Randall E. Junge, MS, DVM
St. Louis Zoological Park, Forest Park, St. Louis, MO, USA
Diseases of lemurs in captivity were identified by review of medical records, literature searches, and experience of species survival plan (SSP) advisors. Diarrhea was one of the most common presenting complaints and may be associated with parasitic (usually protozoal) or bacterial enteritis. Trichobezoars and dental disease also occur. Pneumonia is uncommon unless stress is a factor; cases with Klebsiella pneumoniae infection are often rapidly fatal. Two proliferative periosteal diseases have been reported, one associated with progressive renal disease and death. Integumentary system problems are limited and most often are related to trauma. Renal disease is common in aged lemurs. Other urinary tract disease is uncommon. Diseases of the nervous system and cardiovascular system are less common, although seizures, cerebrovascular accidents, and aneurysms have occurred. Cases of toxoplasmosis (usually fatal) have been reported, most frequently in ground-dwelling species, such as ring-tailed lemurs.
The Malagasy prosimians include five extant families. However, this presentation will focus on lemurs because of their predominance in zoological collections and, therefore, the predominance of medical information available. While prosimians are certainly susceptible to a wide variety of disease syndromes, discussion will be limited to conditions with unique significance to prosimians.
The material in this presentation has been collected from several sources. The initial data collection was generated by a detailed review of medical records of 287 black lemurs13 and an extensive multispecies literature review, which includes medical reviews for lemurs in captivity1,5,11,13 and in the wild.14 This was supplemented with case material presented to lemur SSP advisors, prosimian taxon advisory group (TAG) veterinary advisors, and field research veterinary advisors.
Loose or otherwise abnormal stools were the most common cause for medical intervention in two surveys of diseases in lemurs.5,13 Bacteria isolated from fecal cultures from lemurs with evidence of gastrointestinal disease included Yersinia enterocolitica,4 Campylobacter fetus jejuni, Salmonella typhimurium, E. coli,5 and Klebsiella pneumoniae.1 With cases of bacterial enteritis that are associated with profuse or persistent diarrhea, attention must be given to prevention of dehydration, electrolyte imbalances, and secondary systemic bacterial infections.
Hemochromatosis (hepatic iron storage disease) has historically been considered a common problem in lemurs in captivity. Hemochromatosis is the development of pathological changes in the liver as a result of excess iron storage. Incidences varied with species, with Eulemur macaco most commonly affected, followed by Varecia and Lemur catta. The condition is suspected to be the result of the combination of excess dietary iron, excess ascorbic acid, and lack of tannins in the diet. Recognition of the mechanism of this problem has resulted in a reduced incidence. A common sequela to iron storage disease was the initiation of neoplastic transformation of the damaged cells, which resulted in a high incidence of hepatic neoplasia.1,11,20
Prevalence of gastrointestinal parasitism varies. Parasitism may be a cause of diarrhea in captive lemurs; however, a survey of medical records on black lemurs indicated 61% of fecal examinations positive for parasites were asymptomatic (no diarrhea). Protozoal infestations are more frequently associated with clinical diarrhea than nematode infestations; in the same survey, 53/63 (84%) of parasitic diarrheas were protozoal.13 Commonly identified organisms include Entamoeba, Trichomonas, Giardia, and Balantidium. Protozoal infestations respond to treatment with metronidazole (25 mg/kg BID for 7 days) or paromomycin (12.5 mg/kg BID for 5 days); potentiated sulfas and tetracyclines have also been used.
Common nematode parasites include organisms in the genera Strongylus, Strongyloides, Gongylonema, and Physaloptera, as well as ascarids. Gastrointestinal nematodes respond to a variety of anthelmintics (ivermectin 0.2 mg/kg PO or SC once; mebendazole 10–20 mg/kg PO for 3 days; thiabendazole 50 mg/kg PO once; and pyrantel 5–10 mg/kg PO for 3 days). Physaloptera may present a challenge for diagnosis and treatment. The eggs of this gastric nematode are shed intermittently and may be difficult to find in fecal flotations. In addition, it appears to be resistant to standard anthelmintic regimens. Treatment with ivermectin (0.2 mg/kg PO SID for 7 days) or levamisole (2.5 mg/kg PO SID for 14 days) has been successful.
