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Fatal Lymphoproliferative Disease Associated with a Novel Gammaherpesvirus in a Captive Population of Common Marmosets

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Fatal Lymphoproliferative Disease Associated with a Novel Gammaherpesvirus in a Captive Population of Common Marmosets Laboratory Animal Science Vol 50, No 1 Copyright 2000 February 2000 by the American Association for Laboratory Animal Science Fatal Lymphoproliferative Disease Associated with a Novel Gammaherpesvirus in a Captive Population of Common Marmosets Jan C. Ramer,1* Richard L. Garber,2 Keith E. Steele,3 Jonathan F. Boyson,1† Christine O’Rourke,1†† and James A. Thomson1 Background and Purpose: Callitrichids (marmosets and tamarins) are extremely susceptible to experimental tumor induction by herpesviruses native to other primate species. A colony of common marmosets developed a syndrome of weight loss, inappetence, diarrhea, and in several animals, palpable abdominal masses. Methods: Marmosets in the colony were subjected to histologic examination and serologic testing for Epstein- Barr virus (EBV). The DNA from tumors that developed in the marmosets was subjected to consensus primer poly- merase chain reaction (PCR) analysis designed to amplify conserved regions of herpesvirus genomes. Results: The mesenteric lymph nodes and intestinal mucosa were consistently infiltrated by principally B lym- phocytes, which often obliterated the normal architecture. Of 84 clinically normal marmosets, 52 were seropositive for EBV. The tumor DNA contained previously unreported herpesvirus sequences closely related to but distinct from those of EBV, Herpesvirus papio, and these lymphocryptovirus, a novel gammaherpesvirus. Results of PCR analysis of circulating lymphocytes from EBV-positive, clinically normal marmosets were negative for EBV anti- bodies and were positive for marmoset lymphocryptovirus; PCR analysis of circulating lymphocytes from EBV- negative marmosets yielded negative results for EBV and this novel marmoset lymphocryptovirus. Conclusion: This novel gammaherpesvirus possibly associated with tumor development may have important man- agement implications for captive callitrichids. Most primates, human and non-human, are naturally in- callitrichid New World monkeys) has been known since these fected with species-specific gammaherpesviruses by adulthood viruses were first isolated in 1968 and 1970, but to our knowl- (1, 2). In general, gammaherpesviruses do not cause appreciable edge, spontaneous herpesvirus-induced lymphoproliferative dis- disease at primary infection in the natural host. Animals fre- ease in laboratory or zoo-housed callitrichids has not been quently remain latently infected, and serum antibodies are reported. There are few reports in the literature of spontaneous maintained throughout life. Immunosuppression in latently in- titers to EBV in callitrichids, but not reports of spontaneous fected individuals, or infection in a species that is not the natu- lymphoproliferative disease in these animals (7). We describe ral host, can lead to viral-induced lymphoproliferations, rapidly the clinical, pathologic, and serologic history of an outbreak of fatal malignant lymphoma, or chronic mononucleosis-type dis- spontaneous fatal lymphoproliferative disease in a captive eases (3-12). The best understood gammaherpesvirus is colony of common marmosets, and identification of a novel Epstein-Barr virus (EBV), the most common cause of infectious gammaherpesvirus in the tumors of these animals by use of mononucleosis in humans. EBV has been associated with polymerase chain reaction (PCR) analysis. Burkitt’s lymphoma, nasopharyngeal carcinoma, and Hodgkin’s disease (1, 2, 13-16). Numerous examples of gammaherpesvirus- Case History induced lymphoproliferative disease in nonhuman primates have The Wisconsin Regional Primate Research Center (WRPRC) been reported (2, 4, 5, 11, 17-23). houses an average population of 230 common marmosets It is well documented that callitrichids (marmosets and (Callithrix jacchus), ranging in age from neonates to adults over tamarins) are extremely susceptible to experimental tumor in- 10 years old. The colony was formed in the early 1990s with ani- duction by herpesviruses native to other primate species: H. mals from two sources. The marmosets are pair or family saimiri, present in > 85% of captive squirrel monkeys, H. ateles, housed indoors in four separate rooms, isolated from the present in 50 to 60% of captive spider monkeys, and EBV (6, 9, macaque colony (Macaca mulatta and M. arctoides). Group com- 24-29). The potential for severe spontaneous disease in position changes frequently. Lights were on from 6 AM to 6 PM, callitrichids housed with or near cebid monkeys (all non- ambient temperature was 27ЊC, and relative humidity was ap- proximately 50%. Animals were fed 45 g of Zu/Preem marmoset The Wisconsin Regional Primate Research Center, University