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Etiology of reactive arthritis in Pan paniscus P. troglodytes troglodytes and P

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American Journal of Primatology 66:219–231 (2005)
RESEARCH ARTICLE
Etiology of Reactive Arthritis in Pan paniscus,
P. troglodytes troglodytes, and P. troglodytes
schweinfurthii
BRUCE M. ROTHSCHILD1–5n and FRANK J. RÜHLI6,7
1
Arthritis Center of Northeast Ohio, Youngstown, Ohio
2
Department of Medicine, Northeast Ohio Universities College of Medicine, Rootstown,
Ohio
3
Department of Biomedical Engineering, University of Akron, Akron, Ohio
4
Division of Earth Sciences, Carnegie Institute, Pittsburgh, Pennsylvania
5
Kansas University Museum of Natural History, Lawrence, Kansas
6
Clinical Paleopathology Team, Orthopaedic University Clinic Balgrist and Institute for
the History of Medicine, University of Zurich, Zurich, Switzerland
7
Institute of Anatomy, University of Zurich, Zurich, Switzerland
The character of arthritis has not received the same attention in Pan
paniscus as it has in P. troglodytes. Reactive arthritis (a form of
spondyloarthropathy) in the latter has been considered to be either a
sexually transmitted or an infectious-agent diarrhea-related disorder.
The unique sexual promiscuity of P. paniscus enables us to distinguish
between those hypotheses. The macerated skeletons of 139 adult P.
paniscus, P. troglodytes troglodytes, and P. troglodytes schweinfurthii
were macroscopically analyzed for osseous and articular pathologies. The
sex of the animal was recorded at the time of acquisition. Twenty-one
percent of the P. paniscus, 28% of the P. t. troglodytes, and 27% of the P. t.
schweinfurthii specimens had peripheral and central joint erosive disease
characteristic of spondyloarthropathy. Subchondral pauciarticular distribution and reactive new bone clearly distinguish this disease from
rheumatoid arthritis, osteoarthritis, and direct bone/joint infection. The
fact that P. paniscus and P. t. troglodytes were similar in terms of disease
frequency makes the notion of sexual transmission unlikely. While the
frequencies of spondyloarthropathy were indistinguishable among all
species/subspecies studied, the patterns of joint involvement were
disparate. The Pan paniscus and P. t. troglodytes home ranges are
geographically separate. We assessed possible habitat factors (e.g.,
exposure to specific infectious agents of diarrhea) by comparing P.
paniscus and P. t. troglodytes with P. t. schweinfurthii. The latter shared
similar patterns and habitats (separated by the Congo River) with P.
paniscus. The explanation offered for habitat-specific patterns is
differential bacterial exposure–most likely Shigella or Yersinia in P.
n
Correspondence to: Bruce M. Rothschild, M.D., Arthritis Center of Northeast Ohio, 5500 Market,
Youngstown, OH 44512. E-mail: bmr@neoucom.edu
Received 29 June 2004; revised 23 October 2004; revision accepted 26 November 2004
DOI 10.1002/ajp.20140
Published online in Wiley InterScience (www.interscience.wiley.com).
r
2005 Wiley-Liss, Inc.
220 / Rothschild and Rühli
paniscus and P. t. schweinfurthii. Am. J. Primatol. 66:219–231, 2005.
r 2005 Wiley-Liss, Inc.
Key words: arthritis; spondyloarthropathy; chimpanzee; primate
infectious-agent diarrhea; Shigella
INTRODUCTION
The study of articular and osseous disease in the chimpanzee Pan paniscus
(bonobo, also referred to as the pygmy chimp because it shares a habitat with
pygmies) has been limited to traumatic, congenital abnormalities; direct,
suppurative infections; and ‘‘degenerative articular disease’’ [Jurmain, 1977,
2000; Kano, 1984; Zihlman, 1987], in contrast to Pan troglodytes [Jurmain, 1989;
Lovell, 1991; Rothschild & Woods, 1991a]. Occasional notations of osteoarthritis
and hypertrophic osteoarthropathy in wild-caught P. troglodytes [Marzke &
Merbs, 1984] contrast with the 28% frequency of a form of reactive erosive
arthritis in that species [Rothschild & Woods, 1991a].
