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Dental pathology in Pongo satyrus borneensis.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 98:307-321(1995)
Dental Pathology in Pongo satyrus borneensis
KATHRYN ELIZABETH STONER
Museum of Natural History, Department of Systematics and Ecology,
University of Kansas, Lawrence, Kansas 66045-2454
KEY WORDS
Dental disease, Horizontal bone loss, Orangutan,
Osseous defects, Pongo, Premortem tooth loss
ABSTRACT
The Selenka orangutan collection obtained from 1892 to 1896
from wild-shot specimens in West Borneo, provides a n excellent opportunity
to examine dental pathology in free-ranging primates. Two hundred and
twenty-three skulls from this collection were analyzed for dental conditions,
including carious lesions, local infections (infra-alveolar and periapical osseous defects), horizontal bone loss, and premortem tooth loss. Specimens were
sexed, divided into three broad age groups, and compared to ascertain sexrelated or age-related differences in occurrence of dental pathology.
None of the subadults displays any evidence of dental disease. One individual (2%)in the young adult group has a periapical osseous defect and evidence
of horizontal bone loss, and another (2%) has two adjacent interproximal
carious lesions. The old adults have a much higher prevalence of individuals
afflicted with dental pathologies, including 6% carious lesions, 26% local
infections, 23% horizontal bone loss, and 3%premortem tooth loss. The differences between the young and old adults in number of individuals afflicted
with dental pathologies is statistically significant for local infections and
horizontal bone loss. When compared by sex, the old adult group reveals that
females have a higher occurrence of dental pathologies than males in all types
of lesions recorded and these differences are statistically significant for local
infections and horizontal bone loss. Considering the importance diet plays in
the development of dental disease, it is suggested that ecological separation
of the sexes, with the subsequent dietary differences, could be a n important
factor determining the higher prevalence of dental lesions observed in female
orangutans. Additionally, the importance of local ecological factors, which
may affect dietary patterns, are recognized as a potential source of variation
in dental pathologies among different samples of orangutans.
0 1995 Wiley-Liss, Inc.
Dental pathologies in non-human primates have been recognized in many species
(Arnold and Baram, 1973; Bramblett, 1965,
1967; Cohen, 1960; Colyer, 1936; Hershkovitz, 1970; Jones and Cave, 1960; Kakehashi
et al., 1963; Kilgore, 1989; Lovell, 1990a,b;
Page and Schroeder, 1982; Page et al., 1975;
Rohrer-Ertl et al., 1985; Schultz, 1935,1939;
Skinner, 1986; Smith et al., 1977), and some
non-human primates have been used in dental disease research (Navia, 1977; Page and
0 1995 WILEY-LISS, INC
Schroeder, 1982). A current, comprehensive
review of dental pathologies in non-human
primates is provided by Lovell (1991). In
spite of these data, few studies have associated variation in prevalence of dental pa-
Received February 19, 1993; accepted April 13, 1995.
Address reprint requests to Dr. Kathryn E. Stoner at her current address: Palo Verde Biological Station, Organization for
Tropical Studies, Interlink 341, P.O. Box 02-5635, Miami, FL
33152.
308
K.E. STONER
thologies in wild primates with dietary factors. The effect of diet on dental disease has
been extensively studied in humans, in both
living (Brunelle and Carlos, 1982; Page and
Schroeder, 1982; Schluger et al., 1977; Toth,
1970) and prehistoric groups (Alexandersen,
1967; Brabant, 1967; Costa, 1980; Frayer,
1984; Hildebolt et al., 1988; Molnar and Molnar, 1985; Powell, 1985). Many of the studies
of human dental disease have attempted to
identify dietary patterns that affect the
prevalence of dental disease in different
groups. In recent years, the important role
a high carbohydrate diet plays in the occurrence of oral diseases has been well documented with experimental evidence (Hillson, 1986; Kreitzman, 1976; Newbrun, 1982;
Rugg-Gunn, 1983; Sreebny, 1982; Theilade
and Birkhead, 1986).
Although no clear associations of food
types with prevalence of dental disease have
been made for free-ranging non-human primates, data collected on dental lesions in
primates in the wild have all revealed a general trend of increasing frequency of dental
pathologies with older individuals (Bramblett, 1965, 1967; Colyer, 1936; Hershkovitz,
1970; Kakehashi et al., 1963; Kilgore, 1989;
Schultz, 1935, 1939). In spite of this agedependent relationship, great variation between and within populations has been observed (Bramblett, 1965, 1967; Lovell
1990a,b; Schultz, 1935). Some of the variation in frequency of dental disease within
populations has been attributed to differences between the sexes. For example, differences in the occurrence of dental disease
affecting male and female baboons (Papio
cynocephalus) have been documented
(Bramblett, 1965,1967). Older male baboons
frequently (29%) have severe alveolar destruction which is often associated with decayed or damaged teeth. Alternatively, female baboons rarely (5%) show signs of
periodontal disease. In contrast to baboons,
male and female gorillas (GorilZu gorilla)
have approximately the same frequency of
periodontal disease (Kakehashi et al., 1963).
