{"paper_id":"dfd7c647-def0-4fae-8f60-cfbba5fe0606","body_text":"Abstract\nThere are several disease entities in nonhuman primates that primarily manifest as inflammatory, degenerative, and/or proliferative processes and are not assumed or currently known to be caused by infectious agents. Despite uncertainties in etiology and pathogenesis, a number of these entities such as endometriosis, marmoset wasting syndrome, and chronic segmental lymphocytic enteritis are prominent within colonies with a high degree of morbidity and mortality. Endometriosis is a proliferative disease of unidentified etiology that affects several Old World monkey species with a menstrual cycle, while gluten-sensitive enteropathy of macaques is an inflammatory disease, for which an immune-mediated pathogenesis has been established. Given the similarities of these entities in humans, they have been established as an important translational models of disease. Other entities such as diffuse idiopathic skeletal hyperostosis (DISH) and noninfectious alopecia are less debilitating but remain important entities to further try and understand. DISH presents as a chronic degenerative disorder affecting both Old and New World monkeys, and noninfectious alopecia is a recognized health issue in macaque colonies with poorly understood etiology.\nAccess this chapter\nTax calculation will be finalised at checkout\nPurchases are for personal use only\nSimilar content being viewed by others\nReferences\nMarini RP. Diseases of the urogenital system. In: Marini RP, Wachtman LM, Tardif SD, Masfield K, Fox JG, editors. The common marmoset in captivity and biomedical research. London: Academic Press; 2019. p. 195–212.\nIsobe K, Adachi K, Hayashi S, Ito T, Miyoshi A, Kato A, Suzuki M. Spontaneous glomerular and tubulointerstitial lesions in common marmosets (Callithrix jacchus). Vet Pathol. 2012;49:839–45. https://doi.org/10.1177/0300985811427151.\nYamada N, Sato J, Kanno T, Wako Y, Tsuchitani M. Morphological study of progressive glomerulonephropathy in common marmosets (Callithrix jacchus). Toxicol Pathol. 2013;41:1106–15. https://doi.org/10.1177/0192623313478206.\nBrack M, Rothe H. Chronic tubulointerstitial nephritis and wasting disease in marmosets (Callithrix jacchus). Vet Pathol. 1981;18:45–54. https://doi.org/10.1177/0300985881018s0605.\nCollins MG, Rogers NM, Jesudason S, Kireta S, Brealey J, Coates PT. Spontaneous glomerular mesangial lesions in common marmoset monkeys (Callithrix jacchus): a benign non-progressive glomerulopathy. J Med Primatol. 2014;43:477–87. https://doi.org/10.1111/jmp.12134.\nBrack M. IgM-mesangial nephropathy in callitrichids. Vet Pathol. 1988;25:270–6. https://doi.org/10.1177/030098588802500404.\nBrack M, Schroeder C, Fooke M, Schlumberger W. IgM/IgA nephropathy in callitrichids: antigen studies. Nephron. 1999;82:221–31. https://doi.org/10.1159/000045406.\nWinkelmann, J.M. Kidney alterations in common marmosets (Callithrix jacchus) with wasting marmoset syndrome (German). https://elib.tiho-hannover.de/receive/etd_mods_00001143.\nBrack M, Weber M. Ultrastructural and histochemical mesangial alterations in callitrichid IgM nephropathy (primates: platyrrhina). Nephron. 1995;69:286–92. https://doi.org/10.1159/000188472.