In humans, reactive arthritis, or Reiter’s syndrome, is a predominantly
pauciarticular disorder that predominantly affects the extremities, spine, and
sacroiliac joints [Arnett, 1987; Resnick, 2002; Rothschild, 1982; Rothschild &
Martin, 1993]. The terms ‘‘pauciarticular’’ and ‘‘oligoarticular’’ both describe
arthritis that occurs in less than five peripheral joints. In genetically-predisposed
individuals, this phenomenon, which is a subclass of spondyloarthropathy,
frequently complicates genital infections and infectious-agent diarrhea. Chlamydia and perhaps Mycoplasma have been implicated for the former, while Shigella,
Salmonella, Yersinia, Campylobacter, and enteropathic Escherichia coli have
been implicated for the latter in humans and other primates [Ahvonen et al.,
1969; Bardin & Lathrop, 1992; Bengtsson et al., 1983; Borg et al., 1992; Buxton
et al., 2002; Calin & Fries, 1976; Cheevers and McGuire, 1988; Cohen et al., 1987;
Cole et al., 1970; Deighton, 1993; Dworkin et al., 2001; Graham, 1919; Granfors
et al., 1988; Hannu & Leirisalo-Repo, 1988; Hannu et al., 2002; Held & Whitney,
1978; Herrlinger & Asmussen, 1992; Hughes et al., 1991; Kanakoudi-Tsakalidous
et al., 1998; Katz, 1989; Kvien et al., 1994; Laasila & Leirisalo-Repo, 1999; Leino
et al., 1980; Leirisalo-Repo et al., 1997; Locht & Krogfelt, 2002; Locht et al., 1993,
2002; Maki-Ikola & Granfors, 1992; Maximov et al., 1992; Merilahti-Palo et al.,
1991; Putterman & Rubinow, 1993; Rothschild & Woods, 1993; Rudwaleit et al.,
2001; Simon et al., 1981; Snoy et al., 1985; Solitar et al., 1998; Stein et al., 1980;
Taccetti et al., 1994; Thompson-Handler et al., 1984; Thomson et al., 1994, 1995;
Tupchong et al., 1999; Yli-Kerttula et al., 1995; Zeidler et al., 2004]. Shigellarelated disease has also been documented in nonhuman primates [Brancker,
1985; Chapman & Crowell, 1977; Good et al., 1969; Griner, 1980; Klumpp et al.,
1986; Kourany & Porter, 1969; McClure, 1980; Neiffer et al., 2000; Urvater et al.,
2000].
Disorders in apes that must be distinguished from spondyloarthropathy
include osteoarthritis and infectious arthritis. The primary osseous changes that
occur with osteoarthritis are remodeling with spur or osteophyte formation, an
increase in the density of the subchondral plate, and formation of distal
metaphyseal interosseous cysts [Jaffe, 1972; Moskowitz et al., 1984]. The first
is recognized grossly. Subchondral plate changes and cysts must be identified by
x-rays or cross-sections. Occasionally, with very severe osteoarthritis the articular
surfaces may even become grooved and eburnated. Osteoarthritis is basically a
Bonobo/Chimpanzee Arthritis / 221
noninflammatory type of arthritis. Erosions or holes may disrupt the joint surface
cartilage, but actual erosion of subchondral bone is not found. In osteoarthritis,
overgrowth of bone occurs, but there is no bone resorption. The area between the
cartilage-covered bone and the site of insertion of the synovial membrane into the
bare or marginal area of bone is unaffected in osteoarthritis. It retains its normal
smooth, uninterrupted appearance.
Infectious arthritis is characterized by reactive bone formation with gross
distortion of the joint surface and underlying bone [Resnick, 2002; Rothschild &
Martin, 1993]. While not all infectious arthritis is associated with a filigree type
of bone reaction, such a reaction is essentially pathognomonic for infectious
arthritis. Occasionally, infectious arthritis may so distort the bony architecture
so as to cause actual fusion (bony ankylosis) of the joint. The gross distortion of
bony architecture, as recognized on x-ray, makes the diagnosis obvious. Both
osteoarthritis and infectious arthritis are clearly distinguishable from spondyloarthropathy, which is the subject of this report.
