Pathologic Findings in New World Camelids in Switzerland, with Emphasis on Dicrocoeliosis and Mycobacteriosis
American Association of Zoo Veterinarians Conference 2006
Nadia Robert, DVM, DACVP
Centre for Fish and Wildlife Health, Institute of Animal Pathology, Vetsuisse Faculty, University of Berne, Bern, Switzerland


There is a long tradition of keeping New World camelids in zoological gardens. Llamas and alpacas have gained much popularity among private holders during the last 10 yr, mostly as companion animals or as trekking or breeding animals. Accordingly, knowledge concerning diseases in these species has increased and revealed that the spectrum of diseases differs significantly from those in domestic animals. Direct access and close contact to the animals often occur in zoos and under private ownership, especially with children. Therefore, the recognition of diseases, particularly potential zoonoses, represents a critical issue.

During the past 5 yr, about 130 llamas and alpacas have been necropsied in our institution. Among the neonatal crias (<1 mo of age), the main causes of mortality correlate with the literature1,2 and include low body weight and “poor doers,” lack of milk intake and failure of passive immunoglobulin transfer, postpartum infectious diseases (rotavirus, Streptococcus sp., Enterobacter sp.) and malformations. The exact cause of the “poor doers” is mostly not known, but prematurity and “intrauterine growth retardation” (IURG), as defined by Adams,1 have to be considered. Based on our experience, dicrocoeliosis in the cow should be considered as possible cause of abortion and IUGR secondary to suboptimal uterine environment.

In juveniles and adults, the most important problems are related to parasite infestation, including liver flukes, gastro-intestinal nematodes, and coccidia. Other significant causes of mortality are mostly comparable with the standard literature on new world camelids2,3,7,8 and include dental problems, infectious diseases (especially Listeria monocytogenes and Mycobacterium microti), tumors (lymphosarcoma, C1-squamous cell carcinoma, hemangiosarcoma), obstructive urolithiasis in males, and intoxications (moldy hay, toxic mushrooms, oak bud).

In contrast to the common liver fluke Fasciola hepatica, which is found throughout tropical and temperate regions in the world and has commonly been described in NWC, there are only very rare reports concerning infestation with the lancet fluke Dicrocoelium dendriticum.2,6,7 It is however a common problem in NWC in Central Europe.4,9 Based on our necropsy material, the lancet fluke has a prevalence of about 40%, and is diagnosed as cause of mortality in >25% of NWC older than 6 mo. The parasite is present in pastures that provide adequate conditions (calcareous or alkaline soils) for the survival and development of terrestrial snails and ants, is distributed throughout much of Europe and Asia, and is also found in parts of North America (NE regions) and Australia. This parasite lives in the bile duct and gall bladder of mammal species, mainly ruminants, and its biologic cycle requires two intermediate hosts (a terrestrial snail and an ant). In the end host, the young flukes migrate directly up the biliary duct system of the liver, without penetration of the gut wall, liver capsule, and liver parenchyma in contrast to fascioliasis. Diagnosis and treatment still remain a difficult issue. Clinical diagnosis of dicrocoeliosis is often challenging as symptoms are unspecific and usually associated with very rapid decline in general condition or sudden death. When reported, clinical signs last only hours to few days duration and include decreased appetite, recumbency, dyspnoea, cardiac arrhythmia, and/or abortion. Blood analysis may indicate increased liver values, hypoproteinemia, and/or anemia, however these changes are often not evident and therefore of little diagnostic value. Parasite eggs are passed irregularly in batches into the feces and therefore clinical diagnosis of dicrocoeliosis requires repeated coprologic examinations. Good therapeutic results have been obtained upon oral treatment with a single dose of praziquantel at 50 mg/kg BW.4,9 At necropsy the animals are usually in a good body condition. Severe pulmonary edema and sero-fibrinous exudations in the body cavities (thorax, pericardium and/or abdomen) are consistent, striking changes. The liver is severely enlarged (up to four times the normal weight), with increased consistency and a mottled appearance emphasizing the lobular pattern, and variable numbers of parasites gush out of the biliary ducts on the cut surface. Histologically, the major changes consist of portal bridging fibrosis associated with bile duct proliferation and variable inflammatory infiltrates. Occasionally focal abscesses or granulomas can form around degenerated parasites or eggs. In the lungs, beside severe congestion and alveolar and interstitial edema, a vasculopathy is commonly observed in the middle and small arteries, characterized by endothelial thickening and presence of edema and/or fibrin within or surrounding the vessel wall, accompanied by a variable number of inflammatory cells. Exudative changes are not typical findings in domestic ruminants with dicrocoeliosis, but these severe exudations in the body cavities and lungs found in NWC correlate with the acute symptoms and sudden death. It is however unclear how the permeability problems arise and how they relate to the liver problems. Although the pathogenesis of the pulmonary vascular lesions is unclear, these changes might provide a clue to the exudative mechanism.

