Ankylosing
Spondylitis By Robert
in Nonhuman the Siamang
L. Swezey,
Cathleen
Nonhuman primates are known to be susceptible to many of the arthritides that afflict humans. Psoriaticlike spondyloarthropathies have been reported in gorillas and skeletal hyperostosis in gibbons, rhesus monkeys, and gorillas, and additional cases of both of these conditions occurring in drills (baboons) are noted in this report. One western lowland gorilla and two rhesus monkeys with clinical features consistent with ankylosing spondylitis have been documented previously. Two additional nonhuman
A
VARIETY of spondyloarthropathies as well as many of the common arthritides have been observed in various primate species.‘.’ In one report, up to 20% of a large western lowland gorilla population was found to have some form of arthritis.4 Various reported arthritides include skeletal hyperostosis in rhesus monkeys’; rheumatoid arthritis in a rhesus monkey’; osteoarthritis in gibbons, rhesus monkeys,2.3 and gorillas4; infectious arthritis in rhesus monkeys3 and gorillas4; and calcium pyrophosphate disease (CPPD)* and pulmonary osteoarthropathy in chimpanzees5 gibbons,’ and orangutans.’ In a classic study, Rothschild and Woods4 characterized a spondyloarthropathy in western lowland gorillas (Gorilla gotillu gorilla) with features strongly reminiscent of psoriatic arthritis as distinguished from ankylosing spondylitis. Sokoloff et al’ described inflammatory spondylitis in an adult (181X-year-old) rhesus monkey with radiographic and pathological features strongly suggestive of human ankylosing
From the Arthritis and Back Pain Center, Swezey Institute, Santa Monica, CA; Division of Rheumatology, UCLA, Los Angeles, CA; and the Los Angeles Zoo, Los Angeles, CA. Robert L. Swezey, MD, FACP, FACR: Medical Director, Arthritis and Back Pain Center, Santa Monica, CA, Clinical Professor of Medicine, UCLA, Los Angeles, CA; Cathleen Cox, PhD: Director of Research, Los Angeles Zoo, Los Angeles, CA; Ben Gonzales, DVM: Veterinatian, LosAngeles Zoo, Los Angeles, CA. Address reprint requests to Robert L. Swezey, MD, FACP, FACR, The Arthritis and Back Pain Center, Swezey Institute, 1328 16th St, Santa Monica, CA 90404. Copyright 0 1991 by W.B. Saunders Company 0049-017219112103-0007$5.00/O 170
Seminars
Primates:
The Drill
and
Cox, and Ben Gonzales primate species with radiographic evidence of ankylosing spondylitis are described. A siamang (gibbon) and two drills (baboons) with the classic radiographic features of ankylosing spondylitis, namely a bamboo spine and sacroiliac joint fusion, are reported. Copyright o 1991 by W.B. Saunders Company INDEX WORDS: Spondyloarthropathy; ankylosing spondylitis.
primates;
spondylitis, although the classic bamboo spine and sacroiliac fusion were not found.’ Adams et al discovered a female western lowland gorilla at the Memphis zoo in 1977 with a bamboo spine and large-joint synovitis whose male offspring developed synovitis in a wrist and was found to be “G”LA-B27 (HLA-B27) positive.R In this report, six drills (forest-dwelling baboons, Mandrillus leucophaeus) were observed and/or had radiographs reviewed. Three of the drills had nonspecific spinal abnormalities with spotty anterior longitudinal ligament ossifications, osteophyte formation, and some disk calcifications (Table 1). Two male drills had bamboo spines and sacroiliac fusions consistent with ankylosing spondylitis. In addition, one male siamang (gibbon, Hylobates syndactylus) also was found to have classic radiographic findings of ankylosing spondylitis. A normal female siamang was also observed and showed no abnormalities in the spine or sacroiliac joints on x-ray.