Given the dichotomy of sexual behavior between P. paniscus and
P. troglodytes [Boesch et al., 2002; de Waal, 1995; Dixson, 1998; Kano, 1980], it
is of interest to ascertain differential susceptibility and distribution of arthritis
among the species and subspecies. The especially promiscuous, frequent, and
variable sexual activities of P. paniscus [de Waal, 1995; Kano, 1990] include
female–female genito–genito rubbing, male–male mounting and rump contact,
and juvenile and adolescent copulation without intromission [Badrian & Badrian,
1984; Furuichi, 1987, 1989; Ihobe, 1992; Kano, 1980, 1992, 1996; SavageRumbaugh & Wilkerson, 1978]. The disparate sexual behaviors between these
two species enable investigators to assess the role of sexually-transmitted diseases
(e.g., Chlamydia) [Nunn et al., 2000; Thrall et al., 1997] or AIDS (immunodeficiency virus-related disease) in the development of primate arthritis. Sexual
transmission is considered because in humans, reactive arthritis is 100–200 times
more common in those affected by AIDS [Tehranzadeh et al., 2004], which
suggests a relationship with sexual behavior or the virus itself.
MATERIALS AND METHODS
The articular surfaces of 34 P. paniscus, 79 P. t. troglodytes, and 26 P. t.
schweinfurthii skeletons were examined by both authors, with concurrence on the
findings. Seventy-five percent of the P. paniscus, 30% of the P. t. troglodytes, and
55% of the P. t. schweinfurthii specimens were male. We analyzed the articular
manifestations in seven P. paniscus, 22 P. t. troglodytes, and seven P. t.
schweinfurthii specimens with sacroiliac or erosive disease.
The P. t. troglodytes specimens were examined by B.M.R., with concurrence
by Robert Woods [see Rothschild & Woods, 1991a]. The study was limited to
primates with M3 eruption. The P. paniscus and P. t. schweinfurthii skeletons
(from the Musée Royal de l’Afrique Centrale, Tervuren, Belgium) were compared
with P. t. troglodytes skeletons. All of the specimens were collected in the 1920s
and 1930s from free-ranging animals shot in the wild. The P. t. troglodytes
specimens were taken from the French Cameroons in coastal West Africa, Congo,
Gabon, and Nigeria; and P. t. schweinfurthii and P. paniscus were taken from the
Democratic Republic of Congo between 1935 and 1959. The habitat of P. t.
troglodytes ranges from the mouth of the Congo River into Cameroon. That of
P. Paniscus extends south of the Congo River into Congo and Zaire, while P. t.
schweinfurthii ranges north of the Congo River [Groves, 2001]. The sex of the
specimens was determined on the basis of data recorded at the time of acquisition.
222 / Rothschild and Rühli
The macerated skeletons were treated when they were acquired to remove
the soft tissues, and surveyed for visible evidence of articular and periarticular
joint pathology. Each skeletal element of the sampled individuals was carefully
observed independently by both authors, with concurrence as to whether the
observation represented an erosion, and to rule out artifacts such as postmortem
trauma (e.g., drawer damage). For the purposes of this study, articular surfaces
were considered missing if artifactual damage precluded the demonstration of
joint disease.
RESULTS
Moderate to severe osteoarthritis was present in six P. t. troglodytes, one
P. t. schweinfurthii, and one P. paniscus (Fisher’s exact test, P = 0.0266; Table I).
Infections in a proximal interphalangeal joint and an ischial tuberosity were
noted in two P. t. troglodytes. No osteoarthritis was noted in P. t. schweinfurthii,
and one instance of osteoarthritis (affecting the tibial component of one knee) was
noted in P. paniscus.
