Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-26T19:44:23.620Z Has data issue: false hasContentIssue false
  • English
  • Français

A survey of intestinal helminths in domestic dogs in a human–animal–environmental interface: the Oloisukut Conservancy, Narok County, Kenya

Published online by Cambridge University Press:  13 October 2021

E. Mulinge Open the ORCID record for E. Mulinge [Opens in a new window] ,
E. Zeyhle ,
J. Mpario ,
M. Mugo ,
L. Nungari ,
B. Ngugi ,
B. Sankale ,
P. Gathura ,
J. Magambo  and
M. Kachani
E. Mulinge*
Affiliation:
Kenya Medical Research Institute, Nairobi00200, Kenya
E. Zeyhle
Affiliation:
Meru University of Science and Technology, Meru60200, Kenya
J. Mpario
Affiliation:
Oloisukut Conservancy, Narok20500, Kenya
M. Mugo
Affiliation:
Kenya Medical Research Institute, Nairobi00200, Kenya
L. Nungari
Affiliation:
Kenya Medical Research Institute, Nairobi00200, Kenya
B. Ngugi
Affiliation:
Kenya Medical Research Institute, Nairobi00200, Kenya
B. Sankale
Affiliation:
Oloisukut Conservancy, Narok20500, Kenya
P. Gathura
Affiliation:
University of Nairobi, Nairobi00100, Kenya
J. Magambo
Affiliation:
Meru University of Science and Technology, Meru60200, Kenya
M. Kachani
Affiliation:
Western University of Health Sciences, Pomona, CA91766-1854, USA
*
Author for correspondence: E. Mulinge, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Dogs living in a domestic–wildlife interface can serve as reservoirs and sentinels of parasites shared among humans, domestic animals and wildlife. In Kenya, the epidemiology of intestinal parasites of dogs and their role as reservoirs of zoonoses is poorly understood, especially in domestic–wildlife interfaces. This study aimed to determine the occurrence of intestinal helminths in domestic dogs in the Oloisukut Conservancy. One hundred dog faecal samples were collected per rectum and examined microscopically following zinc chloride flotation and formal-ether concentration techniques. Genotyping of helminths was achieved by nested polymerase chain reaction of NADH dehydrogenase subunit 1, cytochrome oxidase 1 and partial sequencing. Nine genera were detected by microscopy in 65 (65%) dog faecal samples from 54/76 (71.05%) households. The most frequent helminths were hookworm (39%), Spirometra spp. (17%), taeniids (13%), Toxocara spp. (10%), Trichuris spp. (10%), Spirocerca lupi (5%), Physaloptera spp. (2%), Dipylidium caninum (1%) and Strongyloides spp. (1%). Ancylostoma caninum was the only hookworm species detected in dogs, while Taenia serialis and Taenia madoquae were detected in four and one faecal samples, respectively. This study reports for the first time the molecular detection of the cestodes Spirometra theileri, D. caninum and Mesocestoides sp. in dogs in Kenya. The presence of zoonotic helminths in dogs indicates that the residents of this conservancy are exposed to public health risks. The helminths reported here confirm the interaction of domestic dogs with wildlife. An integrated control programme involving the medical, veterinary and wildlife conservation professionals is needed to avert transmission of infectious diseases to humans, domestic animals and wildlife.

