Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
권호 표지
DOI QR코드

DOI QR Code

Genotypes of Echinococcus Species from Cattle in Tanzania

  • Bia, Mohammed Mebarek (Department of Parasitology, Parasitology Research Center and International Parasite Resource Bank, Chungbuk National University, School of Medicine) ;
  • Choe, Seongjun (Department of Parasitology, Parasitology Research Center and International Parasite Resource Bank, Chungbuk National University, School of Medicine) ;
  • Ndosi, Barakaeli Abdieli (Department of Parasitology, Parasitology Research Center and International Parasite Resource Bank, Chungbuk National University, School of Medicine) ;
  • Park, Hansol (Department of Parasitology, Parasitology Research Center and International Parasite Resource Bank, Chungbuk National University, School of Medicine) ;
  • Kang, Yeseul (Department of Parasitology, Parasitology Research Center and International Parasite Resource Bank, Chungbuk National University, School of Medicine) ;
  • Eamudomkarn, Chatanun (Department of Parasitology, Parasitology Research Center and International Parasite Resource Bank, Chungbuk National University, School of Medicine) ;
  • Nath, Tilak Chandra (Department of Parasitology, Parasitology Research Center and International Parasite Resource Bank, Chungbuk National University, School of Medicine) ;
  • Kim, Sunmin (Department of Parasitology, Parasitology Research Center and International Parasite Resource Bank, Chungbuk National University, School of Medicine) ;
  • Jeon, Hyeong-Kyu (Department of Parasitology, Parasitology Research Center and International Parasite Resource Bank, Chungbuk National University, School of Medicine) ;
  • Lee, Dongmin (Department of Parasitology, Parasitology Research Center and International Parasite Resource Bank, Chungbuk National University, School of Medicine) ;
  • Eom, Keeseon S. (Department of Parasitology, Parasitology Research Center and International Parasite Resource Bank, Chungbuk National University, School of Medicine)
  • Received : 2021.01.24
  • Accepted : 2021.10.08
  • Published : 2021.10.31
Download PDF
⟨ Previous Next ⟩

Abstract

Cystic echinococcosis is a zoonotic parasitic disease caused by Echinococcus species. Tanzania is one of the endemic countries with cystic echinococcosis. This study focussed on identifying genotypes of Echinococcus spp. in Tanzania. We collected 7 cysts from cattle in Mwanza municipal (n=4) and Loliondo district (n=3). The cysts from Mwanza were all E. ortleppi and fertile. In contrast, the cysts from Loliondo were all E. granulosus sensu stricto and sterile. Two from the 4 cysts were a new haplotype of E. ortleppi (G5). These results can improve the preventive and control programs for humans and livestock in Tanzania. To our knowledge, this study is considered the first to identify the genotype and haplotype of Echinococcus spp. in Tanzania.

Keywords

Acknowledgement

This research was funded by the National Research Foundation (NRF) with the project "Research life and the Evolutionary ecology of pathogenic Neodermata and construction of a database for species information" (Grant No. 2020R1I1A3A04037914) and the program of Korea Research Fellowship (Grant No. 2020H1D3A1A02081496).