\nSchroeder C, Osman AA, Roggenbuck D, Mothes T. IgA-gliadin antibodies, IgA-containing circulating immune complexes, and IgA glomerular deposits in wasting marmoset syndrome. Nephrol Dial Transplant. 1999;14:1875–80. https://doi.org/10.1093/ndt/14.8.1875.\nAmi Y, Suzaki Y, Goto N. Endometriosis in cynomolgus monkeys retired from breeding. J Vet Med Sci. 1993;55:7–11. https://doi.org/10.1292/jvms.55.7.\nAssaf BT, Miller AD. Pleural endometriosis in an aged rhesus macaque (Macaca mulatta): a histopathologic and immunohistochemical study. Vet Pathol. 2012;49:636–41. https://doi.org/10.1177/0300985811406890.\nBinhazim AA, Tarara RP, Suleman MA. Spontaneous external endometriosis in a De Brazza’s monkey. J Comp Pathol. 1989;101:471–4. https://doi.org/10.1016/0021-9975(89)90031-5.\nDick EJ Jr, Hubbard GB, Martin LJ, Leland MM. Record review of baboons with histologically confirmed endometriosis in a large established colony. J Med Primatol. 2003;32:39–47. https://doi.org/10.1034/j.1600-0684.2003.00008.x.\nMattison JA, Ottinger MA, Powell D, Longo DL, Ingram DK. Endometriosis: clinical monitoring and treatment procedures in rhesus monkeys. J Med Primatol. 2007;36:391–8. https://doi.org/10.1111/j.1600-0684.2006.00208.x.\nNishimoto-Kakiuchi A, Netsu S, Okabayashi S, Taniguchi K, Tanimura H, Kato A, Suzuki M, Sankai T, Konno R. Spontaneous endometriosis in cynomolgus monkeys as a clinically relevant experimental model. Hum Reprod. 2018;33:1228–36. https://doi.org/10.1093/humrep/dey095.\nStory L, Kennedy S. Animal studies in endometriosis: a review. ILAR J. 2004;45:132–8. https://doi.org/10.1093/ilar.45.2.132.\nWaterton JC, Miller D, Morrell JS, Dukes M, West CD, Wadsworth PF. A case of endometriosis in the macaque diagnosed by nuclear magnetic resonance imaging. Lab Anim. 1992;26:59–64. https://doi.org/10.1258/002367792780809066.\nZondervan KT, Weeks DE, Colman R, Cardon LR, Hadfield R, Schleffler J, Trainor AG, Coe CL, Kemnitz JW, Kennedy SH. Familial aggregation of endometriosis in a large pedigree of rhesus macaques. Hum Reprod. 2004;19:448–55. https://doi.org/10.1093/humrep/deh052.\nMiller AD. Neoplasia and proliferative disorders of nonhuman primates. In: Abee CR, Mansfield K, Tardif S, Morris T, editors. Nonhuman primates in biomedical research: diseases. London: Academic Press; 2012. p. 325–56.\nMounsey AL, Wilgus A, Slawson DC. Diagnosis and management of endometriosis. Am Fam Physician. 2006;74:594–600.\nCline JM, Brignolo L, Ford EW. Urogential system. In: Abee CR, Mansfield K, Tardif S, Morris T, editors. Nonhuman primates in biomedical research: diseases. London: Academic Press; 2012. p. 484–562.\nGruber-Dujardin E, Bleyer M, Mätz-Rensing K. Morphological and immunohistochemical characterization of spontaneous endometriosis in rhesus macaques (Macaca mulatta). Primate Biol. 2017;4:77–91. https://doi.org/10.5194/pb-4-77-2017.\nAbrao MS, Neme RM, Carvalho FM, Aldrighi JM, Pinotti JA. Histological classification of endometriosis as a predictor of response to treatment. Int J Gynaecol Obstet. 2003;82:31–40. https://doi.org/10.1016/s0020-7292(03)00079-1.