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Prevalence and genotyping of Echinococcus granulosus in sheep in Narok County, Kenya

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Abstract

Cystic echinococcosis (CE) is a zoonotic disease caused by the larval stage of Echinococcus granulosus species (sensu lato, s.l.). In East Africa, several species/strains occur in livestock, wildlife, and humans, but there is limited information on frequencies of infection by different genotypes in the various mammalian hosts. We have obtained data on E. granulosus infection prevalence in sheep sampled from abattoirs in Narok County, southern Kenya. We inspected carcasses for the presence of hydatid cysts in 180 sheep randomly selected in five sub-locations. The overall prevalence was 16.0% (144/900 animals), with the majority of cysts (50.7%) found in the liver, followed by the lungs (36.8%), while infections involving the liver and lungs were detected in 12.5% of the sheep. PCR–RFLP genotyping of the mitochondrial nad-1 gene in all the 343 cysts identified E. granulosus G1–G3 (sensu stricto, s.s.) as the only genotype. The majority of the cysts (62.1%) were fertile, and 35.2% were sterile, while 2.7% were calcified. Considering cyst fertility, 73.02% of lung cysts were fertile compared to 53.4% in liver cysts. Our data extends previous CE studies in livestock and indicates a high level of CE infection of sheep in Narok, with a predominance of E. granulosus s.s., which is highly pathogenic and commonly infects humans. Given the high fertility rates observed in the cysts, there is an urgent need to determine whether there is a significant incidence of human infection in Narok, and initiate “One Health” control measures.

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References

  • Addy F, Alakonya A, Wamae N, Magambo J, Mbae C, Mulinge E, Zeyhle E, Wassermann M, Kern P, Romig T (2012) Prevalence and diversity of cystic echinococcosis in livestock in Maasailand, Kenya. Parasitol Res 111:2289–2294

    Article  PubMed  Google Scholar 

  • Al-Khalidi NW (1998) Cystic echinococcus in sheep, goats and camels in shahat abattoir Aljabal, Libya. Proceedings of the third annual meeting for animal production under arid condition 1:143–149

  • Alvarez Rojas CA, Romig T, Lightowlers MW (2014) Echinococcus granulosus sensu lato genotypes infecting humans—review of current knowledge. Int J Parasitol Sitol 44:9–18

    Article  Google Scholar 

  • Bowles J, Blair D, McManus DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54:165–173

    Article  PubMed  CAS  Google Scholar 

  • Budke CM, Deplazes P, Torgerson PR (2006) Global socioeconomic impact of cystic echinococcosis. Emerg Infect Dis 12:296–303

    Article  PubMed  PubMed Central  Google Scholar 

  • Cardona GA, Carmena D (2013) A review of the global prevalence, molecular epidemiology and economics of cystic echinococcosis in production animals. Vet Parasitol 192:10–32

    Article  PubMed  Google Scholar 

  • Casulli A, Zeyhle E, Brunetti E, Pozio E, Meroni V, Genco F, Filice C (2010) Molecular evidence of the camel strain (G6 genotype) of Echinococcus granulosus in humans from Turkana, Kenya. Trans R Soc Trop Med Hyg 104:29–32

    Article  PubMed  CAS  Google Scholar 

  • Craig PS, McManus DP, Lightowlers MW, Chabalgoity JA, Garcia HH, Gavidia CM, Gilman RH, Gonzalez AE, Lorca M, Naquira C, Nieto A, Schantz PM (2007) Prevention and control of cystic echinococcosis. Lancet Infect Dis 7:385–394

    Article  PubMed  Google Scholar 

  • Dinkel A, Njoroge EM, Zimmermann A, Wälz M, Zeyhle E, Elmahdi IE, Mackenstedt U, Romig T (2004) A PCR system for detection of species and genotypes of the Echinococcus granulosus-complex, with reference to the epidemiological situation in eastern Africa. Int J Parasitol 34:645–653

    Article  PubMed  CAS  Google Scholar 

  • Eckert J, Deplazes P (2004) Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clin Microbiol Rev 17:107–135

