Amoebic meningoencephalitis and disseminated infection caused by Balamuthia mandrillaris in a Western lowland gorilla (Gorilla gorilla gorilla)

Abstract

CASE DESCRIPTION A 22-year-old male gorilla (Gorilla gorilla gorilla) housed in a zoo was evaluated for signs of lethargy, head-holding, and cervical stiffness followed by development of neurologic abnormalities including signs of depression, lip droop, and tremors. CLINICAL FINDINGS Physical examination under general anesthesia revealed a tooth root abscess and suboptimal body condition. A CBC and serum biochemical analysis revealed mild anemia, neutrophilia and eosinopenia consistent with a stress leukogram, and signs consistent with dehydration. Subsequent CSF analysis revealed lymphocytic pleocytosis and markedly increased total protein concentration. TREATMENT AND OUTCOME Despite treatment with antimicrobials, steroids, and additional supportive care measures, the gorilla's condition progressed to an obtunded mentation with grand mal seizures over the course of 10 days. Therefore, the animal was euthanized and necropsy was performed. Multifocal areas of malacia and hemorrhage were scattered throughout the brain; on histologic examination, these areas consisted of necrosis and hemorrhage associated with mixed inflammation, vascular necrosis, and intralesional amoebic trophozoites. Tan foci were also present in the kidneys and pancreas. Immunohistochemical testing positively labeled free-living amoebae within the brain, kidneys, eyes, pancreas, heart, and pulmonary capillaries. Subsequent PCR assay of CSF and frozen kidney samples identified the organism as Balamuthia mandrillaris, confirming a diagnosis of amoebic meningoencephalitis. CLINICAL RELEVANCE Infection with B mandrillaris has been reported to account for 2.8% of captive gorilla deaths in North America over the past 19 years. Clinicians working with gorillas should have a high index of suspicion for this diagnosis when evaluating and treating animals with signs of centrally localized neurologic disease.

Fatal balamuthosis in a Siberian tiger and a literature review of detection options for free-living amoebic infections in animals

“…Direct examination of CSF was not reported to be useful in any case of B. mandrillaris infection in animals; the inflammatory response detected in CSF is considered to be nonspecific for amoebic infections. 8,9 Diagnosis of encephalitis from B. mandrillaris has not been made in biopsy samples from animals, to our knowledge, likely as a result of the clinical risk of obtaining samples in cases of encephalitis of presumed infectious origin.…”

“…One report used IHC to highlight amoebic organisms but used antibodies that were not specific for a particular amoeba group. 8 Histochemical staining was not used routinely to detect amoebic infections in animals; a few reports used Giemsa and/or periodic acid-Schiff to highlight the organisms in areas of severe inflammation, 8 whereas others suggested that these stains did not adequately highlight the pathogens. 11 Indirect immunofluorescence from tissue has been used to discriminate among B. mandrillaris, N. fowleri, and Acanthamoeba spp.…”

“…4 A variety of molecular methods have been used to identify the causative agent in animals and most frequently targeted the 16S and 18S ribosomal RNA genes as well as the 40S ribosomal protein S11 and RNase P genes. 3,6,8,12,14 To date, B. mandrillaris is the only known pathogenic species in the genus Balamuthia and, regardless of gene target used, B. mandrillaris can be distinguished from related amoebae. In animals, suspicion of amoebiasis may not occur until histology is performed.…”

“…Although a wide variety of animals have been reported to develop severe disease associated with B. mandrillaris infection, 16 we did not find another reported case in a felid after searching “balamuthia” and “tiger” in Google and PubMed. Fatal balamuthosis has been reported in humans worldwide 16 and in at least 5 species of non-human primates in the United States, 8 , 9 , 15 Germany, 14 and Australia, 1 in dogs in the United States 2 , 6 and Australia, 5 , 10 and in sheep, 7 horses, 12 and a flying fox in the United States. 3 Most reports of balamuthosis are individual case reports, and the infections are associated with rare, sporadic mortality, particularly in immunosuppressed hosts.…”

“…The exception is non-human primates, in which infection by B. mandrillaris is commonly implicated in mortality, particularly in gorillas. 8 The reason for this is unclear. We did not find infection by B. mandrillaris in reptiles, amphibians, fish, or birds in searches of Google and PubMed.…”