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Erosive arthritis and spondyloarthropathy in old world primates.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 88:389-400 (1992)
Erosive Arthritis and Spondyloarthropathy in Old World Primates
BRUCE M. ROTHSCHILD AND ROBERT J. WOODS
Arthritis Center of Northeast Ohio, (B.M.R., R.J. W.) Youngstown, Ohio
44512; Northeast Ohio Universities College of Medicine, (B.M.R.)
Rootstown, Ohio 44272; University of Akron, (B.M.R.)Akron, Ohio
44242; The Carnegie Museum, (B.M.R.) Pittsburgh, Pennsylvania 15213;
Ohio State University, (R.J.W.) Columbus, Ohio 43210
KEY WORDS
Skeletal pathology; Primate, Theropithecus, Papio, Cercopithecus, Macaca, Hylobates, Colobus, Presbytis
ABSTRACT
Presence of spine and sacroiliac involvement and the nature
and distribution of the erosive lesions allow definitive diagnosis of spondyloarthropathy. Thus, spondyloarthropathy was identified in Theropithecus,
Papio, Cercopithecus, Macaca, Colobus, Presbytis, and Hylobates. Only
monarticular erosive disease was present in prosimians, precluding a diagnosis of spondyloarthropathy for that group. The distribution of erosive disease
and axial joint involvement in 1,349 non-prosimian Old World primates is
quite characteristic of that noted in human psoriatic arthritis. While Reiter’s
syndrome must also be considered, the histologic appearance of skin lesions in
Macaca is characteristic of psoriasis.
Evidence of spondyloarthropathy abounds in the literature of primate skeletal disease. Environmentally based contagions may be important in the
pathophysiology of spondyloarthropathy. The wide geographic distribution of
the phenomena in monkeys suggests a “panendemic,”with limited individual
susceptibility (compared to that noted in gorillas and chimpanzees). Identical
occurrence of erosive arthritis/spondyloarthropathyin free-ranging and artificially restrained animals suggests that spondyloarthropathy can validly be
studied in artificially restrained populations. This perspective should allow
application of human therapeutic approaches to and perhaps improve the
quality of life for artificially restrained, afflicted individuals.
0 1992 Wiley-Liss, Inc.
Spondyloarthropathy classifies a variety
of arthritis. It is characterized by specific
patterns of erosive joint disease and a tendency to spine and sacroiliac fusion (McEwen et al., 1971; Resnick and Niwayama,
1988; Rothschild, 1982; Woodrow, 1985).
The nomenclature for this classification
might suggest that all individuals have axial joint (spine and sacroiliac) disease. However, axial joints are unaffected in more
than half of all individuals with spondyloarthropathy (McEwen et al., 1971; Resnick
and Niwayama, 1988; Rothschild, 1982;
Rothschild and Woods, 1989). The category
spondyloarthropathy actually is composed
of several disorders which typically, but not
invariably, affect the axial joints. These in0 1992 WILEY-LISS. INC.
clude ankylosing spondylitis, Reiter’s syndrome, psoriatic arthritis, the arthritis of
inflammatory bowel disease, and “undifferentiated spondyloarthropathy” (McEwen et
al., 1971; Mielants et al., 1989; Resnick and
Niwayama, 1988; Rothschild, 1982).
The above perspectives were applied to
analysis of the published literature on arthritis in monkeys. “Articular changes” and
“arthritis deformans” have been reported
in Dynastic Egyptian and contemporary
Received April 12,1990; accepted December 31,1991.
Address reprint requests to Bruce M. Rothschild, Arthritis
Center of Northeast Ohio, 5701 Market Street, Youngstown, OH
44512.
B.M. ROTHSCHILD AND R.J. WOODS
390
monkeys (Bramblett, 1968; Bywaters, 1981;
Driesch, 1985; Ford et al., 1986; Fox, 1939).
