Original Scientific Article
Cystic echinococcosis in slaughtered cattle and sheep from North Macedonia
Ljubica Rashikj ,
Aleksandar Cvetkovikj * ,
Martin Nikolovski ,
Iskra Cvetkovikj ,
Jovana Stefanovska

Mac Vet Rev 2022; 45 (1): 35 - 41

10.2478/macvetrev-2022-0011

Received: 20 October 2021

Received in revised form: 02 December 2021

Accepted: 10 December 2021

Available Online First: 17 January 2022

Published on: 15 March 2022

Correspondence: Aleksandar Cvetkovikj, acvetkovic@fvm.ukim.edu.mk
PDF HTML

Abstract

Cystic echinococcosis is a cosmopolitan zoonotic infection, commonly seen in areas where livestock and dogs are kept together. The objective of this study was to investigate the prevalence of echinococcosis in slaughtered cattle and sheep in North Macedonia and to evaluate the location and fertility/sterility rates of the cysts. A total of 302 slaughtered animals were examined with visual inspection, palpation, and incision of the internal organs in order to detect cysts. Microscopic examination was carried out to determine the presence of protoscoleces. The overall prevalence of echinococcosis in slaughtered cattle and sheep was 60%. The presence of cysts increased with age in cattle. In both cattle and sheep, the most common affected organs were the liver and lungs infected with more than one cyst. The findings showed higher fertility rate in sheep which confirmed their role as the most important intermediate host. This study shows that North Macedonia is an endemic region, and serious control strategies should be implemented, with special emphasis on safety disposal of infected organs and anthelmintic treatment of the dogs.

