Cross-species transmission of human hepatitis B virus to wild Neotropical primates

Abstract

Hepatitis B virus (HBV) infects approximately one-third of the worlds human population and kills over one million people each year. HBV is also prevalent in Old World apes but not in New World primates. Human-to-primate transmission of HBV was suspected in zoo-captive monkeys and Mauritius macaques, but empirical data are scarce. Here, we collected blood and liver samples from 88 monkeys of 27 species in two areas of the Amazon, one with pristine forest and the other highly occupied and deforested by humans. A total of 17 (34.7%) out of 49 specimens from the human-occupied region tested positive for HBV. At this site, there was a positive relationship between human population density in the sampling location and the likelihood of primates being infected by HBV. Conversely, all 39 samples from the pristine forest tested negative for HBV. By sequencing a portion of the HBV S gene in five positive samples, each from a distinct primate genus, we found that four samples were closely related to the globally widespread human HBV-A strain, but not to the Americas-native HBV-F strain. The fifth sample aligned with the human HBV-D type, prevalent in the region where these samples were obtained. To our knowledge, this study represents the first reported cases of HBV in multiple wild New World primate species anywhere in the world. Our results suggest that primates were infected by strains brought into this part of Brazil by human immigrants, where HBV transmission may have been facilitated by the close contact between humans and monkeys due to high human occupation. This shows that the impact of human immigration, occupation and population growth in the Amazon extends beyond habitat loss; it also facilitates cross-species infections, potentially leading to the emergence of new, virulent viral strains that threaten both Amazonian biodiversity and human health. Author SummaryJean P. Boubli: Professor in Primate Ecology and Evolution, School of Science, Engineering and the Environment, University of Salford, Uk Hani R. El Bizri: PhD in Wildlife Conservation with a focus on Amazonian sustainable development. Analyst of Center for International Forestry Research (CIFOR), Bogor, Indonesia Luan F. Botelho-Souza: Masters and doctorate in experimental biology at the Universidade Federal de Rondonia/Brazil, Chrysoula Gubili: Researcher at the Fisheries Research Institute Nea Peramos, Kavala, Greece, specializing in population ecology and conservation genetics. Stephen J. Martin: Professor in Social Insects, School of Science, Engineering and the Environment, University of Salford, Uk Maisa da S. Araujo: Masters and doctorate in experimental biology, at the Universidade Federal de Rondonia/Brazil, Mariluce R. Messias: Professor of Zoology and curator of the Mammalogy Museum at the Universidade Federal de Rondonia/Brazil. Alcione de O. dos Santos: Masters and doctorate in experimental biology at the Universidade Federal de Rondonia/Brazil. Luiz S. Ozaki: Masters degree from Universidade de Brasilia and PhD in Physiological Sciences, Molecular Biology in Fukuoka, Kyushu, Japan. Andre V.C. Pereira: Bachelor in Biology the Universidade Federal de Rondonia/Brazil. Tony H. Katsuragawa: Masters and doctorate in experimental biology, at the Universidade Federal de Rondonia/Brazil. Ana Maisa Passos-Silva: Masters degree in experimental biology from the Federal University of Rondonia/Brazil. Luiz H. S. Gil: Masters in experimental biology, at the Universidade Federal de Rondonia/Brazil. Izeni P. Farias: Professor of Genetics, Universidade Federal do Amazonas, Brazil Juan M.V. Salcedo: Master in Tropical Medicine from the University of Brasilia/Brazil and PhD in Sciences from the University of Sao Paulo/Brazil. Tommy C. Burch: Masters in Biological Sciences and PhD candidate from the University of Salford, UK. Deusilene Vieira: Master in Tropical Medicine from the University of Brasilia/Brazil and PhD in Sciences from the University of Sao Paulo/Brazil.