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Comparison of arthritis characteristics in lowland Gorilla gorilla and mountain Gorilla beringei.

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American Journal of Primatology 66:205–218 (2005)
RESEARCH ARTICLE
Comparison of Arthritis Characteristics in Lowland
Gorilla gorilla and Mountain Gorilla beringei
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
Gorilla gorilla and the less-studied G. beringei occupy very different,
geographically separate habitats. We studied the occurrence of various
forms of arthritis to examine possible nature/nurture causality. The
macerated skeletons of 38 G. beringei and 99 G. gorilla individuals were
examined macroscopically for the presence of articular and osseous
pathologies. Contrasting with only isolated osteoarthritis and infectious
arthritis was the frequent occurrence of a form of erosive arthritis
associated with joint fusion. Twenty-one percent of the G. beringei and
20% of G. gorilla specimens were afflicted, which are statistically
indistinguishable frequencies. While both had prominent axial disease,
they differed in patterns of peripheral arthritis. Whereas G. beringei
showed a pauciarticular pattern, the pattern in G. gorilla was more often
polyarticular. Susceptibility to spondyloarthropathy was apparently
genetically imprinted before Gorilla separated into G. gorilla and G.
beringei. However, the different patterns of peripheral joint involvement
suggest a causality resulting from lifestyle (e.g., the presence/absence or
extent of knuckle walking) or a habitat-related infectious agent. Am. J.
Primatol. 66:205–218, 2005.
r 2005 Wiley-Liss, Inc.
Key words: spondyloarthropathy; gastroenteritis; arthritis
INTRODUCTION
The subfamily Homininae includes great apes and humans [Groves, 2001].
Gorilla gorilla and Homo sapiens vary only 1.6% in their nuclear DNA, and 8.8%
in mitochondrial DNA [Meder, 2004]. This compares to 1.8% and 10.6% variations
n
Correspondence to: Bruce M. Rothschild, M.D., Arthritis Center of Northeast Ohio, 5500 Market,
Youngstown, OH 44512. E-mail: bmr@neoucom.edu
Received 1 July 2004; revised 23 October 2004; revision accepted 26 November 2004
DOI 10.1002/ajp.20139
Published online in Wiley InterScience (www.interscience.wiley.com).
r
2005 Wiley-Liss, Inc.
206 / Rothschild and Rühli
in G. gorilla and Pan troglodytes (chimpanzee) for nuclear and mitochondrial
DNA, respectively [Hayasaka et al., 1988; Koop et al., 1989].
In 1970, Groves initially subdivided G. gorilla into three subspecies: gorilla,
beringei, and graueri [Groves, 2003] Subsequently, Ruvolo et al. [1994] and
Garner and Ryder [1996] divided Gorilla into only G. gorilla (‘‘western’’ or
lowland gorilla) and G. beringei (‘‘eastern’’ or mountain gorilla), and considered
graueri a subspecies of beringei. The latter classification is utilized in the present
analysis (Table I). The habitats of G. gorilla (81 500 E to 181 E and 61 250 N to 51 S)
and G. beringei (261 300 E to 291 450 E and 01 200 N to 31 500 S) are separated by
almost 600 miles, divided by an inhospitable (to gorillas) savannah [Meder, 1993,
2004; Morgan et al., 2003].
We chose to examine arthritis patterns for a comparative study of these
species, since such studies have documented reproducible patterns of disease
across the mammalian spectrum [Rothschild, 1993; Rothschild & Martin, 1993;
Rothschild & Rothschild, 1994, 1996a, b; Rothschild & Woods, 1989, 1991a,
1992a, b, 1996; Rothschild et al., 1993, 1994, 1997, 1998a, b, 2000]. A previous
examination (by B.M.R.) of the limited number of mountain gorilla specimens
scattered among North American collections suggested the occurrence of
spondyloarthropathy, but there were too few available specimens to allow
epidemiologic comparisons with the lowland gorilla.
Since the 1900s, inflammatory arthritis has been referred to generically as
rheumatoid arthritis [Rothschild & Martin, 1993]. Today the ‘‘rheumatoid’’
appellation is limited to individuals with a polyarticular, symmetrical peripheral
erosive arthritis that spares the axial/central joints, such as the sacroiliac and
zygapophyseal [Rothschild & Martin, 1993]. This refinement distinguishes the
second major form of inflammatory arthritis, spondyloarthropathy.
Spondyloarthropathy is the name given to a category of arthritis characterized by predominantly asymmetrical pauciarticular (i.e., involving less than five
peripheral joints) erosive arthritis with occasional peripheral joint fusion, as well
as axial joint involvement. However, despite the name, erosion and/or fusion of
the central sacroiliac and vertebrae often is not present. This category of disease
is divided into five varieties: reactive arthritis, psoriasis-related arthritis,
inflammatory bowel disease-related arthritis, ankylosing spondylitis, and an
undifferentiated form that cannot be labeled as one of the other four types.
TABLE I. Characteristics Distinguishing Gorilla gorilla and Gorilla beringein
Characteristic
Gorilla gorilla
Gorilla beringei
Geography
Habitat
Population size
Average male height
Average male weight
Nose
Hair
Silverback
Arm length
Preferred diet
Tannin content
Aggression
Within groups
Between groups
Western
Lowland
100,000
1.7 meters
140–160 kg
Broader
Short, brown/grey
To hips and upper thighs
Long
Fruit
Increased
Eastern
Mountain
3,380
1.75 meters
160–180 kg
Narrower
Long, black
To back
Short
Shoots/pith Stem/bark
Decreased
Rare
Rare
Rare
Common
n
Derived from Bradley et al. [2004]; Calvert [1985]; Meder [1993, 2004]; Morgan et al. [2003].
