High Prevalence of Ancylostoma ceylanicum Hookworm Infections in Humans, Cambodia, 2012

Tawin Inpankaew

, Fabian Schär, Anders Dalsgaard, Virak Khieu, Wissanuwat Chimnoi, Chamnan Chhoun, Daream Sok, Hanspeter Marti, Sinuon Muth, Peter Odermatt, and Rebecca J. Traub

Author affiliations: University of Copenhagen, Copenhagen, Denmark (T. Inpankaew, A. Dalsgaard); Kasetsart University, Bangkok, Thailand (T. Inpankaew, W. Chimnoi); Swiss Tropical and Public Health Institute, Basel, Switzerland (F. Schär, V. Khieu, H. Marti, P. Odermatt); University of Basel, Basel (F. Schär, V. Khieu, H. Marti, P. Odermatt); National Center for Parasitology, Entomology and Malaria Control, Phnom Penh, Cambodia (V. Khieu, S. Muth); Fisheries Administration, Phnom Penh (C. Chhoun, D. Sok); The University of Queensland, Gatton, Queensland, Australia (R.J. Traub); University of Melbourne, Parkville, Victoria, Australia (R.J. Traub)

Abstract

Ancylostoma ceylanicum, a hookworm of canids and felids in Asia, is becoming the second most common hookworm infecting humans. In 2012, we investigated the prevalence and infection dynamics of and risk factors for hookworm infections in humans and dogs in a rural Cambodian village. Over 57% of the population was infected with hookworms; of those, 52% harbored A. ceylanicum hookworms. The greatest intensities of A. ceylanicum eggs were in persons 21-30 years of age. Over 90% of dogs also harbored A. ceylanicumhookworms. Characterization of the cytochrome oxidase-1 gene divided isolates of A. ceylanicum hookworms into 2 groups, 1 containing isolates from humans only and the other a mix of isolates from humans and animals. We hypothesize that preventative chemotherapy in the absence of concurrent hygiene and animal health programs may be a factor leading to emergence of A. ceylanicum infections; thus, we advocate for a One Health approach to control this zoonosis.

Human infections with Necator americanus and Ancylostoma duodenale hookworms continue to be recognized as a leading cause of iron deficiency anemia and protein malnutrition in developing countries (1). On the basis of parasitologic surveys of fecal samples, hookworms are estimated to infect 576–740 million persons globally, and over half of the infections occur in Asia and the Pacific regions (2). Recent molecular-based epidemiologic surveys have shownAncylostoma ceylanicum to be the second most common hookworm species infecting humans in Asia. In Thailand, Laos, and Malaysia, 6%–23% of persons positive for hookworm eggs were infected with A. ceylanicum helminths (3–6). There are an estimated 19–73 million A. ceylanicumhookworm–infected persons in regions where this zoonotic helminth is known to be endemic (7). Dogs and cats act as natural reservoirs for hookworm transmission to humans, and the prevalence of A. ceylanicum hookworms in these animals ranges from 24% to 92% in the Asia-Pacific region (6,8–10). Much like anthroponotic helminths, A. ceylanicum hookworms have the potential to produce clinical symptoms of ground itch (a pruritic papular hypersensitivity response caused by the entry of helminths into the skin), epigastric pain, diarrhea, and anemia in humans (11–15). However, despite these reports, relatively little is known about the clinical significance and infection dynamics of this zoonotic hookworm in humans, dogs, and cats. Differentiation of the genus of hookworms infecting humans is imperative because each species varies in its biology, life cycle, pathophysiology, and epidemiology, and these differences have key implications when assessing hookworm-associated illnesses and establishing control measures.

The internal transcribed spacer (ITS) –1 and –2 regions and the 5.8S region have been used to detect and characterize hookworm infections directly from eggs in human and animal feces (6,10,16,17). In addition, sequencing of the cytochrome c oxidase subunit 1 (cox1) gene has been successfully used to establish intraspecies genetic differences of many strongylid nematodes, including hookworms (18–21).

The aim of our study was to determine the prevalence, associated risk factors, and infection dynamics of hookworm species infection in humans and dogs living in a rural Cambodian village. To carry out this investigation, we used a combination of conventional parasitologic and molecular epidemiologic approaches.

Acknowledgments

We thank Chhay Somany for his hospitality during sample collection and Darwin Murrell for his guidance and valuable input throughout the study. We gratefully acknowledge staff from the National Center for Parasitology, Entomology and Malaria Control, Cambodia, for their help in collecting fecal samples from humans and dogs and for help with the interviews. Special thanks go to all study participants in Dong village.

This project was financially supported by UBS Optimus Foundation, Zürich, Switzerland, and a PhD fellowship grant (to T.I.) from the Faculty of Health and Medical Sciences, University of Copenhagen, Denmark.

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Suggested citation for this article: Inpankaew T, Schär F, Dalsgaard A, Khieu V, Chimnoi W, Chhoun C, et al. High prevalence of Ancylostoma ceylanicum hookworm infections in humans, Cambodia, 2012. Emerg Infect Dis. 2014 June [date cited].http://dx.doi.org/10.3201/eid2006.131770