We analyzed the articular manifestations in the seven P. paniscus, 22 P. t.
troglodytes, and seven P. t. schweinfurthii individuals with sacroiliac or erosive
disease (Table I). This represents 21% of the P. paniscus, 28% of the P. t.
troglodytes, and 28% of the P. t. schweinfurthii specimens, which are statistically
indistinguishable frequencies (w2=0.6567). In the specimens whose sex was
recorded at the time of acquisition, this form of arthritis was five times more
common in female P. paniscus, compared to a 1:1.5 male predominance in P. t.
troglodytes. The difference was not statistically significant (Fisher’s exact test,
P = 0.3292), but the Beta error associated with such small numbers precludes a
confident exclusion of difference. We were unable to determine the sex ratio in
afflicted P. t. schweinfurthii individuals, because the sex of the affected animals of
that subspecies was not recorded at the time of acquisition.
The erosions (Figs. 1 and 2) were subchondral in distribution. The term
‘‘marginal,’’ as used herein, denotes the zone of metaphyseal bone that is within
the synovial membrane but is extrinsic to the cartilage-lined bone [Martel et al.,
1965; Resnick, 2002; Rothschild & Martin, 1993]. ‘‘Subchondral’’ refers to the
portion of the articular surface that was originally covered by cartilage. All
erosions were associated with the formation of new bone in a peri-erosional
pattern (Fig. 3). The new or reactive bone, bordering the rim of the erosion, was
TABLE I. Patterns of Arthritis in Pan
Species
Character
Osteoarthritis
Infectious arthritis
Spondyloarthropathy
Pauciarticulara
Polyarticulara
Sacroiliac involvementa
Pan paniscus
(34)
Pan t. troglodytes
(79)
Pan t. schweinfurthii
(26)
3
3
21
67
14
100
8
3
28
23
77
18
4
0
27
67
14
71
n
Numbers in parentheses are the number examined. Values represent the % frequency for each of the characters
examined.
a
Of specific Pan species members with spondyloarthropathy.
Bonobo/Chimpanzee Arthritis / 223
Fig. 1. Inferior oblique view of a distal tibia in Pan schweinfurthii. Large marginal erosions disrupt
the articular surface in their subchondral extension.
Fig. 2. Superior oblique view of the distal clavicles in Pan paniscus. Subchondral erosions can be
seen.
distinct from the metaphyseal bone surrounding it. Reactive bone was recognizable as a smooth, billowy, sclerotic growth at the periphery of the resorbed lesion.
Reactive bone was easily distinguished from the cracked and ragged edges
that are typically observed on the border of pseudo-erosions associated with
artifact. A lytic lesion, from which bone tissue has been removed by osteoclasts,
224 / Rothschild and Rühli
Fig. 3. Anterior-oblique view of proximal humeri in Pan paniscus. Marginal erosions with reactive
new bone formation can be seen.
presents smooth, rounded edges of any surfaces within and at the boundaries of
the lesion in dry bone [Leisen, 1987; Rothschild et al., 1988; Rothschild & Woods,
1991b]. Transitions from one plane of bone tissue to another are smoothed. The
edges of all exposed trabeculae, as in metaphyses of dense cortical bone, meet with
a rounded edge. Although inflammation lesions may activate osteoclastic
resorption of perilesional trabeculae, they subsequently activate osteoblastic
deposition in the same region [Leisen, 1987]. Thus, any trabecular edges that
are initially exposed at the lesion boundary by osteolysis subsequently appear
thicker than trabecular edges revealed by postmortem processes in the same
region.
The two groups with erosive disease exhibited different patterns of arthritis:
the erosions in all of the affected P. paniscus, P. t. troglodytes, and P. t.
schweinfurthii individuals were associated with reactive new bone formation
(Figs. 2 and 3; Table I). Peripheral joint erosive disease was predominantly
pauciarticular and symmetrical in two of three P. paniscus (67%) and two of three
P. t. schweinfurthii (67%), but only six of 22 P. t. troglodytes (27%) with peripheral
joint damage. A polyarticular pattern was found in one (14%) afflicted P. paniscus
and one (14%) P. t. schweinfurthii, compared to 17 (77%) P. t. troglodytes (w2 =
13.6192, Po0.0001). Five joints were affected in each of the P. paniscus and P. t.
schweinfurthii specimens with polyarticular disease. Five to 14 affected joints
were found in P. t. troglodytes with polyarticular disease, for an average of nine
affected joints. The same joints were predominantly affected in both P. paniscus
and P. troglodytes. Metacarpal phalangeal and metatarsal phalangeal joints were
more commonly affected in P. t. troglodytes,(w2 = 8.1119, Po0.005). Peripheral
joint fusion of an ankle was present in one P. t. schweinfurthii.
