Browsing by Author "Goldberg, Tony L."
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Item Antibiotic-Resistant Escherichia coli and Class 1 Integrons in Humans, Domestic Animals, and Wild Primates in Rural Uganda(Applied and environmental microbiology, 2018) Weiss, Debora; Wallace, Ryan M.; Rwego, Innocent B.; Gillespie, Thomas R.; Chapman, Colin A.; Singer, Randall S.; Goldberg, Tony L.Antibiotic resistance is a global concern, although it has been studied most extensively in developed countries. We studied Escherichia coli and class 1 integrons in western Uganda by analyzing 1,685 isolates from people, domestic animals, and wild nonhuman primates near two national parks. Overall, 499 isolates (29.6%) were resistant to at least one of 11 antibiotics tested. The frequency of resistance reached 20.3% of isolates for trimethoprim-sulfamethoxazole but was nearly zero for the less commonly available antibiotics ciprofloxacin (0.4%), gentamicin (0.2%), and ceftiofur (0.1%). The frequency of resistance was 57.4% in isolates from people, 19.5% in isolates from domestic animals, and 16.3% in isolates from wild nonhuman primates. Isolates of livestock and primate origin displayed multidrug resistance patterns identical to those of human-origin isolates. The percentage of resistant isolates in people was higher near Kibale National Park (64.3%) than near Bwindi Impenetrable National Park (34.6%), perhaps reflecting local socioeconomic or ecological conditions. Across antibiotics, resistance correlated negatively with the local price of the antibiotic, with the most expensive antibiotics (nalidixic acid and ciprofloxacin) showing near-zero resistance. Among phenotypically resistant isolates, 33.2% harbored class 1 integrons containing 11 common resistance genes arranged into nine distinct gene cassettes, five of which were present in isolates from multiple host species. Overall, these results show that phenotypic resistance and class 1 integrons are distributed broadly among E. coli isolates from different host species in this region, where local socioeconomic and ecological conditions may facilitate widespread diffusion of bacteria or resistance-conferring genetic elements.Item Coinfection of Ugandan Red Colobus (Procolobus [Piliocolobus] rufomitratus tephrosceles) with Novel, Divergent Delta-, Lenti-, and Spumaretroviruses(Journal of virology, 2009) Goldberg, Tony L.; Sintasath, David M.; Chapman, Colin A.; Cameron, Kenneth M.; Karesh, William B.; Tang, Shaohua; Wolfe, Nathan D.; Rwego, Innocent B.; Ting, Nelson; Switzer, William M.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 etroviral phylogeny and that studying retroviral diversity in closely related primate taxa should be particularly informative for understanding host-virus coevolution.Item Demography and Health of “Village Dogs” in Rural Western Uganda(Preventive veterinary medicine, 2017) Hyeroba, David; Friant, Sagan; Acon, Johnson; Acai, James Okwee; Goldberg, Tony L.“Village dogs” in developing economies are assumed to be heavily burdened by infectious disease. We followed a cohort of 61 village dogs in rural western Uganda prospectively for fifteen months to measure changes in health and demographic outcomes, and to examine risk factors for morbidity and mortality. The mean (±standard deviation) number of dogs per household was 2.4 (±2.0), of which 56.0% were male and 44.0% female. For females, average age at first estrus was 1.7 (±0.6) years with a mean litter size of 3.8 (±1.5). In the first, second and third parities, average puppy mortality per litter was 3.2 (±2.5), 2.4 (±2.1) and 3.4 (±2.9), respectively. The main causes of morbidity and mortality were infectious disease (46.1%), culling (euthanasia) by owners (30.8%), and attacks by baboons, Papio anubis (23.1%). Cox proportional hazard regression showed that a clinical diagnosis of anemia significantly predicted morbidity (HR = 4.3 (95% CI: 1.1–17.8); p < 0.05), and younger age significantly predicted mortality (HR = 3.6 (95% CI: 1.2–10.6); p < 0.05). Our results indicate that infectious disease is indeed important to the health and survival in village dogs in this setting, but that cultural practices related to ownership and interactions with wildlife also contribute substantially to morbidity and mortality.Item Forest Fragmentation as Cause of Bacterial Transmission among Nonhuman Primates, Humans, and Livestock, Uganda(Emerging infectious diseases, 2008) Goldberg, Tony L.; Gillespie, Thomas R.; Rwego, Innocent B.; Estoff, Elizabeth L.; Chapman, Colin