Gorilla Spondyloarthropathy / 207
Ankylosing spondylitis is a subgroup of spondyloarthropathy in which central
joint involvement predominates. Involvement uniformly ascends the vertebral
column over time, to eventually produce a frozen spine that mimics in appearance
a bamboo plant stem. Peripheral erosive disease is quite rare. Vertebral bridging
occurs by calcification of the outer layer of the intervertebral disk or anulus
fibrosus; the vertebral bodies, starting with the lower lumbar, are thus smoothly
united.
One variety that mirrors this form of spondyloarthropathy is that caused by
inflammatory bowel disease (e.g., ulcerative colitis and Crohn’s disease). Twenty
percent of humans with inflammatory bowel disease develop spondyloarthropathy, which is indistinguishable in its osseous manifestations from ankylosing
spondylitis. Peripheral joint erosions are rare in both.
The hyperplastic skin condition referred to as ‘‘psoriasis’’ is often
complicated by inflammatory arthritis. This is perhaps the most complicated
form of spondyloarthropathy, because psoriatic arthritis itself can be subdivided
into five varieties according to the distribution of the associated peripheral
arthritis. While the character of associated central joint involvement can mirror
that seen in ankylosing spondylitis, it is variable in the vertebral column
distribution, and frequently and preferentially targets the cervical vertebrae. The
anulus fibrosus bridging in psoriatic arthritis is often associated with exuberant
new bone formation, and produces a bulky bridge rather than the smooth,
continuous calcification seen in ankylosing spondylitis.
An exuberant bone reaction, especially at sites involving tendon, ligament, or
joint capsule insertion into bone, is frequently found in all forms of
spondyloarthropathy, especially in psoriatic arthritis and the fourth form of
spondyloarthropathy: reactive arthritis. Since these areas of insertion are
entheses, the terms ‘‘enthesial’’ and ‘‘enthesitis’’ are applied to the bone
reactions that affect such regions.
This fourth type of spondyloarthropathy was previously referred to as
Reiter’s syndrome. However, because of the controversy regarding the wartime
behavior of the person for whom the disease was originally named, the term
‘‘reactive arthritis’’ is now preferred. The word ‘‘reactive’’ emphasizes the fact
that there is an exaggerated tendency toward new bone formation, which is a
reaction to bacterial challenge. The term ‘‘challenge’’ is used because this is not
the result of direct bacterial invasion and/or growth in the joint, but rather a
phenomenon that occurs subsequent to resolution of the infection itself.
Analogously to Streptococcus-derived rheumatic fever, reactive arthritis complicates infectious agent diarrhea and certain sexually derived infections.
The extent and severity of spondyloarthropathy appeared to be less
significant in mountain gorillas than in their lowland counterparts. Therefore,
we were interested in studying a significant sample of both gorilla species to
ascertain the true population frequency of spondyloarthropathy in the mountain
gorilla, and to assess the perception that the disorder is less severe in the
mountain gorilla. The current study was undertaken to contrast mountain and
lowland gorillas in terms of the frequency and character of reactive arthritis
present in each species, and to utilize behavioral differences to predict which
pathway organisms are responsible for this condition.
MATERIALS AND METHODS
The complete articular skeletons of adult gorillas (G. gorilla and G. beringei)
were examined [Meder, 2004]. Only individuals with fused epiphyses were
208 / Rothschild and Rühli
included in the sample. We compared specimens of G. beringei (mountain gorilla),
from the Musée Royal de l’Afrique Centrale (Tervuren, Belgium), with specimens
of G. gorilla (lowland gorilla). The latter were obtained from the Department of
Anthropology at the Cleveland Museum of Natural History and the Department
of Mammology at the National Museum of Natural History (Smithsonian,
Washington, D.C.), but they represent the repositories of a single collection effort
[Rothschild & Woods, 1989, 1991a]. All of the samples were collected in the 1920s
and 1930s from free-ranging animals shot in the wild. The G. gorilla specimens
were taken from the French Cameroons in coastal West Africa, the Congo, Gabon,
and Nigeria; and the G. beringei specimens were taken from the Democratic
Republic of Congo. The latter, which were received by the museum in 1910–1958,
were subdivided into G. b. beringei from the Uganda-Zaire border and G. b.
graueri from the eastern Congo. Sex was determined on the basis of data recorded
at the time the skeleton was acquired.
The specimens had been previously treated with lye to remove the soft tissue.
They were surveyed for macroscopic evidence of articular and periarticular joint
pathology. Each skeletal element of the sampled G. beringei individuals was
carefully observed by both authors (B.M.R. and F.J.R.), and the G. gorilla samples
were examined by B.M.R. and Robert Woods [Rothschild & Woods, 1989].
Concurrence was obtained to ascertain erosion and rule out postmortem damage.
For the purposes of this study, articulations were listed as missing if any
artifactual damage precluded the demonstration of joint disease.
Chi-square and Fisher’s exact tests were used to assess the frequency of
spondyloarthropathy in both the species and the subspecies, and the frequencies
of the various types of joint involvement.