\nKamergorodsky G, Ribeiro PA, Galvão MA, Abrão MS, Donadio N, Lemos NL, Aoki T. Histologic classification of specimens from women affected by superficial endometriosis, deeply infiltrating endometriosis, and ovarian endometriomas. Fertil Steril. 2009;92:2074–7. https://doi.org/10.1016/j.fertnstert.2009.05.086.\nAtkins HM, Lombardini ED, Caudell DL, Appt SE, Dubois A, Cline JM. Decidualization of endometriosis in macaques. Vet Pathol. 2016;53:1252–8. https://doi.org/10.1177/0300985816646433.\nFazleabas AT, Brudney A, Chai D, Langoi D, Bulun SE. Steroid receptor and aromatase expression in baboon endometriotic lesions. Fertil Steril. 2003;80:820–7. https://doi.org/10.1016/s0015-0282(03)00982-8.\nBrosens IA, Brosens JJ. Endometriosis. Eur J Obstet Gynecol Reprod Biol. 2000;90:159–64. https://doi.org/10.1016/s0301-2115(00)00265-7.\nGiudice LC, Kao LC. Endometriosis. Lancet. 2004;364:1789–99. https://doi.org/10.1016/S0140-6736(04)17403-5.\nLaganà AS, Garzon S, Götte M, Viganò P, Franchi M, Ghezzi F, Martin DC. The pathogenesis of endometriosis: molecular and cell biology insights. Int J Mol Sci. 2019;20:5615. https://doi.org/10.3390/ijms20225615.\nSasson IE, Taylor HS. Stem cells and the pathogenesis of endometriosis. Ann N Y Acad Sci. 2008;1127:106–15. https://doi.org/10.1196/annals.1434.014.\nBethune MT, Borda JT, Ribka E, Liu MX, Phillippi- Falkenstein K, Jandacek RJ, Doxiadis GG, Gray GM, Khosla C, Sestak K. A nonhuman primate model for gluten sensitivity. PLoS One. 2008;3:1614.\nJabri B, Sollid LM. T cells in celiac disease. J Immunol. 2017;198(8):3005–14.\nWagner JD, Jerome CP, Adams MR. Gluten-sensitive enteropathy in a cynomolgus monkey. Lab Anim Sci. 1988;38:592–4.\nBrewers M. Epidemiology of celiac disease: what are the prevalence, incidence, and progression of celiac disease? Gastroenterology. 2005;128:47–51.\nSestak K, Mazumdar K, Midkiff CC, Dufour CC, Dufour J, Borda JT, Alvarez X. Recognition of epidermal transglutaminase by IgA and tissue transglutaminase 2 antibodies in a rare case of rhesus dermatitis. J Vis Exp. 2011;58:3154. https://doi.org/10.3791/3154.\nSestak K, Conroy L, Aye PP, Mehra S, Doxiadis GG, Kaushal D. Improved xenobiotic metabolism and reduced susceptibility to cancer in gluten-sensitive macaques upon introduction of a gluten-free diet. PLoS One. 2011;6(4):18648. https://doi.org/10.1371/journal.pone.0018648.\nHill ID, Dirks MH, Liptak GS, Colletti RB, Fasano A, Guandalini S, Hoffenberg EJ, Horvath K, Murray JA, Pivor M, Seidman EG. Guideline for the diagnosis and treatment of celiac disease in children: recommendations of the North American Society for Pediatric Gastroenterology, Hepatology and Nutrition. J Pediatr Gastroenterol Nutr. 2005;40:1–19.\nVillanacci V, Vanoli A, Giovanni A, Salviato T, Bonetti LR, Baronchelli C, Saragoni L, Parente P. Celiac disease: histology-differential diagnosis-complications. A practical approach. Pathologica. 2020;112:186–96.\nMazumdar K, Xavier A, Borda JT, Dufour J, Martin E, Bethune MT, Kholsa C, Sestak K. Visualization of transepithelial passage of the immunogenic 33-reside peptide from alpha-2 gliadin in gluten sensitive macaques. PLoS One. 2010;5(4):10228. https://doi.org/10.1371/journal.pone.0010228.\nXu H, Feely SL, Wang X, Liu DX, Borda JT, Dufour J, et al. Gluten-sensitive enteropathy coincides with decreased capability of intestinal T cells to secrete IL-17 and IL-22 in a macaque model for celiac disease. Clin Immunol. 