No studies have focused on sexual variation of dental disease in orangutans, but field
studies have revealed much about orangutans diets in the wild that may, in turn,
prove useful in interpreting the prevalence
of dental pathology in these primates.
Orangutans can be characterized a s primarily frugivorous, but there is substantial diversity in orangutan diets which, in addition
to fruit, include flowers, leaves, buds, bark,
and insects (Galdikas, 1978, 1979, 1988;
MacKinnon, 1974; Rodman, 1977, 1988).
Ecological differences between the sexes
have been reported by Galdikas (1978), who
found t h a t adult males range farther per day
and occupy a larger area throughout their
lives than do females. This behavior relates
to males spending much more time on the
ground, consequently eating less bark and
young leaves, but more termites and other
foods found predominantly on the ground.
Conflicting results have been reported from
other areas (Rodman, 1977, 1988); a s a result, it is unclear whether this variation in
resource use is a reflection of idiosyncratic
habits of some males, regional differences,
andlor sampling techniques.
The purpose of this paper is to describe
dental pathologies in a sample of orangutans
and to determine whether there are significant differences between the sexes in the
frequency and severity of dental pathologies.
In addition, the previously established pattern that, within species, older individuals
have more dental pathologies than younger
ones is tested. Finally, qualitative comparisons are made of these results with previous
reports on dental lesions in orangutans (Lovell, 1990b; Schultz, 1935) and other apes
(Kilgore, 1989; Lovell, 1990a; Schultz, 1935).
MATERIALS AND METHODS
Study sample
The Selenka sample was obtained during
1892-1896 from wild-shot orangutans
(Pongo satyrus borneensis) from Skalua,
West Borneo. This collection represents one
of the largest series of orangutans preserved
in museums and is currently housed a t the
Anthropologisches Staatssammlung, Munich. A summary of the material in this sample and a brief history of the collection is
given by Rohrer-Ertl(l984).A historical review of the problems surrounding the nomenclature of the orangutan and the proper
designation of the species satyrus (synonymous with pygnaeus), a s well as evidence
309
DENTAL PATHOLOGY IN PONGO
TABLE 1. Number
of
individuals with dental pathologies in the Selenka sample of Pongo satyrus borneensis
from Skalua, West Borneo, stratified by age class and sex
Carious
lesions
M
F
M
F
Local
infections
M
F
M
F
Subadultl
Young adult
35
36
0
0
0
0
0
0
0
0
22
33
0
1
0
1
0
1
0
0
Old adult
32
62
1
5
4
1
21
0
3
N
20
Horizontal
bone loss
M
F
Premortem
tooth loss
' Three unsexed subadults are not included
for the recognition of the subspecies borneensis is also provided by Rohrer-Ertl
(1983, 1988).
Two hundred and twenty-three skulls
from the Selenka orangutan collection were
examined for dental pathologies. The subadult sample included 35 males, 36 females,
and 3 unidentified sex. The young adult sample consisted of 22 males and 33 females and
the old adult group contained 32 males and
62 females (Table 1).
The orangutans were sexed based on the
distinctively large canines characteristic of
males (Mahler, 1973; Swindler, 19761, as
well as cranial morphology. The development of the sagittal crest is consistently
more pronounced in adult males than females. Some discrepancies between my observations and sex identifications recorded
directly on the specimens were resolved by
Rohrer-Ertl (personal communication).
The sample was divided into three broad
age groups based on dental eruption and degree of occlusal wear. Similar to most other
primates, orangutan molar wear occurs primarily on the lingual cusps in the upper jaw
and the buccal cusps in the lower. However,
according to Welsch (1967), orangutans seldom show dentine bridges between the lingual and buccal cusps, in contrast to humans
(Smith, 1984) and gorillas (Welsch, 1967).
With these unusual patterns of attrition in
mind, the following aging criteria were developed. Subadults consisted of all individuals in which the permanent dentition was
not completely erupted. Young adults were
recognized as having a complete permanent
dentition with no more than small areas of
dentine exposure on the lingual cusps of the
Fig. 1. Maxillary occlusal view of a young adult female with little wear on the lingual cusps of M1, characteristic of the young adult age class. A periapical osseous
defect surrounds the left P3. Also note the crowding in
the maxilla. Missing teeth were considered lost postmortem (specimen 251).
first upper molar (Fig. 1). Old adults included individuals that had enough wear on
the first upper molar to create two large areas of dentine exposure on the lingual cusps,
which were frequently connected; if separated, it was only by a very narrow enamel
bridge (Fig. 2).