RESULTS
Thirty-eight G. beringei (50% male) and 99 G. gorilla (78% male) skeletons
were examined for evidence of articular or osseous pathology. Moderate to severe
osteoarthritis was present in one (3%) G. beringei and eight (8%) G. gorilla
specimens (Table II; Fisher’s exact test, P=0.365, n.s.). Evidence of osseous
infection was present in seven (7%) G. gorilla specimens, but was not found in
any of the G. beringei specimens (Table II; Fisher’s exact test, P=0.571, n.s.).
In the current study we analyzed the articular manifestations in the eight G.
beringei (21% of examined animals were afflicted) and 20 (20%) G. gorilla
individuals with sacroiliac or erosive disease (Table II), and noted the statistically
indistinguishable frequencies (w2=0.4388) in the two species. An examination of
the G. beringei subspecies (b. beringei and b. graueri) revealed that five of 20
(25%) and three of 18 (17%), respectively, were affected. Since those frequencies
did not differ significantly (Fisher’s exact test, P=0.2587, n.s.), and the character
of the disease (e.g., pauciarticular nature and joints affected) was indistinguishable between G. b. beringei and G. b. graueri, we did not consider subspecies
aspects any further in the current analyses. Among those specimens whose sex
was recorded at the time of acquisition, spondyloarthropathy was equally malepredominant (Table II) in G. beringei and G. gorilla (75% and 60%, respectively).
Erosions were marginal (bare area) and 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 [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
Gorilla Spondyloarthropathy / 209
TABLE II. Comparative Pathology in Mountain and Lowland Gorillas
Character
Gorilla beringei
Gorilla gorilla
Number examined
Percent male
Pathology (%)
Fractures (%)
Severe osteoarthritis (%)
Infection (%)
Spondyloarthropathy (%)
Percent male
Affected animal characteristics:
Only sacroiliac affected (%)
Peripheral joints affected (%)
Pauciarticular (%)
Polyarticular (%)
No. affected joints
Distribution (%)
Shoulder
Elbow
Wrist
Metacarpal phalangeal
Proximal interphalangeal
Distal interphalangeal
Hip
Knee
Ankle
Metatarsal phalangeal
Interphalangeal (pedal)
Sacroiliac joint
38
50
99
78
6
3
0
21
75
8
8
7
20
60
75
25
25
0
n. a.
20
80
40
40
5,6,8,10,14,15,15,21
12
0
0
0
0
0
12
12
0
0
0
100
5
20
50
70
60
25
0
15
40
50
40
10
Fig. 1. Palmar view of Gorilla gorilla metacarpals and phalanges. Erosive arthritis with reactive
new bone. Note the strong enthesial reaction in the proximal phalanges.
pattern (Figs. 1 and 2). The new or reactive bone, bordering the rim of the erosion,
was distinct from the metaphyseal bone surrounding it. Reactive bone was recognizable as a smooth, billowy, sclerotic growth at the periphery of the resorbed lesion.
210 / Rothschild and Rühli
Fig. 2. Palmar view of a G. gorilla metacarpal phalangeal joint. Subchondral erosion is prominent
on the proximal phalanx. Reactive new bone formation with remodeling of the metacarpal is
evident.
This growth was easily distinguished from the cracked and ragged edges that
are typically observed on the border of pseudo-erosions associated with artifact. In
dry bone, unmagnified or under magnification of r40 , a lytic lesion, from
which bone tissue has been removed by osteoclasts, presents smooth, rounded
edges of any surfaces within and at the boundaries of the lesion [Leisen et al.,
1987; Rothschild & Woods, 1991b; Rothschild et al., 1988]. Transitions from one
plane of bone tissue to another are smoothed. The edges of all exposed trabeculae
appear smoothed, while intersecting planes of dense cortical bone meet with a
rounded edge. Although inflammation initially may activate osteoclastic resorption of perilesional trabeculae, it subsequently activates osteoblastic deposition in
the same region [Leisen et al., l987]. Thus, any trabecular edges initially exposed
at the lesion boundary by osteolysis subsequently appear thicker than trabecular
edges revealed by postmortem processes in the same region.
In contrast to the minimal or absent peri-erosional bone reaction noted in
human rheumatoid arthritis [Rothschild et al., 1988; Woods & Rothschild, 1988],
that of both species of gorillas corresponded more to the reactive bone seen in
human spondyloarthropathy [Rothschild & Woods, 1991b]. New bone formation
(enthesitis) at sites of tendon, ligament, and capsule (entheses) was also noted.
Two patterns of arthritis were represented among the two species with
regard to erosive disease affecting the peripheral joints. Peripheral joint
involvement was found in 25% (2/8) of afflicted G. beringei (100%) and 80%
(16/20) of afflicted G. gorilla individuals (w2=1.800, n.s.). A polyarticular pattern
was found in none (0%) of the peripherally afflicted G. beringei, as compared to
eight of 16 (50%) afflicted G. gorilla (w2=1.800, n.s., possibly related to sample
size). Five to 21 joints (average=10) were affected in the latter. Different joints
were affected (Table II) in the two species. The metatarsal phalangeal, metacarpal
Gorilla Spondyloarthropathy / 211
phalangeal, and interphalangeal (both manus and pes) joints were more
commonly affected in G. gorilla (w2=8.119, Po0.005).
Limiting the statistical analysis to only afflicted gorillas, all eight (100%) of
the afflicted G. beringei had sacroiliac erosions (Fig. 3) or fusion (Fig. 4), as
compared to two of 20 (10%) G. gorilla (w2=20.160, Po0.0001). The erosions
appeared as multiple small crater-shaped holes with smooth, rounded edges.