    Article  PubMed  PubMed Central  Google Scholar 

  • Eckert J, Conraths FJ, Tackmann K (2000) Echinococcosis: an emerging or re-emerging zoonosis? Int J Parasitol 30:1283–1294

    Article  PubMed  CAS  Google Scholar 

  • EI-Ibrahim JH (2009) Prevalence of sheep hydatidosis in north west Bank-Palestine. MSc thesis, An-Najah National University

  • El-Berbri I, Ducrotoy MJ, Petavy AF, Fassifihri O, Shaw AP, Bouslikhane M, Boue F, Welburn SC, Dakkak A (2015) Knowledge, attitudes and practices with regard to the presence, transmission, impact, and control of cystic echinococcosis in Sidi Kacem Province, Morocco. Infect Dis Poverty 4:48

    Article  PubMed  PubMed Central  Google Scholar 

  • Froyd G (1960) The incidence of liver flukes (Fasciola gigantica) and hydatid cysts (Echinococcus granulosus) in Kenya cattle. J Parasitol 46:659–662

    Article  PubMed  CAS  Google Scholar 

  • Grosso G, Gruttadauria S, Biondi A, Marventano S, Mistretta A (2012) Worldwide epidemiology of liver hydatidosis including the Mediterranean area. World J Gastroenterol 18:1425–1437

    Article  PubMed  PubMed Central  Google Scholar 

  • Hüttner M, Romig T (2009) Echinococcus species in African wildlife. Parasitology 136:1089–1095

    Article  PubMed  Google Scholar 

  • Hüttner M, Nakao M, Wassermann T, Siefert L, Boomker JD, Dinkel A, Sako Y, Mackenstedt U, Romig T, Ito A (2008) Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion. Int J Parasitol 38:861–868

    Article  PubMed  CAS  Google Scholar 

  • Hüttner M, Siefert L, Mackenstedt U, Romig T (2009) A survey of Echinococcus species in wild carnivores and livestock in East Africa. Int J Parasitol 39:1269–1276

    Article  PubMed  Google Scholar 

  • Irshadullah M, Nizami WA, Macpherson CN (1989) Observations on the suitability and importance of the domestic intermediate hosts of Echinococcus granulosus in Uttah Pradesh. Indian J Helminthol 63:39–45

    Article  CAS  Google Scholar 

  • Kagendo D, Magambo J, Agola EL, Njenga SM, Zeyhle E, Mulinge E, Gitonga P, Mbae C, Muchiri E, Wassermann M, Kern P, Romig T (2014) A survey for Echinococcus spp. of carnivores in six wildlife conservation areas in Kenya. Parasitol Int 63:604–611

    Article  PubMed  CAS  Google Scholar 

  • Larrieu E, Mujica G, Gauci CG, Vizcaychipi K, Seleiman M, Herrero E, Labanchi JL, Araya D, Sepúlveda L, Grizmado C, Calabro A, Talmon G, Poggio TV, Crowley P, Cespedes G, Santillán G, García Cachau M, Lamberti R, Gino L, Donadeu M, Lightowlers MW (2015) Pilot field trial of the EG95 vaccine against ovine cystic echinococcosis in Rio Negro, Argentina: second study of impact. Plos Neglect Trop D 9(10):e0004134

    Article  CAS  Google Scholar 

  • Lavikainen A, Lehtinen MJ, Meri T, Hirvelä-Koski V, Meri S (2003) Molecular genetic characterization of the Fennoscandian cervid strain, a new genotypic group (G10) of Echinococcus granulosus. Parasitology 127:207–215

    Article  PubMed  CAS  Google Scholar 

  • Lightowlers MW (1996) Vaccination against cestode parasites. Int J Parasitol 26:819–824

    Article  PubMed  CAS  Google Scholar 

  • Lightowlers MW, Lawrence SB, Gauci CG, Young J, Ralston MJ, Maas D, Heath DD (1996) Vaccination against hydatidosis using a defined recombinant antigen. Parasite Immunol 18:457–462