Keywords

Intestinal helminthsdogszoonosesOne HealthOloisukut ConservancyKenya
Type
Research Paper
Information
Journal of Helminthology , Volume 95 , 2021 , e59
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acosta-Jamett, G, Chalmers, WS, Cunningham, AA, Cleaveland, S, Handel, IG and Bronsvoort, BM (2011) Urban domestic dog populations as a source of canine distemper virus for wild carnivores in the Coquimbo region of Chile. Veterinary Microbiology 152, 247–257.CrossRefGoogle Scholar
Alexander, KA and Appel, MJ (1994) African wild dogs (Lycaon pictus) endangered by a canine distemper epizootic among domestic dogs near the Masai Mara National Reserve, Kenya. Journal of Wildlife Diseases 30, 481–485.CrossRefGoogle ScholarPubMed
Altschul, SF, Madden, TL, Schaffer, AA, Zhang, J, Zhang, Z, Miller, W and Lipman, DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.CrossRefGoogle ScholarPubMed
Anderson, RC, Chabaud, AG and Willmott, S (2009) Keys to the nematode parasites of vertebrates: archival volume. Wallingford, UK, CABI.CrossRefGoogle Scholar
Boubaker, G, Macchiaroli, N, Prada, L, et al. (2013) A multiplex PCR for the simultaneous detection and genotyping of the Echinococcus granulosus complex. PLOS Neglected Tropical Diseases 7, e2017.CrossRefGoogle ScholarPubMed
Boufana, BS, Campos-Ponce, M, Naidich, A, et al. (2008) Evaluation of three PCR assays for the identification of the sheep strain (genotype 1) of Echinococcus granulosus in canid feces and parasite tissues. American Journal of Tropical Medicine and Hygiene 78, 777–783.CrossRefGoogle ScholarPubMed
Bowman, DD (2014) Georgis’ parasitology for veterinarians. Elsevier, St. Louis, Missouri. Vol 10.Google Scholar
Bowman, DD, Montgomery, SP, Zajac, AM, Eberhard, ML and Kazacos, KR (2010) Hookworms of dogs and cats as agents of cutaneous larva migrans. Trends in Parasitology 26, 162–167.CrossRefGoogle ScholarPubMed
Bowser, NH and Anderson, NE (2018) Dogs (Canis familiaris) as sentinels for human infectious disease and application to Canadian populations: a systematic review. Veterinary Science 5, 83.CrossRefGoogle ScholarPubMed
Boyce, W, Shender, L, Schultz, L, et al. (2011) Survival analysis of dogs diagnosed with canine peritoneal larval cestodiasis (Mesocestoides spp.). Veterinary Parasitology 180, 256–261.CrossRefGoogle Scholar
Brodey, RS, Thomson, RG, Sayer, PD and Eugster, B (1977) Spiroceca lupi infection in dogs in Kenya. Veterinary Parasitology 3, 49–59.CrossRefGoogle Scholar
Buishi, I, Njoroge, E, Zeyhle, E, Rogan, MT and Craig, PS (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 and Parasitology 100, 601–610.CrossRefGoogle Scholar
Cheesbrough, M (2009) District laboratory practice in tropical countries. Part 1. 2nd edn. Cambridge, University Press Cambridge.Google Scholar
Cleaveland, S, Appel, MG, Chalmers, WS, Chillingworth, C, Kaare, M and Dye, C (2000) Serological and demographic evidence for domestic dogs as a source of canine distemper virus infection for Serengeti wildlife. Veterinary Microbiology 72, 217–227.CrossRefGoogle ScholarPubMed
Cleaveland, S, Thumbi, SM, Sambo, M, Lugelo, A, Lushasi, K, Hampson, K and Lankester, F (2018) Proof of concept of mass dog vaccination for the control and elimination of canine rabies. Revue Scientifique et Technique (International Office of Epizootics) 37, 559–568.Google ScholarPubMed
Craig, P, Mastin, A, van Kesteren, F and Boufana, B (2015) Echinococcus granulosus: epidemiology and state-of-the-art of diagnostics in animals. Veterinary Parasitology 213, 132–148.CrossRefGoogle ScholarPubMed