Syndesmophytes (calcification in the anulus fibrosus) were present in two
G. beringei (5%) (Figs. 5 and 6) and four G. gorilla (20%) specimens, and
costovertebral joint fusion was observed in one individual of each species.
DISCUSSION
Frequency of Arthritis and Pathophysiology of Spondyloarthritis
The prevalence of all forms of arthritis was indistinguishable between
mountain gorilla (Gorilla bereingei) and their lowland relatives (G. gorilla), and
even within subspecies of the former. This uniform frequency may be related to a
uniform genetic predisposition (i.e., the possession of similar risk factors).
The histocompatibility gene (HLA-B27, MHC class I) predisposes humans to
spondyloarthropathy [Khare et al., 1998; Schlosstein et al., 1973]. Several
hypotheses have been offered to explain this, including a role in antigen
presentation, CD8 T (suppressor) cell modulation, and molecular mimicry
(antigenic similarities between the host tissue and enteropathic bacteria) [Allen
et al., 1999; Burmester et al., 1995]. Insertion into rats with a gene sequence
coding for HLA-B27 demonstrated that this predisposition to spondyloarthropathy is transpecific [Zhou et al., 1998].
HLA-B27 is unique among MHC class I molecules because it possesses a deep
‘‘B’’ pocket or epitope that allows binding of bulky, positively charged (because of
Fig. 3. ‘‘En face’’ view of the auricular portion of a G. gorilla sacroiliac joint. Erosions can be seen
throughout the auricular surface.
212 / Rothschild and Rühli
Fig. 4. Anterior view of a G. gorilla pelvis, showing unilateral right sacroiliac joint fusion. Note
the prominent right-sided lumbar vertebral body osteophytes, with a prominent bulky left
syndesmophyte at the same level.
arginine at the second B-27 position) peptides [Jardetzky et al., 1991; Rammensee
et al., 1995; Rötzschke et al., 1994]. There are more than 20 variations within the
pocket of the B27 molecule, not all of which appear to cause a predisposition to
spondyloarthropathy [Allen et al., 1999; de Castro, 1998]. In addition to the
apparently mandatory second position of arginine, position 45 glutamic acid and
position 67 cysteine apparently are required [Buxton et al., 1992; Rojo et al.,
1993]. The occurrence of spondyloarthropathy depends not only on host
susceptibility, but also on external microorganisms (in the form of infectiousagent diarrhea) [Ahvonen et al., 1969; Bardin & Lathrop, 1992; Borg et al., 1992;
Buxton et al., 2002; Calin & Fries, 1976; Cohen et al., 1987; Deighton, 1993;
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]. Of note is the contraction of
spondyloarthropathy by 20–30% in individuals who develop Shigella dysentery, if
they possess HLA-B27. This contrasts with a frequency of 0.25% if they do not
[Keat, 1988]. It has been suggested that 60–80% of human individuals with at
least the reactive form of spondyloarthropathy have HLA-B27, an allele that is
present in 8–13% of Caucasian populations [Märker-Hermann et al., 2004].
Gorillas have HLA-A, B, and C loci, but do not have a specific histocompatibility equivalent to human HLA-B27 [Lawler et al., 1991; Watkins et al., 1991].
Gorilla Spondyloarthropathy / 213
They do, however, have a region with partial sequence and functional homology
[Urvater et al., 2001]. That sequence is not relatable to the sequence of human
HLA-B27, but only to the epitope (the focal site in which binding of the abovementioned molecules occurs). While systematic screening of gorillas to assess the
frequency of this epitope has not been completed, almost all specimens examined
to date (lowland G. gorilla, independently of spondyloarthropathy affliction) have
had this epitope [Urvater et al., 2001]. The gorilla epitope most similar to HLAB27 was labeled Gogo B01. Gogo B0101 differs from HLA-Bn1513 by 21 residues,
and from HLA-Bn2702 by 22 residues [Urvater et al., 2001]. Most (15) of the
differences occurred in the peptide binding region, the polymorphic alpha-1 and
alpha-2 domains. Residues 71–90 of the alpha-1 domain are identical to HLABn2702, a sequence that is not unique to HLA-B27 in humans, and is not even
conserved among all types of human B27, such as 2705. Substitutions of
methionine (for glutamic acid at position 45) and serine (for cysteine at position
67) are noted in Gogo B01 (contrasted with B27). Such substitutions in human
B27 significantly decrease arginine peptide binding. They shrink the epitope pocket
size and change the charge from negative to neutral. Such a modification usually
interferes with binding and thus with susceptibility to spondyloarthropathy.
Character of Arthritis
The G. beringei and G. gorilla specimens differed significantly in terms of
skeletal distribution and severity of erosive peripheral disease. This represents
an unusual phenomenon in data-based skeletal analysis, and is similar only to
previous observations in Pan (Rothschild and Rühli, 2005, this issue). The
reproducibility of disease characteristics across mammalian species lines has been
clearly documented for spondyloarthropathy [Rothschild, 1993; Rothschild &
Martin, 1993; Rothschild & Rothschild, 1994, 1996a, b; Rothschild & Woods, 1989,
1991a, 1992a, b, 1996; Rothschild et al., 1993, 1994, 1997, 1998a, b, 2000]. The
severity may vary, but the skeletal distribution is reproducible. Population
frequency has shown significant variation over time in a number of species, but
apparently is independent of geography [Rothschild & Rothschild, 1993, 1996a, b;
Rothschild & Woods, 1992c].