Recognizing dental pathologies
Dental pathologies were categorized a s (1)
caries, (2) local infections (infra-alveolar osseous defects and periapical osseous defects), (3) horizontal bone loss, or (4)premortem tooth loss. Standards for recognizing the
310
K.E. STONER
Fig. 2. Maxillary occlusal view Of an old adult female
with the right
showing much wear On the lingual
cusps, which have been worn down and are connected
through dentine exposure. The left M1 shows large dentine exposures on both lingual cusps, but they are still
separated by a small enamel bridge. Also note the periapical osseous defect associated with the left M1 lingual
root (specimen 185).
~ i 3, ~occlusa1
,
view of a young adult female with
a large occlusal cavity on the right maxillary M2 (specimen 114).
presence and seventy of pathological states
in these orangutans were based on previous
methodology applied to humans (Alexandersen, 1967; Brothwell, 1963; Koritzer,
1977; Molnar and Molnar, 1985).
Caries. Carious lesions were recorded by
position on the affected tooth and were categorized into occlusal, interproximal, or root
caries types (Molnar and Molnar, 1985). The
presence of occlusal caries was initially determined by macroscopic inspection followed
by further inspection with a hand lens and
probe. Carious lesions were recorded only
when the crown surface had collapsed and
a cavity was formed that could be probed
(Fig. 3). This is the sixth phase of development of enamel caries and represents a late
stage in the disease (Hillson, 1986); earlier
stages of enamel caries are difficult to detect
macroscopically (Howat et al., 1981).
Interproximal caries, limited to the
enamel surface, were recognized in a similar
fashion to occlusal caries (Figs. 4,5). I t was
sometimes difficult to evaluate the presence
of interproximal lesions due to the close in-
Fig. 4. Occlusal view of interproximal caries affecting maxillary right and left central incisors of an old
adult female (specimen 101).
terproximal articulations between the teeth
that allow little space for probing to ascertain the status of the coronal wall on the
interproximal surface. Therefore, interproximal caries may have been underestimated
in this study.
Severity of interproximal and occlusal caries was recorded using a 1 4 scale developed
by Koritzer (1977), who considered 1a small
pit or fissure lesion; 2 a moderate pit, fissure,
or smooth surface lesion; 3 any lesion that
DENTAL PATHOLOGY IN PONGO
Fig. 5 . Occhsal view of an old adult female with
a small interproximal cavity on the mesial surface of
311
Fig. 7. Left lateral view of a n old adult male maxilla
with several periapical osseous defects and horizontal
bone loss. A large periapical defect is located at the
root tip of the left canine which is connected to another
osseous defect associated with the third premolar. Two
more osseous defects are located around the first molar,
one on the mesial buccal root and another on the distal
buccal root (specimen 238),
maxillary left P4. The buccal roots of left M1 were lost
premortem and this area has been resorbed. The left I1
and P3 were considered lost postmortem due to the lack
of remodeling in the tooth sockets (specimen 84).
Fig. 8. Left lateral view of a young adult female maxilla with horizontal bone loss and periapical osseous
defects above P4 and the distal buccal root of M2 (specimen 251).
Fig. 6. Mandibular lingual view of cemental root caries affecting the distal root of right M1 and the mesial
root of right M2 in an old adult female (specimen 243).
endangers the pulp; and 4 exposure of the
dental pulp.
Root caries were recognized as dark, invaginated lesions surrounding one or more root
surfaces of a tooth. When present, these occurred near the cemento-enamel junction
and proceeded apically for varying distances
(Fig. 6). Although two types of root caries
have been observed in human skeletal sam-
ples including cemental type and cervical
type (Molnar and Molnar, 19851, only the
cemental type was identified in this sample.
Local infections. Local infections included
periapical osseous defects and infra-alveolar
osseous defects. Periapical defects were recognized as discrete areas of bone resorption
surrounding root tips. These usually had
regular borders and were approximately
round or oval in shape with a variable depth
(Figs. 1, 7, 8). Infra-alveolar defects occasionally were found interproximally, but
312
K.E. STONER
Fig. 9. Right lateral view of mandible from old adult
female with an infra-alveolar osseous defect surrounding M1 and M2 and horizontal bone loss in the
entire mandible (specimen 181).
Fig. 10. Left lateral view of maxilla and mandible
from an old adult female with horizontal bone loss in
the upper and lower jaw (specimen 201).
were primarily located on the lingual and
buccal borders of the alveolar margin between the cemento-enamel junction and the
apex of the root. These defects had regular
borders similar to periapical defects, but instead of being completely round or oval, the
resorbed area was usually semilunar in
shape with the open side directed toward
the alveolar border (Fig. 9). When one defect
encompassed the area between two teeth it
was considered associated with the more mesial tooth to avoid counting the defect twice.
Areas of bone fenestrations and dehiscences
were not considered pathological (Hall e t al.,
1967; Page and Schroeder, 1982).No attempt
was made to measure the depth of the defects
due to time constraints.