Did these animals actually have spondyloarthropathy? “Arthritic changes” were reported in two elbows, one wrist, two hips,
and two knees of a Papio cynocephalus
(Bramlett, 1968). This distribution pattern,
sparing the small joints of the hands, occurs
in spondyloarthropathy (Resnick and Niwayama, 1988; Rothschild, 1982; Rothschild
and Woods, 1989). Asymmetrical erosive arthritis and proximal interphalangeal and
metacarpal phalangeal joint marginal erosions with ankylosis have been reported in
Macaca mulatta (Bywaters, 1981; Obeck
et al., 1976). These patterns are also highly
suggestive of spondyloarthropathy (Resnick
and Niwayama, 1988; Rothschild, 1982;
Rothschild and Woods, 1989). That diagnostic suspicion is supported by observation of
“spondylitis” in “sacred monkeys of the ancient temples near Thebes” (Ruffer, 1921)
and in contemporary Macaca by Sokoloff
et al. (1968). Observation of 10 cases of inflammatory arthritis each year in a 2,000
monkeys Macaca mulatta breeding colony
suggests that this phenomena may not be
uncommon (Ford et al., 1986).
Among humans, the frequent association
of spine and sacroiliac pathology with peripheral joint disease characterizes spondyloarthropathy (Resnick and Niwayama,
1988; Rothschild, 1982; Rothschild and
Woods, 1989). This is sometimes also called
reactive arthritis (Ah0 et al., 1985; Woodrow, 1985). This association has been clearly
demonstrated in the great African apes, Gorilla and Pan (Rothschild and Woods, 1989,
1991b). Recognition of a n erosive disease of
the spondyloarthropathy variety, indistinguishable in gorillas from human psoriatic
arthritis, stimulated this systemic review of
Old World primates.
METHODS
The articular skeletons of adult Old World
primates were examined from the following
collections: American Museum of Natural
History (AMNH) (New York City), Carnegie
Museum (CM) (Pittsburgh, PA), Cleveland
Museum of Natural History (CMNH) (Ohio),
Field Museum of Natural History (FMNH)
(Chicago, IL), Florida State Museum (UF
TABLE 1. Erosive DatholoPv in Drosimians
Isolated’
lesions
Genera
Galago
Euoticus
Lemur
Propithecus
Microcebus
Daubentonia
Tamandua
Hapalemur
Tarsius
Varecia
Lepilemur
Cheirogaleus
Indri
Nycticebus
Periodicticus
Avahi
Pot0
Tupaia
Arctocebus
Loris
Joint
affected
%
#
1.1
0
2.9
0
0
0
0
0
0
0
5.0
20.0
12.5
3.3
0
0
0
0
0
1
MCP2
2
MCP, knee
Total
examined
94
1
70
14
26
4
1
1
1
1
MTP3
Carpus
MTP
Elbow
n
1
10
19
8
20
5
8
33
19
3
1
5
3
i_n”
’Isolated indicates monoarticular disease.
‘MCP = metacarpal phalangeal joint.
“MTP = metatarsal phalangeal joint.
and FSM) (Gainesville, FL), Museum of
Comparative Zoology (MCZ) (Harvard University, Cambridge, MA), National Museum
of Natural History (NMNH) (Washington,
D.C.), University of Washington (PHY) (Seattle, WA), and Wake Forest University
(WFU) (Winston-Salem, NC). Closure of peripheral epiphyses was accepted as evidence
of maturity. All animals were either freeranging or had been raised in colonies or
zoos.
The macerated primate skeletons were
surveyed for visible evidence of articular
and periarticular joint and spine pathology.
Most of the macerated specimens had been
treated with lye to remove the soft tissues.
Examined post-cranial skeletons were, with
rare exception (representing less than 1% of
examined specimens), completely preserved. Each skeletal element of all sampled
individuals was carefully observed by both
authors (Tables 1, 2). Concurrence was obtained to a specific observation representing
an erosion and ruling out artifact, such a s
post-mortem trauma (e.g., drawer damage).
