Diagnostic evaluation of fatal Balamuthia mandrillaris meningoencephalitis in a captive Bornean orangutan ( Pongo pygmae

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ORIGINAL ARTICLE

Diagnostic evaluation of fatal Balamuthia mandrillaris meningoencephalitis in a captive Bornean orangutan (Pongo pygmaeus) with identification of potential environmental source and evidence of chronic exposure Shawna J. Hawkins1,5   · Jason D. Struthers2 · Kristen Phair1 · Ibne Karim M. Ali3 · Shantanu Roy3 · Bonnie Mull4 · Gary West1 Received: 22 February 2020 / Accepted: 21 August 2020 © Japan Monkey Centre and Springer Japan KK, part of Springer Nature 2020

Abstract A female Bornean orangutan (Pongo pygmaeus) aged 11 years and 6 months was examined by veterinarians after caretakers observed lethargy and facial grimacing. Within 72 h the primate had left-sided hemiparesis that worsened over the next week. An MRI revealed a focal right-sided cerebral mass suspected to be a neoplasm. Ten days after onset of clinical signs, the orangutan died. On postmortem exam, the medial right parietal lobe was replaced by a 7 × 4 × 3.5 cm focus of neuromalacia and hemorrhage that displaced the lateral ventricle and abutted the corpus callosum. Histopathology of the cerebral lesion revealed pyogranulomatous meningoencephalitis with intralesional amoeba trophozoites and rare cysts. Fresh parietal lobe was submitted to the Centers for Disease Control and Prevention lab for multiplex free-living amoebae real-time PCR and detected Balamuthia mandrillaris DNA at a high burden. Mitochondrial DNA was sequenced, and a 760-bp locus 19443F/20251R was compared to several human infections of B. mandrillaris and shown to be identical to the isolates from four human cases of encephalitis: 1998 in Australia, 1999 in California, 2000 in New York, and 2010 in Arizona. Indirect immunofluorescent antibody testing of stored serum samples indicated exposure to B. mandrillaris for at least 2 years prior to death. Within 1 week of the orangutan’s death, water from the exhibit was analyzed and identified the presence of B. mandrillaris DNA, elucidating a possible source of exposure. B. mandrillaris, first reported in a mandrill in 1986, has since occurred in humans and animals and is now considered an important emerging pathogen. Keywords  Balamuthia mandrillaris · Bornean orangutan · Indirect immunofluorescence antibody (IFA) assay · Magnetic resonance imaging · Pongo pygmaeus

Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s1032​9-020-00860​-z) contains supplementary material, which is available to authorized users. * Shawna J. Hawkins [email protected] 1



Phoenix Zoo Arizona Center for Nature Conservation, Phoenix, AZ, USA

2



Midwestern University College of Veterinary Medicine, Glendale, AZ, USA

3

Centers for Disease Control and Prevention (CDC), Atlanta, GA, USA

4

Biological Consulting Services of North Florida, Inc, Gainesville, FL, USA

5

UW Veterinary Care, 2015 Linden Drive, Madison, WI 53706, USA



Introduction Pathogenic free-living amoebae are a global health risk to humans and animals (Perez and Bush 2007). These opportunistic protozoa are ubiquitous, amp