Bonobo/Chimpanzee Arthritis / 225
Fig. 4. En face view of the auricular area of the iliac portion of the sacroiliac joint in Pan troglodytes
schweinfurthii. Erosions with reactive new bone formation are evident.
Four (18%) of the afflicted P. t. troglodytes had sacroiliac erosions (Fig. 4) or
fusion, as did five of seven (71%) of P. t. schweinfurthii (Fisher’s exact test, P =
0.0170) and all seven P. paniscus (w2 = 15.099, Po0.0001). The erosions appeared
as multiple small crater-shaped holes with smooth, rounded edges. Syndesmophytes, presenting as calcification in the anulus fibrosus, and costovertebral joint
fusion were present in a single P. paniscus specimen.
DISCUSSION
Osteoarthritis
The occurrence of osteoarthritis in Pan was documented in previous studies
[Goodall, 1986; Rothschild & Woods, 1991a; Woods, 1986]. Osteoarthritis is
pathologically quite distinct from the erosive disease described in the current
study.
Infectious Arthritis
Infectious arthritis was actually quite rare in all of the Pan specimens
studied. Another variety of joint disease is erosive arthritis. This type of arthritis
leads to disruption of bone in either the marginal area or the subchondral bone,
resulting in grooves or holes (Figs. 1–4).
Spondyloarthropathy
In humans, spondyloarthropathy is generally associated with spinal involvement, similar to that noted in chimpanzees. Appendicular reactive erosive disease
in chimpanzees displays characteristics and distribution patterns similar to those
of spondyloarthropathy in humans [Rothschild & Woods, 1991a,b]. Given the
226 / Rothschild and Rühli
pattern of involvement, and the nature of the lesions, erosive disease in Pan
appears to be attributable to a specific clinical diagnosis: spondyloarthropathy
[Rothschild et al., 1988; Woods & Rothschild, 1988; Rothschild & Woods, 1991b].
Reactive arthritis is the most likely variety.
The remodeling that occurred around erosions (Figs. 2–4) was more
exuberant than that seen in human rheumatoid arthritis [Rothschild et al.,
1988; Woods & Rothschild, 1988], but was quite similar to that noted in human
spondyloarthropathy [Rothschild & Woods, 1991b]. In contrast to the minimal or
absent peri-erosional bone reaction noted in human rheumatoid arthritis
[Rothschild et al., 1988; Woods & Rothschild, 1988], the bone alterations in all
species of chimpanzees corresponded more to the reactive bone seen in human
spondyloarthropathy [Rothschild & Woods, 1991b].
Reactive Arthritis: Phylogenetic, Behavioral, or Environmental
Derivation
The original purpose of this study was to compare the frequency and
character of spondyloarthropathy (reactive arthritis) in P. paniscus and
P. troglodytes (specifically P. t. troglodytes). While the frequencies and
characteristics of disease were identical in the two groups (w2=0.6567), skeletal
distribution (w2 = 8.1119, Po0.005), extent of peripheral erosive disease
(w2 = 13.6192, Po0.0001), extent of sacroiliac joint disease (w2=15.099,
Po0.0001), and perhaps sex ratios (Fisher’s exact test, P = 0.3292, large Beta
error) varied. The identical frequency of reactive arthritis in hypersexed bonobos
and in chimpanzees with more conventional sexual activity is strong evidence
against the sexual-transmission hypothesis, and therefore of a role for
Chlamydia, Mycoplasma, or AIDS in its dénouement. This supports the notion
of an infectious-agent diarrhea etiology, but raises an interesting question: Is the
difference in patterns related to habitat?