For purposes of this study, articular surfaces were treated a s missing if artifactual
damage precluded demonstration of joint
disease. The latter was a very infrequent
SPONDYLOARTHROPATHY IN OLD WORLD MONKEYS
391
TABLE 3. Bone pathology in Old World monkeys
and prosimians
*
c
.-
~ 0 0 0 0q
,o
4
q 0 0 0 c9
0 0
c
m
..-
In
mC
6
m
c
d
m
3
Condition
Erosions
Isolated
Oligo/Polyarticular
Fusion
Peripheral joint or
symphysis pubis
Axial joint
Diffuse Idiopathic
Skeletal hyperostosis
Prosimian
Old World
monkev
7 (2.0%)
0
27 (2.1%)
16 (1.2%)
1 (0.3%)
13 (1.0%)
0
14 (1.1%)
0
9 (0.7%)
occurrence. The spine and sacroiliac joints
were also assessed in a n additional 17 Colobus and 42 Presbytis. All pathologic specimens were subjected to radiologic examination in the anatomical position, in which
they would be viewed during in vivo radiology.
RESULTS
Isolated erosions
Isolated erosions or holes were noted in
2.0% of prosimians (Table 3). These were
predominantly localized to metacarpal phalangeal and metatarsal phalangeal joints
(Table 1). Such isolated erosions or holes
were present in 2.1% of bon-prosimian Old
World primates (Table 2). These were localized predominantly to carpals and elbows.
Occurrence of isolated erosions was independent of geographic distribution (Table 4).
The carpus and elbow are most commonly
affected (76%) in Old World primates (Tables 1, 2). Eighteen percent of isolated lesions were localized to the knee, metacarpal
phalangeal, or metatarsal phalangeal joints.
Six percent of isolated lesions were localized
to the shoulder or ulnar styloid. Isolated lesions were typically small and therefore
below the threshold for radiologic detection. Those lesions observed on x-ray were
“punched out” articular margin or surface
lesions, without associated peri-articular osteopenia. New bone formation was occasionally noted, but the bone immediately surrounding the areas of “bone accretionn
revealed no other evidence of architectural
distortion.
B.M. ROTHSCHILD AND R.J. WOODS
392
TABLE 4. Occurrence of isolated erosions on a function of Old World primate geographic distribution
Primate
Erosions
Africa
+
+
Arabia
Prosimians
Galago
Propithecus
Daubentonia
Tarsius
Cheirogaleus
Indri
Nycticebus
Periodicticus
Tupaia
Loris
Old World monkeys
Papio
Theropithecw
Colobus
Nasalis
Cercopithecus
Macaca
Erythrocebus
Pygathrix
Rhinopithecus
Cercoceb us
Hylobates
Asia
+
+
+
Borneo
Madagascar
i
+
+
+
+
+
+c
+
+
+
+
+
+
+
+
+
+
+
t
+
+
+
tion in Table 2, and species susceptibility in
Table 5. Peripheral joint fusion was found
only in non-prosimian Old World primates.
Carpal, metacarpal, and metatarsal fusion
were each noted a s isolated findings in
D
X
PIP
Macaca.
Osteoarthritis and calcium pyroDIP
phosphate
deposition disease occurred once
* a .
ma
mo*
a .
*
as
a
secondary
phenomenon (Fig. 3).
. o
shaldr
The distribution of erosions among Old
m
*
*
ON
World primates was shoulders (26%), elI(nr
Mde
bows (44%),wrists (62%), metacarpal phax
* *
YTP
langeal joints (12%), proximal interphaSI
langeal joints (7%), hips (O%), knees (34%),
ankles (31%), and metatarsal phalangeal
joints (27%). Most lesions were below the
threshold of x-ray resolution. The density of
the surrounding bone was maintained in
those erosions that were visualized radiologically. No periarticular osteopenia was
present. A sclerotic margin (to the erosion)
Oligo- and polyarticular erosive disease
was present in approximately 50% of eroErosive disease, not limited in distribu- sions visible on x-ray.
tion to a single joint, was not found in prosCalcification of the anulus fibrosus formimians (Tables 2,3; Figs. 1-3). Such erosive ing syndesmophytes and sacroiliac erosions
disease was found in 1.2% of free-ranging or fusion were not found in any of the prosnon-prosimian primates, compared to 1.1% imians examined (Figs. 4, 5). Such axial leof primates from zoos or colonies (Chi square sions were found in sixteen (1.2%)non-pros= 0.14, non-significant). Distribution of
imian Old World primates (Figs. 4,5; Tables
joint involvement in each individual skele- 2, 5). As not all individuals with axial diston is illustrated in Figure 1, sex distribu- ease had erosions and not all individuals
b
0
0
b
0
* I
0
0
0 .
