Innocent B. Rwego

Forest Fragmentation as Cause of Bacterial Transmission among Nonhuman Primates, Humans, and Livestock, Uganda

Anthropogenic disturbance increases bacterial transmission.

Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda.

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.

Molecular epidemiology of cross-species Giardia duodenalis transmission in western Uganda.

Background Giardia duodenalis is prevalent in tropical settings where diverse opportunities exist for transmission between people and animals. We conducted a cross-sectional study of G. duodenalis in people, livestock, and wild primates near Kibale National Park, Uganda, where human-livestock-wildlife interaction is high due to habitat disturbance. Our goal was to infer the cross-species transmission potential of G. duodenalis using molecular methods and to investigate clinical consequences of infection. Methodology/Principal Findings Real-time PCR on DNA extracted from fecal samples revealed a combined prevalence of G. duodenalis in people from three villages of 44/108 (40.7%), with prevalence reaching 67.5% in one village. Prevalence rates in livestock and primates were 12.4% and 11.1%, respectively. Age was associated with G. duodenalis infection in people (higher prevalence in individuals ≤15 years) and livestock (higher prevalence in subadult versus adult animals), but other potential risk factors in people (gender, contact with domestic animals, working in fields, working in forests, source of drinking water, and medication use) were not. G. duodenalis infection was not associated with gastrointestinal symptoms in people, nor was clinical disease noted in livestock or primates. Sequence analysis of four G. duodenalis genes identified assemblage AII in humans, assemblage BIV in humans and endangered red colobus monkeys, and assemblage E in livestock and red colobus, representing the first documentation of assemblage E in a non-human primate. In addition, genetic relationships within the BIV assemblage revealed sub-clades of identical G. duodenalis sequences from humans and red colobus. Conclusions/Significance Our finding of G. duodenalis in people and primates (assemblage BIV) and livestock and primates (assemblage E) underscores that cross-species transmission of multiple G. duodenalis assemblages may occur in locations such as western Uganda where people, livestock, and primates overlap in their use of habitat. Our data also demonstrate a high but locally variable prevalence of G. duodenalis in people from western Uganda, but little evidence of associated clinical disease. Reverse zoonotic G. duodenalis transmission may be particularly frequent in tropical settings where anthropogenic habitat disturbance forces people and livestock to interact at high rates with wildlife, and this could have negative consequences for wildlife conservation.

Giardia sp. and Cryptosporidium sp. infections in primates in fragmented and undisturbed forest in western Uganda.

In June 2005, we collected 115 fecal samples from wild primates in western Uganda and examined them for Cryptosporidium sp. and Giardia sp. with the use of immunofluorescent antibody (IFA) detection. We sampled primates from an undisturbed forest in Kibale National Park and from 3 highly disturbed forest fragments outside the park. Of disturbed forest samples, red colobus (Pilocolobus tephrosceles) and red-tailed guenons (Cercopithecus ascanius) harbored species of Cryptosporidium or Giardia, but black-and-white colobus (Colobus guereza) did not. All primate samples from undisturbed forest were negative for both parasites. Seven of 35 (20%) red colobus and 1 of 20 red-tailed guenons (5%) from forest fragments were infected with either Cryptosporidium sp. or Giardia sp. The presence of Cryptosporidium and Giardia species in primates living in forest fragments, but not in primates in undisturbed forest, suggests that habitat disturbance may play a role in transmission or persistence of these pathogens.

Coinfection of Ugandan Red Colobus (Procolobus [Piliocolobus] rufomitratus tephrosceles) with Novel, Divergent Delta-, Lenti-, and Spumaretroviruses

ABSTRACT Nonhuman primates host a plethora of potentially zoonotic microbes, with simian retroviruses receiving heightened attention due to their roles in the origins of human immunodeficiency viruses type 1 (HIV-1) and HIV-2. However, incomplete taxonomic and geographic sampling of potential hosts, especially the African colobines, has left the full range of primate retrovirus diversity unexplored. Blood samples collected from 31 wild-living red colobus monkeys (Procolobus [Piliocolobus] rufomitratus tephrosceles) from Kibale National Park, Uganda, were tested for antibodies to simian immunodeficiency virus (SIV), simian T-cell lymphotrophic virus (STLV), and simian foamy virus (SFV) and for nucleic acids of these same viruses using genus-specific PCRs. Of 31 red colobus tested, 22.6% were seroreactive to SIV, 6.4% were seroreactive to STLV, and 97% were seroreactive to SFV. Phylogenetic analyses of SIV polymerase (pol), STLV tax and long terminal repeat (LTR), and SFV pol and LTR sequences revealed unique SIV and SFV strains and a novel STLV lineage, each divergent from corresponding retroviral lineages previously described in Western red colobus (Procolobus badius badius) or black-and-white colobus (Colobus guereza). Phylogenetic analyses of host mitochondrial DNA sequences revealed that red colobus populations in East and West Africa diverged from one another approximately 4.25 million years ago. These results indicate that geographic subdivisions within the red colobus taxonomic complex exert a strong influence on retroviral phylogeny and that studying retroviral diversity in closely related primate taxa should be particularly informative for understanding host-virus coevolution.