The present study focused on the molar
teeth in the maxilla and mandible and conservatively recognized only condition 4 a s
evidence for horizontal bone loss. When horizontal bone loss was present under the molars it usually continued around the entire
margin of the mandible or maxilla, therefore,
recording horizontal bone loss in the molar
region appeared to be representative of the
entire maxilla or mandible (Figs. 7, 9, 10).
Given time constraints, it was not possible
to analyze each individual tooth €or the presence of periodontal pockets or irregular porous surfaces for direct evidence of periodontitis.
Premortem tooth loss. Premortem tooth
loss was identified by examining the alveolus for each missing tooth to determine
that involves a n even lowering of the alveo- whether it was lost postmortem from hanlar margin has been described a s horizontal dling andfor the preparation processes or
bone loss (Hillson, 1986; Karn et al., 1984). was lost during the life of the individual.
In this study horizontal bone loss was scored As a first step, each vacant tooth socket was
a s present or absent based on a modified examined to see if any bone remodeling had
version of procedures described by Alexan- occurred (Ortner and Putschar, 1981). If the
dersen (1967) and Koritzer (1977). These re- margins were sharp with no evidence of bone
searchers measured horizontal bone loss be- in-filling, it was considered to be lost posttween the cemento-enamel junction and the mortem (Fig. 1).If the alveolus was partially
alveolar margin and designated four discrete filled with bone and the socket walls were
categories. The categories ranged from remodeled so that the sharpness of the
“bone-loss not exceeding 2 millimeters” in socket contour was lost or the socket was
category 1, to category 4, which included filled completely with bone, the tooth was
“bone-loss of approximately half the root considered to be lost premortem (Fig. 11)or
length or exposure of any molar root furca- congenitally absent. When present, the teeth
tion” (Koritzer, 1977).
surrounding a completely closed alveolus
Horizontal bone loss. Alveolar resorption
313
DENTAL PATHOLOGY IN PONGO
RESULTS
Fig. 11. Occlusal view of maxilla from old adult female with extensive premortem tooth loss. Teeth lost
premortem with resorption of the socket include right
M2, M1, P4, P3, I1 and left M3, M2, M1, and P4 (specimen 92).
were examined for interproximal wear facets
to rule out the possibility of congenital absence. Missing teeth due to congenital absence, a s well as teeth that had been broken
premortem but still retained the root or
roots, were not included in the category of
premortem tooth loss.
Comparisons
To test for sexual dimorphism of dental
pathologies, the number of males and females affected by each category of dental
pathology in the old adult group were compared with a Fisher exact test (Sokal and
Rohlf, 1981). I n addition, a Fisher exact test
was used to compare the young adult and
old adult samples to determine if the proportion of individuals amicted with dental pathologies varied significantly with age. Finally, teeth afflicted by carious lesions, local
infections, and premortem tooth loss, were
described within the old adult group to recognize any patterns of teeth affected by pathologies. No statistical comparisons were
made between teeth amicted with various
dental lesions because of the problem of assuming independence of teeth.
Caries
Within the old adult group, a slightly
higher proportion of females (8%) are affected by carious lesions than males (3%)
(Table l ) , but this difference is not statistically significant (Fisher P = 0.63). In the
subadult age group no individuals have carious lesions, while one individual (2%) in the
young adult group, and six (6%) in the old
adult group have at least one carious lesion
(Table 1). The difference between the old and
young adults is not statistically significant
(Fisher P = 0.38).
Given the low occurrence of caries found
in the Selenka sample, it is difficult to observe any regularity in teeth affected by carious lesions a t the level of individual teeth
(Table 2); nevertheless, some possible patterns are discernible when the teeth are combined into anterior (canines and incisors)
and posterior (premolars and molars) tooth
classes or separated as to their location in
the maxilla as opposed to the mandible (Table 3). The trends suggested include (1)in
females, carious lesions are more common
in the posterior and maxillary teeth than in
the anterior and mandibular teeth, and (2) in
males, caries are only found in the anterior
maxillary teeth.
The most common types of caries observed
in this sample are interproximal and root
caries, each accounting for 40% of the total
carious lesions observed, followed by occlusal caries, which account for the remaining
20% (Table 4). The severity of enamel caries
is most commonly category 2 (Koritzer,
1977), which is defined a s a moderate-sized
fissure or surface lesion (Figs. 4,5).One category 3 occlusal cavity destroyed a large part
of the occlusal surface and appears to be
approaching the pulp cavity (Fig. 3). Additionally, one category 4 lesion penetrated the
entire occlusal surface, pulp cavity, and root
(Fig. 12).
