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Molecular identification of zoonotic hookworms in dogs from four counties of Kenya

Published online by Cambridge University Press:  28 February 2019

E. Mulinge*
Affiliation:
Kenya Medical Research Institute, Nairobi, Kenya School of Biological Sciences, University of Nairobi, Nairobi, Kenya
S.M. Njenga
Affiliation:
Kenya Medical Research Institute, Nairobi, Kenya
D. Odongo
Affiliation:
School of Biological Sciences, University of Nairobi, Nairobi, Kenya
J. Magambo
Affiliation:
Meru University of Science and Technology, Meru, Kenya
E. Zeyhle
Affiliation:
Meru University of Science and Technology, Meru, Kenya
C. Mbae
Affiliation:
Kenya Medical Research Institute, Nairobi, Kenya
D. Kagendo
Affiliation:
Meru University of Science and Technology, Meru, Kenya
H. Kanyi
Affiliation:
Kenya Medical Research Institute, Nairobi, Kenya
R.J. Traub
Affiliation:
Faculty of Veterinary and Agricultural Science, University of Melbourne, Parkville, Australia
M. Wassermann
Affiliation:
Parasitology Unit, University of Hohenheim, Stuttgart, Germany
P. Kern
Affiliation:
University Hospital Ulm, Department of Medicine III, Ulm, Germany
T. Romig
Affiliation:
Parasitology Unit, University of Hohenheim, Stuttgart, Germany
*
Author for correspondence: E. Mulinge E-mail: [email protected]

Abstract

All canine hookworms are known to be zoonotic, causing infections ranging from transient skin irritations to prolonged ‘creeping eruptions’, eosinophilic enteritis and even patent intestinal infections. There is little information on canine hookworm species and their public health significance in sub-Saharan Africa. This study determined the prevalence and species of hookworms in dogs from different climatic zones of Kenya. Dog faecal samples were collected from the environment, and hookworm eggs were isolated by zinc chloride flotation and subjected to DNA extraction. Polymerase chain reaction (PCR) assays targeting the internal transcribed spacer (ITS) 1 and 2, 5.8S and 28S ribosomal RNA of Ancylostoma spp. and Uncinaria stenocephala were performed, and hookworm species were identified by PCR-restriction fragment length polymorphism (RFLP) or DNA sequencing. Hookworm eggs were detected by microscopy in 490/1621 (30.23%, 95% CI 28.01–32.54) faecal samples. Estimates of faecal prevalence were 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 faecal samples, Ancylostoma caninum (n = 59) was the most common species, followed by A. braziliense (n = 10) and A. cf. duodenale (n = 1). This study reports for the first time the detection of A. cf. duodenale in dog faeces and zoonotic hookworm species in Kenyan dogs. These findings emphasize the need for control measures such as enforcing laws for restraining stray dogs, regular deworming of dogs, and public health awareness programmes aimed at informing communities on outdoor use of footwear.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2019 

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References

Arndt, MB et al. (2013) Impact of helminth diagnostic test performance on estimation of risk factors and outcomes in HIV-positive adults. PLoS ONE 8, e81915.Google Scholar
Blackwell, V and Vega-Lopez, F (2001) Cutaneous larva migrans: clinical features and management of 44 cases presenting in the returning traveller. British Journal of Dermatology 145, 434437.Google Scholar
Bouchaud, O et al. (2000) Cutaneous larva migrans in travelers: a prospective study, with assessment of therapy with ivermectin. Clinical Infectious Diseases 31, 493498.Google Scholar
Bowman, DD et al. (2010) Hookworms of dogs and cats as agents of cutaneous larva migrans. Trends in Parasitology 26, 162167.Google Scholar
Bradbury, R and Traub, RJ (2016) Hookworm infection in Oceania. In Loukas, A (ed), Neglected Tropical Diseases - Oceania. Cham: Springer International Publishing, pp. 3368.Google Scholar
Bradbury, R et al. (2017) Ancylostoma ceylanicum hookworm in the Solomon Islands. Emerging Infectious Diseases 23, 252257.Google Scholar
