrounding the teeth. Hausmann (1992) reported two factors contributing to
radiographic changes besides the true alveolar changes are investigator error in making
measurements and different x-ray projection angulation. The location of anatomical
landmarks is often difficulty to objectively locate with certainty and can be chosen more
or less arbitrarily. In addition, inter-observer variations have been reported by previous
studies. By utilizing one observer and reducing the sample variations by using computer
software to identify and measure, amount of human error due to was minimized in this
study.
Using radiographs necessitates that both buccal and lingual plates are projected as
overlapped images. Therefore, even if intrafurcal problems are present with significant

33
loss on either buccal or lingual plate, it would still be projected with limited bone loss
over the furcation (Bjorn et al. 1969). In a study that tested the reliability of radiographs
in the measurement of bone loss, a significant underestimation of bone loss over the
buccal and lingual surfaces was found (Theilade 1960). This implies that bone loss over
the furcation site may be misinterpreted in a considerable portion of cases. Thus teeth
with recurrent periodontal infection due to bone loss in buccal and lingual surfaces,
radiographs may show presence of bone. For the future studies, combination of
radiographic examination with clinical examination over the furcation would decrease the
chances of underestimation and reveal the true changes.
Digital subtraction radiography (DSR) would be an ideal method to compare and
measure the radiographic bone loss to minimize the inherent problem of different in x-ray
beam angulation in non-standardized radiographs. Optimal results produced by
subtraction radiography method require identical image geometry from the initial
recording process from the preparation (Wenzel 1989). Film contrast and density, as well
as the angle, need to be controlled in order to enhance the information from subtraction
radiography. Since this requires sensitive technique, quality of results is good. Angular
distortion and error need to be minimized. Subtraction images from geometrically non-
identical radiographs produced significant angulation variation and can hinder the ability
to demonstrate periodontal bone lesion due to misalignment (Rudoph et al. 1987). In our
study, radiographs had already been taken without calibrated methods, thereby resulting
different angulations and other parameters making it difficult to achieve entirely
eliminated structured noises. Manual superimposition and positioning of reference points

34
is improved with films with better contrast and more sharply defined edges. In order to
achieve replicability of the same angle, prefabricated stents or holders are necessary to
standardize the technique. (Eickholz et al. 1996) By using the standardized technique, a
higher reproducibility of the images can be achieved; therefore, smaller bony changes in
the alveolar crest can be measured using DSR.
In this study, anatomical landmarks were used as reference points to measure
distances. This technique is less sensitive to changes of projection geometry or angular
distortion than subtraction radiography (Benn 1990, Eickholz et al. 1996). The present
study was a proportional assessment describing bony changes in relation to root length in
a serial radiographs, thus it provided relative, not absolute measurement in millimeters
(Schei et al. 1959, Eickholz et al. 1996). Subtraction radiography detects the density
differences between serial radiographs, whereas linear measurement detects bone changes
in contact with the root surface. (Eickholz et al. 1996) Previous studies (Papapanou et al.
1989) reported limitations of using anatomical landmark to measure alveolar bone loss.
However, these studies used one reference point (CEJ), measured the distance to the
alveolar crest, and reported error due to x-ray angulation. Our study used two reference
points; thus, regardless of angulation, root length will be the same in a serial radiographs.
However, expressing bone loss as a percentage of root length has shortcomings. Since
absolute number is not measured and the percentage of bone loss is relation to the root
length, small bone loss on a tooth with short root may be interpreted as the same
percentage of bone loss in a tooth with long root. Therefore, results from this study
should be interpreted with care.

35
Limitations of this study include the short time interval and the small number of
study sample sites. Albandar et al. (1986) in their longitudinal radiographic study
described minimal changes in bone level where 94% of sites did not show bone loss
>2mm during a 2-year observation period. In the current study, percentage change
ranges from 0.5% to 3% over 6.3 years. Considering the entire root length these small
changes may seem negligible clinically. Also, in order to calculate the attachment loss
over time, the process has to be steady and unremitting. Therefore, if activity was latent
during chosen study period then the measurement would not be an accurate reflection of
true disease progression. The small number of patients in this study presents a risk of
bias inherent in the method of generalization that has been previously noted in small
samples. However, difficulty of finding study samples that met all inclusion criteria at a
teaching university setting did not permit a larger sample in longer term study.
The present study investigated vertical bone loss in the interradicular bone, i.e.
apico-coronal loss in the furcation. Cury et al. (2004) argued that repeated
measurements of vertical clinical attachment level are not adequately reliable for early
diagnosis of furcation defects. But, at this point in time, we can only speculate how the
entire process of periodontal destruction progresses in terms of clinical attachment level
over the bone surface area or horizontally. However, this issue can only be elucidated in
future studies employing both radiographic and clinical exams. A main problem is that
furcation involvement is reported to be horizontal bone loss between roots due to
minimal or no improvement in horizontal fill after regeneration therapy (Pontoriero et al.
1988, Metzler et al. 1991). Authors reported inconsistency and lack of information from

36
the measuring vertical attachment level alone and instead advocated for using horizontal
probing attachment level as a precise and reliable tool to monitor disease progression and
treatment outcomes (Eickholz & Staehle 1994, Cury et al. 2004). Thus, future studies
should combine the radiographic and clinical exam, including vertical and horizontal
attachment level, to monitor the disease process. When using radiographs to measure the
bone loss, a program that automatically detects and identifies the landmarks on
radiographs to eliminate the errors associated with human hand-eye coordination is
recommended to make reproducible placement of landmarks.

37
Chapter 5: Conclusion
Within limitations of the present retrospective study, we may draw the following
conclusions. The progression of bone loss in furcation-involved teeth between furcation
sites and interproximal sites shows no difference. However, patients who are compliant
with their periodontal recall schedule lose less bone in furcation sites than patients with
erratic periodontal recall schedule. Gender, age, presence of the interproximal
restorations, chronic systemic diseases, and site adjacency to another tooth or to an
edentulous area are not significantly associated with bone loss in the furcation.
A thorough and detailed diagnosis of all aspects of furcation involvement presents
a demanding clinical experimentation. Novel treatment modalities compel the therapist
to acquire the necessary data and to correctly interpret the respective observations. The
more irreversible treatment measures may only be justified, if the practitioner is able to
give additional information and value to the decision making and treatment. Results
obtained from this research can be applied clinically to improve the diagnostic, predictive
value and significance of clinical evaluations of furcation-involved teeth.

38
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Asset Metadata

Creator Kim, Clara S. (author)

Core Title Rate of bone loss in furcation-involved molars: a retrospective analysis

School School of Dentistry

Degree Master of Science

Degree Program Craniofacial Biology

Publication Date 06/01/2010

Defense Date 05/28/2010

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

Tag furcation,mandibular,molars,OAI-PMH Harvest

Language English

Contributor Electronically uploaded by the author (provenance)

Advisor Nowzari, Hessam (committee chair), Navazesh, Mahvash (committee member), Rich, Sandra (committee member)

Creator Email clarakim79@gmail.com,soojk1207@hotmail.com

Permanent Link (DOI) https://doi.org/10.25549/usctheses-m3107

Unique identifier UC177881

Identifier etd-Kim-3779 (filename),usctheses-m40 (legacy collection record id),usctheses-c127-330801 (legacy record id),usctheses-m3107 (legacy record id)

Legacy Identifier etd-Kim-3779.pdf

Dmrecord 330801

Document Type Thesis

Rights Kim, Clara S.

Type texts

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

Repository Name Libraries, University of Southern California

Repository Location Los Angeles, California

Repository Email cisadmin@lib.usc.edu