0
.
# I D
0 )
,
.*
I
.
.
SPONDYLOARTHROPATHY IN OLD WORLD MONKEYS
393
Fig. 2. Erosive arthritis. a: Pupio distal radius erosion with minimal reactive new bone formation. b:
Macucu distal humeral erosion with reactive new bone formation.
TABLE 5. Frequency of oligo- and polyarticular
erosive arthritis and axial lesions among speciated
Cercopithecus and Macaca
Percent affected
Erosive Axial
Cercopithecus
neglectus
mitis
kolbi
aethiops
nictitanus
pygery thrus
albogularis
Macaca
nemestrinus
fuscutus
arctoides
mulatta
maurus
fascicularis
Fig. 3. Distribution of erosive arthritis in Pupio
FMNH 123072, with notation of distribution of secondary osteoarthritis and calcium pyrophosphate deposition disease.
with erosions had axial disease, these
groups overlap in Table 2. Examination of
the spine and sacroiliac joints of an addi-
Number examined
10.0
7.7
0
0
0
0
0
20.0
7.7
25.0
0
0
0
0
10
14
4
135
14
9.4
14.3
2.0
2.9
0
6.3
0
0
2.9
50.0
32
n
n
14
12
7
50
34
2
118
tional42 Presbytis and 17 Colobus revealed
sacroiliac erosions in one Presbytis (AMNH
43078) and one Colobus (AMNH 52334). The
sacroiliac joint erosions in Colobus AMNH
52334 were associated with elbow and carpal erosions. The axial lesions were frequently associated with zygoapophyseal
joint fusion (Fig. 4). Occasional fusion of
costovertebral joints (Fig. 4) or of the symphysis pubis was noted (Table 2).
Ossification of longitudinal ligaments of
the spine is referred to as diffuse idiopathic
skeletal hyperostosis, or DISH (Resnick and
Niwayama, 1988; Rothschild, 1982,1985).It
was found in only 10 (0.74%)non-prosimian
394
B.M. ROTHSCHILD AND R.J. WOODS
in a single individual is quite remote (McCarty, 1989; Rothschild, 1982). Too many of
the Old World primates studied had involvement of both peripheral and axial joints to
suggest co-occurrence of two diseases. The
nature and distribution of the erosions in
Old World primates were identical, independent of spine or sacroiliac (axial joint) involvement. This again suggests that all were
manifestations of a single disease.
The term oligo-articular implies involvement of less than 5 peripheral joints, while
polyarticular is used when 5 or more peripheral joints are affected. The oligo-articular
distribution of arthritis in Macaca, Cercopithecus, Colobus, Presbytis, and Hylobates
is actually the most common appearance of
spondyloarthropathy in humans (McCarty,
1989; Rothschild, 1982). The radiologic picture of erosions with sclerotic margins and
no peri-articular osteopenia is also characteristic of spondyloarthropathy (Resnick
and Niwayama, 1988; Rothschild, 1982;
Rothschild and Woods, 1989, 1991a). Both
Fig. 4. Macaca spine with classic syndesmophytes oligo-articular and polyarticular disease
producing fusion through the anulus fibrosus. Zygoapo- were noted, similar to patterns noted in the
physeal and costovertebral joint fusion are also promispectrum of human disease (Fig. 1) (Mcnent.
Carty, 1989; Rothschild, 1982).
The nature and distribution of the lesions
and the occurrence and frequency of spine
Old World primates (Fig. 6; Table 2). All afand sacroiliac involvement allow definitive
fected individuals of determinate sex were
diagnosis of spondyloarthropathy in Theromale and all but two were from artificial pithecus, Papio, Cercopithecus, Macaca, Coloenvironments.
bus, Presbytis, and Hylobates. The presence
of anulus fibrosus calcification, sacroiliac
DISCUSSION
fusion, or erosions is sufficient and diagnosDiagnosis
tic (Resnick and Niwayama, 1989; RothsErosive disease, not limited in distribu- child, 1982; Rothschild and Woods, 1988).