2013;147(1):40–9. https://doi.org/10.1016/j.clim.2013.02.012. Epub 2013 Feb 28\nLaing ST, Merriam D, Shock BC, Mills S, Spinner A, Reader R, Hartigan-O’Conner DJ. Idiopathic colitis in rhesus macaques is associated with dysbiosis, abundant enterochromaffin cells and altered T-cell cytokine expression. Vet Pathol. 2018;55:741–52.\nBeglinger R, Illgen B, Pfister R, Heider K. The parasite Trichospirura leptostoma associated with wasting diseases in a colony of common marmosets, Callithrix jacchus. Folia Primatol. 1988;51:45–51.\nPotkay S. Diseases of the callitrichidae: a review. J Med Primatol. 1992;21:189–236.\nChalifoux LV, Broncin RT, Escajadillo A, McKenna S. An analysis of the association of the gastroenteric lesions with chronic wasting syndrome of marmosets. Vet Pathol. 1982;19:141–62.\nDavid JM, Dick ED Jr, Hubbard GB. Spontaneous pathology of the common marmoset (Callithrix jacchus) and tamarins (Sanguinis oedipus, Sanguinis mystax). J Med Primatol. 2009;38:347–59.\nBaxter VK, Shaw GC, Sotuyo NP, Carlson CS, Olson EJ, Zink MC, Mankowski JL, Adams RJ, Hutchinson EK, Metcalf Pate KA. Serum albumin and body weight as biomarkers for the antemortem identification of bone and gastrointestinal disease in the common marmoset. PLoS One. 2012;8:1–10. https://doi.org/10.1371/journal.pone.0082747.\nLogan AC, Kahn KNM. Clinical pathologic changes in two marmosets with wasting syndrome. Toxicol Pathol. 1996;24:707–9.\nLudlage E, Mansfield K. Clinical care and disease of the common marmoset (Callithrix jacchus). Comp Med. 2003;53:369–82.\nNakashima E, Okano Y, Nimi K, Takahashi E. Detection of calprotectin and apoptotic activity in the colon of marmosets with chronic diarrhea. J Vet Med Sci. 2013;75:1633–6.\nRoss C, Davis K, Dobek G, Tardif S. Aging phenotypes of common marmosets (Callithrix jacchus). J Aging Res. 2012;2012:1. https://doi.org/10.1155/2012/567143.\nRichards-Rios P, Wigley P, Lopez J, Wormell D, Barbon A. Changes in the faecal microbiome of pied tamarins (Sanguines bicolor) associated with chronic, recurrent diarrhoea and weight loss. Anim Microbiome. 2021;3:1. https://doi.org/10.1186/s42523-020-00062-4.\nHeffron AS, Lauck M, Somsen ED, Townsend EC, Bailey AL, Sosa M, Eickhoff J, Capuano S III, Newman CM, Kuhn JH, Mejia A, Simmons HA, O’Conner DH. Discovery of a novel pegivirus in common marmosets (Callithrix jacchus) with lymphocytic enterocolitis. Microorganisms. 2020;8:1509. https://doi.org/10.3390/microorganisms8101509.\nParambeth JC, Ross CN, Miller AD, Austad AD, Lidbury JA, Suchodolski JS, Steiner JM. Serum cobalamin and folate concentrations in common marmosets (Callithrix jacchus) with chronic lymphocytic enteritis. Comp Med. 2019;69:135–43.\nResnick D, Niwayama G. Radiographic and pathologic features of spinal involvement in diffuse idiopathic skeletal hyperostosis (DISH). Radiology. 1976;119:559–68. https://doi.org/10.1148/119.3.559.\nWilson DJ, Kay V, Charig M, Hughes DG, Creasey TS. Skeletal hyperostosis and extraosseous calcification in patients receiving long-term etretinate (Tigason). Br J Dermatol. 1988;119:597–607.