Gorillas appear to differ in terms of the character of the resultant arthritis,
rather than in susceptibility. Is this a manifestation of habitat? Does the high
frequency of hand involvement in lowland gorillas (apparently related to knuckle
walking) reflect the absence of knuckle walking in mountain gorillas [Bradley
et al., 2004; Tuttle & Watts, 1985]? Enthesitis was equally represented in both
groups, implying that activity levels probably did not differ much between the
species [Shaibani et al., 1993].
Thus, another factor may be more significant: Spondyloarthropathy is a type
of arthritis that is inducible by infectious-agent diarrhea [Resnick, 2002;
Rothschild & Martin, 1993]. Several enteropathic organisms have been
recognized as playing a role in this disease, and have been associated with
specific joint distributions and ancillary abnormalities. Perhaps the difference
between mountain and lowland gorillas can be explained by the presence of
different habitat-related pathogens.
Escherichia coli, Salmonella, Campylobacter, Streptococcus pyogenes, Yersinia, Shigella, Clostridium difficile, and Giardia lambdia can all cause infectiousagent diarrhea and spondyloarthropathy in humans [Ahvonen et al., 1969; Bardin
& Lathrop, 1992; Borg et al., 1992; Buxton et al., 2002; Calin & Fries, 1976; Cohen
et al., 1987; Deighton, 1993; Dworkin et al., 2001; Graham, 1919; Hannu &
214 / Rothschild and Rühli
Fig. 5. Anterior view of a G. beringei pelvis and lumbar vertebrae, showing partial sacroiliac joint
fusion and prominent syndesmophytes.
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; Maki-Ikola & 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].
Escherichia coli, Salmonella, Campylobacter, S. pyogenes, C. difficile, and G.
lambdia all cause a predominantly polyarticular arthritis, while pauciarticular
disease is caused by Yersinia and Shigella.
We suggest that there are identical susceptibility, but different ‘‘precipitating’’ organisms in G. gorilla and G. bereingei, and that Shigella or Yersinia is the
likely infecting agent in G. bereingei (as it is in Pan paniscus (Rothschild and
Rühli, submitted)). The notion that exposure to an infecting organism, rather
than species specificity, is the important factor in these findings is supported by a
comparison of wild-caught and zoological park-derived G. gorilla individuals. The
pattern of arthritis in wild-caught gorillas is polyarticular, suggesting a possible
role for E. coli, Salmonella, Campylobacter, S. pyogenes, C. difficile, or G.
lambdia. Shigella is well recognized as the stimulus for spondyloarthropathy in
Gorilla Spondyloarthropathy / 215
Fig. 6. Anterior oblique view of a G. beringei lumbar spine, showing syndesmophytes effacing disk
space visibility, and zygapophyseal (facet) joint fusion.
captive G. gorilla individuals, which manifest a pauciarticular pattern of arthritis
[Neiffer et al., 2000; Raphael et al., 1995], producing a pauciarticular pattern of
arthritis. Thus the pattern is habitat-specific, rather than species-specific. A
similarity between bacterial contamination in zoo and natural Gorilla bereingei
habitats is suggested.
Gorilla habitats include primary and secondary rain forest, swamp forest,
montane forest, and marshy clearings (bais) [Meder, 2004]. The speculation that
tannin (which is increased in the diet of G. gorilla [Calvert, 1985]) binds excess
dietary iron or helps to maintain a healthy population of gut microbes [Remis,
2001] may be pertinent to the issue of which microorganisms precipitate
spondyloarthropathy. Gorillas do ingest their own feces, which may promote
microbial infection [Harcourt & Stewart, 1978].
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 Robert Woods and Linda Gorden (National Museum of Natural
History) for examining the collection and providing logistical and technical
support.
REFERENCES
Ahvonen P, Sievers K, Aho K. 1969. Arthritis
associated with Yersinia enterocolitica infection. Acta Rheum Scand 15:232–253.
Allen RL, Bowness P, McMichael A. 1999. The
role of HLA-b27 in spondyloarthritis. Immunogenetics 50:220–227.
216 / Rothschild and Rühli
Bardin T, Lathrop GM. 1992. Postvenereal
Reiter’s syndrome in Greenland. Rheum
Dis Clin North Am 18:1–93.
Borg AA, Gray J, Dawes PT. 1992. Yersiniarelated arthritis in the United Kingdom. A
report of 12 cases and review of the
literature. Q J Med New Ser 84:575–582.
Bradley BJ, Doran-Sheehy DM, Lukas D,
Boesch C, Vigilant L. 2004. Dispersed male
networks in western gorillas. Curr Biol
14:510–513.
Burmester BR, Daser A, Kabradi T, Krause A,
Mitchison NA, Sieper J, Wolf N. 1995.
Immunology of reactive arthritides. Annu
Rev Immunol 13:229–250.
Buxton SE, Benjamin RJ, Clayberger C,
Parham P, Krensky AM. 1992. Anchoring
pockets in human histocompatibility complex leukocyte antigen (HLA) class I molecular analysis of the conserved B(‘‘45’’)
pocket of HLA B27. J Exp Med 175:
809–820.
Buxton JA, Fyfe M, Berger S, Cox MB, Northcott KA, Multiprovincial Salmonella typhimurium Case-Control Study Group. 2002.
Reactive arthritis and other sequelae following sporadic Salmonella typhimurium infection in British Columbia, Canada: a case
control study. J Rheumatol 29:2154–2158.