Fusion of the symphysis pubis was
tion to a single joint, was found in 1.2% of
non-prosimian Old World primates (Figs. 2, present only in genera of Old World pri3). Attribution of a single diagnosis to this mates susceptible to spondyloarthropathy
phenomenon is predicated upon a major (Papio, Cercopithecus, Macaca, and Hyloassumption. An anthropomorphizing ap- bates). As one-fifth of symphysis pubis fuproach is utilized. “Human” characteristics sions were associated with sacroiliac fusion
are extended to non-human primates from or anulus fibrosus syndesmophyte formahuman disease. Relatively few erosive disor- tion, such fusion may represent part of the
ders (that are not predominantly monoartic- spectrum of spondyloarthropathy or at least
ular) occur with any frequency within hu- a tendency to fusion in susceptible groups
man populations. Rheumatoid arthritis and (Table 2). Similarly, the peripheral joint fuspondyloarthropathy are the prime diagnos- sion noted in Macaca may represent part of
tic candidates (McCarty, 1989; Resnick and the spectrum of spondyloarthropathy, as it
Niwayama, 1988; Rothschild, 1982). The does in humans (Rothschild and Woods,
likelihood of co-occurrence of both diseases 1991a).
SPONDYLOARTHROPATHYIN OLD WORLD MONKEYS
395
Fig. 5. Sacroiliac joint fusion. A: Anterior view of Mucacu sacroiliac joint fusion. B: Radiograph of
Hylobutes pelvis revealing fusion of the right sacroiliac joint.
Isolated erosions were statistically analyzed as to their genus frequency and geographic distribution (Table 6). They were
uniformly distributed among genera of
spondyloarthropathy-afflicted Old World
primates, with the exception of Macaca (Tables 1, 2, 4). The significance of sparing of
Erythrocebus is unclear at this time. Isolated lesions were typically small. Their significance is difficult to assess as their size
was below the threshold for radiologic detection. The distortion of osseous architecture,
typically noted with infectious lesions, was
notably absent (Resnick and Niwayama,
1989; Rothschild, 1982). It is therefore difficult to identify the etiology of these isolated
erosions.
The pattern of distribution of erosive diseases in humans is a diagnostic criterium,
which assists in distinguishing among them
(Rothschild et al., 1988; Rothschild and
Woods, 1989; Woods and Rothschild, 1988).
While isolated lesions are usually not interpretable, the similarity of their distribution
in non-prosimian Old World primates to the
general distribution of joint disease in those
with oligo- and polyarticular disease raises
an interesting possibility (Fig. 2; Table 2).
Could these isolated lesions represent
“forme fruste” or aborted cases of spondyloarthropathy? While there did not appear
to be a relationship to skeletal maturity, torrelation with age is currently under investigation in an age-verified skeletal population.
Fig. 6. Lateral view of Pupio spine. Diffuse idiopathic skeletal hyperostosis is manifest as calcification
of the anterior longitudinal ligament. Space is visualized between the areas of calcification and the anterior
portion ofthe
body,
396
B.M. ROTHSCHILD AND R.J. WOODS
TABLE 6. Geographic distribution of Old World
primates with spondyloarthropathy
Primate
Papio
Theropithecus
Cercopithecus
Macca
Colobus
Pres bytis
Hvlo bates
Africa
+
+
+
+
+
Asia
Arabia
+
t
+
+
Frequency implications
The frequency of oligo- or polyarticular
erosive disease (spondyloarthropathy) in
Theropithecus was significantly greater
than that in Papio, Colobus, Presbytis, Cercopithecus, Macaca, and Hylobates (Chi
square = 12.65, 6 d.f., P < .05). The latter
combined the data from the other afflicted
genera, for comparison with Theropithecus.
A curious species specificity in Cercopithecus and Macaca was also noted (Table 5). It
is unclear if genetic, geographic, or food
gathering or intersocial habits might be implicated.