Keywords: Echinococcosis, North Macedonia, cattle, sheep, prevalence

References

  1. Otero-Abad, B., Torgerson, P.R. (2013). A systematic review of the epidemiology of echinococcosis in domestic and wild animals. PLoS Negl Trop Dis. 7(6): e2249. https://doi.org/10.1371/journal.pntd.0002249 PMid:23755310 PMCid:PMC3674998
  2. Budke, C.M., Casulli, A., Kern, P., Vuitton, D.A. (2017). Cystic and alveolar echinococcosis: Successes and continuing challenges. PLoS Negl Trop Dis. 11(4): e0005477. https://doi.org/10.1371/journal.pntd.0005477 PMid:28426657 PMCid:PMC5398475
  3. Restrepo, A.M.C., Yang, Y.R., McManus, D.P., Gray, D.J., Giraudoux, P., Barnes, T.S., Williams, G.M., et al. (2016). The landscape epidemiology of echinococcosis. Infect Dis Poverty. 5(1): 1-13. https://doi.org/10.1186/s40249-016-0109-x PMid:26895758 PMCid:PMC4759770
  4. Eckert, J., Deplazes, P. (2004). Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clin Microbiol Rev. 17(1): 107-135. https://doi.org/10.1128/CMR.17.1.107-135.2004 PMid:14726458 PMCid:PMC321468
  5. Romig, T., Deplazes, P., Jenkins, D., Giraudoux, P., Massolo, A., Craig, P.S., Wassermann, M., et al. (2017). Ecology and life cycle patterns of echinococcus species. Adv Parasitol. 95, 213-314. https://doi.org/10.1016/bs.apar.2016.11.002 PMid:28131364
  6. Monteiro, K.M., de Carvalho, M.O., Zaha, A., Ferreira, H.B. (2010). Proteomic analysis of the Echinococcus granulosus metacestode during infection of its intermediate host. Proteomics 10(10): 1985-1999. https://doi.org/10.1002/pmic.200900506 PMid:20217864
  7. Saeed, I., Kapel, C., Saida, L.A., Willingham, L., Nansen, P. (2000). Epidemiology of Echinococcus granulosus in Arbil province, Northern Iraq, 1990- 1998. J Helminthol. 74(1): 83-88. https://doi.org/10.1017/S0022149X00000111 PMid:10831057
  8. Cardona, G.A., Carmena, D. (2013). A review of the global prevalence, molecular epidemiology and economics of cystic echinococcosis in production animals. Vet Parasitol. 192(1-3): 10-32. https://doi.org/10.1016/j.vetpar.2012.09.027 PMid:23084536
  9. Ahmadi, N.A., Meshkehkar, M. (2010). An abattoirbased study on the prevalence and economic losses due to cystic echinococcosis in slaughtered herbivores in Ahwaz, south-western Iran J Helminthol. 85(1): 33-39. https://doi.org/10.1017/S0022149X10000234 PMid:20398435
  10. Getaw, A., Beyene, D., Ayana, D., Megers, B., Abunna, F. (2010). Hydatidosis: Prevalence and its economic importance in ruminants slaughtered at Adama municipal abattoir, Central Oromia, Ethiopia. Acta Trop. 113(3): 221-225. https://doi.org/10.1016/j.actatropica.2009.10.019 PMid:19883622
  11. Ito, A. (2017). Review of "Echinococcus and Echinococcosis, Part A." edited by R.C. Andrew Thompson, Alan J. Lymbery and Peter Deplazes. Parasites Vectors 10, 408. https://doi.org/10.1186/s13071-017-2345-8 PMid:28870244 PMCid:PMC5583985
  12. Grosso, G., Gruttadauria, S., Biondi, A., Marventan, O.S., Mistretta, A. (2012). Worldwide epidemiology of liver hydatidosis including the Mediterranean area. World J Gastroenterol. 18(13): 1425-1437. https://doi.org/10.3748/wjg.v18.i13.1425 PMid:22509074 PMCid:PMC3319938
  13. Mitrea, I.L., Ionita, M., Wassermann, M., Solcan, G., Romig, T. (2012). Cystic echinococcosis in Romania: an epidemiological survey of livestock demonstrates the persistence of hyperendemicity. Foodborne Pathog Dis. 9(11): 980-985. https://doi.org/10.1089/fpd.2012.1237 PMid:23075460
  14. Derylo, A., Szilman, P. (1998). Prevalence of echinococcosis in swine, beef-cattle, ships and goats in Poland during 1996, 1997. Wiadomości Parazytologiczne 44(3): 413.
  15. Carabin, H., Balsera-Rodriguez, F.J., Rebollar-Saenz, J., Benner, C.T., Benito, A., Fernandez-Crespo, J.C., Carmena, D. (2014). Cystic echinococcosis in the Province of Álava, North Spain: The monetary burden of a disease no longer under surveillance. PLoS Negl Trop Dis. 8(8): e3069. https://doi.org/10.1371/journal.pntd.0003069 PMid:25102173 PMCid:PMC4125306