Brooker, S, Clements, AC and Bundy, DA (2006) Global epidemiology, ecology and control of soil-transmitted helminth infections. Advances in Parasitology 62, 221261.Google Scholar
Buishi, I et al. (2006) Canine echinococcosis in Turkana (north-western Kenya): a coproantigen survey in the previous hydatid-control area and an analysis of risk factors. Annals of Tropical Medicine & Parasitology 100, 601610.Google Scholar
Caumes, E (2000) Treatment of cutaneous larva migrans. Clinical Infectious Diseases 30, 811814.Google Scholar
Coelho, WM et al. (2011) Occurrence of Ancylostoma in dogs, cats and public places from Andradina city, Sao Paulo state, Brazil. Revista Do Instituto De Medicina Tropical De Sao Paulo 53, 181184.Google Scholar
Conlan, JV et al. (2012) Soil-transmitted helminthiasis in Laos: a community-wide cross-sectional study of humans and dogs in a mass drug administration environment. American Journal of Tropical Medicine and Hygiene 86, 624634.Google Scholar
Crompton, DW (2001) Ascaris and ascariasis. Advances in Parasitology 48, 285375.Google Scholar
Davoust, B et al. (2008) Epidemiological survey on gastro-intestinal and blood-borne helminths of dogs in north-east Gabon. Onderstepoort Journal of Veterinary Research 75, 359364.Google Scholar
Del Giudice, P et al. (2002) Loeffler's syndrome and cutaneous larva migrans: a rare association. British Journal of Dermatology 147, 386388.Google Scholar
Dhir, L, O'Dempsey, T and Watts, MT (2010) Cutaneous larva migrans with optic disc edema: a case report. Journal of Medical Case Reports 4, 209.Google Scholar
Dias, SR et al. (2013) Evaluation of parasitological and immunological aspects of acute infection by Ancylostoma caninum and Ancylostoma braziliense in mixed-breed dogs. Parasitology Research 112, 21512157.Google Scholar
Dinkel, A et al. (1998) Detection of Echinococcus multilocularis in the definitive host: coprodiagnosis by PCR as an alternative to necropsy. Journal of Clinical Microbiology 36, 18711876.Google Scholar
e Silva, LM et al. (2006) Differential diagnosis of dog hookworms based on PCR-RFLP from the ITS region of their rDNA. Veterinary Parasitology 140, 373377.Google Scholar
Easton, AV et al. (2016) Multi-parallel qPCR provides increased sensitivity and diagnostic breadth for gastrointestinal parasites of humans: field-based inferences on the impact of mass deworming. Parasite & Vectors 9, 38.Google Scholar
Fahrion, AS et al. (2011) Toxocara eggs shed by dogs and cats and their molecular and morphometric species-specific identification: is the finding of T. cati eggs shed by dogs of epidemiological relevance? Veterinary Parasitology 177, 186189.Google Scholar
Frenkel, JK et al. (2003) Dogs as possible mechanical carriers of Toxoplasma, and their fur as a source of infection of young children. International Journal of Infectious Diseases 7, 292293.Google Scholar
Galanti, B, Fusco, FM and Nardiello, S (2002) Outbreak of cutaneous larva migrans in Naples, southern Italy. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 491492.Google Scholar
Gasser, RB et al. (1993) Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Research 21, 25252526.Google Scholar
George, S et al. (2016) Molecular identification of hookworm isolates in humans, dogs and soil in a tribal area in Tamil Nadu, India. PLoS Neglected Tropical Diseases 10, e0004891.Google Scholar
Georgi, JR, LeJambre, LF and Ractliffe, LH (1969) Ancylostoma caninum burden in relationship to erythrocyte loss in dogs. Journal of Parasitology 55, 12051211.Google Scholar
Hochedez, P and Caumes, E (2007) Hookworm-related cutaneous larva migrans. Journal of Travel Medicine 14, 326333.Google Scholar
Hu, M, Chilton, NB and Gasser, RB. (2002) The mitochondrial genomes of the human hookworms, Ancylostoma duodenale and Necator americanus (Nematoda: Secernentea). International Journal for Parasitology 32, 145158.Google Scholar
Hu, W et al. (2016) Levels of Ancylostoma infections and phylogenetic analysis of cox 1 gene of A. ceylanicum in stray cat faecal samples from Guangzhou, China. Journal of Helminthology 90, 392397.Google Scholar