METHODS
Radiographs of a male siamang from the Los Angeles Zoo were recognized as showing arthritic changes and were brought to the attention of the first author (R.L.S.) for review. This animal died during anesthesia for treatment of a fracture. Serial x-rays were available. Unfortunately, no joint or spinal tissue was observed at necropsy. Spinal x-rays from one female siamang were normal. Indications of arthritis in drills at the Los Angeles Zoo were further explored. Six drills
in Arthritis
andRheumatism,
Vol21. No 3 (December), 1991: pp 170-174
ALKYLOSING
SPONDYLITIS
171
IN PRIMATES
Table
1: Clinical
and Radiographic
Clinical
Primate
Sex
Age
Peripheral
(vr)
Joints
Drill B
F
23
Swan
Drill E
F
24
Normal
neck, left 4th digit
Correlations Radiographic
_ Spine
Spine
Normal
Anterior
Humped
ALLO, T-l l-L-1;
fusion,
Ll-2 osteophyte,
SI Joints Normal Normal
L2-3 Drill L
F
10
Normal
Normal
Normal
Normal
Drill N
M
19
Knees flexed
Humped
ALLO, TlO-L-5
Normal
Drill R
M
8
Normal
Normal
Calcified anterior disk T-l 2-L-3
Normal
Drill S
M
19
Contracture, right knee
Normal
Beaklike anterior osteophytes,
Fused
dorsal spine; bamboo lumbar spine* Siamang
F
27
Normal
Normal
Normal
Normal
Siamang
M
18%
OA, hips
Normal
Bamboo spine*
Fused ___
Abbreviations:
ALLO, anterior longitudinal ligament ossification; SI, sacroiliac; OA, osteoarthritis.
*See x-ray report in text.
were observed, and spinal x-rays were reviewed. Clinical observations showed one drill (drill N) to be “hump-backed,” arthritic, and “unable or unwilling to use his rear legs.” He became ill due to anal fistulae and abscesses resulting from locomoting in a sitting position and was euthanatized at age 20 years for humanitarian reasons. His premortem and postmortem x-rays are reported. A second drill (drill S) had an apparent arthritic knee but did not show obvious spinal involvement. His x-rays, however, showed the typical bamboo spine and obliteration of sacroiliac joints. A third drill, a female (drill E), was noted premorbidly to have a humpback. She died at age 24 years of congestive heart failure. Her x-rays showed anterior longitudinal ligament ossification from T-11 through L-l. The sacroiliac joints were normal, and no other significant spinal abnormalities were noted. A fourth drill, a 23-year-old female (drill B) with a single swan neck deformity, also had spinal bony fusion anteriorly between the bodies of L-l and L-2. The remaining two drills were clinically normal, but radiographically the subadult male (drill R) showed calcification of the anterior disks. RESULTS
X-rays of an adult male siamang (Los Angeles Zoo case 1233) and two adult male drills (Los Angeles Zoo cases 90-210 and 2331) are reported.
Radiographs (February 16, 1983)~Siamang (case 1233)
A lateral view of the entire spine shows some proliferative changes on the anterior aspect of the bodies of C-6 and C-7 which are characterized as large bony projections that point downward and represent anterior longitudinal ligament ossification. The cervical intervertebral disk spaces in the affected areas and throughout the cervical spine are well maintained. The opposing surfaces of the lower dorsal vertebrae show irregularities consistent with mild epiphysitis and minimal evidence of osteophyte formation. No syndesmophytes are noted. An anteroposterior (AP) view of the lower part of the skull, neck, dorsolumbar spine, and upper portions of the pelvis shows calcifications that appear to be in the bladder. The glenohumeral joints are normal, and there is apparent fusion of both sacroiliac joints. The lumbar spine in the AP view shows a typical bamboo spine with ossification of the lateral ligaments at each intervertebral disk level. Radiographs (March 17, 1983)Siamang (case 1233)
Both sacroiliac joints appear to be fused. There is a small erosion on the superior aspect of the right femoral head, consistent with early inflammatory arthritis.