Dental disease may occur in captive lemurs. Plaque and tartar accumulation is common, and tooth root abscesses are reported. Trichobezoars may occur, especially in ruffed lemurs (Varecia). Surgical intervention may be required to alleviate gastric obstruction in severe cases. Regular administration (weekly or biweekly) of laxatives or lubricants (such as oral cat laxatives) will prevent the occurrence.
Bacterial pneumonia in lemurs is not common under good management conditions; however, in stressful conditions, such as acclimating to a new environment, it can occur. Cases have been reported in newly captive animals that have been exposed to environmental changes. Clinical signs are as expected and include fever, inappetence, and labored breathing. Incidences of Klebsiella pneumoniae pneumonia are often peracute and fulminant, resulting in rapid fatalities.
The incidence of tuberculosis in prosimians appears to be low, with eight cases in three species reported.7,10,16,19 Two cases involved ring-tailed lemurs living in a North American zoo, the others were recent imports (mongoose lemurs) or in captivity in Madagascar. Lesions were described as typical tuberculosis granulomas in lungs, liver, spleen, kidney, and lymph nodes, with acid-fast bacilli.7,10,16,19 Culture results from two cases produced “typical human tubercle bacilli”16 and M. tuberculosis.10 Of the three infected mongoose lemurs tested by intradermal tuberculin injection, one was positive, one equivocal, and one negative. Among black lemurs in North American zoos, 222 intradermal tuberculin tests in 112 individuals were reported, with no positive results. The current prosimian taxon advisory group testing recommendation is to use 0.1 ml modified old tuberculin intradermally.
Pleural effusion has been reported several times in ring-tailed lemurs. Effusions have been related to systemic fungal disease,6 but they have also apparently been spontaneous. Spontaneous cases have been managed conservatively with repeated thoracocentesis and have resolved. Cytological examination and culture of aspirates have identified the fluid as a sterile transudate.
Two significant skeletal diseases have been reported in lemurs. A familial bone disease involving periarticular new bone formation coincident with progressive renal failure has been described in black lemurs.15 This disease, described as periarticular hyperostosis (PH), is characterized by nonpainful enlargement of knee and ankle joints initially, with concomitant progressive renal disease. Proliferation of bone and degeneration of kidneys continue throughout the course of illness and, typically, progress to death due to end-stage renal disease or euthanasia in 6–12 months. The etiology of PH in lemurs is not known.
A second syndrome was described in ruffed lemurs (Varecia variegata) and is characterized by irregular periosteal bone proliferation along the diaphyses of long bones (primarily tibia, fibula, radius, and ulna). This syndrome has been theorized to be a nonspecific inflammatory response.21
Age-related degenerative arthritis is uncommon in prosimians. A variety of analgesic drugs has been used with apparent success. Traumatic skeletal injury also occurs infrequently and seems to respond well to standard techniques of fracture repair. Either external stabilization by casting or internal fixation with pins works well. Skeletal trauma to small appendages (digits, distal tail) is often managed by amputation, with few complications.
A common cause for medical intervention for the integumentary system, as well as for all systems combined, is traumatic injuries to the skin (lacerations and abrasions).5,9,13 Lacerations are usually superficial fight wounds, but may be caused by enclosure features as well, and may occasionally be deep and involve other tissues. Most heal well with little intervention; however, suturing and prophylactic antibiotics may be appropriate. Bite wounds inflicted by lemurs do not seem to be prone to producing an abscess.
