Ancylostoma ceylanicum: The Neglected Zoonotic Parasite of Community Dogs in Thailand and Its Genetic Diversity among Asian Countries

SIMPLE SUMMARY: Ancylostomiasis is a zoonotic disease caused by the Ancylostoma hookworm infection of dogs, cats, and other wildlife species and is frequently found in Asia and tropical regions. The present study had confirmed the species of hookworm in dogs and soil environments collected from temple communities. In addition, we investigated the association of hookworm-contaminated soil in temple areas to increase awareness and establish a regimen to prevent zoonotic hookworm transmission. Lastly, we analyzed the genetic diversity and evolution of hookworm in dogs and soil environments among Thai A. ceylanicum and other Asian populations and disclosed insight into their fundamental genetic relationship. ABSTRACT: Ancylostoma ceylanicum is a zoonotic helminth that is commonly found in domestic dogs and cats throughout Asia but is largely neglected in many countries. This study aimed to confirm the species of hookworm in dogs and soil environments and investigate the evolutionary analyses of A. ceylanicum among Thai and Asian populations. In a total of 299 dog fecal samples and 212 soil samples from 53 temples, the prevalence rates of hookworm infection by microscopic examination were 26.4% (79/299) and 10.4% (22/212) in dog and soil samples, respectively. A PCR-RFLP targeting the ITS region was then utilized to identify the hookworm species. In dogs, A. ceylanicum was the main hookworm species, and the rates of A. ceylanicum and A. caninum infections were 96.6% and 3.5%, respectively. The genetic characterization and diversity indices of the A. ceylanicum cox1 gene among Thai and Asian populations were evaluated. Nine haplotypes were identified from Thai A. ceylanicum, in which the haplotype diversity and the nucleotide diversity were 0.4436 and 0.0036, respectively. The highest nucleotide diversity of Chinese A. ceylanicum populations suggested that it could be the ancestor of the populations. Pairwise fixation indices indicated that Thai A. ceylanicum was closely related to the Malaysian population, suggesting a gene flow between these populations. The temples with hookworm-positive dogs were associated with the presence of hookworm-contaminated soil, as these levels showed an approximately four-fold increase compared with those in temples with hookworm-negative dogs (OR = 4.38, 95% CI: 1.55–12.37). Interestingly, the genotypes of A. ceylanicum in the contaminating soil and infecting dogs were identical. Therefore, increased awareness and concern from the wider public communities with regard to the responsibility of temples and municipal offices to provide proper deworming programs to community dogs should be strongly endorsed to reduce the risk of the transmission of this zoonotic disease. In addition, parasitic examination and treatment should be strongly implemented before dogs are imported and exported worldwide.