172
Radiographs (case 1233)
SWEZEY, COX, AND GONZALES
(April 8, 1985)-Siamang
On bladder survey, the bamboo appearance of the lumbar spine is again noted. The sternoclavicular joint shows some sclerosis and smudging of the joint margins consistent with an inflammatory process. The left hip shows moderate osteoarthritic changes with some erosion and narrowing of the joint space and prominent osteophytes. The joint space on the right hip is narrowed superiorly with a prominent superior osteophyte at the acetabular rim. These findings are consistent with osteoarthritis of the hips, which may be secondary to underlying ankylosing spondylitis (Fig 1). Radiographs I989) -Drill
(Postmortem; November 21, N (case 90-210)
On the lateral view, the cervical, dorsal, and lumbar spine show anterior longitudinal liga-
mentous ossification with syndesmophyte formation in all areas. There is diffuse interspinous ligament ossification with ankylosis of the majority of facet joints. On the AP view, there is a bamboo appearance of the lower lumbar spine due to anterior and lateral ligamentous ossification, Prominent osteophytes are noted in the lateral aspects of the L4-5 intervertebral disk space. The sacroiliac joints are ankylosed, and the hips are disarticulated. Radiograph
(April 17, 1990)-Dtill
S (case 2331)
On the AP and lateral views of the dorsal and lumbar spine, there is diffuse ossification of the anterior longitudinal ligament. The lateral view of the dorsal spine shows large anterior beaking osteophytic projections at essentially all levels. The lumbar spine shows diffuse flowing ossification of the anterior longitudinal ligament with preservation of intervertebral disk spaces (Fig 2). On the AP view, the lumbar spine has a bamboo appearance with bony bridging extending laterally from the mid-vertebral bodies over the periphery of the disk areas from L-l to L-5. At L-5-S-l there are prominent bilateral osteophytes. The sacroiliac joints appear fused (Fig 3). These findings are consistent with ankylosing spondylitis or variant spondylitis, although the beaked appearance of the prominent dorsal spine osteophytes is atypical. The clinical and radiographic observations on the animals in this study are summarized in Table 1 and Figs 1 through 3. DISCUSSION
Fig 1: Male siamong (case 1233). Arrow A indicates bamboo spine, B indicates the area of the fused sacroiliac joint, C indicates superficial erosions on the right hip, and D indicates an osteophyte on the left hip.
The presence of arthritic disorders in various primate species that closely resemble their human counterparts is now widely recognized.‘.” The evidence of psoriaticlike spondyloarthropathy occurring commonly in western lowland gorillas has been documented.4 Only three examples of “classical” ankylosing spondylitis in nonhuman primates have been described.‘,’ An adult rhesus monkey studied by Sokoloff et al showed pathological evidence of an inflammatory lesion, presumably an enthesopathy, and sacroiliac erosions and facet bony ankylosis.’ In addition, radiographic evidence of diffuse posterior element and facet joint bony ankylosis without disk or anterior longitudinal ligament involvement was seen.’ Sokoloff et al also de-
ALKYLOSING
SPONDYLITIS
173
IN PRIMATES
showed no other evidence of spinal or other joint arthropathies. He was treated for a bladder calculus. His death was attributed to a traumatic hemopericardium resulting from an anesthetic dart injury that occurred when he was anesthetized for treatment of a fractured forelimb. At necropsy he had a cornea1 ulceration of the right eye; no other significant lesions were noted. Various spondyloarthropathies, osteoarthritis, and/or DISH-like changes were also noted radiographically in five of the six drills. Two of these drills had roentgenographic changes of spondyloarthritis. Multiple skeletal traumas causing arthropathies were noted in the chimpanzee population of Gombe observed by Jane Goodall.’ CPPD
Fig 2:
Drill (case 2331).
lateral
view
of the
lumbar spine. Arrow A indicates the area of diffuse anterior longitudinal ligament ossification.
scribed another rhesus monkey with sacroiliac joint fusion.’ As previously noted, Adams et al reported a female western lowland gorilla with a bamboo spine and peripheral large joint involvement who had a “G”LA-B27 (HLAB27) male offspring.’ In this study, x-rays of an adult (27-year-old) male siamang showed both sacroiliac bony fusion and a classic bamboo spine typical of ankylosing spondylitis. In addition, his hip x-rays showed progressive arthritic changes suggestive of inflammatory arthropathy leading to secondary degenerative joint disease. This animal
Fig 3:
Drill (case 2331), anteroposterior
view of
the lumbar spine. Arrow A indicates bamboo spine, and 6 indicates the area of the fused sacroiliac joint.