    Article  PubMed  CAS  Google Scholar 

  • Lightowlers MW, Jensen O, Fernandez E, Iriarte JA, Woollard DJ, Gauci CG, Jenkins DJ, Heath DD (1999) Vaccination trials in Australia and Argentina confirm the effectiveness of the EG95 hydatid vaccine in sheep. Int J Parasitol 29:531–534

    Article  PubMed  CAS  Google Scholar 

  • Lightowlers MW, Flisser A, Gauci CG, Heath DD, Jensen O, Rolfe R (2000) Vaccination against cysticercosis and hydatid disease. Parasitol Today 16:191–196

    Article  PubMed  CAS  Google Scholar 

  • MacPherson CNL (1985) Epidemiology of hydatid disease in Kenya: a study of domestic intermediate hosts in Maasailand. Trans R Soc Trop Med Hyg 79:209–217

    Article  PubMed  CAS  Google Scholar 

  • Magambo J, Njoroge E, Zeyhle E (2006) Epidemiology and control of echinococcosis in sub-Saharan Africa. Parasitol Int 55:S193–S195

    Article  PubMed  Google Scholar 

  • Mbaya H, Magambo J, Njenga S, Zeyhle E, Mbae C, Mulinge E, Wassermann M, Kern P, Romig T (2014) Echinococcus spp. in Central Kenya: a different story. Parasitol Res 113:3789–3794

    Article  PubMed  CAS  Google Scholar 

  • McManus DP, Thompson RC (2003) Molecular epidemiology of cystic Echinococcus. Parasitology 127:S37–S51

    Article  PubMed  CAS  Google Scholar 

  • Moro P, Schantz PM (2009) Echinococcosis: a review. Int J Infect Dis 13:125–133

    Article  PubMed  CAS  Google Scholar 

  • Mutwiri T, Magambo J, Zeyhle E, Mkoji GM, Wamae CN, Mulinge E, Wassermann H, Kern P, Romig T (2013) Molecular characterisation of Echinococcus granulosus species/strains in human infections from Turkana, Kenya. East Afr Med J 90:235–240

    PubMed  CAS  Google Scholar 

  • Nakao M, Sako Y, Ito A (2003) Isolation of polymorphic microsatellite loci from the tapeworm Echinococcus multilocularis. Infect Genet Evol 3:159–163

    Article  PubMed  CAS  Google Scholar 

  • Njoroge EM, Mbithi PM, Gathuma JM, Wachira TM, Gathura PB, Magambo JK, Zeyhle E (2002) A study of cystic echinococcosis in slaughter animals in three selected areas of northern Turkana, Kenya. Vet Parasitol 104:85–91

    Article  PubMed  CAS  Google Scholar 

  • Omer RA, Dinkel A, Romig T, Mackensted U, Elnahas AA, Aradaib IE, Ahmed ME, Elmalik KH, Adam A (2010) A molecular survey of cystic echinococcosis in Sudan. Vet Parasitol 169:340–346

    Article  PubMed  CAS  Google Scholar 

  • Romig T, Omer RA, Zeyhle E, Hüttner M, Dinkel A, Siefert L, Elmahdi IE, Magambo J, Ocaido M, Menezes CN, Ahmed ME, Mbae C, Grobusch MP, Kern P (2011) Echinococcosis in sub-Saharan Africa: emerging complexity. Vet Parasitol 181:43–47

    Article  PubMed  CAS  Google Scholar 

  • Sadjjadi SM (2006) Present situation of echinococcosis in the Middle East and Arabic North Africa. Parasitol Int 55:S197–S202

    Article  PubMed  Google Scholar 

  • Scott JC, Stefaniak J, Pawlowski ZS, McManus DP (1997) Molecular genetic analysis of human cystic hydatid cases from Poland: identification of a new genotypic group (G9) of Echinococcus granulosus. Parasitology 114:37–43

    Article  PubMed  CAS  Google Scholar 

  • Thompson RC, McManus DP (2002) Towards a taxonomic revision of the genus Echinococcus. Trends Parasitol 18:452–457

