Epidemiological and Genetic Data Supporting the Transmission of Ancylostoma ceylanicum among Human and Domestic Animals

Abstract

BackgroundCurrently, information on species-specific hookworm infection is unavailable in Malaysia and is restricted worldwide due to limited application of molecular diagnostic tools. Given the importance of accurate identification of hookworms, this study was conducted as part of an ongoing molecular epidemiological investigation aimed at providing the first documented data on species-specific hookworm infection, associated risk factors and the role of domestic animals as reservoirs for hookworm infections in endemic communities of Malaysia.Methods/FindingsA total of 634 human and 105 domestic canine and feline fecal samples were randomly collected. The overall prevalence of hookworm in humans and animals determined via microscopy was 9.1% (95% CI = 7.0–11.7%) and 61.9% (95% CI = 51.2–71.2%), respectively. Multivariate analysis indicated that participants without the provision of proper latrine systems (OR = 3.5; 95% CI = 1.53–8.00; p = 0.003), walking barefooted (OR = 5.6; 95% CI = 2.91–10.73; p<0.001) and in close contact with pets or livestock (OR = 2.9; 95% CI = 1.19–7.15; p = 0.009) were more likely to be infected with hookworms. Molecular analysis revealed that while most hookworm-positive individuals were infected with Necator americanus, Ancylostoma ceylanicum constituted 12.8% of single infections and 10.6% mixed infections with N. americanus. As for cats and dogs, 52.0% were positive for A. ceylanicum, 46.0% for Ancylostoma caninum and 2.0% for Ancylostoma braziliense and all were single infections.ConclusionThis present study provided evidence based on the combination of epidemiological, conventional diagnostic and molecular tools that A. ceylanicum infection is common and that its transmission dynamic in endemic areas in Malaysia is heightened by the close contact of human and domestic animal (i.e., dogs and cats) populations.

Patterns and Risk Factors of Soil-Transmitted Helminthiasis Among Orang Asli Subgroups in Peninsular Malaysia

“…In many other studies, lack of footwear in association with the presence of free-roaming dogs provide a strong predictor for STH infections, particularly hookworm. 33,34 Moreover, more studies are reporting on the zoonotic ancylostomiasis caused by A. ceylanicum in humans in endemic areas in Southeast Asia. 23,[34][35][36] A recent genetic study to provide further evidence on zoonotic transmission of A. ceylanicum between humans and animals in Malaysia showed that some of the A. ceylanicum strains from both the human and animal host in the same geographical location are clustered together within the same group.…”

“…These findings confirmed the previous epidemiological survey indicating that individuals who had close contact with dogs were more likely to be infected with A. ceylanicum. [33][34][35] Although the notion of zoonotic transmission of A. lumbricoides and T. trichiura between humans and dogs is still largely unclear, these animals may act as significant mechanical transmitter of ascariasis in the human population especially in communities where the habit of indiscriminate defecation exist. Molecular-based tool studies have shown that dogs act as disseminators and environmental contaminators of A. lumbricoides in communities where indiscriminate defecation is common.…”

First Molecular Identifications of Necator americanus and Ancylostoma ceylanicum Infecting Rural Communities in Lower Myanmar

“…4,5 Ancylostoma ceylanicum is now the second most common hookworm species infecting humans in Asia and possible cause of cutaneous larvae migrans or abdominal symptoms in infected patients, with reported high egg-positivity rates in Thailand, Laos, Cambodia, and Malaysia. [6][7][8][9][10] National surveys on the prevalence of soil-transmitted helminths (STHs) in Myanmar reported a reduction in hookworm prevalence in schoolchildren from 6.5% to 0.3% 7 years after a national deworming program. 11,12 A diagnosis of hookworm infection was usually made by microscopic examination of eggs or larvae in the fecal samples.…”

Ancylostoma ceylanicum metalloprotease 6 DNA vaccination induces partial protection against hookworm challenge infection

“…Necator americanus is the most prevalent species of hookworm, whereas A. duodenale occurs in more geographically restricted areas . Ancylostoma ceylanicum is considered as a zoonotic species (Fujiwara et al 2006), but can cause patent infection in humans (Ngui et al 2012). Other species like Ancylostoma caninum and Ancylostoma brasiliense cause eosinophilic enteritis and cutaneous larva migrans syndrome and also cause zoonoses (Fujiwara et al 2006).…”