3-year-old intact male ring-tailed lemur (Lemur catta).The lemur was part of the breeding group of the German Primate Center (GPC), kept in a partly indoor and partly outdoor facility. Until found in an ill condition, the animal was an active part of his social group. He was found in the morning, apart from his family with signs of abdominal tumefaction, pressing and passive behavior. Treatment with Butylscopolamin, Metamizole and Dexamethasone followed. The general condition declined two days later, so blood samples were taken, the medical treatment was sustained and an intravenous drip was administered for rehydration.
The next day, ultrasonic examination of the abdomen was made without proper results, so a laparotomy was performed. Within the abdomen there was ascites and severe multifocal necrotizing hepatitis, so a biopsy of the liver was taken. One day after the surgery the ring-tailed lemur was found dead in his cage.
At necropsy, the lemur was in good nutritional condition.Â The main pathologic finding was severe hepatomegaly.Â The liver parenchyma was diffusely interspersed with small partly confluent whitish lesions.Â The spleen was enlarged and a serofibrinous peritonitis was manifest, accompanied by ascites.Â Parts of the small intestine, mesentery and pancreas were clotted together.Â In addition the mesenteric lymph nodes were hyperplastic.Â Focal petechial hemorrhage was found in parts of the duodenum and ileum.Â There was also severe, diffuse edema in the lung.
Liver: Within the parenchyma there are numerous multifocal to coalescing areas of necrosis and inflammation, characterized by karyorrhectic debris, degradation of cells and a mild infiltration of leukocytes.Â The foci are sharply bounded from healthy liver tissue and randomly scattered throughout the liver.
Liver: Necrotizing hepatitis, acute, multifocal to coalescing, with necrotizing serositis, ring-tailed lemur (Lemur catta), nonhuman primate.
AST (392 U/L) and LDI (2079 U/L) were markedly increased.Â BUN (72 mg/dl) and creatinine (1.66 mg/dl) were moderately increased.Â
Listeria monocytogenes was isolated from heart, lung, liver, spleen, kidney and central nervous system by bacteriological culture and confirmed by PCR.
Immunohistochemistry using a polyclonal anti-Listeria monocytogenes-antibody revealed a positive reaction in liver, gallbladder, spleen, kidney, urinary bladder, large and small intestine, mesentery, pancreas, palatine tonsil, mesenteric lymph nodes and periorchium.
Listeriosis is an important foodborne disease, found in a large range of species.Â It is most frequently apparent in ruminants, but it is also an important issue in human medicine, especially in geriatrics, neonatology and diseases of immunocompromised patients.
The disease is caused by Listeria monocytogenes, a facultative anaerobic, gram-positive, rod-shaped bacterium which has the ability to invade cells and duplicate in the cytoplasm.Â Listeria monocytogenes is a ubiquitous pathogen; it is found in the natural microbial flora in ruminants, in the feces of birds and wild animals and it persists in the environment as a saprophyte, especially on decaying vegetation, such as inadequately soured silage.Â Listeria monocytogenes is known to cause three different clinical presentations.Â The cerebral form, with meningitis and encephalitis, is the most common in sheep.Â The pregnancy-associated form leads to stillbirths, abortion and premature birth.Â The third form is the septicemic form.Â Most cases of listeriosis remain clinically silent in healthy individuals.
Relatively few cases of listeriosis are reported in nonhuman primates (NHP) and there are no case reports in ring-tailed lemurs.Â Most of the reported incidences in NHP are accompanied by reproductive failure with abortion, stillbirth or neonatal death due to septicemia or cerebral complications.(1,6,11) There is one report of a free-living guereza in Kenya with similar pathologic findings to this case.(8)
The severe nature and rapid progression of the disease in the present case could be secondary to immune suppression, as lymphoid depletion is noted in multiple lymph nodes throughout the body.Â
Liver: Hepatitis, necrotizing, acute, multifocal to coalescing, moderate, with hepatocellular dissociation and individual hepatocyte necrosis
Listeria monocytogenes is most notorious in veterinary medicine for its effects in the CNS and reproductive system, although a septicemic form appears to be the culprit in this case.Â In ruminants and horses, unilateral or bilateral rhombencephalitis (and occasional meningitis/meningoencephalitis), with microabscessation, is the typical clinical manifestation of listeriosis, however this bacterium can also localize to the pregnant uterus, causing sporadic abortion and stillbirth.(10) Abortion due to Listeria has also been reported in rabbits,(7) and listeriosis has become an increasingly significant cause of reproductive failure and fetal septicemia in non-human primates.(2) Additionally, there is at least one report of spontaneous meningoencephalitis in an immunocompetent rhesus macaque,(7) and enteric listeriosis, though infrequent, has been reported in New Zealand sheep.(4)
There is evidence that Listeria localizes to the ruminant brainstem via retrograde axonal migration along cranial nerve branches after crossing the oral epithelium, with potential spread into more rostral brain regions by intracerebral axonal migration.Â This is in contrast to human CNS infections where a hematogenous route is hypothesized.(3) It has also been suggested that E-cadherin (expressed by oral epithelium and Schwann cells) could bind internalin on the surface of Listeria to facilitate entry into the brainstem, however this has not yet been demonstrated.(3,4) Listerial abortions in ruminants occur during the last trimester of pregnancy with fetal infection or septicemia caused by hematogenous spread from the placenta.Â If the dam is infected at the beginning of the last trimester, there is rapid fetal infection and abortion with only mild maternal disease.Â If the infection occurs closer to parturition, dystocia with severe metritis, placentitis and septicemia are more likely.(10)
Histologic lesions of listeriosis are typically characterized by necrosis with a mild neutrophilic infiltrate.(8) Conference participants explored several potential differential diagnoses for necrotizing hepatitis in a NHP, briefly discussing Francisella tularensis, Clostridium piliforme and alphaherpesviruses.Â Hepatic conditions specifically reported in lemurs include cirrhosis, hemochromatosis and hepatocellular carcinoma.(5,8)
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6.Â Glenn KM, Campbell JL, Rotstein D, Williams CV.Â Retrospective evaluation of the incidence and severity of hemosiderosis in a large captive lemur population.Â Am J Primatol.Â 2006;68(4):369-81.Â
7.Â Heldstab A, R+ï¿½-+edi D.Â Listeriosis in an adult female chimpanzee (Pan troglodytes).Â J Comp Pathol.Â 1982;92(4):609-612.Â
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9.Â Kock ND, Kock RA, Wambua E, et al.Â Listeriosis in a free-ranging colobus monkey (Colobus guerezacaudatus) in Kenya.Â Vet Rec.Â 2003;152(5):141-142.
10.Â Nemeth NM, Blas-Machado U, Cazzini P, et al.Â Well-differentiated hepatocellular carcinoma in a ring-tailed lemur (Lemur catta).Â J Comp Pathol.Â 2013;148(2-3):283-287.
11.Â Schlafer DH, Miller RB.Â Female genital system.Â In: Maxie MG, ed.Â Jubb, Kennedy and Palmers Pathology of Domestic Animals.Â 5th ed.Â Vol.Â 3.Â Philadelphia, PA: Elsevier Saunders; 2007:492-493.
12.Â Simmons J, Gibson S.Â Bacterial and mycotic diseases of nonhuman primates.Â In: Abee CR, Mansfield K, Tardif S, Morris T, eds.Â 2nd ed.Â Nonhuman Primates in Biomedical Research: Diseases.Â San Diego, CA: Academic Press; 2012:105-172.Â