Epidemiology and Molecular Relationships of Cryptosporidium spp. in People, Primates, and Livestock from Western Uganda

Background Cryptosporidium is one of the most common parasitic diarrheal agents in the world and is a known zoonosis. We studied Cryptosporidium in people, livestock, and non-human primates in the region of Kibale National Park, Uganda. Land use change near the park has resulted in fragmented forest patches containing small, remnant populations of wild primates that interact intensively with local people and livestock. Our goal was to investigate risk factors for Cryptosporidium infection and to assess cross-species transmission using molecular methods. Methodology/Principal Findings Diagnostic PCR revealed a prevalence of Cryptosporidium of 32.4% in humans, 11.1% in non-human primates, and 2.2% in livestock. In the case of humans, residence in one particular community was associated with increased risk of infection, as was fetching water from an open water source. Although 48.5% of infected people reported gastrointestinal symptoms, this frequency was not significantly different in people who tested negative (44.7%) for Cryptosporidium, nor was co-infection with Giardia duodenalis associated with increased reporting of gastrointestinal symptoms. Fecal consistency was no different in infected versus uninfected people or animals. DNA sequences of the Cryptosporidium oocyst wall protein gene placed all infections within a well-supported C. parvum/C. hominis clade. However, the only two sequences recovered from primates in the core of the parks protected area fell into a divergent sub-clade and were identical to published sequences from C. parvum, C. hominis, and C. cuniculus, suggesting the possibility of a separate sylvatic transmission cycle. Conclusions/Significance Cryptosporidium may be transmitted frequently among species in western Uganda where people, livestock, and wildlife interact intensively as a result of anthropogenic changes to forests, but the parasite may undergo more host-specific transmission where such interactions do not occur. The parasite does not appear to have strong effects on human or animal health, perhaps because of persistent low-level shedding and immunity.

High Rates of Escherichia coli Transmission between Livestock and Humans in Rural Uganda

ABSTRACT Escherichia coli is a zoonotic bacterium that is important to both public health and livestock economics. To date, most studies of zoonotic E. coli transmission have been conducted in developed nations with industrialized agricultural economies. In this study, E. coli bacteria were collected from people and livestock in two communities in rural western Uganda in order to investigate patterns of interspecific bacterial transmission in a developing rural economy characterized by very close human-livestock associations. Six hundred seventy-two E. coli isolates were genotyped using repetitive element-PCR (Rep-PCR) fingerprinting, and genetic distances between populations of bacteria from different hosts and locations were calculated. Genetic distances between human and livestock bacteria were generally very low, indicating high rates of bacterial gene flow among host species. Bacteria from humans and livestock in the same communities were virtually indistinguishable genetically. Data from surveys administered at the time of sample collection showed that people who did not regularly wash their hands before eating harbored bacteria approximately twice as similar genetically to bacteria of their livestock as did people who regularly washed their hands before eating. These results suggest that both rates of human-livestock interactions and patterns of human hygiene affect human-livestock bacterial transmission in this setting. This conclusion has implications not only for human and livestock health in subsistence-based agricultural economies but also for the emergence of zoonotic diseases out of such areas as a result of increasing globalization.

Knowledge and perceptions of brucellosis in the pastoral communities adjacent to Lake Mburo National Park, Uganda

BackgroundBrucellosis is one of the most common zoonotic infections globally. Lack of knowledge about brucellosis may affect the health-seeking behavior of patients, thus leading to sustained transmission in these communities. Our study assessed knowledge and perceptions of brucellosis among pastoral communities adjacent to Lake Mburo National Park (LMNP), Kiruhura District, Uganda.MethodsA community cross-sectional questionnaire survey involving 371 randomly selected household heads from three sub-counties neighboring LMNP were interviewed between June and August 2012. Data collected included communities’ knowledge on causes, symptoms, transmission, treatment, prevention and risk factors of brucellosis. Multivariable logistic regression analysis was performed to explore strength of association between overall knowledge of brucellosis and various individual factors using odds ratios and 95% confidence intervals.ResultsOnly 70 (19%) knew the symptoms of brucellosis in animals, and three quarters (279, 75.5%) mentioned joint and muscle pain as a common symptom in humans. Almost all participants (370, 99.3%) had ever heard about brucellosis, majority (311, 84.7%) believed it affects all sexes and two thirds (67.7%) of the respondents believed close proximity to wildlife contributes to the presence of the disease. Almost all (352, 95.4%) knew that brucellosis in humans could be treatable using modern drugs. The main routes of infection in humans such as consumption of unpasteurized dairy products were known by 97% (360/371); eating of half-cooked meat by 91.4% and eating contaminated pasture in animals by 97.4%. There was moderate overall knowledge of brucellosis 197 (53.1%). Factors associated with higher overall knowledge were being agro-pastoralists (aOR: 2.08, CI: 1.17-3.71) compared to pure pastoralists while those who reported that the disease was a health problem (aOR: 0.18, CI: 0.06-0.56) compared to those who said it was not were less likely to be knowledgeable.ConclusionsThere was moderate overall knowledge of human and animal brucellosis among the participants. Majority of the participants believed that close proximity to wildlife contributes to the presence of the disease in the area. There is a need for collaboration between the public health, veterinary and wildlife sectors to provide health education on brucellosis for better management of the disease in the communities.