More than half (57%) of the individuals
aMicted with caries have more than one such
lesion, with a n average of two cavities per
individual (Table 4). I t is also apparent that
adjacent teeth are frequently involved in carious lesions. The most extreme example of
this is found in specimen 243, which has root
314
K.E. STONER
TABLE 2. Dental lesions in the old adult orangutans by dental element and sex (females n
Maxilla
Females
No. of teeth
Carious lesions
Local infections
Premortem tooth loss
=
62; males n
=
32)
I1
I2
C
P3
P4
M1
M2
M3
108
2
0
1
112
0
3
0
110
0
3
114
2
116
2
4
2
118
2
8
3
120
116
2
2
1
1
61
62
0
3
0
62
0
1
0
62
0
0
0
120
0
0
5
1
0
Males
No. of teeth
Carious lesions
Local infections
Premortem tooth loss
Mandible
Females
No. of teeth
Carious lesions
Local infections
Premortem tooth loss
54
2
3
0
58
0
0
0
54
0
109
0
2
0
114
0
5
0
Males
No. of teeth
Carious lesions
Local infections
Premortem tooth loss
58
0
4
0
58
0
62
0
3
0
1
0
0
0
0
109
0
4
1
121
0
4
0
120
0
1
0
121
120
1
1
7
0
0
0
55
0
2
60
0
60
0
2
60
0
60
0
0
2
60
0
0
0
0
0
0
0
0
1
0
1
0
1
0
TABLE 3. Dental pathologies according to anterior or posterior categories and
upper or lower jaws stratified by sex (only old adults)
Pathology
Female
Carious lesions
Local infections
Horizontal bone loss
Premortem tooth loss
Male
Canous lesions
Local infections
Horizontal hone loss
Premortem tooth loss
Anterior
Posterior
Maxillary
Mandibular
2
17
9
32
2
10
9
26
14
10
2
23
16
2
2
11
0
11
0
0
2
11
1
0
0
11
1
0
caries on the maxillary right P3 and P4 (not
pictured) and the mandibular right M 1 and
M2 (Fig. 6). With the exception of root caries,
carious lesions are not associated with periapical or infra-alveolar osseous defects.
Local infections
There is a statistically significant difference (Fisher P = 0.05) in the frequency of
individuals with local infections between the
old adult females (32%)and males (13%) (Table 1). In addition, the proportion of individuals afflicted with local infections is significantly different (Fisher P = 0.00004)
between the young and old adult groups.
None of the subadults and only one (2%) of
the young adults (Figs. 1,8)have local infec-
tions, while 24 (26%) of the old adults have
infra-alveolar or periapical osseous defects
(Table 1).
Local infections were also recorded by affected tooth in order to discern any patterns
of areas in which osseous defects occur (Table 2), although, again, patterns are hard to
discern. When the teeth affected were
grouped into anterior versus posterior and
maxillary versus mandibular (Table 3) the
following patterns emerged: (1) posterior
teeth are more often affected (65%)than anterior (35%) in females, while in males they
are equally affected (50% each); and (2) maxillary and mandibular teeth are involved
approximately the same in females (53%
DENTAL PATHOLOGY IN PONGO
315
dence of this pathology (Table l).When compared to the young adults, the old adult
group h a s a significantly (Fisher P = 0.001)
higher proportion of individuals with horizontal bone loss. None of the subadults, and
only one (2%) of the young adults (Fig, 8)
have horizontal bone loss; however, 22 (23%)
of the individuals in the old adult group have
horizontal bone loss (Table 1).
Premortem tooth loss
There are no significant differences in the
frequency of individuals with premortem
tooth loss between males and females
(Fisher P = 0.51). No instances of premortem tooth loss are found in the males and
only three females (5%)have lost teeth premortem (Table 1).Similarly, there are no significant differences between the young and
Fig. 12. Lingual view of t h e right side of t h e maxilla
old adult groups in the frequency of premorfrom a n old adult female with a n extensive carious lesion
tem tooth loss (Fisher P = 0.90). Premortem
on M2, which penetrates t h e occlusal surface and continues into the lingual roots of M1 and M 2 (specimen 999). tooth loss does not occur in the subadult or
young adult groups and is relatively rare
(3%) in individuals in the old adult sample
(Table 1).
TABLE 4. Caries type, severity, and tooth affected
The most extreme case of premortem tooth
per indiuidual’
loss
of the three old adult females is found
Specimen
Tooth
5Pe
Severity
in specimen 92 (Fig. 11). A total of 10 teeth
LP‘
Interproximal
84
2
were lost premortem, including maxillary
LPA
101
Interproximal
2
right 11, P3, P4, M1, M2 and left P4, M1,
101
RI’
Interproximal
2
LI’
Interproximal
101
2
M2, M3, and mandibular right M3. The other
114
RM2
0cc1usa 1
3
two cases of premortem tooth loss affected
LM1
176
Occlusal
2
RI’
242
single teeth. Specimen 84 has lost the two
Interproximal
2
242
LI’
Interproximal
2
buccal
roots of the upper left M1 premortem
Root
243
RPj
and the area has been resorbed (Fig. 5). The
Root
RP‘
243
Root
243
last example of premortem tooth loss is
RMI
Root
243
RM2
found
in specimen 223, which has lost the
RM’
999
Occlusal and root
4
Root
lower left canine with subsequent complete
999
RM’
’ Specimen 114, young adult female; specimen 242, old adult male; resorption in the area (not pictured). When
specimens 84, 101, 176, 243, 999, old adult females.
all dental elements were considered by location, the teeth most often affected by premortem loss in the old adult females are the
and 47% respectively), a s well as in males posterior maxillary teeth (Tables 2, 3).