A.We conducted a prospective study of bacterial transmission among humans, nonhuman primates (primates hereafter), and livestock in western Uganda. Humans living near forest fragments harbored Escherichia coli bacteria that were ≈75% more similar to bacteria from primates in those fragments than to bacteria from primates in nearby undisturbed forests. Genetic similarity between human/livestock and primate bacteria increased ≈3-fold as anthropogenic disturbance within forest fragments increased from moderate to high. Bacteria harbored by humans and livestock were approximately twice as similar to those of red-tailed guenons, which habitually enter human settlements to raid crops, than to bacteria of other primate species. Tending livestock, experiencing gastrointestinal symptoms, and residing near a disturbed forest fragment increased genetic similarity between a participant’s bacteria and those of nearby primates. Forest fragmentation, anthropogenic disturbance within fragments, primate ecology, and human behavior all influence bidirectional, interspecific bacterial transmission. Targeted interventions on any of these levels should reduce disease transmission and emergence.Item Giardia sp. and Cryptosporidium sp. Infections in Primates in Fragmented and Undisturbed Forest in Western Uganda(Journal of Parasitology, 2007) Salzer, Johanna S.; Rwego, Innocent B.; Goldberg, Tony L.; Kuhlenschmidt, Mark S.; Gillespie, Thomas R.The molecular identification of species and genotypes of Giardia spp. infecting wild mammals represents the most reliable tool to understand the role played by these animals as reservoirs of cysts infectious for human and other animals. Of 139 fecal samples collected from fallow deer (Dama dama L.) hunted in a Natural Reserve of northern Italy, the prevalence of Giardia sp. was 11.5% (16 of 139 animals), and it was higher in fawns than in older animals. Fragments of the beta-giardin and triose phosphate isomerase (tpi) genes were successfully polymerase chain reaction amplified and sequenced from 8 isolates. No sequence variation was observed between isolates at the 2 genetic loci. Sequence and phylogenetic analyses identified a Giardia duodenalis subtype that clusters with assemblage A isolates and that shows homologies of 98 and 97% at the beta-giardin and tpi loci, respectively, compared with the A1 subtype. Because the G. duodenalis subtype found in fecal samples of fallow deer has never been detected previously, its role as a pathogen for humans and domestic animals is unknown, but, considering its genetic distinctiveness, it is likely to be low.Item High Rates of Escherichia coli Transmission between Livestock and Humans in Rural Uganda(Journal of Clinical Microbiology, 2008) Rwego, Innocent B.; Gillespie, Thomas R.; Basuta, Gilbert Isabirye; Goldberg, Tony L.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.Item Kanyawara Virus: A Novel Rhabdovirus Infecting Newly Discovered Nycteribiid Bat Flies Infesting Previously Unknown Pteropodid Bats in Uganda(Scientific Reports, 2017) Goldberg, Tony L.; Bennett, Andrew J.; Kityo, Robert; Kuhn, Jens H.; Chapman, Colin A.Bats are natural reservoir hosts of highly virulent pathogens such as Marburg virus, Nipah virus, and SARS coronavirus. However, little is known about the role of bat ectoparasites in transmitting and maintaining such viruses. The intricate relationship between bats and their ectoparasites suggests that ectoparasites might serve as viral vectors, but evidence to date is scant. Bat flies, in particular, are highly specialized obligate hematophagous ectoparasites that incidentally bite humans. Using nextgeneration sequencing, we discovered a novel ledantevirus (mononegaviral family Rhabdoviridae, genus Ledantevirus) in nycteribiid bat flies infesting pteropodid bats in western Uganda. Mitochondrial DNA analyses revealed that both the bat flies and their bat hosts belong to putative new species. The coding-complete genome of the new virus, named Kanyawara virus (KYAV), is only distantly related to that of its closest known relative, Mount Elgon bat virus, and was found at high titers in bat flies but not in blood or on mucosal surfaces of host bats. Viral genome analysis indicates unusually low CpG dinucleotide depletion in KYAV compared to other ledanteviruses and rhabdovirus groups, with KYAV displaying values similar to rhabdoviruses of arthropods. Our findings highlight the possibility of a yetto- be-discovered diversity of potentially pathogenic viruses in bat ectoparasites.Item Killing