Skip to main content Accessibility help
×
Home
Hostname: page-component-79b67bcb76-ncjtf Total loading time: 0.362 Render date: 2021-05-15T18:26:18.053Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": false, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true }

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
Corresponding
E-mail address:

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 

Access options

Get access to the full version of this content by using one of the access options below.

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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Bouchaud, O et al. (2000) Cutaneous larva migrans in travelers: a prospective study, with assessment of therapy with ivermectin. Clinical Infectious Diseases 31, 493498.CrossRefGoogle ScholarPubMed
Bowman, DD et al. (2010) Hookworms of dogs and cats as agents of cutaneous larva migrans. Trends in Parasitology 26, 162167.CrossRefGoogle ScholarPubMed
Bradbury, R and Traub, RJ (2016) Hookworm infection in Oceania. In Loukas, A (ed), Neglected Tropical Diseases - Oceania. Cham: Springer International Publishing, pp. 3368.CrossRefGoogle Scholar
Bradbury, R et al. (2017) Ancylostoma ceylanicum hookworm in the Solomon Islands. Emerging Infectious Diseases 23, 252257.CrossRefGoogle ScholarPubMed
Brooker, S, Clements, AC and Bundy, DA (2006) Global epidemiology, ecology and control of soil-transmitted helminth infections. Advances in Parasitology 62, 221261.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Caumes, E (2000) Treatment of cutaneous larva migrans. Clinical Infectious Diseases 30, 811814.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Crompton, DW (2001) Ascaris and ascariasis. Advances in Parasitology 48, 285375.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Del Giudice, P et al. (2002) Loeffler's syndrome and cutaneous larva migrans: a rare association. British Journal of Dermatology 147, 386388.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Gasser, RB et al. (1993) Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Research 21, 25252526.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Georgi, JR, LeJambre, LF and Ractliffe, LH (1969) Ancylostoma caninum burden in relationship to erythrocyte loss in dogs. Journal of Parasitology 55, 12051211.CrossRefGoogle ScholarPubMed
Hochedez, P and Caumes, E (2007) Hookworm-related cutaneous larva migrans. Journal of Travel Medicine 14, 326333.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Huttner, M et al. (2009) A survey of Echinococcus species in wild carnivores and livestock in East Africa. International Journal for Parasitology 39, 12691276.CrossRefGoogle ScholarPubMed
Inpankaew, T et al. (2014) High prevalence of Ancylostoma ceylanicum hookworm infections in humans, Cambodia, 2012. Emerging Infectious Diseases 20, 976982.CrossRefGoogle ScholarPubMed
Jelinek, T et al. (1994) Cutaneous larva migrans in travelers: synopsis of histories, symptoms, and treatment of 98 patients. Clinical Infectious Diseases 19, 10621066.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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 ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Kagendo, D et al. (2014) A survey for Echinococcus spp. of carnivores in six wildlife conservation areas in Kenya. Parasitology International 63, 604611.CrossRefGoogle ScholarPubMed
Kelkar, R (2007) Cutaneous larva migrans in England: a case in a returning traveller. Journal of Emergency Medicine 24, 678.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Landmann, JK and Prociv, P (2003) Experimental human infection with the dog hookworm, Ancylostoma caninum. Medical Journal of Australia 178, 6971.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Lindsay, DS et al. (1997) Mechanical transmission of Toxoplasma gondii oocysts by dogs. Veterinary Parasitology 73, 2733.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Mahdy, MA et al. (2012) Prevalence and zoonotic potential of canine hookworms in Malaysia. Parasite & Vectors 5, 88.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Miller, TA (1968) Pathogenesis and immunity in hookworm infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 62, 473489.CrossRefGoogle ScholarPubMed
Miller, TA (1970) Studies on the incidence of hookworm infection in East Africa. East African Medical Journal 47, 354363.Google ScholarPubMed
Mudenda, NB et al. (2012) Modelling the ecological niche of hookworm in Brazil based on climate. Geospatial Health 6, S111123.CrossRefGoogle ScholarPubMed
Mulinge, E et al. (2018) Molecular characterization of Echinococcus species in dogs from four regions of Kenya. Veterinary Parasitology 255, 4957.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Nijsse, R et al. (2014) Coprophagy in dogs interferes in the diagnosis of parasitic infections by faecal examination. Veterinary Parasitology 204, 304309.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Pullan, RL and Brooker, SJ (2012) The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasite & Vectors 5, 81.CrossRefGoogle ScholarPubMed
Repetto, SA et al. (2013) An improved DNA isolation technique for PCR detection of Strongyloides stercoralis in stool samples. Acta Tropica 126, 110114.CrossRefGoogle ScholarPubMed
Rinaldi, L et al. (2006) Canine faecal contamination and parasitic risk in the city of Naples (southern Italy). BMC Veterinary Research 2, 29.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Schaub, N, Perruchoud, AP and Buechner, S (2002) Cutaneous larva migrans associated with Loffler's syndrome. Dermatology 205, 207209.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Sowemimo, OA (2009) The prevalence and intensity of gastrointestinal parasites of dogs in Ile-Ife, Nigeria. Journal of Helminthology 83, 2731.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Traub, RJ (2013) Ancylostoma ceylanicum, a re-emerging but neglected parasitic zoonosis. International Journal for Parasitology 43, 10091015.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Udonsi, JK and Atata, G (1987) Necator americanus: temperature, pH, light, and larval development, longevity, and desiccation tolerance. Experimental Parasitology 63, 136142.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Ziem, JB et al. (2006) Distribution and clustering of Oesophagostomum bifurcum and hookworm infections in northern Ghana. Parasitology 132, 525534.CrossRefGoogle ScholarPubMed
Supplementary material: File

Mulinge et al. supplementary material

Mulinge et al. supplementary material 1

Download Mulinge et al. supplementary material(File)
File 46 KB

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Molecular identification of zoonotic hookworms in dogs from four counties of Kenya
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Molecular identification of zoonotic hookworms in dogs from four counties of Kenya
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Molecular identification of zoonotic hookworms in dogs from four counties of Kenya
Available formats
×
×

Reply to: Submit a response


Your details


Conflicting interests

Do you have any conflicting interests? *