Mountain gorilla lymphocryptovirus has Epstein-Barr virus-like epidemiology and pathology in infants

Tierra Smiley Evans,Jonna A K Mazet,Jean Felix Kinani,Tracey Goldstein,Kirsten V Gilardi,Peter A Barry,Linda J Lowenstine,Jean Bosco Noheri,Christine Kreuder Johnson,Fred Nizeyimana,Michael R Cranfield,Benard J Ssebide,Antoine Mudakikwa

doi:10.1038/s41598-017-04877-1

Abstract

Epstein-Barr virus (EBV) infects greater than 90% of humans, is recognized as a significant comorbidity with HIV/AIDS, and is an etiologic agent for some human cancers. The critically endangered mountain gorilla population was suspected of infection with an EBV-like virus based on serology and infant histopathology similar to pulmonary reactive lymphoid hyperplasia (PRLH), a condition associated with EBV in HIV-infected children. To further examine the presence of EBV or an EBV-like virus in mountain gorillas, we conducted the first population-wide survey of oral samples for an EBV-like virus in a nonhuman great ape. We discovered that mountain gorillas are widely infected (n = 143/332) with a specific strain of lymphocryptovirus 1 (GbbLCV-1). Fifty-two percent of infant mountain gorillas were orally shedding GbbLCV-1, suggesting primary infection during this stage of life, similar to what is seen in humans in less developed countries. We then identified GbbLCV-1 in post-mortem infant lung tissues demonstrating histopathological lesions consistent with PRLH, suggesting primary infection with GbbLCV-1 is associated with PRLH in infants. Together, our findings demonstrate that mountain gorilla’s infection with GbbLCV-1 could provide valuable information for human disease in a natural great ape setting and have potential conservation implications in this critically endangered species.

Highlights

We identified the first evidence of an Epstein-Barr virus (EBV)-like virus, a mountain gorilla-specific strain of lymphocryptovirus 1 (GbbLCV-1), in wild mountain gorillas as well as herpesviruses in the cytomegalovirus and rhadinovirus subfamilies
Contrary to previous serologic evidence for ubiquitous EBV exposure in mountain gorillas[35], our population-wide survey did not detect shedding of EBV in the wild or captivity during our study period and alternatively demonstrated that the lymphocryptovirus circulating in mountain gorillas is a mountain gorilla-specific strain of lymphocryptovirus 1, GbbLCV-1
Epstein-Barr virus serologic assays used previously were likely cross-reactive with GbbLCV-1

Summary

Introduction

Epstein-Barr virus (EBV) infects greater than 90% of humans, is recognized as a significant comorbidity with HIV/AIDS, and is an etiologic agent for some human cancers. The critically endangered mountain gorilla population was suspected of infection with an EBV-like virus based on serology and infant histopathology similar to pulmonary reactive lymphoid hyperplasia (PRLH), a condition associated with EBV in HIV-infected children. To further examine the presence of EBV or an EBV-like virus in mountain gorillas, we conducted the first population-wide survey of oral samples for an EBV-like virus in a nonhuman great ape. Fifty-two percent of infant mountain gorillas were orally shedding GbbLCV-1, suggesting primary infection during this stage of life, similar to what is seen in humans in less developed countries. Our findings demonstrate that mountain gorilla’s infection with GbbLCV-1 could provide valuable information for human disease in a natural great ape setting and have potential conservation implications in this critically endangered species. A recent analysis of gammaherpesviral sequences from a wide range of mammals indicated that cross-species transmissions have historically occurred more frequently than previously estimated, with most attributable to bats and primates[34]

Methods

Results

Conclusion