Calin A, Fries JF. 1976. An ‘experimental’
epidemic of Reiter’s syndrome revisited:
follow-up evidence on genetic and environmental factors. Ann Intern Med 84:564–566.
Calvert JJ. 1985. Food selection by western
lowland gorillas in relation to food chemistry. Oecologia 65:236–246.
Cohen JI, Bartlett JA, Corey GR. 1987. Extraintestinal manifestations of Salmonella infections. Medicine 66:349–388.
de Castro JA. 1998. The pathogenetic role of
HLA-b27 in chronic arthritis. Curr Opin
Immunol 10:59–66.
Deighton C. 1993. Beta hemolytic streptococci
and reactive arthritis in adults. Ann Rheum
Dis 52:475–482.
Dworkin MS, Shoemaker PC, Goldoft MJ,
Kobayashi JM. 2001. Reactive arthritis and
Reiter’s syndrome following an outbreak of
gastroenteritis caused by Salmonella enteritidis. Clin Infect Dis 33:1010–1014.
Garner KJ, Ryder OA. 1996. Mitochondrial
DNA diversity in gorillas. Mol Phylogenet
Evol 6:39–48.
Graham G. 1919. Arthritis in dysentery: its
causation, prognosis and treatment. Proc R
Soc Med Lond 13:23–42.
Groves CP. 2001. Primate taxonomy. Washington: Smithsonian Institution Press.
280 p.
Groves CP. 2003. A history of gorilla taxonomy. In: Taylor AB, Goldsmith ML, editors.
Gorilla biology. Cambridge: Cambridge University Press. p 15–34.
Hannu TJ, Leirisalo-Repo M. 1988. Clinical
picture of reactive Salmonella arthritis.
J Rheumatol 15:1668–1671.
Hannu T, Mattila L, Rautelin H, Pelkonen P,
Lahdenne P, Siitonen A, Leirisalo-Repo M.
2002. Campylobacter-triggered reactive arthritis: a population-based study. Rheumatology 41:312–318.
Hannu T, Kauppi M, Tuomala M, Laaksonen I,
Klemets P, Kuusi M. 2004. Reactive arthritis following an outbreak of Campylobacter
jejuni infection. J Rheumatol 31:528–530.
Harcourt AH, Stewart KJ. 1978. Coprophagy
by wild mountain gorillas. East Afr Wildl J
16:223–225.
Hayasaka K, Gojobori T, Hovai S. 1988.
Molecular phylogeny and evolution of primate mitochondrial DNA. Mol Biol Evol
5:626–644.
Herrlinger JD, Asmussen J-U. 1992. Long
term prognosis in Yersinia arthritis: clinical
and serological findings. Ann Rheum Dis
51:1332–1334.
Hughes RA, Hyder E, Tehame JD, Keat AC.
1991. Intra-articular chlamydial antigen
and inflammatory arthritis. Q J Med
80:575–588.
Jardetzky TS, Lane WS, Robinson RA, Madden DR, Wiley DC. 1991. Identification of
self peptides bound to purified HLA B27.
Nature 353:326–329.
Kanakoudi-Tsakalidous F, Pardalos G, Pratsidou-Gertsi P, Kansouzidou-Kanakoudi A,
Tsangaropoulou-Stinga H. 1998. Persistent
of severe course of reactive arthritis following Salmonella enteritidis infection. Scand J
Rheumatol 27:431–434.
Keat A. 1988. Reiter’s syndrome and reactive
arthritis in perspective. N Engl J Med
309:1606–1616.
Khare SD, Bull MJ, Hanson J, Luthra HS,
David CS. 1998. Spontaneous inflammatory
disease in HLA-B27 transgenic mice is
independent of MHC class II molecules: a
direct role for B27 heavy chains and not B27derived peptides. J Immunol 160:101–106.
Koop BF, Tagel Dan, Goodman M, Slightom
JL. 1989. A molecular view of primate
phylogeny and important systematic and
evolutionary questions. Mol Biol Evol 6:
580–612.
Kvien TK, Glennas A, Melby K, Granfors K,
Andrup O, Karstensen B, Thoen JE. 1994.
Reactive arthritis: incidence, triggering
agents and clinical presentation. J Rheumatol 21:115–122.
Laasila K, Leirisalo-Repo M. 1999. Recurrent
reactive arthritis associated with urinary
tract infection by Escherichia coli. J Rheumatol 26:2277–2279.
Lawler DA, Warren D, Taylor P, Parham P.
1991. Gorilla class I major histocompatibility complex alleles: comparison to human
Gorilla Spondyloarthropathy / 217
and chimpanzee class I. J Exp Med
174:1491–1509.
Leino R, Makela A-L, Tiilikainen A, Toivanen
A. 1980. Yersinia arthritis in children.
Scand J Rheumatol 9:245–249.
Leirisalo-Repo M, Helenius P, Hannu T,
Lehtinen A, Kreula J, Taavitsainen M,
Koskimies S. 1997. Long term prognosis of
reactive Salmonella arthritis. Ann Rheum
Dis 56:516–520.
Leisen JC, Duncan H, Riddle JM, Pitchford WC.
1987. The erosive front: a topographic study
of the junction between the pannus and the
subchondral plate in the macerated rheumatoid metacarpal head. J Rheumatol 15:17–22.
Locht H, Kihlstrom E, Lindstrom FD. 1993.
Reactive arthritis after Salmonella among
medical doctors–study of an outbreak.
J Rheumatol 20:845–848.