Health and disease in the people, primates, and domestic animals of Kibale National Park: Implications for conservation

Preface Richard Leakey Foreword Ian Redmond and Melanie Virtue 1. Why the link between long-term research and conservation is a case worth making Richard Wrangham 2. Links between research and protected area management in Uganda Moses Mapesa 3. The use of research: how science in Ugandas national parks has been applied William Olupot and Andrew J. Plumptre 4. Long-term research and conservation in Kibale National Park Thomas Struhsaker 5. Monitoring forest-savannah dynamics in Kibale National Park with satellite imagery (1989-2003): implications for the management of wildlife habitat Nadine Laporte, Wayne Walker, Jared Stabach, and Florence Landsberg 6. Long-term studies reveal the conservation potential for integrating habit restoration and animal nutrition Colin A. Chapman, Lauren J. Chapman, Patrick A. Omeja and Dennis Twinomugisha 7. Long-term perspectives on forest conservation: lessons from research in Kibale National Park Jeremiah S. Lwanga and G. Isabirye-Basuta 8. Health and disease in the people, primates, and domestic animals of Kibale National Park: implications for conservation Tony L. Goldberg, Thomas R. Gillespie and Innocent B. Rwego 9. The importance of training national and international scientists for conservation research Rosie Trevelyan and Clive Nuttman 10. Community benefits from long-term research programs: a case study from Kibale National Park, Uganda John M. Kasenene and Elizabeth A. Ross 11. Potential interactions of research with the development and management of eco-tourism Arthur Mugisha 12. The human landscape around the island park: impacts and responses to Kibale National Park Abe Goldman, Joel Hartter, Jane Southworth and Michael Binford 13. Conservation and research in the Budongo Forest Reserve, Masindi District, Western Uganda Fred Babweteera, Vernon Reynolds and Klaus Zuberbuhler 14. Long-term research and conservation in Gombe National Park, Tanzania Anthony Collins and Jane Goodall 15. Long-term research and conservation in the Mahale Mountains, Tanzania Toshisada Nishida and Michio Nakamura 16. The contribution of long-term research by the Tai Chimpanzee Project to conservation Christophe Boesch, Hedwige Boesch, Zoro Bertin Gone Bi, Emmanuelle Normand and Ilka Herbinger 17. The Green Corridor Project: long-term research and conservation in Bossou, Guinea Tetsuro Matsuzawa and Makan Kourouma 18. Long-term research and conservation of the Virunga mountain gorillas Elizabeth A. Williamson and Katie A. Fawcett 19. Long-term research and conservation of great apes: a global future Natarajan Ishwaran 20. Long-term research and conservation: the way forward Richard Wrangham and Elizabeth Ross.

Health and disease in the people, primates, and domestic animals of Kibale National Park

In the not-too-distant past, infectious disease was viewed as akin to fire, earthquake, and tornado in its propensity to impact wild primates. Outbreaks were considered inherently unpredictable, “sweeping through” primate populations, wreaking havoc, and then subsiding. Primates were generally thought to rebound, such that the overall effect was a “blip on the radar,” a transient reduction in population numbers. The last approximately 10 years have demonstrated the “disease as natural disaster” paradigm to be woefully inaccurate. Infectious disease has emerged as a major threat to primate conservation. The case of Ebola virus and its devastating effects on chimpanzees ( Pan troglodytes ) and gorillas ( Gorilla gorilla ) in Gabon and Congo is perhaps the most dramatic example, with some estimates of local population declines above 80% (Leroy et al ., 2004; Bermejo et al ., 2006). Other pathogens such as Bacillus anthracis (the causative agent of anthrax), polio virus, and yellow fever virus have also caused epidemic mortality in apes and monkeys, to the extent that they are now seen as important drivers of primate population declines (Chapman et al ., 2005; Leendertz et al ., 2006; Nunn and Altizer, 2006). Despite these dramatic examples, the majority of primate pathogens probably exert chronic, sublethal effects on primates in the wild (most parasitic protozoa, helminths, and arthropods probably fall into this category). Although researchers are paying increasing attention to such agents, most studies to date have been either “prevalence surveys” or comparisons of prevalence across locations or habitat types.