(50% each).
DISCUSSION
Horizontal bone loss
General trends that can be identified reA statistically significant difference garding dental pathologies in the Selenka
(Fisher P = 0.003) between the sexes is orangutan sample include the following.
found in the frequency of individuals with First, sex differences occur in the proportion
horizontal bone loss. Thirty-four percent of of individuals affected by dental pathologies,
the old adult females have horizontal bone the females showing a higher prevalence in
loss, while only 3% of the males have evi- all types of dental lesions recorded. This sex
316
K.E. STONER
difference is statistically significant for horizontal bone loss and local infections. Second,
the occurrence of dental pathologies in subadults and young adults is extremely rare,
but increases markedly with old age. This
increase is statistically significant for local
infections and horizontal bone loss. Third,
individuals aMicted with local infections or
horizontal bone loss are much more common
than those with carious lesions or premortem tooth loss. Fourth, maxillary teeth may
be more often affected by carious lesions and
premortem tooth loss than mandibular
teeth. Local infections and alveolar resorption occur in the upper and lower jaw with
approximately the same frequency. Fifth,
caries, local infections, and premortem tooth
loss may aMict the postcanine teeth more
than the anterior teeth. Although these results reveal some sex-related and age-related differences in dental pathologies in
orangutans, the ultimate causes of this observed variability are difficult to discern
given the complex etiology of oral disease
(Navia, 1977).
Causes of dental disease
Dental disease is a multifactorial problem
with many possible variables affecting its
development and expression.
Caries. Dental caries is a consequence of
the fermentation of carbohydrates by oral
bacteria (Rugg-Gunn, 1983). The process of
fermentation produces organic acids as a byproduct that lowers the pH in the dental
plaque and causes demineralization of the
enamel, dentine, and cementum resulting in
the development of caries (Hillson, 1986).
Several factors contribute to the development of caries, but the most important is the
consumption of fermentable carbohydrates
(Kreitzman, 1976; Newbrun, 1982; RuggGunn, 1983; Sreebny, 1982; Theilade and
Birkhead, 1986).
penetrating the pulp cavity, severe attrition,
or a traumatic fracture of the coronal surface
of the tooth (Hillson, 1986). Infra-alveolar
osseous defects are most often due to a periodontal infection (Costa, 1980; Karn et al.,
1984) but occasionally result from trauma
to the area (Hillson, 1986).
Horizontal bone loss. In addition to creating local infections which cause infra-alveolar osseous defects, periodontitis is one of
the primary causes of horizontal bone loss
(Hillson, 1986).Although there is little doubt
that bacteria in dental plaque are the underlying cause of periodontitis (Page and
Schroeder, 1982; Schluger et al., 19771, the
etiology of this disease is multifaceted and
many factors influence its development. Soft
carbohydrate-rich foods cling to teeth and
dental plaque, thus enhancing the supply
of nutrients for bacteria (Hillson, 1986;
Schluger et al., 1977). Other factors correlated with periodontitis include crowding
of teeth and malocclusion, (Hillson, 1986;
Schluger et al., 19771, root caries (Newbrun
et al., 1984) and pregnancy (Hillson, 1986).
Finally, the influence of heredity on the development of periodontitis has not clearly
been established, but is believed to be an
important variable (Schluger et al., 1977).
Horizontal bone loss has also been attributed to extensive chewing forces produced
by mastication. Watson (1986) argues that
alveolar recession in humans should be considered indicative of age-related phenomenon associated with heavy masticating and
not necessarily a result of periodontal disease. However, a study of howler monkeys
by Hall et al. (1967)found no association between extensive tooth wear and alveolar resorption. In addition, a study of gorillas and
humans came to the conclusion that there is
no significant relationship between occlusal
wear and horizontal bone loss (Baer et al.,
1963).