of a Pearl-Spotted Owlet (Glaucidium perlatum) by Male Red Colobus Monkeys (Procolobus tephrosceles) in a Forest Fragment Near Kibale National Park, Uganda(Official Journal of the American Society of Primatologists, 2006) Goldberg, Tony L.; Gillespie, Thomas R.; Rwego, Innocent B.; Kaganzi, ClovisAdult male red colobus (Procolobus tephrosceles) were observed capturing and killing an owl (Glaucidium perlatum) in the Rurama forest fragment near Kibale National Park in western Uganda. The owl was not subsequently eaten by the colobus, their conspecifics, or the other primates present during the attack. Because the incident was preceded by an agonistic encounter with a raptor, the event is best interpreted as a misdirected antipredator behavior. Although antipredator behaviors are not unknown in red colobus, this is the first such incident directed against a raptor to be documented. Am. J. Primatol. 68:1–5, 2006. © 2006 Wiley-Liss, Inc.Item Molecular Epidemiology of Cross-Species Giardia duodenalis Transmission in Western Uganda(PLoS neglected tropical diseases, 2010) Johnston, Amanda R.; Gillespie, Thomas R.; Rwego, Innocent B.; McLachlan, Traci L. Tranby; Kent, Angela D.; Goldberg, Tony L.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.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.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. .Item Patterns Of Gastrointestinal Bacterial Exchange Between Chimpanzees And Humans Involved In Research And Tourism In Western Uganda(Biological Conservation, 2007) Goldberg, Tony L.; Gillespie, Thomas R.; Rwego, Innocent B.; Wheeler, Emily; Estoff, Elizabeth L.; Chapman, Colin A.Ecological overlap may increase the risks of microbial exchange between humans and wild non-human primates. Escherichia coli bacteria were collected from chimpanzees and humans in Kibale National Park, western Uganda, in May and June 2004, in order to examine whether interaction between humans and apes in the wild might affect gastrointestinal bacterial communities in the two species. Chimpanzees harbored bacteria genetically more similar to those of humans employed in chimpanzee-directed research and tourism than to those of humans from a local village. Most humans (81.6%) and 4.4% of chimpanzees harbored at least one isolate resistant to locally available antibiotics. In isolates from both humans and chimpanzees, resistance was higher to five of these antibiotics than to Ceftiofur, an antibiotic not available in the region. These data indicate that humans and apes interacting in the wild can share genetically and phenotypically similar gastrointestinal bacteria, presumably originating from common environmental sources. Strategies to limit transmission of pathogens between humans and primates, whether that transmission is direct or indirect, would benefit both human health and primate conservation.Item Selective deforestation and exposure of African wildlife to bat-borne viruses(Nature Publishing Group UK, 2024-04) Fedurek, Pawel; Asiimwe, Caroline; Rice, Gregory K.; Akankwasa, Walter J; Reynolds, Vernon; Hobaiter, Catherine; Kityo, Robert; Muhanguzi, Geoffrey; Zuberbühler, Klaus; Crockford, Catherine; Cer, Regina Z; Bennett, Andrew J; Rothman, Jessica M; Bishop-Lilly, Kimberly A; Goldberg, Tony L.Proposed mechanisms of zoonotic virus spillover often posit that wildlife transmission and amplification precede human outbreaks. Between 2006 and 2012, the palm Raphia farinifera , a rich source of dietary minerals for wildlife, was nearly extirpated from Budongo Forest, Uganda. Since then, chimpanzees, black-and-white colobus, and red duiker were observed feeding on bat guano, a behavior not previously observed. Here we show that guano consumption may be a response to dietary mineral scarcity and may expose wildlife to bat-borne viruses. Videos from 2017–2019 recorded 839 instances of guano consumption by the aforementioned species. Nutritional analysis of the guano revealed high concentrations of sodium, potassium, magnesium and phosphorus. Metagenomic analyses of the guano identified 27 eukaryotic viruses, including a novel betacoronavirus. Our findings illustrate how “upstream” drivers such as socioeconomics and resource extraction can initiate elaborate chains of causation, ultimately increasing virus spillover risk. A study in Uganda found that local extirpation of a mineral-rich tree species used in tobacco farming forced wildlife to obtain minerals by eating bat guano, in which 27 eukaryotic viruses were identified, including a novel betacoronavirus.