Although spondyloarthropathy was unrepresented in Nasalis, Pygathrix, and Cercocebus, the small number of specimens
available for assessment precludes confident exclusion of the disease in those populations. The difficulty of sample size is emphasized by Erythrocebus. Although no
examples of oligo- or polyarticular erosive
disease were noted among the 59 individuals studied, a disease occurring with a population frequency of 0.6 to 3.9% could easily
be missed. Absence of oligo- or polyarticular
erosive disease in 344 prosimians, by contrast, suggests that group is spared (Chi
square = 4.53, P < .04).
Differential diagnosis
Differentiation of diffuse idiopathic skeletal hyperostosis (DISH) from spondyloarthropathy is important. DISH is a pain-free
skeletal phenomenon, which rarely affects
ability to function (McCarty, 1989; Resnick
and Niwayama, 1988; Rothschild, 1985,
1987). It does not cause erosive damage to
joints. Spondyloarthropathy is a frequently
erosive disorder which is typically painful
and often compromises function (McCarty,
1989; Resnick and Niwayama, 1988; Rothschild, 1982). DISH has been well recognized
in primates (Rothschild, 1985, 1987; Rothschild and Woods, 1988; Sokoloff et al., 1968).
It is clearly distinguishable in the primates
examined, on the basis of calcification of longitudinal ligaments. The anulus fibrosus
and zygoapophyseal and costovertebral
joints are spared in DISH. Predominant occurrence of DISH in artificially restrained
primates could reflect longer survival of
such animals (compared to free-ranging), a
hypothesis which will be testable when criteria are established for aging free-ranging
primates. Limitation of DISH in Old World
primates to males is not surprising, in view
of the relatively small number of afflicted
primates (11 individuals) and the 7:l male
predominance of DISH in geriatric humans
(Rothschild, 1991). Its very frequency assures co-occurrence with various forms of arthritis including spondyloarthropathy, a s
was observed in this study.
Rheumatoid arthritis is a symmetrical,
but essentially a n axial joint sparing arthritis (Katz, 1989; McCarty, 1989; Resnick and
Niwayama, 1988; Rothschild, 1982; Rothschild et al., 1990). Erosion of the odontoid
process of the second cervical vertebrae is
one of the few axial skeleton changes found
in rheumatoid arthritis. This is clearly distinguishable from the spondyloarthropathy
noted in Old World primates. The limited
number of joints involved in Old World primates is clearly at variance with the involvement of almost every peripheral diarthrodial joint found in rheumatoid arthritis
(Resnick and Niwayama, 1989; Rothschild,
1982; Rothschild et al., 1990).
While erosions with sclerotic margins
may be found in gout or infectious arthritis,
epidemiologic study reveals major differences from that observed in Old World primates (Katz, 1989; McCarty, 1989; Rothschild, 1982; Rothschild and Woods, 1991a).
Gout and infectious arthritis also are predominantly monoarticular disorders, in contrast to the oligo- and polyarticular erosive
arthritis observed in Old World primates.
Overgrowth of periosteum adjacent to gout
erosions forms a highly characteristic overhanging edge (Katz, 1989; McCarty, 1989;
SPONDYLOARTHROPATHY IN OLD WORLD MONKEYS
397
TABLE 7. Skeletal distribution of erosive arthritis in Old World primates and of symptomatic
spondyloarthropathy (Spondylo), Reiter’s syndrome, psoriatic arthritis, and rheumatoid arthritis (RA) in
Homo Sapiens’
Primates
Spondylo
Reiter
Psoriatic
RA
Joint
#
%
%
%
%
%
Shoulder
Elbow
Wrist
MCP’
PIP2
Hip
Knee
Ankle
7
12
16
3
2
0
26
44
62
12
7
0
21
9
17
13
20
17
9
8
34
31
27
30
42
8
18
24-65
2-40
13-21
10-14
16-34
7-46
5-31
5-28
67-70
45-65
57
24-65
13-82
4-23
10-43
44-62
34-53
11-40
0-38
27-72
28-63
33-34
52
5-24
46
66
92
70
40
12
82
54
70
0
0
MTP’
SI2
Spine
7
8
11
8
‘Derived from Bitar, 1980; Dryll et al., 1975; Fletcherand Rowley, 1952; Kammeret al., 1979; Kouse, 1978; Martel et al., 1965; Martioet al.,
1980; McEwen et al., 1971; Moll, 1979 Peterson and Silbiger, 1967; Rothschild and Woods, 1989 Scarpa et al., 1984; Serre et al., 1970;
Weissberg et al., 1978; Weldon and Scalettar, 1961.