Dado, D, Izquierdo, F, Vera, O, et al. (2012) Detection of zoonotic intestinal parasites in public parks of Spain. Potential epidemiological role of microsporidia. Zoonoses and Public Health 59, 23–28.CrossRefGoogle ScholarPubMed
Dantas-Torres, F, Ketzis, J, Mihalca, AD, et al. (2020) TroCCAP recommendations for the diagnosis, prevention and treatment of parasitic infections in dogs and cats in the tropics. Veterinary Parasitology 283, 109–167.CrossRefGoogle ScholarPubMed
Deplazes, P, van Knapen, F, Schweiger, A and Overgaauw, PA (2011) Role of pet dogs and cats in the transmission of helminthic zoonoses in Europe, with a focus on echinococcosis and toxocarosis. Veterinary Parasitology 182, 41–53.CrossRefGoogle ScholarPubMed
Deplazes, P, Eichenberger, RM and Grimm, F (2019) Wildlife-transmitted Taenia and Versteria cysticercosis and coenurosis in humans and other primates. International Journal for Parasitology. Parasites and Wildlife 9, 342–358.CrossRefGoogle ScholarPubMed
Engh, AL, Nelson, KG, Peebles, R, Hernandez, AD, Hubbard, KK and Holekamp, KE (2003) Coprologic survey of parasites of spotted hyenas (Crocuta crocuta) in the Masai Mara National Reserve, Kenya. Journal of Wildlife Diseases 39, 224–227.CrossRefGoogle ScholarPubMed
Eom, KS, Park, H, Lee, D, et al. (2019) Identity of Spirometra theileri from a leopard (Panthera pardus) and spotted hyena (Crocuta crocuta) in Tanzania. Korean Journal of Parasitology 57, 639–645.CrossRefGoogle ScholarPubMed
Furtado, LFV, Dias, LTO, Rodrigues, TO, Silva, VJD, Oliveira, V and Rabelo, ÉML (2020) Egg genotyping reveals the possibility of patent Ancylostoma caninum infection in human intestine. Scientific Reports 10, 3006.CrossRefGoogle ScholarPubMed
George, S, Levecke, B, Kattula, D, Velusamy, V, Roy, S, Geldhof, P, Sarkar, R and Kang, G (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, 1205–1211.CrossRefGoogle ScholarPubMed
Hahn, NE, Proulx, D, Muruthi, PM, Alberts, S and Altmann, J (2003) Gastrointestinal parasites in free-ranging Kenyan baboons (Papio cynocephalus and P. anubis). International Journal of Primatology 24, 271–279.CrossRefGoogle Scholar
Holland, CV (2017) Knowledge gaps in the epidemiology of Toxocara: the enigma remains. Parasitology 144, 81–94.CrossRefGoogle ScholarPubMed
Jones, A, Allsopp, BA, Macpherson, CNL and Allsopp, MTEP (1988) The identity, life-cycle and isoenzyme characteristics of Taenia madoquae (Pellegrini, 1950) n. comb. from silver-backed jackal (Canis mesomelas Schreber, 1775) in east Africa. Systematic Parasitology 11, 31–38.CrossRefGoogle Scholar
Kagira, J and Kanyari, P (2000) Parasitic diseases as causes of mortality in dogs in Kenya. A retrospective study of 351 cases (1984–1998). Israel Journal of Veterinary Medicine 56, 11–99.Google Scholar
Karamon, J, Dabrowska, J, Kochanowski, M, Samorek-Pierog, M, Sroka, J, Rozycki, M, Bilska-Zajac, E, Zdybel, J and Cencek, T (2018) Prevalence of intestinal helminths of red foxes (Vulpes vulpes) in central Europe (Poland): a significant zoonotic threat. Parasites & Vectors 11, 436.Google ScholarPubMed
Kenny, JV, MacCabe, RJ, Smith, HV and Holland, C (1995) Serological evidence for the presence of toxocariasis in the Turkana District of Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 377–378.CrossRefGoogle ScholarPubMed
Lillis, WG (1967) Helminth survey of dogs and cats in New Jersey. Journal of Parasitology 53, 1082–1084.CrossRefGoogle ScholarPubMed
Lindsay, DS, Dubey, JP and Blagburn, BL (1997) Biology of Isospora spp. from humans, nonhuman primates, and domestic animals. Clinical Microbiology Reviews 10, 19–34.CrossRefGoogle ScholarPubMed