174
SWEZEY, COX, AND GONZALES
has been commonly found in nonhuman primates.” In this connection, it should be noted that CPPD has been associated with disk calcification, bony spurs, and bony intervertebral bridging in humans.” The role, if any, of CPPD in the animals in this study has not been determined. A group of mandrills (Mandrillus sphinx) in Toronto, Canada, have spondyloarthritis, and preliminary observations indicate HLA-B27 antigenicity (Inman R, McKibbon C, personal communication). Tissue typing is underway on several drills in this study (Weinberg K, personal communication). In view of the apparent widespread prevalence of ankylosing spondylitis, its association with HLA-B27 positivity in Gorilla gorilla gorilla and perhaps Mandrillus is of interest. This is in sharp contrast to the rarity of human spondyloarthropathies in Zimbabwe, Africa, and the further observation that none of nine Zimbabwe patients with ankylosing spondylitis were HLA-B27 positive.” Seven of 10 patients in Zimbabwe with Reiter’s syndrome and spondyloarthropathy had the B-7-CREG antigen.‘* Granting that the primates in this report were
raised in captivity, a further observation merits comment. Because many nonhuman primates living in the wild develop a variety of arthropathies, including spondyloarthropathies, there is an apparent lack of protection against a variety of rheumatological disorders provided by consuming a herbiverous diet consisting of unadulterated, largely “natural” foods. CONCLUSION
These are the first reported cases of ankylosing spondylitis in a siamang (gibbon) and two drills (baboons), the third and fourth nonhuman primate species in which ankylosing spondylitis or variant spondylitis has been observed. The possibility of further elucidating environmental and genetic factors pertaining to ankylosing spondylitis by studying nonhuman primates may be potentially rewarding. ACKNOWLEDGMENT The authors gratefully acknowledge Mary and Harlan Deckert, dedicated docents at the Los Angeles Zoo, Christine Marason, Los Angeles Zoo Veterinarian Assistant, and H.J. Holshuh, pathologist, for their invaluable assistance in this project.
REFERENCES 1. Sokoloff L, Snell KC, Stewart HL: Spinal ankylosis in old rhesus monkeys. Clin Orthop Rel Res 61:285-293,196X 2. DeRousseau CJ: Osteoarthritis in rhesus monkeys and gibbons: A locomotor model of joint degeneration. Basel, Switzerland, Karger, 1988, pp 2,35,51, 99 3. Obeck DK, Toft JD II, Dupuy HJ: Severe polyarthritis in a rhesus monkey: Suggested mycoplasma etiology. Lab Anim Sci 26:613-618,1976 4. Rothschild BM, Woods RJ: Spondyloarthropathy in gorillas. Semin Arthritis Rheum 18:267-276, 1989 5. Marzke MW, Merbs CF: Evidence of hypertrophic pulmonary osteoarthropathy in a chimpanzee, Pan troglodyfes. J Med Primatol 13:135-145, 1984 6. Ryder-Davies P, Hime JM: Hypertrophic osteoarthropathy in a gibbon (Hylobates lar). J Small Anim Pratt 13:655-658,1972 7. Hime JM, Keymer IF, Appleby EC: Hypertrophic
pulmonary osteoarthopathy maeus). Vet Ret 91:334-337,
in an orang-utan 1972
(Pongo pyg-
8. Adams RF, Finn GS, Douglas M: Ankylosing spondylitis in a non-human primate: A monkey tail. Arthritis Rheum 30:956-957,
1987
9. Bywaters monkeys.
EG: Observations
in chronic
polyarthritis
in
J R Sot Med 74:47-55,198l
10. Bauer B: Biographies skeletons reveal memoirs 138(7):106-108,199O
etched in bone-Chimpanzees’ of life in the wild. Sci News
11. Weinberger A, Myers AR: Intervertebral disc calcification in adults: Review. Semin Arthritis Rheum 869-75, 1978 12. Stein M, Davis P, Emmanuel .I, et al: The spondyloarthropathies in Zimbabwe: A clinical and immunogenetic profile. J Rheum 17:1337-1339, 1990
Spondylitis By Robert
in Nonhuman the Siamang
L. Swezey,
Cathleen
Nonhuman primates are known to be susceptible to many of the arthritides that afflict humans. Psoriaticlike spondyloarthropathies have been reported in gorillas and skeletal hyperostosis in gibbons, rhesus monkeys, and gorillas, and additional cases of both of these conditions occurring in drills (baboons) are noted in this report. One western lowland gorilla and two rhesus monkeys with clinical features consistent with ankylosing spondylitis have been documented previously. Two additional nonhuman
A