Huttner, M et al. (2009) A survey of Echinococcus species in wild carnivores and livestock in East Africa. International Journal for Parasitology 39, 12691276.Google Scholar
Inpankaew, T et al. (2014) High prevalence of Ancylostoma ceylanicum hookworm infections in humans, Cambodia, 2012. Emerging Infectious Diseases 20, 976982.Google Scholar
Jelinek, T et al. (1994) Cutaneous larva migrans in travelers: synopsis of histories, symptoms, and treatment of 98 patients. Clinical Infectious Diseases 19, 10621066.Google Scholar
Jiraanankul, V et al. (2011) Incidence and risk factors of hookworm infection in a rural community of central Thailand. American Journal of Tropical Medicine and Hygiene 84, 594598.Google Scholar
Joshi, BN and Sabne, SS (1977) Incidence of Toxocara canis infection in stray dogs in Miraj area. Indian Journal of Pathology and Microbiology 20, 239242.Google Scholar
Jozefzoon, LM and Oostburg, BF (1994) Detection of hookworm and hookworm-like larvae in human fecocultures in Suriname. American Journal of Tropical Medicine and Hygiene 51, 501505.Google Scholar
Kagendo, D et al. (2014) A survey for Echinococcus spp. of carnivores in six wildlife conservation areas in Kenya. Parasitology International 63, 604611.Google Scholar
Kelkar, R (2007) Cutaneous larva migrans in England: a case in a returning traveller. Journal of Emergency Medicine 24, 678.Google Scholar
Koehler, AV et al. (2013) Genetic characterization of selected parasites from people with histories of gastrointestinal disorders using a mutation scanning-coupled approach. Electrophoresis 34, 17201728.Google Scholar
Landmann, JK and Prociv, P (2003) Experimental human infection with the dog hookworm, Ancylostoma caninum. Medical Journal of Australia 178, 6971.Google Scholar
Levecke, B et al. (2011) A comparison of the sensitivity and fecal egg counts of the McMaster egg counting and Kato-Katz thick smear methods for soil-transmitted helminths. PLoS Neglected Tropical Diseases 5, e1201.Google Scholar
Lindsay, DS et al. (1997) Mechanical transmission of Toxoplasma gondii oocysts by dogs. Veterinary Parasitology 73, 2733.Google Scholar
Liu, YJ et al. (2015) Molecular identification of hookworms in stray and shelter dogs from Guangzhou city, China using ITS sequences. Journal of Helminthology 89, 196202.Google Scholar
Loukas, A et al. (2005) Vaccination with recombinant aspartic hemoglobinase reduces parasite load and blood loss after hookworm infection in dogs. PLoS Medicine 2, e295.Google Scholar
Macpherson, CNL and Craig, PS (1991) The African hookworm problem: an overview. In Macpherson, CNL and Craig, PS (eds), Parasitic Helminths and Zoonoses in Africa. Dordrecht: Springer Netherlands, pp. 101137.Google Scholar
Mahdy, MA et al. (2012) Prevalence and zoonotic potential of canine hookworms in Malaysia. Parasite & Vectors 5, 88.Google Scholar
Malgor, R et al. (1996) High prevalence of Ancylostoma spp. infection in dogs, associated with endemic focus of human cutaneous larva migrans, in Tacuarembo, Uruguay. Parasite 3, 131134.Google Scholar
Mathis, A, Deplazes, P and Eckert, J (1996) An improved test system for PCR-based specific detection of Echinococcus multilocularis eggs. Journal of Helminthology 70, 219222.Google Scholar
Merino-Tejedor, A et al. (2018) Molecular identification of zoonotic hookworm species in dog faeces from Tanzania. Journal of Helminthology, doi: 10.1017/S0022149X18000263.Google Scholar
Miller, TA (1968) Pathogenesis and immunity in hookworm infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 62, 473489.Google Scholar
Miller, TA (1970) Studies on the incidence of hookworm infection in East Africa. East African Medical Journal 47, 354363.Google Scholar
Mudenda, NB et al. (2012) Modelling the ecological niche of hookworm in Brazil based on climate. Geospatial Health 6, S111123.Google Scholar
Mulinge, E et al. (2018) Molecular characterization of Echinococcus species in dogs from four regions of Kenya. Veterinary Parasitology 255, 4957.Google Scholar
Ngui, R et al. (2012) Epidemiological and genetic data supporting the transmission of Ancylostoma ceylanicum among human and domestic animals. PLoS Neglected Tropical Diseases 6, e1522.Google Scholar