Locht H, Krogfelt KA. 2002. Comparison of
rheumatologic and gastrointestinal symptoms after infection with Campylobacter
jejuni/coli and entertoxigenic Escherichia
coli. Ann Rheum Dis 61:448–452.
Locht H, Molbak K, Krogfelt KA. 2002. High
frequency of reactive joint symptoms after
an outbreak of Salmonella enteritidis.
J Rheumatol 29:767–771.
Maki-Ikola O, Granfors K. 1992. Salmonellatriggered reactive arthritis. Scand J Rheumatol 21:265–270.
Märker-Hermann E, Frauendorf E, Zeidler H,
Sieper J. 2004. Pathogeneses der ankylosierenden Spondylitis–Mechanismen der
Krankheitsentstehung und Chronifizierung. Zeitschrift Rheumatol 63:187–192.
Maximov AA, Shaikov AV, Lovell DJ, Giannini
EH, Soldatova SL. 1992. Chlamydia associated syndrome of arthritis and eye involvement in young children. J Rheumatol
19:1794–1797.
Meder A. 1993. Gorillas. Ökologie und Verhalten. Heidelberg: Springer. 186 p.
Meder A. 2004. Http://www.angela-meder.de/
publik/eep.pdf
Merilahti-Palo R, Soderstrom K-O, LahesmaaRantala R, Granfors K, Toivanen A. 1991.
Bacterial antigens in synovial biopsy specimens in Yersinia triggered reactive arthritis. Ann Rheum Dis 50:87–90.
Morgan BJ, Chris W, Atanga E. 2003. Newly
discovered gorilla population in the Ebo
Forest, Littoral Province, Cameroon. Int J
Primatol 24:1129–1137.
Neiffer DL, Rothschild BM, Marks SK, Urvater JA, Watkins DI. 2000. Management of
reactive arthritis in a juvenile gorilla (Gorilla gorilla gorilla) with long-term sulfasalazine therapy. J Zoo Wildl Med 31:539–551.
Putterman C, Rubinow A. 1993. Reactive
arthritis associated with Clostridium difficile pseudomembranous colitis. Semin
Arthritis Rheum 22:420–426.
Rammensee II G, Friede T, Stevanovic S.
1995. MHC ligands and peptide motifs: first
listing. Immunogenetics 41:178–228.
Raphael BL, Calle PP, Haramati N, Watkins
DI, Stetter MD, Cook RA. 1995. Reactive
arthritis subsequent to Shigella flexneri in
two juvenile lowland gorillas (Gorilla gorilla gorilla). J Zoo Wildl Med 26:132–138.
Remis MJ. 2001. Ranging and grouping
patterns of a western lowland gorilla group
at Bai Hokou, Central African Republic. Am
J Primatol 43:111–133.
Resnick D. 2002. Diagnosis of bone and joint
disorders. Philadelphia: W.B. Saunders.
4944 p.
Rojo S, Garcia F, Villadangos JA, de Castro JA.
1993. Changes in the repertoire of peptides
bound to HLA-B27 subtypes and to site
specific mutants inside and outside pocket
B. J Exp Med 177:613–620.
Rothschild BM, Turner KR, DeLuca MA. 1988.
Symmetrical erosive peripheral polyarthritis in the late archaic period of Alabama.
Science 241:1498–1501.
Rothschild BM, Woods RJ. 1989. Spondyloarthropathy in gorillas. Semin Arthritis
Rheum 18:267–276.
Rothschild BM, Woods RJ. 1991a. Reactive
erosive arthritis in chimpanzees. Am J
Primatol 25:49–56.
Rothschild BM, Woods RJ. 1991b. Spondyloarthropathy: erosive arthritis in representative defleshed bones. Am J Phys Anthropol
85:125–134.
Rothschild BM, Woods RJ. 1992a. Spondyloarthropathy as an Old World phenomenon.
Semin Arthritis Rheum 21:306–316.
Rothschild BM, Woods RJ. 1992b. Erosive
arthritis and spondyloarthropathy in Old
World primates. Am J Phys Anthropol 88:
389–400.
Rothschild BM, Woods RJ. 1992c. Character of
pre-Columbian North American spondyloarthropathy. J Rheumatol 19:1229–1235.
Rothschild BM. 1993. Arthritis in Callithrix
jacchus: calcium pyrophosphate deposition
disease and spondyloarthropathy. J Med
Primatol 22:313–316.
Rothschild BM, Martin L. 1993. Paleopathology: disease in the fossil record. London:
CRC Press. 386 p.
Rothschild BM, Rothschild C. 1993. Nineteenth century spondyloarthropathy independent of socioeconomic status: lack of
skeletal collection bias. J Rheumatol
20:314–319.
Rothschild BM, Wang X-M, Cifelli R. 1993.
Spondyloarthropathy in Ursidae: a sexually
transmitted disease? Natl Geogr Res Explor
9:382–384.
Rothschild BM, Rothschild C. 1994. No laughing matter: spondyloarthropathy in Hyaenidae. J Zoo Wildl Med 25:259–263.
218 / Rothschild and Rühli
Rothschild BM, Wang X-M, Shoshani J. 1994.
Spondyloarthropathy in proboscideans.
J Zoo Wildl Med 25:360–366.
Rothschild BM, Rothschild C. 1996a. Epidemic
of spondyloarthropathy in baboons. J Med
Primatol 25:69–70.