Local infections. Local infections may result from various disease processes. Periapical abscesses and ultimately periapical osseous defects can occur when the pulp chamber
is exposed and infected with bacteria from
the mouth which migrate down the root canal to the apex of the root. Exposure of the
pulp canal can result from a carious lesion
Premortem tooth loss. Premortem tooth
loss can also result from a variety of dental
diseases that are very difficult to separate
(e.g., advanced caries, severe attrition, and
periodontal infections) (Hillson, 1986). The
most likely cause of premortem tooth loss
is the cumulative effect of these variables
DENTAL PATHOLOGY IN PONGO
317
(Koritzer, 1968). Advanced attrition or a seAge differences
vere cavity may allow the pulp chamber to
The significantly higher proportion of old
become infected, resulting in a periapical ab- adults afflicted with local infections and
scess and bone loss surrounding the root tip. horizontal bone loss, compared to young
However, according to Koritzer (19681, most adults, as well a s the higher (but insignifiperiodontal disease results in bone loss sur- cant) number with carious lesions and prerounding the sides of the teeth, not apically. mortem tooth loss is not unexpected. ObserKoritzer (1968) argues that i t is the combina- vations in various primate species have
tion of these processes that loosens the tooth revealed that the occurrence and severity of
enough to be lost from the socket. In a sample dental pathologies increases in older individof Egyptian human skeletal material which uals (Bramblett, 1965, 1967; Colyer,, 1936;
had a very low caries rate, Koritzer (1968) Hershkovitz, 1970; Kakehashi et al., 1963;
noted that premortem tooth loss occurred Kilgore, 1989; Lovell, 1990a, 1990b; Schultz,
when both advanced attrition and periodon- 1935, 1939).
In the Selenka sample there are two extal disease (measured by presence of calculus
deposits) were present. Premortem tooth ceptions to this phenomenon of increasing
loss was rarely observed when only one of dental pathologies with age. One young
adult female (specimen 25 1)exhibits alveothese pathological conditions was present.
lar
bone resorption and one periapical abWith these inherent difficulties of identiscess
above the left upper P3 (Figs. 1,8).This
fying and interpreting dental lesions in
may
be
a result of the crowding apparent in
mind, some possible explanations for the rethe maxilla. The other exception to the agesults of the dental pathologies observed in
related development of dental disease in this
the Selenka orangutan collection are presample is a young adult female with a large
sented below.
occlusal cavity on the upper left M2 (Fig. 3).
This condition could be due to any combination of factors affecting the development of
Sex differences in old adults
dental caries mentioned above or simply to
The higher frequency of dental pathologies idiosyncratic variation.
in females than males may result from the
exploitation of different microhabitats and
Sample differences
subsequent dietary differences in terms of
Comparisons
of the old adults in the Selthe proportion of types of foods eaten. At the
Kutai Nature Reserve, East Borneo, Rod- enka orangutan collection with observations
man (1977, 1988) noted that males eat less of dental pathologies in other orangutan
fruit and more bark than females. Although samples show that there is variability in
Galdikas (1978, 1979, 1988) did not observe prevalence of dental pathologies among the
this same pattern at the Tanjung Puting Re- available data. Although I recognize the difserve, Central Borneo, she did note that ficulties of comparing dental pathology data
males spend more time using a variety of collected from various investigators (Alexandersen, 19671, I would like to summarize the
ground resources that females do not regudifferences and discuss some factors that
larly exploit. Due to the significant effect a
may be responsible for these differences. The
soft carbohydrate-rich diet has on the devel- frequency of individuals afflicted with caries
opment of periodontal disease (Hillson, in different orangutan samples was 2% of
1986; Schluger et al., 19771, a higher con- all individuals (N = 255) (Colyer, 1936),29%
sumption of fruit by the females might affect of old adults (N = 45) (Schultz, 1935), and
the development of caries and periodontitis 20% of old adults (N = 15) in a sample of
and the subsequent horizontal bone loss and Bornean orangutans (Lovell, 1990b).No carlocal infections. Similarly, a less varied diet ious lesions were found in the young adults
in terms offood items eaten might contribute or juveniles (N = 11) in Lovell’s sample,
to the processes affecting the development while 6% of the young individuals from the
of dental disease.
Schultz sample had caries.
318
K.E. STONER
Schultz recorded osseous defects (abscesses) in 62% of old adults and 26% of
young adults while Lovell recorded the frequency of individuals with osseous defects
in her total sample as 26% (N = 27); 71% of
the osseous defects were in old adults, and
29% were found in young adults.
Using a comparable technique to the one
used here, Lovell found that 15% of her total
orangutan sample had a similar level of horizontal bone loss to that observed in the Selenka collection (Lovell’s scale, moderate or
severe). All individuals that had horizontal
bone loss in her sample were old adults. Premortem tooth loss was observed in only one
individual from Lovell’s Bornean sample.
Compared to the old adults in the Selenka
collection, Lovell, in a considerably smaller
sample, found a much higher proportion of
individuals with carious lesions. The frequencies of premortem tooth loss, local infections, and horizontal bone loss were more
similar between the Selenka and Lovell samples, but Lovell found a much higher frequency of osseous defects in young adults
and juveniles.
The old adults in the Selenka sample have
a much lower proportion (6%)of individuals
affected by carious lesions than those (29%)
reported for old adults by Schultz (1935).