VARIETY of spondyloarthropathies as well as many of the common arthritides have been observed in various primate species.‘.’ In one report, up to 20% of a large western lowland gorilla population was found to have some form of arthritis.4 Various reported arthritides include skeletal hyperostosis in rhesus monkeys’; rheumatoid arthritis in a rhesus monkey’; osteoarthritis in gibbons, rhesus monkeys,2.3 and gorillas4; infectious arthritis in rhesus monkeys3 and gorillas4; and calcium pyrophosphate disease (CPPD)* and pulmonary osteoarthropathy in chimpanzees5 gibbons,’ and orangutans.’ In a classic study, Rothschild and Woods4 characterized a spondyloarthropathy in western lowland gorillas (Gorilla gotillu gorilla) with features strongly reminiscent of psoriatic arthritis as distinguished from ankylosing spondylitis. Sokoloff et al’ described inflammatory spondylitis in an adult (181X-year-old) rhesus monkey with radiographic and pathological features strongly suggestive of human ankylosing
From the Arthritis and Back Pain Center, Swezey Institute, Santa Monica, CA; Division of Rheumatology, UCLA, Los Angeles, CA; and the Los Angeles Zoo, Los Angeles, CA. Robert L. Swezey, MD, FACP, FACR: Medical Director, Arthritis and Back Pain Center, Santa Monica, CA, Clinical Professor of Medicine, UCLA, Los Angeles, CA; Cathleen Cox, PhD: Director of Research, Los Angeles Zoo, Los Angeles, CA; Ben Gonzales, DVM: Veterinatian, LosAngeles Zoo, Los Angeles, CA. Address reprint requests to Robert L. Swezey, MD, FACP, FACR, The Arthritis and Back Pain Center, Swezey Institute, 1328 16th St, Santa Monica, CA 90404. Copyright 0 1991 by W.B. Saunders Company 0049-017219112103-0007$5.00/O 170
Seminars
Primates:
The Drill
and
Cox, and Ben Gonzales primate species with radiographic evidence of ankylosing spondylitis are described. A siamang (gibbon) and two drills (baboons) with the classic radiographic features of ankylosing spondylitis, namely a bamboo spine and sacroiliac joint fusion, are reported. Copyright o 1991 by W.B. Saunders Company INDEX WORDS: Spondyloarthropathy; ankylosing spondylitis.
primates;
spondylitis, although the classic bamboo spine and sacroiliac fusion were not found.’ Adams et al discovered a female western lowland gorilla at the Memphis zoo in 1977 with a bamboo spine and large-joint synovitis whose male offspring developed synovitis in a wrist and was found to be “G”LA-B27 (HLA-B27) positive.R In this report, six drills (forest-dwelling baboons, Mandrillus leucophaeus) were observed and/or had radiographs reviewed. Three of the drills had nonspecific spinal abnormalities with spotty anterior longitudinal ligament ossifications, osteophyte formation, and some disk calcifications (Table 1). Two male drills had bamboo spines and sacroiliac fusions consistent with ankylosing spondylitis. In addition, one male siamang (gibbon, Hylobates syndactylus) also was found to have classic radiographic findings of ankylosing spondylitis. A normal female siamang was also observed and showed no abnormalities in the spine or sacroiliac joints on x-ray.
METHODS
Radiographs of a male siamang from the Los Angeles Zoo were recognized as showing arthritic changes and were brought to the attention of the first author (R.L.S.) for review. This animal died during anesthesia for treatment of a fracture. Serial x-rays were available. Unfortunately, no joint or spinal tissue was observed at necropsy. Spinal x-rays from one female siamang were normal. Indications of arthritis in drills at the Los Angeles Zoo were further explored. Six drills
in Arthritis
andRheumatism,
Vol21. No 3 (December), 1991: pp 170-174
ALKYLOSING
SPONDYLITIS
171
IN PRIMATES
Table
1: Clinical
and Radiographic
Clinical
Primate
Sex
Age
Peripheral
(vr)
Joints
Drill B
F
23
Swan
Drill E
F
24
Normal
neck, left 4th digit
Correlations Radiographic
_ Spine
Spine
Normal
Anterior
Humped
ALLO, T-l l-L-1;
fusion,
Ll-2 osteophyte,
SI Joints Normal Normal
L2-3 Drill L
F
10
Normal
Normal
Normal
Normal
Drill N
M
19
Knees flexed
Humped
ALLO, TlO-L-5
Normal
Drill R
M
8
Normal
Normal
Calcified anterior disk T-l 2-L-3
Normal
Drill S
M
19
Contracture, right knee
Normal
Beaklike anterior osteophytes,
Fused
dorsal spine; bamboo lumbar spine* Siamang
F
27
Normal
Normal
Normal
Normal
Siamang
M
18%
OA, hips
Normal
Bamboo spine*
Fused ___
Abbreviations:
ALLO, anterior longitudinal ligament ossification; SI, sacroiliac; OA, osteoarthritis.