Liu, CN, Lou, ZZ, Li, L, et al. (2015) Discrimination between E. granulosus sensu stricto, E. multilocularis and E. shiquicus using a multiplex PCR assay. PLOS Neglected Tropical Diseases 9, e0004084.CrossRefGoogle Scholar
Loos-Frank, B (1991) One or two intermediate hosts in the life cycle of Mesocestoides (Cyclophyllidea, Mesocestoididae)? Parasitology Research 77, 726–728.CrossRefGoogle ScholarPubMed
Løvschal, M, Håkonsson, DD and Amoke, I (2019) Are goats the new elephants in the room? Changing land-use strategies in Greater Mara, Kenya. Land Use Policy 80, 395–399.CrossRefGoogle Scholar
Ma, G, Holland, CV, Wang, T, Hofmann, A, Fan, CK, Maizels, RM, Hotez, PJ and Gasser, RB (2018) Human toxocariasis. Lancet Infectious Diseases 18, e14–e24.CrossRefGoogle ScholarPubMed
Macpherson, CN (2013) The epidemiology and public health importance of toxocariasis: a zoonosis of global importance. International Journal for Parasitology 43, 999–1008.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, 219–222.CrossRefGoogle ScholarPubMed
Meloni, BP, Thompson, RC, Hopkins, RM, Reynoldson, JA and Gracey, M (1993) The prevalence of Giardia and other intestinal parasites in children, dogs and cats from aboriginal communities in the Kimberley. Medical Journal of Australia 158, 157–159.CrossRefGoogle ScholarPubMed
Ministry of Health, Kenya (MOH K) (2016) Report for the medical reconnaissance visit to Narok County following an increase in Sparganosis cases. Nairobi. pp. 1–21.Google Scholar
Mulinge, E (2020) Molecular epidemiology of Echinococcus and Taenia species in dogs from cystic echinococcosis endemic areas of Kenya. PhD thesis, University of Nairobi, Nairobi, Kenya. 209 pp.Google Scholar
Mulinge, E, Magambo, J, Odongo, D, et al. (2018) Molecular characterization of Echinococcus species in dogs from four regions of Kenya. Veterinary Parasitology 255, 49–57.CrossRefGoogle ScholarPubMed
Mulinge, E, Njenga, SM, Odongo, D, et al. (2019) Molecular identification of zoonotic hookworms in dogs from four counties of Kenya. Journal of Helminthology 94, e43.CrossRefGoogle ScholarPubMed
Mulinge, E, Odongo, D, Magambo, J, et al. (2020) Diversity of Taenia and Hydatigera (Cestoda: Taeniidae) in domestic dogs in Kenya. Parasitology Research 119, 2863–2875.CrossRefGoogle ScholarPubMed
Munyua, PM, Njenga, MK, Osoro, EM, et al. (2019) Successes and challenges of the One Health approach in Kenya over the last decade. BMC Public Health 19, 465.CrossRefGoogle ScholarPubMed
Murray, M (1968) Incidence and pathology of Spirocerca lupi in Kenya. Journal of Comparative Pathology 78, 401–405.CrossRefGoogle ScholarPubMed
Nakao, M, Lavikainen, A, Iwaki, T, Haukisalmi, V, Konyaev, S, Oku, Y, Okamoto, M and Ito, A (2013) Molecular phylogeny of the genus Taenia (Cestoda: Taeniidae): proposals for the resurrection of Hydatigera Lamarck, 1816 and the creation of a new genus Versteria. International Journal for Parasitology 43, 427–437.CrossRefGoogle ScholarPubMed
Nelson, GS, Pester, FR and Rickman, R (1965) The significance of wild animals in the transmission of cestodes of medical importance in Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 59, 507–524.CrossRefGoogle ScholarPubMed
Ngcamphalala, P, Lamb, J and Mukaratirwa, S (2019) Molecular identification of hookworm isolates from stray dogs, humans and selected wildlife from South Africa. Journal of Helminthology 94, e39.CrossRefGoogle ScholarPubMed
Nthiwa, D, Alonso, S, Odongo, D, Kenya, E and Bett, B (2019) A participatory epidemiological study of major cattle diseases amongst Maasai pastoralists living in wildlife-livestock interfaces in Maasai Mara, Kenya. Tropical Animal Health and Production 51, 1097–1103.CrossRefGoogle Scholar