Renal disease is common in aged lemurs.1,3,5,13 Glomerulonephritis, glomerulosclerosis, and chronic interstitial nephritis are diagnosed at postmortem examination of aged individuals. Urethral obstructions also have occurred but are not common. Urethral obstructions due to coagulum plugs may occur after electroejaculation. In these cases, coagulum material produced by electroejaculation became lodged in the urethra at the ischial arch and required surgical intervention for removal.13
Reproductive complications are not common. Dystocia is rare and is usually associated with multiple births (note: multiple births are normal in Varecia). A vaginal prolapse in a black lemur was associated with multiparity (11 offspring in seven pregnancies); correction was attempted unsuccessfully with several surgical interventions, and the animal was eventually euthanatized. Vaginitis and vaginal discharge have been associated with a variety of bacteria (Proteus, Staphylococcus, Streptococcus, E. coli, Citrobacter) and have responded to systemic antibiotics or antiseptic flushes.13
Seizures may occur in relation to several generalized or system illnesses. Epilepsy (recurrent seizures of unknown etiology) may occur rarely, and in cases where the incidence of seizures is high, anticonvulsant therapy may be warranted. Oral phenobarbital has been effective in a black lemur.
Both viral and bacterial encephalitis has been diagnosed. A case of nonsuppurative meningoencephalitis in a ruffed lemur was caused by a herpesvirus. The clinical signs associated with the disease included intermittent rear limb lameness, progressing to seizures, coma, and death.17 Bacterial meningitis and encephalitis caused by Klebsiella pneumoniae have been diagnosed in a ruffed lemur and a black lemur.13
Dissection and rupture of aortic aneurysms have been among the most common causes of mortality among captive lemurs in Madagascar.2,7 Aneurysms occurred as the result of migration of the parasite Spirocerca lupi. Dissecting aneurysms and cardiac tamponade have occurred in crowned and black lemurs; in the black lemur, the aneurysm was suspected to be secondary to hypertension based on signs of cardiac hypertrophy.1 Atherosclerosis, myocardial scarring, thickening of aortic valve leaves, “heart failure,” and myocardial infarction have been recorded in pathology surveys.1,5,9,12
Systemic Diseases and Miscellaneous Conditions
Lemurs are quite sensitive to fatal disease associated with Toxoplasma gondii infection. Malaria parasites have been identified in blood samples of Eulemur species in Madagascar. Several species of Plasmodium have been described; these organisms are not pathogenic in the lemur hosts and do not infect humans.18 Toxicoses are not common. Nightshade toxicosis8 and aflatoxicosis have been reported.13
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11. Griner L.A. 1983. Pathology of Zoo Animals. San Diego, Zoological Society of San Diego.
12. Hamerton, A.E. 1931. Report on the deaths occurring in the society’s gardens during the year 1930. Proc. Zool. Soc. London. Pp. 527–555.
13. Junge, R.E. Medical management of the black lemur (Eulemur macaco macaco) in captivity. In preparation.
14. Junge, R.E. and D. Garell. 1995. Veterinary evaluation of ruffed lemurs (Varecia variegata) in Madagascar. Primate Conserv. 16:44–46.
15. Junge, R.E., K.G. Mehren, T.P. Meehan, G.J. Crawshaw, M.C. Duncan, L. Gilula, F. Gannon, G. Finkel, and M.P. Whyte. 1994. Periarticular hyperostosis and renal disease in six black lemurs of two family groups. J. Am. Vet. Med. Assoc. 205:1024–1029.
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17. Kornegay, R.W., T.J. Baldwin, and G. Pirie. 1991. Herpesvirus encephalitis in a ruffed lemur (Varecia variegatus). J. Zoo Wildl. Med. 24:196–203.
18. Landau, L., J.P. Lepers, R. Rabetafika, D. Baggam, W. Peters, and P. Coulanges. 1989. Plasmodies de lemuriens malagaches. Ann. Parasitol. Hum. Comp. 64:171–184.
19. Schmidt RE. 1975. Tuberculosis in a ring-tailed lemur (Lemur catta). J. Zoo Anim. Med. 6:11–12.
20. Spelman, L.H., K.G. Osborn, and M.P. Anderson. 1989. Pathogenesis of hemosiderosis in lemurs; role of dietary iron, tannin, and ascorbic acid. Zoo Biol. 8:239–251.
21. Weber, M.A., N. Lamberski, and K. Heriot. 1995. An idiopathic proliferative disease of bone in two subspecies of ruffed lemur (Varecia variegata variegata and Varecia variegata rubra). Proc. Joint Conf. Am. Assoc. Zoo Vet. Wildl. Dis. Assoc. Am. Assoc. Wildl. Vet. Pp. 268.