*See x-ray report in text.
were observed, and spinal x-rays were reviewed. Clinical observations showed one drill (drill N) to be “hump-backed,” arthritic, and “unable or unwilling to use his rear legs.” He became ill due to anal fistulae and abscesses resulting from locomoting in a sitting position and was euthanatized at age 20 years for humanitarian reasons. His premortem and postmortem x-rays are reported. A second drill (drill S) had an apparent arthritic knee but did not show obvious spinal involvement. His x-rays, however, showed the typical bamboo spine and obliteration of sacroiliac joints. A third drill, a female (drill E), was noted premorbidly to have a humpback. She died at age 24 years of congestive heart failure. Her x-rays showed anterior longitudinal ligament ossification from T-11 through L-l. The sacroiliac joints were normal, and no other significant spinal abnormalities were noted. A fourth drill, a 23-year-old female (drill B) with a single swan neck deformity, also had spinal bony fusion anteriorly between the bodies of L-l and L-2. The remaining two drills were clinically normal, but radiographically the subadult male (drill R) showed calcification of the anterior disks. RESULTS
X-rays of an adult male siamang (Los Angeles Zoo case 1233) and two adult male drills (Los Angeles Zoo cases 90-210 and 2331) are reported.
Radiographs (February 16, 1983)~Siamang (case 1233)
A lateral view of the entire spine shows some proliferative changes on the anterior aspect of the bodies of C-6 and C-7 which are characterized as large bony projections that point downward and represent anterior longitudinal ligament ossification. The cervical intervertebral disk spaces in the affected areas and throughout the cervical spine are well maintained. The opposing surfaces of the lower dorsal vertebrae show irregularities consistent with mild epiphysitis and minimal evidence of osteophyte formation. No syndesmophytes are noted. An anteroposterior (AP) view of the lower part of the skull, neck, dorsolumbar spine, and upper portions of the pelvis shows calcifications that appear to be in the bladder. The glenohumeral joints are normal, and there is apparent fusion of both sacroiliac joints. The lumbar spine in the AP view shows a typical bamboo spine with ossification of the lateral ligaments at each intervertebral disk level. Radiographs (March 17, 1983)Siamang (case 1233)
Both sacroiliac joints appear to be fused. There is a small erosion on the superior aspect of the right femoral head, consistent with early inflammatory arthritis.
172
Radiographs (case 1233)
SWEZEY, COX, AND GONZALES
(April 8, 1985)-Siamang
On bladder survey, the bamboo appearance of the lumbar spine is again noted. The sternoclavicular joint shows some sclerosis and smudging of the joint margins consistent with an inflammatory process. The left hip shows moderate osteoarthritic changes with some erosion and narrowing of the joint space and prominent osteophytes. The joint space on the right hip is narrowed superiorly with a prominent superior osteophyte at the acetabular rim. These findings are consistent with osteoarthritis of the hips, which may be secondary to underlying ankylosing spondylitis (Fig 1). Radiographs I989) -Drill
(Postmortem; November 21, N (case 90-210)
On the lateral view, the cervical, dorsal, and lumbar spine show anterior longitudinal liga-
mentous ossification with syndesmophyte formation in all areas. There is diffuse interspinous ligament ossification with ankylosis of the majority of facet joints. On the AP view, there is a bamboo appearance of the lower lumbar spine due to anterior and lateral ligamentous ossification, Prominent osteophytes are noted in the lateral aspects of the L4-5 intervertebral disk space. The sacroiliac joints are ankylosed, and the hips are disarticulated. Radiograph
(April 17, 1990)-Dtill
S (case 2331)
On the AP and lateral views of the dorsal and lumbar spine, there is diffuse ossification of the anterior longitudinal ligament. The lateral view of the dorsal spine shows large anterior beaking osteophytic projections at essentially all levels. The lumbar spine shows diffuse flowing ossification of the anterior longitudinal ligament with preservation of intervertebral disk spaces (Fig 2). On the AP view, the lumbar spine has a bamboo appearance with bony bridging extending laterally from the mid-vertebral bodies over the periphery of the disk areas from L-l to L-5. At L-5-S-l there are prominent bilateral osteophytes. The sacroiliac joints appear fused (Fig 3). These findings are consistent with ankylosing spondylitis or variant spondylitis, although the beaked appearance of the prominent dorsal spine osteophytes is atypical. The clinical and radiographic observations on the animals in this study are summarized in Table 1 and Figs 1 through 3. DISCUSSION
Fig 1: Male siamong (case 1233). Arrow A indicates bamboo spine, B indicates the area of the fused sacroiliac joint, C indicates superficial erosions on the right hip, and D indicates an osteophyte on the left hip.