    Article  PubMed  Google Scholar 

  • Tigre W, Deresa B, Haile A, Gabriël S, Victor B, Pelt JV, Devleesschauwer B, Vercruysse J, Dorny P (2016) Molecular characterization of Echinococcus granulosus s.l. cysts from cattle, camels, goats and pigs in Ethiopia. Vet Parasitol 215:17–21

    Article  PubMed  CAS  Google Scholar 

  • Torgerson PR, Heath DD (2003) Transmission dynamics and control options for Echinococcus granulosus. Parasitology 127(Suppl):S143–S158

    Article  PubMed  Google Scholar 

  • Torgerson PR, Ziadinov I, Aknazarov D, Nurgaziev R, Deplazes P (2009) Modelling the age variation of larval protoscoleces of Echinococcus granulosus in sheep. Int J Parasitol 39:1031–1035

    Article  PubMed  CAS  Google Scholar 

  • Toulah FH, El Shafei AA, Alsolami MN (2012) Prevalence of hydatidosis among slaughtered animals in Jeddah, Kingdom of Saudi Arabia. J Egypt Soc Parasitol 42:563–572

    Article  PubMed  Google Scholar 

  • Varcasia A, Canu S, Lightowlers MW, Scala A, Garippa G (2006) Molecular characterization of Echinococcus granulosus strains in Sardinia. Parasitol Res 98:273–277

    Article  PubMed  CAS  Google Scholar 

  • Varcasia A, Canu S, Kogkos A, Pipia AP, Scala A, Garippa G, Seimenis A (2007) Molecular characterization of Echinococcus granulosus in sheep and goats of Peloponnesus, Greece. Parasitol Res 101:1135–1139

    Article  PubMed  CAS  Google Scholar 

  • Wachira TM, Bowles J, Zeyhle E, McManus DP (1993) Molecular examination of the sympatry and distribution of sheep and camel strains of Echinococcus granulosus in Kenya. Am J Trop Med Hyg 48:473–479

    Article  PubMed  CAS  Google Scholar 

  • Wahlers K, Menezes CN, Wong ML, Zeyhle E, Ahmed ME, Ocaido M, Stijnis C, Romig T, Kern P, Grobusch MP (2012) Cystic echinococcosis in sub-Saharan Africa. Lancet Infect Dis 12:871–880

    Article  PubMed  Google Scholar 

  • WHO (2006) In: Maudlin I, Weber-Mosdorf S (eds) Control of zoonotic diseases. World Health Organization, Geneva

    Google Scholar 

  • WHO (2016a) http://www.who.int/mediacentre/factsheets/fs377/en/ Accessed 22 Nov 2017

  • WHO (2016b) Informal Working Group on Echinococcosis (IWGE), Geneva, Switzerland. http://www.who.int/neglected_diseases/events/WHO_informal_working_group_on_echinococcosis/en/ Accessed 22 Nov 2017

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Funding

The study was financially supported by the Deutsche Forschungsgemeinschaft (Cystic Echinococcosis in sub-Saharan Africa Research Initiative (CESSARi), DFG projects KE282/7-1, -8-1, RO3753/1-1, -2-1). David Odongo was a research fellow supported by the Biosciences eastern and central Africa (BecA-ILRI) which is implemented under the New Partnership for Africa’s Development (NEPAD), through funding from the Canadian International Development Agency (CIDA). We acknowledge the financial support provided to the Biosciences eastern and central Africa Hub at the International Livestock Research Institute (BecA-ILRI Hub) by the Australian Agency for International Development (AusAID) through a partnership between Australia’s Commonwealth Scientific and Industrial Research Organization (CSIRO) and the BecA-ILRI Hub, and by the Syngenta Foundation for Sustainable Agriculture (SFSA).

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Correspondence to D. O. Odongo.

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All applicable national and institutional guidelines for the care and use of animals were followed.

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The authors declare that they have no conflict of interest.

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Section Editor: Bruno Gottstein

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Odongo, D.O., Tiampati, C.M., Mulinge, E. et al. Prevalence and genotyping of Echinococcus granulosus in sheep in Narok County, Kenya. Parasitol Res 117, 2065–2073 (2018). https://doi.org/10.1007/s00436-018-5889-4

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