Over the last 5 yr mycobacteriosis, caused by Mycobacterium microti, was diagnosed in our institute in five llamas and one alpaca from three different owners. Three llamas and the alpaca had been imported from South America several years previously, whereas the remaining two llamas were offspring from imported, unaffected animals. Clinical signs lasted from several weeks to several months and were non-unspecific, including appetite and weight loss, recumbency, increased respiratory and cardiac frequency, cardiac arrhythmia, and/or abortion. Concerning the clinical pathologic investigations, the only consistent clinical pathology changes were hypoproteinemia with hypoalbuminemia, increased blood urea nitrogen, and decreased hemoglobin, whereas other chemical and hematologic values showed inconsistent deviations from normal values. Antemortem intradermal tuberculin testing was performed on three llamas several months prior to death and was negative. At the time of death or euthanasia the body condition varied from good to cachectic and necropsy revealed in all cases caseous nodules (1 to 10 cm in diameter) in various organs, including lungs, liver, spleen, mediastinal and mesenterial lymph nodes, and serosal surfaces, in all cases. On the cut section, the nodules were yellowish and firm, and sometimes showed an onion skin-like structure and mineralized centre. On histology, the caseous nodules presented as granulomas composed of large numbers of closely packed, epithelioid macrophages and multinucleated giant cells, admixed with various numbers of lymphocytes, plasma cells, and neutrophils. Ziehl-Neelsen and Fite-Faraco staining revealed in three cases abundant acid-fast bacilli (AFB) within the macrophages in three cases, whereas in the other three cases AFB were extremely rarely seen. The AFB were identified by spoligotyping as Mycobacterium microti, vole type.5 M. microti belongs to the M. tuberculosis complex whose members (M. tuberculosis, M. bovis, M. bovis BCG vaccine strain, M. africanum, M. canetti and M. microti) share an identical 16S rRNA gene and show >90% relatedness (85 to 89% relatedness for M. microti) at the DNA level. The natural hosts and reservoirs of M. microti are small rodents such as field voles (Microtus agrestis), wood mice (Apodemus sylvaticus) and shrews (Sorex araneus). Sporadic cases of M. microti infections were previously reported in Europe in cats, pigs, a ferret, a cow, a badger, and a captive vicuña. M. microti has to be considered as a potential zoonotic agent, since it has been detected in pulmonary tuberculosis in humans in several European countries, affecting immunocompromised as well as immunocompetent patients. Investigations regarding clinical serologic diagnosis of mycobacteriosis using a multi-antigen print immunoassay (MAPIA) are in progress in the groups of llamas from which the affected cases originated.

Literature Cited

1.  Adams R, F Garry. 1994. Llama neonatology. In: The Veterinary Clinics of North America - Food Animal Medicine - Update on Llama Medicine. E. Hunt, L.W. Johnson, eds. W.B. Saunders Company, Philadelphia. Pp. 209–227.

2.  Fowler ME. 1998. Medicine and Surgery of South American Camelids. Iowa State University Press, Ames.

3.  Fowler ME. 2003. Camelidae. In: ME Fowler, RE Miller, eds. Zoo and Wild Animal Medicine. Saunders Elsevier Science. Pp. 612–624.

4.  Gunsser I, T Hänichen, J Maierl. 1999. Leberegelbefall bei Neuweltkameliden: Parasitologie, Pathologie, Klinik und Therapie. Tierärztl. Prax. 27(G):187–192.

5.  Oevermann A, GE Pfyffer, P Zanolari, M Meylan, N Robert. 2004. Generalized tuberculosis in llamas (Lama glama) due to Mycobacterium microti. J. Clin. Microbiol. 42(4):1819–1821.

6.  Puente GL. 1997. Acute and subacute fascioliasis of alpacas (Lama pacos) and treatment with triclabendazole. Trop. Anim. Health Prod. 29:31–32.

7.  Rickard LG. 1994. Parasites. In: The Veterinary Clinics of North America - Food Animal Medicine - Update on Llama Medicine. E Hunt, LW Johnson, eds. W.B. Saunders Company, Philadelphia. Pp. 239–247.

8.  Smith JA. 1989. Non-infectious Diseases. In: The Veterinary Clinics of North America - Food Animal Medicine. L.W. Johnson. W.B. Saunders Company, Philadelphia. Pp. 101–143.

9.  Wenker Ch, J-M Hatt, H Hertzberger, P Ossent, T Hänichen, A Brack, E Isenbügel. 1998. Dikrozöliose bei Neuweltkameliden. Tierärztl. Prax. 26(G):355–361.


Speaker Information
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Nadia Robert, DVM, DACVP
Centre for Fish and Wildlife Health
Institute of Animal Pathology
Vetsuisse Faculty
University of Berne
Bern, Switzerland

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