\nBelanger TA, Rowe DE. Diffuse idiopathic skeletal hyperostosis: musculoskeletal manifestations. J Am Acad Orthop Surg. 2001;9:258–67. https://doi.org/10.5435/00124635-200107000-00006.\nMader R, Verlaan JJ, Buskila D. Diffuse idiopathic skeletal hyperostosis: clinical features and pathogenic mechanisms. Nat Rev Rheumatol. 2013;9:741–50. https://doi.org/10.1038/nrrheum.2013.165.\nNascimento FA, Gatto LA, Lages RO, Neto HM, Demartini Z, Koppe GL. Diffuse idiopathic skeletal hyperostosis: a review. Surg Neurol Int. 2014;5(Suppl 3):122–5. https://doi.org/10.4103/2152-7806.130675.\nKandel RA, Renlund RC, Cheng PT, Rapley WA, Mehren KG, Pritzker KP. Calcium pyrophosphate dihydrate crystal deposition disease with concurrent vertebral hyperostosis in a Barbary ape. Arthritis Rheum. 1983;26:682–7. https://doi.org/10.1002/art.1780260518.\nLivingstone B, Kitchener AC, Hull G, Schwarz T, Vijayanathan S, Allen MJ, et al. Diffuse idiopathic skeletal hyperostosis in captive gorillas (Gorilla spp.): appearances and diagnosis. J Zoo Wildl Med. 2020;51:578–90. https://doi.org/10.1638/2019-0180.\nLovell NC. Skeletal and dental pathology of free-ranging mountain gorillas. Am J Phys Anthropol. 1990;81:399–412. https://doi.org/10.1002/ajpa.1330810309.\nRatliff C, Waller KR, Steinberg H, Clyde VL. Diffuse idiopathic skeletal hyperostosis with secondary dysphagia in a black-handed spider monkey (Ateles geoffroyi). J Zoo Wildl Med. 2020;51:455–8. https://doi.org/10.1638/2018-0240.\nSokoloff L, Snell KC, Stewart HC. Spinal ankyloses in old rhesus monkeys. Clin Orthop. 1968;61:285–93.\nMader R, Verlaan JJ, Eshed I, Bruges-Armas J, Puttini PS, Atzeni F, et al. Diffuse idiopathic skeletal hyperostosis (DISH): where we are now and where to go next. RMD Open. 2017;3:e000472. https://doi.org/10.1136/rmdopen-2017-000472.\nOrtega M, Gonçalves R, Haley A, Wessmann A, Penderis J. Spondylosis deformans and diffuse idiopathic skeletal hyperostosis (DISH) resulting in adjacent segment disease. Vet Radiol Ultrasound. 2012;53:128–34. https://doi.org/10.1111/j.1740-8261.2011.01891.x.\nMader R, Sarzi-Puttini P, Atzeni F, Olivieri I, Pappone N, Verlaan JJ, et al. Extraspinal manifestations of diffuse idiopathic skeletal hyperostosis. Rheumatology (Oxford). 2009;48:1478–81. https://doi.org/10.1093/rheumatology/kep308.\nPritzker KPH, Kessler MJ. Arthritis, muscle, adipose tissue, and bone diseases of nonhuman primates. In: Abee CR, Mansfield K, Tardif S, Morris T, editors. Nonhuman primates in biomedical research: diseases. London: Academic Press; 2012. p. 629–97.\nFournier DE, Kiser PK, Beach RJ, Dixon SJ, Séguin CA. Dystrophic calcification and heterotopic ossification in fibrocartilaginous tissues of the spine in diffuse idiopathic skeletal hyperostosis (DISH). Bone Res. 2020;8:16. https://doi.org/10.1038/s41413-020-0091-6.\nKuperus JS, Westerveld LA, Rutges JP, Alblas J, van Rijen MH, Bleys RL, et al. Histological characteristics of diffuse idiopathic skeletal hyperostosis. J Orthop Res. 2017;35:140–6. https://doi.org/10.1002/jor.23267.\nOlivieri I, D’Angelo S, Palazzi C, Padula A, Mader R, Khan MA. Diffuse idiopathic skeletal hyperostosis: differentiation from ankylosing spondylitis. Curr Rheumatol Rep. 2009;11:321–8. https://doi.org/10.1007/s11926-009-0046-9.