Another potential contribution by behavior was knuckle walking, attributed
to P. paniscus [Boesch et al., 2002]. However, knuckle involvement is
characteristically noted in P. t. troglodytes, not P. paniscus. This and observations
in mountain Gorilla beringei and lowland G. gorilla (Rothschild and Ruhli, 2005,
this issue) do not support that possibility.
To address the question about habitat, we examined a second subspecies of
chimpanzee: P. t. schweinfurthii. This subspecies exhibits different sexual habits,
but shares habitats (separated only by the Congo River) with P. paniscus. Agents
of infectious diarrhea may be differentially represented in lowland animals (i.e.,
P. t. troglodytes) and those who live in more mountainous terrain (i.e., P. paniscus
and P. t. schweinfurthii).
We analyzed arthritis in the P. t. troglodytes, P. paniscus, and P. t.
schweinfurthii specimens to determine whether the difference in skeletal
distribution correlated with species or habitat. Infections were rare and occurred
at indistinguishable frequencies among all three. However, osteoarthritis was
more common in P. t. troglodytes than in either P. t. schweinfurthii or P. paniscus
(Fisher’s exact test, P = 0.0266), confirming this was not determined by species,
but was rather a subspecies phenomenon. The frequencies of osteoarthritis,
however, were indistinguishable between P. t. schweinfurthii and P. paniscus
(Fisher’s exact test, P = 0.4994), suggesting that a habitat-dependent factor
might be more important. While their habitats are separated by a river (the
Congo River) [Groves, 2001], we hypothesize that conditions may have been
sufficiently similar on both sides of the river to ‘‘cultivate’’ similar bacterial flora.
Bonobo/Chimpanzee Arthritis / 227
Osteoarthritis was more common in the lowland animals than in those that lived
in a mountainous terrain. It is difficult to compare our results with those reported
by Jurmain [2000], because of the sample sizes and the different diagnostic
criteria used in the previous study, which may not have distinguished between
osteoarthritis and reactive arthritis.
Reactive arthritis in P. paniscus and P. t. schweinfurthii was indistinguishable in frequency, skeletal distribution, and extent of erosive peripheral joint and
sacroiliac joint disease. The indistinguishable character and statistics across
(rather than within) species lines further suggest that the character of reactive
arthritis is determined by a habitat-related factor.
Habitat and Microorganisms
In humans, the causative organisms Escherichia coli, Salmonella, Campylobacter, Streptococcus pyogenes, Clostridium difficile, and Giardia lambdia are
predominantly associated with polyarticular disease, while Yersinia, Shigella, and
Chlamydia are associated with a pauciarticular pattern of arthritis (Table II). We
propose that this suggests identical susceptibility, but different ‘‘precipitating’’
organisms in P. paniscus and P. troglodytes (Escherichi coli, Salmonella, or
Camplyobacter for the former, and Shigella or Yersinia for the latter). The
patterns of disease in P. t. schweinfurthii and P. paniscus were indistinguishable.
Therefore, sexually transmitted/derived spondyloarthropathy is less likely. That
leaves the possibility that P. paniscus and P. t. schweinfurthii were both exposed
to the same organism–most likely Yersinia or Shigella. We believe the different
patterns of disease are not related to the primate species or subspecies, but rather
to the infecting organism. Similar patterns of disease have been demonstrated in
humans (Table II) [Ahvonen et al., 1969; Bardin & Lathrop, 1992; Bengtsson
et al., 1983; Borg et al., 1992; Buxton et al., 2002; Calin & Fries, 1976; Cheevers
and McGuire, 1988; Cohen et al., 1987; Cole et al., 1970; Deighton, 1993;
TABLE II. Frequency and Character of Reactive Arthritis Complicating Infectious Agent
Diarrhean
Organism
Frequency
(%)
Oliogoarticular
(%)
Polyarticular
(%)
Mean number of
affected joints
Streptococcus pyogenes
Escherichia coli
Salmonella typhimuriu
Salmonella enteritidis
Giardia lambdia
Clostridium difficile
Camplobacter jejuni
Chlamydia
Yersinia enterocolitica
Shigella flexneii
n.a.