The presence of arthritic disorders in various primate species that closely resemble their human counterparts is now widely recognized.‘.” The evidence of psoriaticlike spondyloarthropathy occurring commonly in western lowland gorillas has been documented.4 Only three examples of “classical” ankylosing spondylitis in nonhuman primates have been described.‘,’ An adult rhesus monkey studied by Sokoloff et al showed pathological evidence of an inflammatory lesion, presumably an enthesopathy, and sacroiliac erosions and facet bony ankylosis.’ In addition, radiographic evidence of diffuse posterior element and facet joint bony ankylosis without disk or anterior longitudinal ligament involvement was seen.’ Sokoloff et al also de-
ALKYLOSING
SPONDYLITIS
173
IN PRIMATES
showed no other evidence of spinal or other joint arthropathies. He was treated for a bladder calculus. His death was attributed to a traumatic hemopericardium resulting from an anesthetic dart injury that occurred when he was anesthetized for treatment of a fractured forelimb. At necropsy he had a cornea1 ulceration of the right eye; no other significant lesions were noted. Various spondyloarthropathies, osteoarthritis, and/or DISH-like changes were also noted radiographically in five of the six drills. Two of these drills had roentgenographic changes of spondyloarthritis. Multiple skeletal traumas causing arthropathies were noted in the chimpanzee population of Gombe observed by Jane Goodall.’ CPPD
Fig 2:
Drill (case 2331).
lateral
view
of the
lumbar spine. Arrow A indicates the area of diffuse anterior longitudinal ligament ossification.
scribed another rhesus monkey with sacroiliac joint fusion.’ As previously noted, Adams et al reported a female western lowland gorilla with a bamboo spine and peripheral large joint involvement who had a “G”LA-B27 (HLAB27) male offspring.’ In this study, x-rays of an adult (27-year-old) male siamang showed both sacroiliac bony fusion and a classic bamboo spine typical of ankylosing spondylitis. In addition, his hip x-rays showed progressive arthritic changes suggestive of inflammatory arthropathy leading to secondary degenerative joint disease. This animal
Fig 3:
Drill (case 2331), anteroposterior
view of
the lumbar spine. Arrow A indicates bamboo spine, and 6 indicates the area of the fused sacroiliac joint.
174
SWEZEY, COX, AND GONZALES
has been commonly found in nonhuman primates.” In this connection, it should be noted that CPPD has been associated with disk calcification, bony spurs, and bony intervertebral bridging in humans.” The role, if any, of CPPD in the animals in this study has not been determined. A group of mandrills (Mandrillus sphinx) in Toronto, Canada, have spondyloarthritis, and preliminary observations indicate HLA-B27 antigenicity (Inman R, McKibbon C, personal communication). Tissue typing is underway on several drills in this study (Weinberg K, personal communication). In view of the apparent widespread prevalence of ankylosing spondylitis, its association with HLA-B27 positivity in Gorilla gorilla gorilla and perhaps Mandrillus is of interest. This is in sharp contrast to the rarity of human spondyloarthropathies in Zimbabwe, Africa, and the further observation that none of nine Zimbabwe patients with ankylosing spondylitis were HLA-B27 positive.” Seven of 10 patients in Zimbabwe with Reiter’s syndrome and spondyloarthropathy had the B-7-CREG antigen.‘* Granting that the primates in this report were
raised in captivity, a further observation merits comment. Because many nonhuman primates living in the wild develop a variety of arthropathies, including spondyloarthropathies, there is an apparent lack of protection against a variety of rheumatological disorders provided by consuming a herbiverous diet consisting of unadulterated, largely “natural” foods. CONCLUSION
These are the first reported cases of ankylosing spondylitis in a siamang (gibbon) and two drills (baboons), the third and fourth nonhuman primate species in which ankylosing spondylitis or variant spondylitis has been observed. The possibility of further elucidating environmental and genetic factors pertaining to ankylosing spondylitis by studying nonhuman primates may be potentially rewarding. ACKNOWLEDGMENT The authors gratefully acknowledge Mary and Harlan Deckert, dedicated docents at the Los Angeles Zoo, Christine Marason, Los Angeles Zoo Veterinarian Assistant, and H.J. Holshuh, pathologist, for their invaluable assistance in this project.
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