References

  1. Wen H, Vuitton L, Tuxun T, Li J, Vuitton DA, Zhang W, McManus DP. Echinococcosis: advances in the 21st century. Clin Microbiol Rev 2019; 32: e00075-18. https://doi.org/10.1128/CMR.00075-18
  2. Bowles J, Blair D, McManus DP. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 1992; 54: 165-173. https://doi.org/10.1016/0166-6851(92)90109-W
  3. Romig T, Ebi D, Wassermann M. Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Vet Parasitol 2015; 213: 76-84. https://doi.org/10.1016/j.vetpar.2015.07.035
  4. Kinkar L, Laurimae T, Balkaya I, Casulli A, Zait H, Irshadullah M, Sharbatkhori M, Mirhendi H, Rostami-Nejad M, Ponce-Gordo F, Rehbein S, Kia EB, Simsek S, Snabel V, Umhang G, Varcasia A, Saarma U. Genetic diversity and phylogeography of the elusive, but epidemiologically important Echinococcus granulosus sensu stricto genotype G3. Parasitology 2018; 145: 1613-1622. https://doi.org/10.1017/S0031182018000549
  5. Laurimae T, Kinkar L, Romig T, Omer RA, Casulli A, Umhang G, Gasser RB, Jabbar A, Sharbatkhori M, Mirhendi H, Ponce-Gordo F, Lazzarini LE, Soriano SV, Varcasia A, Rostami Nejad M, Andresiuk V, Maravilla P, Gonzalez LM, Dybicz M, Gawor J, Sarkunas M, Snabel V, Kuzmina T, Saarma U. The benefits of analysing complete mitochondrial genomes: Deep insights into the phylogeny and population structure of Echinococcus granulosus sensu lato genotypes G6 and G7. Infect Genet Evol 2018; 64: 85-94. https://doi.org/10.1016/j.meegid.2018.06.016
  6. Yanagida T, Mohammadzadeh T, Kamhawi S, Nakao M, Sadjjadi SM, Hijjawi N, Abdel-Hafez SK, Sako Y, Okamoto M, Ito A. Genetic polymorphisms of Echinococcus granulosus sensu stricto in the Middle East. Parasitol Int 2012; 61: 599-603. https://doi.org/10.1016/j.parint.2012.05.014
  7. Thompson RC, Lymbery AJ. Echinococcus and Hydatid Disease. Wallingford, USA. CAB International 1995. http://researchrepository.murdoch.edu.au/id/eprint/13362
  8. Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS. WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern. 2002. Paris, France. World Organization for Animal Health (Office international des epizooties). https://apps.who.int/iris/bitstream/handle/10665/42427/929044522X.pdf
  9. Ernest E, Nonga HE, Kassuku AA, Kazwala RR. Hydatidosis of slaughtered animals in Ngorongoro district of Arusha region, Tanzania. Trop Anim Health Prod 2009; 41: 1179-1185. https://doi.org/10.1007/s11250-008-9298-z
  10. Macpherson CN, Craig PS, Romig T, Zeyhle E, Watsghinger H. Observations on human echinococcosis (hydatidosis) and evaluation of transmission factors in the Maasai of northern Tanzania. Ann Trop Med Parasitol 1989; 83: 489-497. https://doi.org/10.1080/00034983.1989.11812377
  11. Jusabani AM, Kalambo CF, Jusabani M, Surani S. Myocardial echinococcosis: rare manifestation of a common parasitic disease in northern Tanzania. Cureus 2020; 12: e8681. https://doi.org/10.7759/cureus.8681
  12. Ernest E, Nonga HE, Kynsieri N, Cleaveland S. A retrospective survey of human hydatidosis based on hospital records during the period 1990-2003 in Ngorongoro, Tanzania. Zoonoses Public Health. 2010 Dec; 57: 124-129. https://doi.org/10.1111/j.1863-2378.2009.01297.x
  13. Galindo M, Gonzalez MJ, Galanti N. Echinococcus granulosus protoscolex formation in natural infections. Biol Res 2002; 35: 365-371. http://dx.doi.org/10.4067/S0716-97602002000300011
  14. Cielecka D, Salamatin R, and Garbacewicz A. Usage of the Hoyer's medium for diagnostics and morphological studies of some parasites. Wiad Parazytol 2009; 55: 265-270 (in Polish). https://europepmc.org/article/med/19856844
  15. Gordo FP and Bandera CC. Differentiation of Spanish strains of Echinococcus granulosus using larval rostellar hook morphometry. Int J Parasitol 1997; 27: 41-49. https://doi.org/10.1016/S0020-7519(96)00173-7