6
2–15
14–33
n.a.
n.a.
1–24
n.a.
11–33
14–24
20
20
20
24
25
42
50
67
64–84
80–100
80
80
80
76
75
58
50
33
8–36
0–20
5+
5+
10
4.7–8.0
6
4+
5+
3
3.3–3.8
2.3–2.8
n
Derived from Ahvonen et al. [1969]; Bardin and Lathrop [1992]; Borg et al. [1992]; Buxton et al. [2002]; Calin
and Fries [1976]; Cohen et al. [1987]; Deighton [1993]; Dworkin et al. [2001]; Graham [1919]; Hannu and
Leirisalo-Repo [1988]; Hannu et al. [2002]; Herrlinger and Asmussen [1992]; Hughes et al. [1991]; KanakoudiTsakalidous et al. [1998]; Kvien et al. [1994]; Laasila and Leirisalo-Repo [1999]; Leino et al. [1980]; Leirisalo-Repo
et al. [1997]; Locht and Krogfelt [2002]; Locht et al. [1993, 2002]; Maki-Ikola and Granfors [1992]; Maximov et al.
[1992]; Merilahti-Palo et al. [1991]; Putterman and Rubinow [1993]; Rudwaleit et al. [2001]; Simon et al. [1981];
Solitar et al. [1998]; Stein et al. [1980]; Taccetti et al. [1994]; Thompson et al. [1994, 1995]; Tupchong et al. [1999];
Yli-Kerttula et al. [1995].
228 / Rothschild and Rühli
Dworkin et al., 2001; Graham, 1919; Hannu & Leirisalo-Repo, 1988; Hannu et al.,
2002; Herrlinger & Asmussen, 1992; Hughes et al., 1991; Kanakoudi-Tsakalidous
et al., 1998; Kvien et al., 1994; Laasila & Leirisalo-Repo, 1999; Leino et al., 1980;
Leirisalo-Repo et al., 1997; Locht & Krogfelt, 2002; Locht et al., 1993, 2002; MakiIkola & Granfors, 1992; Maximov et al., 1992; Merilahti-Palo et al., 1991;
Putterman & Rubinow, 1993; Rudwaleit et al., 2001; Simon et al., 1981; Solitar
et al., 1998; Stein et al., 1980; Taccetti et al., 1994; Thomson et al., 1994, 1995;
Tupchong et al., 1999; Yli-Kerttula et al., 1995].
The indistinguishable population penetrance in all three chimpanzee species/
subspecies (28% for P. t. troglodytes, 27% for P. t. schweinfurthii, and 21% for
P. paniscus) suggest that this is not the pertinent issue. This pattern is similar to
that observed in lowland gorillas (G. g. gorilla), 20% of which are afflicted
[Rothschild & Woods, 1991a], and with whom eastern chimpanzees share similar
habitat and extent and severity of disease, all much greater than the disease
in the mountain gorilla G. beringei habitat shared by P. t. troglodytes and
P. paniscus. Different habitat-related enteropathic infections are suspected.
Shigella-associated spondyloarthropathy presents as pauciarticular disease in zoo
colonies of lowland apes. In the wild, lowland apes exhibit spondyloarthropathy
with the same frequency, but with a polyarticular pattern [Rothschild & Woods,
1989]. This supports the notion that the occurrence of this disease is influenced
more by habitat (and probably organism) than by species or subspecies.
CONCLUSIONS
The characteristics of spondyloarthropathy in Pan enable us to distinguish
between sexual transmission and infectious-agent diarrhea transmission as
disease vectors, and to identify the latter as the predominant cause of this disease
in nonhuman primates. Chimpanzees and humans share a heritage and
susceptibility to infectious-agent diarrhea-related pathologies. Further genetic
and habitat analyses may help identify new approaches for preventing this
common scourge.
ACKNOWLEDGMENTS
We thank Drs. Wim van Neer and Wim Wendelen (Musée Royal de l’Afrique
Centrale), Bruce Lattimer and Lyman Jellema (Cleveland Museum of Natural
History), and Linda Gorden (National Museum of Natural History) for their
logistical and technical support in examining the collection.
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