of Wisconsin, Madison, Wisconsin1; PathoGenesis Corporation, Seattle, Washington2; and U.S. Diet (Hill’s Pet Products, Topeka, KS) topped with 1 tsp of plain Army Medical Research Institute of Infectious Diseases, Fort Detrick, Mary- yogurt mixed with 5 IU of calcium, 250 IU of vitamin D3, and 3 land3 *Address correspondence and requests for reprints to: J. C. Ramer, India- mg of vitamin C once daily. Continuous access to water was pro- napolis Zoo, 1200 West Washington Street, Indianapolis, IN 46222. vided by an in-line automatic watering system. All personnel †Present address is Department of Molecular and Cellular Biology, Harvard entering the area wore coveralls, masks, gloves, and protective University, Cambridge, Massachusetts. ††Present address is Wyeth-Ayerst Research, Chazy, New York. boots. Daily health records were kept for each animal. All ani- 59 Vol 50, No 1 Comparative Medicine February 2000 mal care met or exceeded standards outlined in the NIH Guide for the Care and Use of Laboratory Animals and the Animal Welfare Act and subsequent amendments. From 1992 to 1996, 16 cases of lymphoproliferative disease in adult common marmosets from the WRPRC were diagnosed at necropsy Affected animals ranged in age from 16 months to 9 years; six male and 10 female animals were affected. There was no appreciable familial relationship among the affected ani- mals, as determined by low coefficient of relatedness (0.02). Affected animals typically developed weight loss, inappe- tence, and diarrhea. Frequently, a firm palpable mass was de- tected in the mid-portion of the abdomen, and several marmosets developed intestinal obstruction. In two marmosets, peripheral lymphadenopathy was observed. Results of complete blood count and serum biochemical analysis on marmosets were variable, ranging from within normal limits for this species in the WRPRC laboratory to neutrophilia with left shift and high liver enzyme activities. Atypical circulating lymphocytes were Figure 1. Photomicrograph of a section of marmoset gastrointestinal evident on blood smears from the two marmosets that had pe- tract with enlarged mesenteric lymph nodes. Bar = 1 cm. ripheral lymphadenopathy, but not on those from the remaining animals. Bacteriologic culture of feces from animals with diar- serosa of intestinal sections were identified as B lymphocytes rhea yielded negative results for Salmonella, Shigella, and (Figure 7), whereas scattered cells were identified as T lympho- Campylobacter species, and results of fecal flotation were nega- cytes. Many of the CD20-expressing cells had atypical morpho- tive for pathogens. logic features. Atypical lymphoid cells in the spleens also were Complete necropsy was performed on all 16 marmosets. A labeled with the B-lymphocyte marker. The CD3-labeled cells, consistent finding was grossly large mesenteric lymph nodes however, had normal lymphocyte features. Some, but not all, (Figure 1), which corresponded to the abdominal masses de- spleens also contained cells that were labeled by the EBV LMP- tected clinically. Tissues were fixed in neutral-buffered 10% for- 1 antibody (Figure 8). The LMP-expressing cells varied from malin, embedded in paraffin, sectioned at 5-␮m-thickness, and morphologically normal lymphocytes to small cells with smudgy stained with hematoxylin and eosin. In all instances, the me- nuclei to larger, atypical lymphoid cells and some histiocytoid senteric lymph node architecture was obliterated by heteroge- cells. They were observed principally within the red pulp and neous sheets of neoplastic round cells (Figure 2). Most cells had often in clusters. In marmoset tumor tissue, there was equivocal moderate amounts of eosinophilic cytoplasm, obscure cell bor- staining of rare lymphoid cells for LMP-1. ders, and round or oval to irregular nuclei (moderate nuclear A representative group of animals was tested for antibodies pleomorphism). Nuclei had finely granular, dispersed chromatin to EBV (Virus Reference Laboratory, Inc., Sam Antonio, TX). and one or more prominent nucleoli. Nuclear diameter varied Serum was obtained from 84 clinically normal marmosets rang- up to threefold. Mitotic figures were present at 1 to 2/high- ing in age from 1 year to 11 years. Indirect immunofluorescent power field. In some sections, the larger neoplastic cells were antibody (IFA) assays, using the viral capsid antigen (VCA; Gull intermixed with cells that were small, had scant cytoplasm, and Laboratory Kit, Salt Lake City, Utah) of EBV, were performed. had round nuclei with heterochromatic chromatin and one or Of the 84 marmosets, 52 were antibody positive, with titer rang- more inconspicuous nucleoli. All proximal colon sections had in- ing from 1:10 to 1:40. Nine marmosets were tested for antibod- filtrates of neoplastic round cells, similar to those described for ies to H. saimiri, using a dot immunobinding assay (30), and all the mesenteric
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