Research Article: Epidemiology and Molecular Characterization of Cryptosporidium spp. in Humans, Wild Primates, and Domesticated Animals in the Greater Gombe Ecosystem, Tanzania

Date Published: February 20, 2015

Publisher: Public Library of Science

Author(s): Michele B. Parsons, Dominic Travis, Elizabeth V. Lonsdorf, Iddi Lipende, Dawn M. Anthony Roellig, Shadrack Kamenya, Hongwei Zhang, Lihua Xiao, Thomas R. Gillespie, Stephen Baker. http://doi.org/10.1371/journal.pntd.0003529

Abstract: Cryptosporidium is an important zoonotic parasite globally. Few studies have examined the ecology and epidemiology of this pathogen in rural tropical systems characterized by high rates of overlap among humans, domesticated animals, and wildlife. We investigated risk factors for Cryptosporidium infection and assessed cross-species transmission potential among people, non-human primates, and domestic animals in the Gombe Ecosystem, Kigoma District, Tanzania. A cross-sectional survey was designed to determine the occurrence and risk factors for Cryptosporidium infection in humans, domestic animals and wildlife living in and around Gombe National Park. Diagnostic PCR revealed Cryptosporidium infection rates of 4.3% in humans, 16.0% in non-human primates, and 9.6% in livestock. Local streams sampled were negative. DNA sequencing uncovered a complex epidemiology for Cryptosporidium in this system, with humans, baboons and a subset of chimpanzees infected with C. hominis subtype IfA12G2; another subset of chimpanzees infected with C. suis; and all positive goats and sheep infected with C. xiaoi. For humans, residence location was associated with increased risk of infection in Mwamgongo village compared to one camp (Kasekela), and there was an increased odds for infection when living in a household with another positive person. Fecal consistency and other gastrointestinal signs did not predict Cryptosporidium infection. Despite a high degree of habitat overlap between village people and livestock, our results suggest that there are distinct Cryptosporidium transmission dynamics for humans and livestock in this system. The dominance of C. hominis subtype IfA12G2 among humans and non-human primates suggest cross-species transmission. Interestingly, a subset of chimpanzees was infected with C. suis. We hypothesize that there is cross-species transmission from bush pigs (Potaochoerus larvatus) to chimpanzees in Gombe forest, since domesticated pigs are regionally absent. Our findings demonstrate a complex nature of Cryptosporidium in sympatric primates, including humans, and stress the need for further studies.

Partial Text: Cryptosporidium is one of the most important parasitic diarrheal agents in humans in the world, is among the top four causes of moderate-to-severe diarrheal disease in young children in developing nations, and is problematic as an opportunistic co-infection with HIV due to increased morbidity and mortality [1,2]. Cryptosporidium is well adapted to zoonotic, waterborne, and foodborne transmission, with a life cycle occurring in suitable hosts and transmission by the fecal-oral route [3]. Zoonoses represent the majority of diseases emerging globally with potential to expand to new host systems, [4] yet despite these health threats, few studies have examined the ecology and epidemiology of this pathogen in rural tropical forest systems characterized by high rates of overlap among humans, domesticated animals, and wildlife [5,6].

Six hundred and eighty-four fecal specimens were screened for Cryptosporidium including 254 human, 99 domestic animal (n = 76 goat, n = 14 sheep, n = 9 dog) and 331 wildlife (n = 251 chimpanzee, n = 80 baboon) specimens. Cryptosporidium spp, were detected by PCR from 40 (5.8%) fecal samples but was not detected in any water samples (n = 42). The infection rate of Cryptosporidium was highest among 21/131 (16.0%) nonhuman primates tested, compared to 7/73 (9.6%) livestock and 8/185 (4.3%) humans. No significant differences in frequency were observed between chimpanzees and baboons (Table 1, Fisher’s exact test p = 0.457) or between the two chimpanzee communities (Table 1, Fisher’s exact test p = 0.7655). Of the 8 cases of Cryptosporidium detected in humans, 7 (87.5%) resided in Mwamgongo village and one (12.5%) in Mitumba camp. No human cases were detected in the Kasekela camp. Sheep had the highest occurrence of Cryptosporidium (22%) compared to goat (9%) and dogs (0%) but small sample size prevented evaluation of significance.

Of 90 humans residing in camps within Gombe National Park, only one Cryptosporidium infection was observed (1%). In contrast, Cryptosporidium infection in residents of Mwamgongo village reached 10% during the drier months. These frequencies are comparable to those reported in some studies from children and adults without HIV, ranging from 0–18% [25–27], though frequencies as high as 32% have been reported elsewhere [28]. Site and HIV prevalence would seem to be important factors in human occurrence rates. Although HIV testing was beyond the scope of this study, a recent country report [9] indicates a low HIV prevalence (< 1%) from the Kigoma region where the study occurred. Infection was not statistically associated with gastrointestinal illness or stool consistency for humans or wildlife, findings consistent with earlier studies [28–32]. Surprisingly, unsafe drinking water (i.e. untreated/unboiled water, open water source) was not found to increase risk of Cryptosporidium infection, which could be the result of degradation or improper tapping of the water line, exposing water to environmental contamination [33]. This warrants further study as consumption of contaminated ground water has been repeatedly associated with Cryptosporidium infection [34,35]. Source: http://doi.org/10.1371/journal.pntd.0003529

 

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