Similarly, a lower proportion of old adults
in the Selenka sample are affected by local
infections (26%) when compared to the
Schultz sample (62%). This is difficult to interpret for various reasons. First, although
Schultz divided his sample into young and
old adults, no division was made between
the sexes. Because the Selenka orangutans
show sex differences in the frequency of dental pathologies, it is possible that unequal
sex distributions in the two samples may
account for the intergroup differences. Second, exact locality information for the
Schultz sample is not provided. Orangutan
specimens from both Borneo and Sumatra
were included in the analysis by Schultz
(1935) without separating individuals collected from different areas. Thus, the
Schultz sample appears to be drawn from a
wider and perhaps ecologically more diverse area.
Surely, some of the variation in dental pathologies among these samples is due to dif-
ferences in the ages and possibly proportion
of sexes within each sample, a s well a s various criteria for recognizing dental lesions.
However, the considerable variation in the
prevalence of dental pathologies among different orangutan samples may also relate to
the varying ecological conditions from which
the samples were drawn. One important factor could be ecological constraints that lead
to dietary differences among various areas.
Rodman (1988) stated that “despite a superficial appearance of uniformity of the southeast Asian forest, there is considerable variation between locations and within
smaller areas.”
Although orangutans are characterized by
frugivory, much variation has been found in
the time spent utilizing different food resources (Galdikas, 1978, 1979, 1988; MacKinnon, 1974; Rodman, 1977, 1988). Local
dietary habits in wild orangutan populations
have been noted by Galdikas (19781, who
found that the greatest difference between
the Tanjung Puting Reserve and other areas
of orangutan studies was the absence of
large fig trees in this region. Yet, figs comprise a major portion of orangutan diets a t
many other locations (Galdikas, 1978). Exploitation of different types of foods in different areas might account for the variation
observed in the occurrence of dental lesions
between the Selenka and Schultz samples.
For example, the ingestion of trace elements
(Hildebolt e t al., 1988; Leverett, 1982; Ludwig and Bibby, 1969) or particularly sticky
fruits (figs) are known to affect the development of caries in humans (Theilade and
Birkhead, 1986). They may well influence
the onset of dental disease in orangutans
from different populations. Unfortunately,
the precise location of where these samples
came from is not available, so it is impossible
to test this ecological hypothesis.
Differences between primates
Finally, comparisons of the prevalence of
dental pathologies observed in this sample
of orangutans to the frequency of individuals
with dental lesions in some other apes, indicate that orangutans have a slightly higher
occurrence of caries (6%)than gorillas, which
range from 1%to 3% (Lovell, 1990a; Schultz,
1935), but lower than observations of chim-
DENTAL PATHOLOGY IN PONGO
panzees, which range from 6% to 15% (Kil
gore, 1989; Lovell, 1990a; Schultz, 1935;
Schuman and Sognnaes, 1956).Ahigh occurrence of infra-alveolar or periapical osseous
defects (26%)and severe horizontal bone loss
(23%) is evident in the old adults in the
Selenka sample, which parallels results
from studies of gorillas and chimpanzees
(Kilgore, 1989; Lovell, 1990a; Schultz, 1935).
Premortem tooth loss is somewhat rare in
the Selenka orangutans (3%),unlike observations on chimpanzees and gorillas (Kilgore, 1989; Lovell, 1990a, 1990b; Schultz,
1935), in which premortem tooth loss is
much higher. In sum, compared to gorillas
and chimpanzees, orangutans may have a
relatively intermediate level of caries, a rare
frequency of premortem tooth loss, and a n
approximately comparable amount of osseous defects and horizontal bone loss.
~
CONCLUSIONS
This study demonstrates significant sexual differences in frequency of dental pathologies in orangutans. It is suggested that
these differences may be related to dietary
differences resulting from ecological separation of the sexes and exploitation of different
resources. In addition, this study supports
earlier observations which have documented
a n increase in dental pathologies with age
in wild primates. Finally, I suggest that differences in expression of dental disease between the Selenka orangutan sample and
other samples of orangutans are likely a result of local ecological differences that, in
turn, affect patterns of food consumption and
subsequent dental disease. Due to the absence of specific dietary components for all
samples it is impossible to explicitly test this
hypothesis with the current available data.
Additional long-term studies of foraging
in wild orangutans documenting differences
between the sexes and differences between
populations will help identify some of the
dietary factors affecting oral pathologies in
these animals. Furthermore, it would be useful to collect foraging data and dental disease
data from populations of orangutans from
known localities, for direct comparison of the
occurrence of oral disease with regional ecological factors.
319
ACKNOWLEDGMENTS
I would like to thank P. Schroter a t the
Anthropologisches Staatssammlung, Munchen, for help in gaining access to the Selenka collection and 0. Rohrer-Ertl for providing reprints and additional information
regarding his research on the Selenka collection. I thank the Department of Systematics
and Ecology, Division of Mammals, a t the
University of Kansas for providing financial
assistance for the photographs. I am grateful
to D.W. Frayer for the photographs and he,
L.S. Dryden, R.M. Timm, and a n anonymous
reviewer for critical comments and suggestions on a previous draft of this manuscript.
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