\nBeisner BA, Isbell LA. Factors influencing hair loss among female captive rhesus macaques (Macaca mulatta). Appl Anim Behav Sci. 2009;119:91–100. https://doi.org/10.1016/j.applanim.2009.03.016.\nBellanca RU, Lee GH, Vogel K, Ahrens J, Kroeker R, Thom JP, Worlein JM. A simple alopecia scoring system for use in colony management of laboratory-housed primates. J Med Primatol. 2014;43:153–61. https://doi.org/10.1111/jmp.12107.\nKramer J, Fahey M, Santos R, Carville A, Wachtman L, Mansfield K. Alopecia in rhesus macaques correlates with immunophenotypic alterations in dermal inflammatory infiltrates consistent with hypersensitivity etiology. J Med Primatol. 2010;39:112–22. https://doi.org/10.1111/j.1600-0684.2010.00402.x.\nLutz CK, Coleman K, Worlein J, Novak MA. Hair loss and hair-pulling in rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci. 2013;52:454–7.\nSteinmetz HW, Kaumanns W, Dix I, Heistermann M, Fox M, Kaup FJ. Coat condition, housing condition and measurement of faecal cortisol metabolites--a non-invasive study about alopecia in captive rhesus macaques (Macaca mulatta). J Med Primatol. 2006;35:3–11. https://doi.org/10.1111/j.1600-0684.2005.00141.x.\nNovak MA, Meyer JS. Alopecia: possible causes and treatments, particularly in captive nonhuman primates. Comp Med. 2009;59:18–26.\nSteinmetz HW, Kaumanns W, Neimeier KA, Kaup FJ. Dermatologic investigation of alopecia in rhesus macaques (Macaca mulatta). J Zoo Wildl Med. 2005;36:229–38. https://doi.org/10.1638/04-054.1.\nHoness P, Gimpel J, Wolfensohn S, Mason G. Alopecia scoring: the quantitative assessment of hair loss in captive macaques. Altern Lab Anim. 2005;33:193–206. https://doi.org/10.1177/026119290503300308.\nKramer JA, Mansfield KG, Simmons JH, Bernstein JA. Psychogenic alopecia in rhesus macaques presenting as focally extensive alopecia of the distal limb. Comp Med. 2011;61:263–8.\nLuchins KR, Baker KC, Gilbert MH, Blanchard JL, Liu DX, Myers L, Bohm RP. Application of the diagnostic evaluation for alopecia in traditional veterinary species to laboratory rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci. 2011;50:926–38.\nArdeshir A, Oslunf KL, Ventimiglia F, Yee J, Lerche NW, Hyde DM. Idiopathic microscopic colitis of rhesus macaques: quantitative assessment of colonic mucosa. Anat Rec (Hoboken). 2013;296:1169–79.\nAuthor information\nAuthors and Affiliations\nCorresponding author\nEditor information\nEditors and Affiliations\nRights and permissions\nCopyright information\n© 2024 The Author(s), under exclusive license to Springer Nature Switzerland AG\nAbout this chapter\nCite this chapter\nOlstad, K.J., Bleyer, M. (2024). Other Noninfectious Conditions (Inflammatory/Degenerative/Proliferative, Immune-Mediated/Idiopathic/Unknown) in Nonhuman Primates. In: Kondova - Perseng, I., Mansfield, K.G., Miller, A.D. (eds) Atlas of Diagnostic Pathology in Nonhuman Primates. Springer, Cham. https://doi.org/10.1007/978-3-031-41280-6_7\nDownload citation\nDOI: https://doi.org/10.1007/978-3-031-41280-6_7\nPublished:\nPublisher Name: Springer, Cham\nPrint ISBN: 978-3-031-41279-0\nOnline ISBN: 978-3-031-41280-6\neBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)","source_license":"CC0","license_restricted":false}