‘MCP = metacarpal phalangeal; PIP = proximal interphalangeal; MTP = metatarsal phalangeal; SI = sacroiliac.
Ortner and Putschar, 1981; Rothschild,
1982).No evidence of such a phenomena was
present in Old World primates.
While amyloidosis does occur as a complication of Shigella or tuberculosis infections
in primates (Chapman and Crowell, 1977),
amyloid only rarely produces radiologically
detectable erosions (Resnick and Niwayama, 1988; Rothschild, 1982). Erosions
of amyloid classically have a punched out
appearance, similar to those of gout (Chapman and Crowell, 1977; Resnick and Niwayama, 1988; Rothschild, 1982). This is
quite dissimilar to the erosions noted in the
Old World primates studied.
7). An attempt was therefore made to identify the specific variety of spondyloarthropathy present in Old World primates.
Ankylosing spondylitis and inflammatory
bowel disease-associated axial (spine) disease starts in the lumbar spine and
progresses cephaladly in a symmetrical,
uniform manner (Katz, 1989; McCarty,
1989; Rothschild, 1982). While Reiter’s syndrome, psoriatic arthritis, and undifferentiated spondyloarthropathies may present in
a similar manner, they tend to be asymmetrical and more limited in distribution.
The pattern of spine involvement in Old
World primates suggest Reiter’s syndrome,
psoriatic arthritis, or undifferentiated
spondyloarthropathy, rather than ankylosVariety of spondyloarthropathy
ing spondylitis or the arthritis of inflammaSpondyloarthropathy in humans is di- tory bowel disease.
vided into a number of varieties: ankylosing
Reiter’s syndrome or reactive arthritis is a
spondylitis, psoriatic arthritis, Reiter’s syn- reasonable consideration in Old World primates (Resnick and Niwayama, 1988;
drome, inflammatory bowel disease-related
arthritis, and undifferentiated spondyloar- Rothschild, 1982). Reiter’s syndrome may be
thropathy (McEwen et al., 1971; Mielants of venereal or infectious agent diarrhea oriet al., 1989; Resnick and Niwayama, 1989). gin (Rothschild, 1982). Occurrence of
The term undifferentiated spondyloarthrop- spondyloarthropathy in monogamous Old
athy is applied when insufficient evidence is World primates (e.g., Hylobates) makes the
present to diagnose one of the first four. venereal variety unlikely (Smuts et al.,
Failure of findings in Old World primates to 1986). Among the causes of infectious agent
correlate with the “generic” spondyloar- diarrhea are Salmonella, Shigella, Yersinia,
thropathy group perhaps suggests that Camplobacter, and enteropathic Escherispondyloarthropathy in Old World monkeys chia coli. These are “commonly” noted “in
reflects one disease process, rather than recently imported non-human primates”
several forms of spondyloarthropathy (Table (Brancker, 1985; Klumpp et al., 1986; Mc-
398
B.M. ROTHSCHILD AND R.J. WOODS
Clure, 1980; Reinhardt et al., 1987). Clamydial infections are associated with human
venereally transmitted reactive arthritis
and have been found in Cynomolgus monkeys (Quinn e t al., 1986).
