Molecular Identification of Hookworm Isolates in Humans, Dogs and Soil in a Tribal Area in Tamil Nadu, India

Citation: George S, Levecke B, Kattula D, Velusamy V, Roy S, Geldhof P, et al. (2016) Molecular Identification of Hookworm Isolates in Humans, Dogs and Soil in a Tribal Area in Tamil Nadu, India. PLoS Negl Trop Dis 10(8): e0004891. doi:10.1371/journal.pntd.0004891
Published: August 3, 2016

Abstract
HookwormsBackground: Hookworms (Necator americanus and Ancylostoma duodenale) remain a major public health problem worldwide. Infections with hookworms (e.g., A. caninum, A. ceylanicum and A. braziliense) are also prevalent in dogs, but the role of dogs as a reservoir for zoonotic hookworm infections in humans needs to be further explored.
Methodology/Principal Findings: As part of an open-label community based cluster-randomized trial in a tribal area in Tamil Nadu (India; 2013–2015), a total of 143 isolates of hookworm eggs from human stool were speciated based on a previously described PCR-RFLP methodology. The presence of hookworm DNA was confirmed in 119 of 143 human samples. N. americanus (100%) was the most prevalent species, followed by A. caninum (16.8%) and A. duodenale (8.4%). Because of the high prevalence of A. caninum in humans, dog samples were also collected to assess the prevalence of A. caninum in dogs. In 68 out of 77 canine stool samples the presence of hookworms was confirmed using PCR-RFLP. In dogs, both A. caninum (76.4%) and A. ceylanicum (27.9%) were identified. Additionally, to determine the contamination of soil with zoonotic hookworm larvae, topsoil was collected from defecating areas. Hookworm DNA was detected in 72 out of 78 soil samples that revealed presence of hookworm-like nematode larvae. In soil, different hookworm species were identified, with animal hookworms being more prevalent (A. ceylanicum: 60.2%, A. caninum: 29.4%, A. duodenale: 16.6%, N. americanus: 1.4%, A. braziliense: 1.4%).
Conclusions/Significance: In our study we regularly detected the presence of A. caninum DNA in the stool of humans. Whether this is the result of infection is currently unknown but it does warrant a closer look at dogs as a potential reservoir.

Author Summary: Hookworm infections remain a major public health problem in both tropical and subtropical parts of the world. To control the disease burden attributable to hookworms, large-scale deworming programs, in which drugs are administered to schoolchildren regardless of their infection status, are currently being implemented in endemic regions. However, these programs face some difficulties. One of them is the uncertainty about the role of animals in the transmission of hookworm infections. It is commonly believed that human-specific hookworms cause these infections, but there is growing evidence that the role of some animal-specific hookworms as cause of infection in humans should not be underestimated. We determined the different hookworms in humans, dogs and soil (eggs excreted by adult hookworms in stool are non-infectious, and need to develop and hatch on the soil before larvae can transmit disease by penetrating the skin) in a tribal area in India. In this area, the transmission of hookworms between humans and dogs is possible. Our results highlight the presence of DNA from animal-specific hookworms in both soil and human stool. Although these findings suggest that these animals could act as reservoir for zoonotic hookworm infections in humans, they should be interpreted with caution. This is because we lack the evidence to confirm A. caninum infections in our study population. Other potential reasons for the presence of DNA in stool are contamination of stool with environmental eggs or larvae during sample collection and passive passage in which eggs or larvae are ingested but did result in any infection.

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