Molecular Epidemiology Of Echinococcus And Taenia Species In Dogs From Cystic Echinococcosis Endemic Areas In Kenya

Abstract

Dogs are reservoirs and hosts for several parasites which cause zoonoses of public health significance worldwide. All four hookworm species of canines are zoonotic and cause infections ranging from transient skin irritations to prolonged ‘creeping eruptions’, eosinophilic enteritis and patent intestinal infections. Cestodes belonging to the Taeniidae family are of medical and veterinary importance in resource poor communities and cause cystic echinococcosis (CE), cysticercosis and coenurosis in livestock and humans. There is scanty data on the prevalence of intestinal parasites of dogs and their impact on public health in Kenya. Furthermore, the role of domestic dogs in maintaining the transmission cycles and environmental contamination with infective stages of these parasites remains unknown in Kenya. This study aimed at establishing the prevalence and distribution of Echinococcus granulosus sensu lato (s. l.), Taenia spp. and other zoonotic intestinal parasites in dogs from CE endemic areas of Kenya. Dog faecal samples were collected from the environment in Turkana, Meru, Isiolo and Narok (Maasai Mara) counties and microscopically examined for the detection of intestinal parasites using McMaster and zinc chloride flotation-sieving technique. Genotyping of hookworms, Echinococcus and Taenia spp. was performed by polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) and or DNA sequencing. Echinococcus and Taenia spp. haplotypes were determined by sequencing and analysis of cytochrome C oxidase subunit 1 gene (cox1) and NADH dehydrogenase subunit 1 (nad1) genes respectively. Of the 1,621 faecal samples, 701 (43.24%) contained at least one parasite. Eleven parasites genera/families were identified namely hookworms, Taeniidae, Spirometra spp., Coccidia, Toxocara spp., Trichuris spp., Toxascaris leonina, Dipylidium caninum, Anoplocephala spp., Mesostephanus spp. and Uncinaria stenocephala (in order of frequency). Hookworms were the most common parasites detected followed by taeniids. Microscopy detected hookworm eggs in 490/1621 (30.23%, 95% CI 27.99–32.53) faecal samples. The prevalence of hookworms was high in counties receiving higher rainfall (Narok 46.80%, Meru 44.88%) and low in those with a more arid climate (Isiolo 19.73%, Turkana 11.83%). In a subset of 70 hookworm eggs positive faecal samples Ancylostoma caninum (n = 59), A. braziliense (n = 10) and A. cf. duodenale (n = 1) were identified. Eleven percent (178/1,621) of faecal samples had taeniid eggs, among them 4.4% (71/1,621) were Echinococcus spp. eggs. Area-wise, the faecal prevalence of Echinococcus spp. was 9.2% (48/524) in Turkana, 4.0% (20/500) in Maasai Mara, 0.7% (2/294) in Isiolo and 0.3% iv (1/303) in Meru. Four Echinococcus spp. were identified with E. granulosus sensu stricto (s. s.) being the dominant Echinococcus taxon, followed by E. canadensis (G6/7) that was detected in 51 and 23 faecal samples, respectively. E. ortleppi and E. felidis were rare and only detected in 5 and 2 faecal samples respectively. Overall 79/1621 (4.9%) faecal samples contained eggs of Taenia or Hydatigera (8.0% in Turkana, 4.8% in Isiolo, 3.8% in Maasai Mara and 1.3% in Meru). Taenia hydatigena and T. multiceps were the most frequent, found in 36 and 15 samples, respectively. Other eggs detected in the faecal samples belonged to T. serialis (sensu lato), T. madoquae (the first record in domestic dogs), T. ovis, T. saginata and Hydatigera taeniaeformis. Polymorphism of nad1 sequences revealed 22 and 8 haplotypes of T. hydatigena and T. multiceps, respectively, but only a few haplotypes showed wide geographical distribution for both species. This study identified zoonotic parasites in dogs that pose potential public health risk to humans. Canine hookworm species and genetic variability of T. hydatigena and T. multiceps are reported for the first time in Kenya. The data confirms differences in diversity and abundance of Echinococcus and Taenia spp. between regions of Kenya and demonstrates that domestic dogs play a role in linking the domestic and sylvatic cycles of Echinococcus and Taenia spp. The unusual detection of A. cf. duodenale, T. saginata and E. felidis in dog faeces indicates coprophagy as a common behaviour of dogs. These findings emphasize the need for control measures such as enforcing laws for restraining stray dogs, dog population management, regular deworming of dogs, proper disposal of slaughter offal and dog faeces and public health educational awareness programmes.