Table 7 assesses the similarity of distribution of erosive lesions in Old World monkeys
to the distribution in human spondyloarthropathies. Spondyloarthropathy in the table refers to frequency of involvement in a
series of patients. Ankylosing spondylitis,
psoriatic arthritis, Reiter’s syndrome, and
inflammatory bowel disease-related arthritis are grouped in Table 7 under the category of “generic” spondyloarthropathy. The
distribution of erosions among Old World
primates was shoulders 25%, elbows 44%,
wrists 60%, metacarpal phalangeal joints
13%, proximal interphalangeal joints 7%,
hips 0%, knees 34%, ankles 31%, and metatarsal phalangeal joints 27%. This falls outside the range previously reported in Reiter’s syndrome and rheumatoid arthritis
(Table 7). That range has proven quite valid
for comparison of skeletal and clinical distributions (Rothschild and Woods, 1989,
1991a,b; Rothschild et al., 1988, 1990). We
were surprised that the findings in monkeys
were so disparate from that noted for Reiter’s syndrome. As joint distribution in Reiter’s disease varies with causative organism,
perhaps a different proportion of those organisms in the various affected monkeys
would explain this apparent variation. Reiter’s syndrome could therefore still be responsible.
The distribution of erosive disease and axial joint involvement in Old World primates
is actually quite similar to that noted for
human psoriatic arthritis (Table 7). The observation of Obeck et al. (1976) of a n oligoarticular arthritis associated with ankylosis
in a rhesus monkey is in keeping with this
diagnosis. Equal representation in male and
female Papio, Presbytis, and Hylobates is in
keeping with that noted in human psoriatic
arthritis (Rothschild, 1982; Rothschild and
Woods, 1989). Male predominance in the
other afflicted genera may reflect a real difference, but is not statistically distinguishable from a 1:l ratio. Concluding that the
spondyloarthropathy in Old World monkeys
probably is related to psoriatic arthritis is
perhaps not surprising, as skin lesions with
the gross visual and histologic appearance of
psoriasis have been reported in Macaca (Zanolli et al., 1988). These psoriatic lesions
were described as “erythematous plaques
with adherent white scale, spongiform pustules and Munro microabscesses, clinically
and histologically indistinguishable from
psoriasis.”
One further possibility remains. While
ankylosing spondylitis and inflammatory
bowel disease are clearly not responsible for
the primate spondyloarthropathy described
in this report, Reiter’s syndrome certainly
remains a possibility. Could the spondyloarthropathy in Old World primates represent
a mixture of psoriatic arthritis and Reiter’s
syndrome? Transition of Reiter’s syndrome
to psoriatic arthritis and vice versa has
clearly been recognized in humans (Katz
1989; McCarty, 1989; Rothschild, 1982). As
the gross appearance of the skin and histopathology of the two diseases may at times
be indistinguishable, this consideration cannot be further resolved a t this time (Katz
1989; McCarty, 1989; Rothschild, 19821.
Observation of Reiter’s syndrome, as a
complication of human immunodeficiency
(AIDS) virus infection, requires consideration of a n analogous retrovirus phenomenon in these primates (Davis et al., 1989;
Mielants and Veys, 1990; Reveille et al.,
1990). This is less likely, as AIDS appears to
be a relatively new phenomenon, while most
of the affected animals were collected in the
early part of the century. However, retroviruses have been implicated in the etiology of
psoriasis and are certainly worth exploring
in the pathophysiology of arthritis in monkeys (Gladman, 1990).
Implications
Evidence of spondyloarthropathyabounds
in the literature of primate skeletal disease
(Ortner and Putschar, 1981; Rothschild and
Woods, 1989; Sokoloff et al., 1968; Wells,
1962). The variety observed in Old World
primates is indistinguishable from human
psoriatic arthritis. Other than the relationship of the articular disease to the skin condition, the etiology of psoriatic arthritis is
unknown. Reiter’s syndrome must also be
considered.
SPONDYLOARTHROPATHY IN OLD WORLD MONKEYS
399
This analysis also provides insights for and Musculoskeletal and Skin Disease
analysis of other, less studied primate grant AFt35736-03.
groups. Future documentation even of peripheral joint or symphysis pubis fusion
should stimulate full population skeletal
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We wish to express our appreciation to
Drs. Dana E. Austin, Philip Hershkovitz,
Lyman Jellema, Bruce Latimer, William R.
Maples, Guy Musser, D. Patterson, Dwayne
Schlitter, Darren Swindler, Richard Thorington, and David Weaver for their assistance in facilitating our examination of the
collections they curate.
This work was supported in part by NIH
Division of Diagnostic Resources grant
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