Nijsse, R et al. (2014) Coprophagy in dogs interferes in the diagnosis of parasitic infections by faecal examination. Veterinary Parasitology 204, 304309.Google Scholar
Oliveira-Arbex, AP et al. (2017) Molecular identification of Ancylostoma species from dogs and an assessment of zoonotic risk in low-income households, Sao Paulo State, Brazil. Journal of Helminthology 91, 1419.Google Scholar
Palmer, CS et al. (2007) The veterinary and public health significance of hookworm in dogs and cats in Australia and the status of A. ceylanicum. Veterinary Parasitology 145, 304313.Google Scholar
Pullan, RL and Brooker, SJ (2012) The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasite & Vectors 5, 81.Google Scholar
Repetto, SA et al. (2013) An improved DNA isolation technique for PCR detection of Strongyloides stercoralis in stool samples. Acta Tropica 126, 110114.Google Scholar
Rinaldi, L et al. (2006) Canine faecal contamination and parasitic risk in the city of Naples (southern Italy). BMC Veterinary Research 2, 29.Google Scholar
Sato, M et al. (2010) Copro-molecular identification of infections with hookworm eggs in rural Lao PDR. Transactions of the Royal Society of Tropical Medicine and Hygiene 104, 617622.Google Scholar
Schaub, N, Perruchoud, AP and Buechner, S (2002) Cutaneous larva migrans associated with Loffler's syndrome. Dermatology 205, 207209.Google Scholar
Smout, FA et al. (2017) The hookworm Ancylostoma ceylanicum: an emerging public health risk in Australian tropical rainforests and Indigenous communities. One Health 3, 6669.Google Scholar
Sowemimo, OA (2009) The prevalence and intensity of gastrointestinal parasites of dogs in Ile-Ife, Nigeria. Journal of Helminthology 83, 2731.Google Scholar
Speare, R, Bradbury, RS and Croese, J (2016) A case of Ancylostoma ceylanicum infection occurring in an Australian soldier returned from Solomon Islands. Korean Journal of Parasitology 54, 533536.Google Scholar
Traub, RJ (2013) Ancylostoma ceylanicum, a re-emerging but neglected parasitic zoonosis. International Journal for Parasitology 43, 10091015.Google Scholar
Traub, RJ et al. (2002) The role of dogs in transmission of gastrointestinal parasites in a remote tea-growing community in northeastern India. American Journal of Tropical Medicine and Hygiene 67, 539545.Google Scholar
Traub, RJ et al. (2003) Humans, dogs and parasitic zoonoses–unravelling the relationships in a remote endemic community in northeast India using molecular tools. Parasitology Research 90 Suppl 3, S156157.Google Scholar
Traub, RJ et al. (2004) Application of a species-specific PCR-RFLP to identify Ancylostoma eggs directly from canine faeces. Veterinary Parasitology 123, 245255.Google Scholar
Traub, RJ et al. (2007) A case of mistaken identity–reappraisal of the species of canid and felid hookworms (Ancylostoma) present in Australia and India. Parasitology 134, 113119.Google Scholar
Traub, RJ et al. (2008) PCR-based coprodiagnostic tools reveal dogs as reservoirs of zoonotic ancylostomiasis caused by Ancylostoma ceylanicum in temple communities in Bangkok. Veterinary Parasitology 155, 6773.Google Scholar
Udonsi, JK and Atata, G (1987) Necator americanus: temperature, pH, light, and larval development, longevity, and desiccation tolerance. Experimental Parasitology 63, 136142.Google Scholar
Verster, AJ (1965) Review of Echinococcus species in South Africa. Onderstepoort Journal of Veterinary Research 32, 7118.Google Scholar
Wachira, TM et al. (1993) Intestinal helminths of public health importance in dogs in Nairobi. East African Medical Journal 70, 617619.Google Scholar
Werneck, JS et al. (2007) Mites in clinical stool specimens: potential misidentification as helminth eggs. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 11541156.Google Scholar
Ziem, JB et al. (2006) Distribution and clustering of Oesophagostomum bifurcum and hookworm infections in northern Ghana. Parasitology 132, 525534.Google Scholar
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