Nyambura Njuguna, A, Kagira, JM, Muturi Karanja, S, Ngotho, M, Mutharia, L and Wangari Maina, N (2017) Prevalence of Toxoplasma gondii and other gastrointestinal parasites in domestic cats from households in Thika region, Kenya. BioMed Research International 2017, 7615810.CrossRefGoogle Scholar
Otranto, D and Deplazes, P (2019) Zoonotic nematodes of wild carnivores. International Journal for Parasitology. Parasites and Wildlife 9, 370–383.CrossRefGoogle ScholarPubMed
Pullan, RL, Smith, JL, Jasrasaria, R and Brooker, SJ (2014) Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasites & Vectors 7, 37.CrossRefGoogle ScholarPubMed
Roelke-Parker, ME, Munson, L, Packer, C, et al. (1996) A canine distemper virus epidemic in Serengeti lions (Panthera leo). Nature 379, 441–445.CrossRefGoogle Scholar
Sarvi, S, Daryani, A, Sharif, M, Rahimi, MT, Kohansal, MH, Mirshafiee, S, Siyadatpanah, A, Hosseini, SA and Gholami, S (2018) Zoonotic intestinal parasites of carnivores: a systematic review in Iran. Veterinary World 11, 58–65.CrossRefGoogle ScholarPubMed
Schmid, H and Watschinger, H (1972) Sparganosis in the Masailand. Acta Tropica 29, 218–230.Google ScholarPubMed
Shalaby, HA, Abdel-Shafy, S and Derbala, AA (2010) The role of dogs in transmission of Ascaris lumbricoides for humans. Parasitology Research 106, 1021–1026.CrossRefGoogle ScholarPubMed
Soulsby, EJL (1968) Helminths, arthropods and protozoa of domesticated animals. London, Bailliėre, Tindall and Cassell, pp 824.Google Scholar
Sparkes, J, Fleming, PJ, Ballard, G, Scott-Orr, H, Durr, S and Ward, MP (2015) Canine rabies in Australia: a review of preparedness and research needs. Zoonoses and Public Health 62, 237–253.CrossRefGoogle ScholarPubMed
Stefanić, S, Shaikenov, BS, Deplazes, P, Dinkel, A, Torgerson, PR and Mathis, A (2004) Polymerase chain reaction for detection of patent infections of Echinococcus granulosus (‘sheep strain’) in naturally infected dogs. Parasitology Research 92, 347–351.CrossRefGoogle Scholar
Szell, Z, Tolnai, Z and Sreter, T (2015) Environmental determinants of the spatial distribution of Mesocestoides spp. and sensitivity of flotation method for the diagnosis of mesocestoidosis. Veterinary Parasitology 212, 427–430.CrossRefGoogle Scholar
Thienpont, D, Rochette, F and Vanparijs, OFJ (1986) Diagnosing helminthiasis by coprological examination. Beerse, Belgium, Janssen Research Foundation.Google Scholar
Trachsel, D, Deplazes, P and Mathis, A (2007) Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134, 911–920.CrossRefGoogle ScholarPubMed
Traub, RJ, Robertson, ID, Irwin, P, Mencke, N and Thompson, RC (2004) Application of a species-specific PCR-RFLP to identify Ancylostoma eggs directly from canine faeces. Veterinary Parasitology 123, 245–255.CrossRefGoogle ScholarPubMed
Wachira, TM, Sattran, M, Zeyhle, E and Njenga, MK (1993) Intestinal helminths of public health importance in dogs in Nairobi. East African Medical Journal 70, 617–619.Google ScholarPubMed
Wandera, J (1976) Further observations on canine spirocercosis in Kenya. Veterinary Record 99, 348–351.CrossRefGoogle ScholarPubMed
Zhang, L, Hu, M, Jones, A, Allsopp, BA, Beveridge, I, Schindler, AR and Gasser, RB (2007) Characterization of Taenia madoquae and Taenia regis from carnivores in Kenya using genetic markers in nuclear and mitochondrial DNA, and their relationships with other selected taeniids. Molecular and Cellular Probes 21, 379–385.CrossRefGoogle ScholarPubMed