  16. Arbabi M, Pirestani M, Delavari M, Hooshyar H, Abdoli A, Sarvi S. Molecular and morphological characterizations of Echinococcus granulosus from human and animal isolates in Kashan, Markazi Province, Iran. Iran J Parasitol 2017; 12: 177-187. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5527027/
  17. Said IM, Abdel-Hafez SK, Al-Yaman FM. Morphological variation of Echinococcus granulosus protoscoleces from hydatid cysts of human and various domestic animals in Jordan. Int J Parasitol 1988; 18: 1111-1114. https://doi.org/10.1016/0020-7519(88)90083-5
  18. Salamatin R, Kowal J, Nosal P, Kornas S, Cielecka D, Janczak D, Patkowski W, Gawor J, Kornyushin V, Golab E, Snabel V. Cystic echinococcosis in Poland: genetic variability and the first record of Echinococcus granulosus sensu stricto (G1 genotype) in the country. Parasitol Res 2017; 116: 3077-3085. https://doi.org/10.1007/s00436-017-5618-4
  19. Morgan JA, Blair D. Relative merits of nuclear ribosomal internal transcribed spacers and mitochondrial CO1 and ND1 genes for distinguishing among Echinostoma species (Trematoda). Parasitology 1998; 116: 289-297. https://doi.org/10.1017/S0031182097002217
  20. Olsen C, Qaadri K, Moir R, Kearse M, Buxton S, Cheung M. Geneious R7: A Bioinformatics Platform for Biologists. Newark, USA. Biomatters, Inc. 2014. https://www.eposters.net/pdfs/geneious-r7-a-bioinformatics-platform-for-biologists.pdf
  21. Jeon HK, Kim KH, Eom KS. Complete sequence of the mitochondrial genome of Taenia saginata: comparison with T. solium and T. asiatica. Parasitol Int 2007; 56: 243-246. https://doi.org/10.1016/j.parint.2007.04.001
  22. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30: 2725-2729. https://doi.org/10.1093/molbev/mst197
  23. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17: 368-376. https://doi.org/10.1007/BF01734359
  24. Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sanchez-Gracia A. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 2017; 34: 3299-3302. https://doi.org/10.1093/molbev/msx248
  25. Sharma M, Sehgal R, Fomda BA, Malhotra A, Malla N. Molecular characterization of Echinococcus granulosus cysts in north Indian patients: identification of G1, G3, G5 and G6 genotypes. PLoS Negl Trop Dis 2013; 7: e2262. https://doi.org/10.1371/journal.pntd.0002262
  26. Rojas CA, Ebi D, Gauci CG, Scheerlinck JP, Wassermann M, Jenkins DJ, Lightowlers MW, Romig T. Microdiversity of Echinococcus granulosus sensu stricto in Australia. Parasitology 2016; 143: 1026-1033. https://doi.org/10.1017/S0031182016000445
  27. Barazesh A, Sarkari B, Sarisu G, Hami M, Mikaeili F, Aydin A, Ekici A, Ebrahimi S. Comparative genotyping of Echinococcus granulosus infecting livestock in Turkey and Iran. Turkiye Parasitol Derg 2019; 43: 123-129. https://doi.org/10.4274/tpd.galenos.2019.6117
  28. Nakao M, Li T, Han X, Ma X, Xiao N, Qiu J, Wang H, Yanagida T, Mamuti W, Wen H, Moro PL, Giraudoux P, Craig PS, Ito A. Genetic polymorphisms of Echinococcus tapeworms in China as determined by mitochondrial and nuclear DNA sequences. Int J Parasitol 2010; 40: 379-385. https://doi.org/10.1016/j.ijpara.2009.09.006
  29. Nakao M, Yokoyama N, Sako Y, Fukunaga M, Ito A. The complete mitochondrial DNA sequence of the cestode Echinococcus multilocularis (Cyclophyllidea: Taeniidae). Mitochondrion 2002; 1: 497-509. https://doi.org/10.1016/S1567-7249(02)00040-5
  30. Nakao M, McManus DP, Schantz PM, Craig PS, Ito A. A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 2007; 134: 713-722. https://doi.org/10.1017/S0031182006001934
