Gastrointestinal Bacterial Transmission among Humans, Mountain Gorillas, and Livestock in Bwindi Impenetrable National Park, Uganda

Abstract

Habitat overlap can increase the risks of anthroponotic and zoonotic pathogen transmission between humans, livestock, and wild apes. We collected Escherichia coli bacteria from humans, livestock, and mountain gorillas (Gorilla gorilla beringei) in Bwindi Impenetrable National Park, Uganda, from May to August 2005 to examine whether habitat overlap influences rates and patterns of pathogen transmission between humans and apes and whether livestock might facilitate transmission. We genotyped 496 E. coli isolates with repetitive extragenic palindromic polymerase chain reaction fingerprinting and measured susceptibility to 11 antibiotics with the disc-diffusion method. We conducted population genetic analyses to examine genetic differences among populations of bacteria from different hosts and locations. Gorilla populations that overlapped in their use of habitat at high rates with people and livestock harbored E. coli that were genetically similar to E. coli from those people and livestock, whereas E. coli from gorillas that did not overlap in their use of habitats with people and livestock were more distantly related to human or livestock bacteria. Thirty-five percent of isolates from humans, 27% of isolates from livestock, and 17% of isolates from gorillas were clinically resistant to at least one antibiotic used by local people, and the proportion of individual gorillas harboring resistant isolates declined across populations in proportion to decreasing degrees of habitat overlap with humans. These patterns of genetic similarity and antibiotic resistance among E. coli from populations of apes, humans, and livestock indicate that habitat overlap between species affects the dynamics of gastrointestinal bacterial transmission, perhaps through domestic animal intermediates and the physical environment. Limiting such transmission would benefit human and domestic animal health and ape conservation.

‘Disperse abroad in the land’: the role of wildlife in the dissemination of antimicrobial resistance

“…However, the few studies that identify potential sources of AMR and can make comparisons across sites differing in contamination provide insights into the potential for wildlife to disseminate clinically relevant AMR. Studies in South America and Africa found AMR to be more common in gut bacteria from non-human primates living close to humans than in those from more isolated populations [28,29]. Ugandan gorilla populations, for example, with home ranges that overlapped human settlements harboured resistant bacteria that were genetically similar to E. coli from those people and livestock, compared with apes more remotely located [28].…”

“…Studies in South America and Africa found AMR to be more common in gut bacteria from non-human primates living close to humans than in those from more isolated populations [28,29]. Ugandan gorilla populations, for example, with home ranges that overlapped human settlements harboured resistant bacteria that were genetically similar to E. coli from those people and livestock, compared with apes more remotely located [28]. In northern elephant seals, Mirounga angustirostris, the probability of shedding antimicrobial-resistant E. coli was found to be directly correlated with the size of local human populations [30].…”

“…in soil and water) with horizontal transmission of AMR possible in both. Such models could be based on spatial movements in relation to a common environmental source of AMR contamination such as a refuse dump [28]. Sewage treatment plants, for example, are hotspots of AMR, which can provide valuable pockets of semi-natural habitat for birds and bats, attracted by the invertebrates that themselves feed in the sewage [38].…”

Lignes directrices pour de meilleures pratiques en matière de suivi de la santé et de contrôle des maladies des populations de grands singes

“…La proximité immédiate entre grands singes et humains est connue pour entrainer la transmission de bactéries comme Escherichia coli, Salmonella et Shigella ; les gorilles et chimpanzés qui vivent près des humains sont connus pour être porteurs dans leur tractus gastro-intestinal d'E. coli multi-résistantes à des antibiotiques utilisés par l'homme (Goldberg et al 2007 ;Rwego et al 2008 ;Janatova et al 2014 Compte tenu du statut inquiétant de conservation des grands singes dans le monde entier et du fait que les épidémies au sein de petites populations peuvent être catastrophiques, l'application du principe de précaution en matière de santé des grands singes est justifiée. En l'absence de preuve scientifique qu'un agent pathogène ou qu'une action ou politique humaine représente ou non un risque ou un danger pour les grands singes, il est plus sûr de supposer que cet agent ou cette action pose un risque pour la santé des grands singes jusqu'à preuve scientifique du contraire.…”

“…Par exemple, une nouvelle bactérie du charbon Bacillus cereus biovar anthracis est létale pour les gorilles et les chimpanzés et a été trouvée au Cameroun, en Côte d'Ivoire et en République centrafricaine (Klee et al 2010) ; Pasteurella multocida et Streptococcus pneumoniae ont joué un rôle dans le foyer de maladie respiratoire chez les chimpanzés d'Afrique occidentale (Chi et al 2007 ;Köndgen et al 2008) ; des bactéries gastro-intestinales et des bactéries multi-résistantes, potentiellement dérivées de l'homme, ont été dépistées chez des grands singes vivant dans un habitat perturbé par l'homme (Nizeyi et al 2001 ;Rwego et al 2008) ; des souches pathogènes de Staphylococcus aureus ont été isolées chez des chimpanzés sauvages (Schaumburg et al 2012) tandis que Campylobacter jejuni associée à la diarrhée a été documentée chez les gorilles de montagne (Whittier et al 2010).…”