Rothschild BM, Rothschild C. 1996b. Transmammalian pandemic of inflammatory
arthritis (spondyloarthropathy variety):
persistence since the Pleistocene. Paleontol
Soc Publ 8:330.
Rothschild BM, Woods RJ. 1996. Inflammatory arthritis in Pongo. J Med Primatol
25:414–418.
Rothschild BM, Hong N, Turnquist JE. 1997.
Naturally occurring spondyloarthropathy in
Cayo Santiago rhesus macaques. Clin Exp
Rheumatol 15:45–51.
Rothschild BM, Rothschild C, Woods RJ.
1998a. Inflammatory arthritis in large cats:
an expanded spectrum of spondyloarthropathy. J Zoo Wildl Med 29:279–284.
Rothschild BM, Sebes JI, Rothschild C. 1998b.
Antiquity of arthritis: spondyloarthropathy
identified in the paleocene of North America. Clin Exp Rheumatol 16:573–575.
Rothschild BM, Rothschild C, Woods JR. 2000.
Inflammatory arthritis in canids: spondyloarthropathy. J Wildl Med 32:58–64.
Rothschild BM, Rühli FJ. 2005. Etiology of
reactive arthritis in Pan paniscus, P. troglodytes troglodytes, and P. troglodytes Schweinfurthii. Am J Primatol 66:219–231.
Rötzschke O, Falk K, Stevanovic S, Gnau V,
Jung GN, Rammensee H-G. 1994. Dominant aromatic/aliphatic C-terminal anchor
in HLA-Bn2702 and Bn2705 peptide motifs.
Immunogenetics 39:74–77.
Rudwaleit M, Richter S, Braun J, Sieper J.
2001. Low incidence of reactive arthritis in
children following a Salmonella outbreak.
Ann Rheum Dis 60:1055–1057.
Ruvolo M, Pan D, Zehr S, Goldberg T, Disotell
TR, Von Dornum M. 1994. Gene trees and
hominoid phylogeny. Proc Natl Acad Sci U S
A 91:8900–8904.
Schlosstein L, Terasaki PL, Bluestone R,
Pearson CM. 1973. High association of an
HL-A antigen, w27, with ankylosing spondylitis. N Engl J Med 288:704–706.
Shaibani A, Workman R, Rothschild B. 1993.
The significance of enthesitis as a skeletal
phenomenon. Clin Exp Rheumatol 11:
399–403.
Simon DG, Kaslow RA, Rosenbaum J, Kaye
RL, Calin A. 1981. Reiter’s syndrome
following epidemic shigellosis. J Rheumatol
8:969–973.
Solitar BM, Lozada CJ, Tseng C-E, Lowe, AM.
1998. Reiter’s syndrome among Asian shipboard immigrants: the case of the Golden
Venture. Semin Arthritis Rheum 27:
293–300.
Stein HB, Abdullah A, Robinson HS, Ford DK.
1980. Salmonella reactive arthritis in British Columbia. Arthritis Rheum 23:206–210.
Taccetti G, Trapani S, Ermini M, Falcini F.
1994. Reactive arthritis triggered by Yersinia enterocolitica: a review of 18 pediatric
cases. Clin Exp Rheum 12:681–684.
Thomson GT, Alfa M, Orr K, Thomson BR,
Olson N. 1994. Secretory immune response
and clinical sequelae of Salmonella infection in a point source cohort. J Rheumatol
21:132–137.
Thomson GT, DeRubeis DA, Hodge MA,
Rajanayagam C, Inman RD. 1995. PostSalmonella reactive arthritis: late clinical
sequelae in a point source cohort. Am J Med
98:13–21.
Tupchong M, Simor A, Dewar C. 1999. Beaver
fever–a rare cause of reactive arthritis. J
Rheumatol 26:2701–2702.
Tuttle RH, Watts DP. 1985. The positional behavior and adaptive complexes of Pan and
Gorilla. In: Kondo S, editor. Primate locomotor behavior, morphophysiology and bipedalism. Tokyo: Tokyo University Press.
p 261–288.
Urvater JA, Hickman H, Dzuris JL, Prilliman
K, Allen TM, Schwartz KJ, Lorentzen D,
Shufflebotham C, Collins EJ, Neiffer DL,
Raphael B, Hildebrand W, Sette A, Watkins
DJ. 2001. Gorillas with spondyloarthropathies express an MHC class I molecule with
only limited sequence similarity to HLAB27 that binds peptides with arginine at P2.
J Immunol 166:3334–3344.
Watkins DI, Chen ZW, Garber TL, Hughes
AL, Levin NL. 1991. Segmental exchange
between MHC class I genes in a higher
primate: recombination in the gorilla between the ancestor of a human non-functional gene and an A locus gene.
Immunogenetics 34:185–191.
Woods RJ, Rothschild BM. 1988. Population
analysis of symmetrical erosive arthritis
in Ohio woodland Indians (1200 years
before the present time). J Rheumatol 15:
1258–1263.
Yli-Kerttula T, Tertti R, Toivanen A. 1995.
Ten-year follow up study of patients from a
Yersinia pseudotuberculosis III outbreak.
Clin Exp Rheumatol 13:333–337.
Zhou M, Sayad A, Simmons A, Jones RC,
Maika SD, Satumtira N, Dorris ML, Caskell
SJ, Bordoli RS, Sarter RB. 1998. The
specificity of peptides bound to human
histocompatibility
leucocyte
antigen
(HLA)-B27 influences the prevalence of
arthritis in HLA-B27 transgenic rats. J
Exp Med 188:877–886.
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