  31. Le TH, Pearson MS, Blair D, Dai N, Zhang LH, McManus DP. Complete mitochondrial genomes confirm the distinctiveness of the horse-dog and sheep-dog strains of Echinococcus granulosus. Parasitology 2002; 124: 97-112. https://doi.org/10.1017/S0031182001008976
  32. Denk D, Boufana B, Masters NJ, Stidworthy MF. Fatal echinococcosis in three lemurs in the United Kingdom-a case series. Vet Parasitol 2016; 218: 10-14. https://doi.org/10.1016/j.vetpar.2015.12.033
  33. Kinkar L, Laurimae T, Sharbatkhori M, Mirhendi H, Kia EB, Ponce-Gordo F, Andresiuk V, Simsek S, Lavikainen A, Irshadullah M, Umhang G, Oudni-M'rad M, Acosta-Jamett G, Rehbein S, Saarma U. New mitogenome and nuclear evidence on the phylogeny and taxonomy of the highly zoonotic tapeworm Echinococcus granulosus sensu stricto. Infect Genet Evol 2017; 52: 52-58. https://doi.org/10.1016/j.meegid.2017.04.023
  34. Hodzic A, Alic A, Supic J, Skapur V, Duscher GG. Echinococcus ortleppi, the cattle strain in a crested porcupine (Hystrix cristata): a new host record. Vet Parasitol 2018; 256: 32-34. https://doi.org/10.1016/j.vetpar.2018.05.004
  35. Addy F, Wassermann M, Banda F, Mbaya H, Aschenborn J, Aschenborn O, Koskei P, Umhang G, DE LA Rue M, Elmahdi IE, Mackenstedt U, Kern P, Romig T. Genetic polymorphism and population structure of Echinococcus ortleppi. Parasitology 2017; 144: 450-458. https://doi.org/10.1017/S0031182016001840
  36. Miran MB, Kasuku AA, Swai ES. Prevalence of echinococcosis and Taenia hydatigena cysticercosis in slaughtered small ruminants at the livestock-wildlife interface areas of Ngorongoro, Tanzania. Vet world 2017; 10: 411-417. https://doi.org/10.14202/vetworld.2017.411-417
  37. Ngowi HA, Kassuku AA, Maeda GE, Boa ME, Willingham AL. A slaughter slab survey for extra-intestinal porcine helminth infections in northern Tanzania. Trop Anim Health Prod 2004; 36: 335-340. https://doi.org/10.1023/B:TROP.0000026663.07862.2a
  38. Terefe Y, Addy F, Alemu S, Mackenstedt U, Romig T, Wassermann M. Genetic characterization of Echinococcus species in eastern Ethiopia. Vet Parasitol Reg Stud Reports 2019; 17: 100302. https://doi.org/10.1016/j.vprsr.2019.100302
  39. Ohiolei JA, Li L, Ebhodaghe F, Yan HB, Isaac C, Bo XW, Fu BQ, Jia WZ. Prevalence and distribution of Echinococcus spp. in wild and domestic animals across Africa: a systematic review and meta-analysis. Transbound Emerg Dis 2020; 2345-2364. https://doi.org/10.1111/tbed.13571
  40. Amer S, Helal IB, Kamau E, Feng Y, Xiao L. Molecular characterization of Echinococcus granulosus sensu lato from farm animals in Egypt. PLoS One 2015; 10: e0118509. https://doi.org/10.1371/journal.pone.0118509
  41. Bardonnet K, Piarroux R, Dia L, Schneegans F, Beurdeley A, Godot V, Vuitton DA. Combined eco-epidemiological and molecular biology approaches to assess Echinococcus granulosus transmission to humans in Mauritania: occurrence of the 'camel' strain and human cystic echinococcosis. Trans R Soc Trop Med Hyg 2002; 96: 383-386. https://doi.org/10.1016/S0035-9203(02)90369-X
  42. Ohiolei JA, Yan HB, Li L, Magaji AA, Luka J, Zhu GQ, Isaac C, Odoya ME, Wu YT, Alvi MA, Muku RJ, Fu BQ, Jia WZ. Cystic echinococcosis in Nigeria: first insight into the genotypes of Echinococcus granulosus in animals. Parasites Vectors 2019; 12: 392. https:// doi.org/10.1186/s13071-019-3644-z
  43. Mogoye BK, Menezes CN, Wong ML, Stacey S, von Delft D, Wahlers K, Wassermann M, Romig T, Kern P, Grobusch MP, Frean J. First insights into species and genotypes of Echinococcus in South Africa. Vet Parasitol 2013; 196: 427-432. https://doi.org/10.1016/j.vetpar.2013.03.033
  44. Kamhawi S, Hijjawi N, Abu-Gazaleh A, Abbass M. Prevalence of hydatid cysts in livestock from five regions of Jordan. Ann Trop Med Parasitol 1995; 89: 621-629. https://doi.org/10.1080/00034983.1995.11812996