  16. Umhang, G., Richomme, C., Boucher, J. M., Hormaz, V., Boué, F. (2013). Prevalence survey and first molecular characterization of Echinococcus granulosus in France. Parasitol Res. 112(4): 1809-1812. https://doi.org/10.1007/s00436-012-3245-7 PMid:23271567 PMCid:PMC3597331
  17. Alishani, M., Sherifi, K., Rexhepi, A., Hamidi, A., Armua-Fernandez, M.T., Grimm, F., Hegglin, D., Deplazes, P. (2017). The impact of socio-cultural factors on transmission of Taenia spp. And Echinococcus granulosus in Kosovo. Parasitology 144, 1736-1742. https://doi.org/10.1017/S0031182017000750 PMid:28799892
  18. Zuko, A., Obradović, Z. (2014). Echinococcosis in Bosnia and Herzegovina - an overview. ESCCAP Echinococcus meeting, Abstract booklet, October, 8-9, (p.21), Vilnius, Lithuania
  19. Xhaxhiu, D., Kusi, I., Rapti, D., Kondi, E., Postoli, R., Rinaldi, L., Dimitrova, Z.M., et al. (2011). Principal intestinal parasites of dogs in Tirana, Albania. Parasitol Res. 108(2): 341-353. https://doi.org/10.1007/s00436-010-2067-8 PMid:20878182
  20. Chaligiannis, I., Maillard, B., Ghalia, S., Markus, S., Anastasios, G., Bruno, S. (2015). Echinococcus granulosus infection dynamics in livestock of Greece. Acta Trop. 150, 64-70. https://doi.org/10.1016/j.actatropica.2015.06.021 PMid:26123192
  21. Breyer, I., Georgieva, D., Kurdova, R., Gottstein, B. (2004). Echinococcus granulosus strain typing in Bulgaria: The G1 genotype is predominant in intermediate and definitive wild hosts. Parasitol Res. 93(2): 127-130. https://doi.org/10.1007/s00436-004-1116-6 PMid:15127295
  22. Bobic, B., Nikolic, A., Katic Radivojevic, S., Klun, I., Djurkovic-Djakovic, O. (2012). Echinococcosis in Serbia: An Issue for the 21st Century? Foodborne Pathog Dis. 9(11): 967-73. https://doi.org/10.1089/fpd.2012.1227 PMid:23113724
  23. Daryani, A., Sharif, M., Amouei, A., Nasrolahei, M. (2009). Fertility and viability rates of hydatid cysts in slaughtered animals in the Mazandaran Province, Northern Iran. Trop Anim Health Prod. 41(8): 1701-1705. https://doi.org/10.1007/s11250-009-9368-x PMid:19455399
  24. Craig, P., Mastin, A., Kesteren, F., Boufana, B. (2015). Echinococcus granulosus: Epidemiology and state-of-the-art of diagnostics in animals. Vet Parasitol. 213(3): 132-148. https://doi.org/10.1016/j.vetpar.2015.07.028 PMid:26321135
  25. Abdulhameed, M.F. (2018). The epidemiology and impact of cystic echinococcosis in humans and domesticated animals in Basrah Province, Iraq. Doctoral dissertation, Murdoch University
  26. World Organisation for Animal Health (OIE) (2021). Echinococcosis (infection with Echinococcus granulosus and with E. multilocularis) manual of diagnostic tests and vaccines for terrestrial animals. Chapter 3.1.6. OIE, Paris.
  27. Joanny, G., Cappai, M.G., Nonnis, F., Tamponi, C., Dessì, G., Mehmood, N., Dahdah, J., et al. (2021). Human cystic echinococcosis in Lebanon: A retrospective study and molecular epidemiology. Acta Parasit. 1-10. https://doi.org/10.1007/s11686-021-00453-w PMid:34264443
  28. Khan, S.N., Ali, R., Khan, S., Norin, S., Rooman, M., Akbar, N.U., Khan, T.A., et al. (2021). Cystic echinococcosis: an emerging zoonosis in southern regions of Khyber Pakhtunkhwa, Pakistan. BMC Vet Res. 17(1): 1-11. https://doi.org/10.1186/s12917-021-02830-z PMid:33794898 PMCid:PMC8015088
  29. El-Dakhly, K.M., Arafa, W.M., El-Nahass, E.N., Shokier, K.A.M., Noaman, A.F. (2019). The current prevalence and diversity of cystic echinococcosis in slaughtered animals in Egypt. J Parasit Dis. 43(4): 711-717. https://doi.org/10.1007/s12639-019-01151-1 PMid:31749543 PMCid:PMC6841774
  30. Kere, O.J., Joseph, E., Jessika, B.L., Maina, K.J. (2019). Prevalence and monetary loss due to cystic Echinococcosis in slaughterhouse livestock: A case study of Migori County, Kenya. Parasite Epidemiol. Control 5: e00105. https://doi.org/10.1016/j.parepi.2019.e00105 PMid:31193569 PMCid:PMC6536491
  31. Rinaldi, L., Maurelli, M.P., Capuano, F., Perugini, A.G., Veneziano, V., Cringoli, S. (2008). Molecular update on cystic echinococcosis in cattle and water buffaloes of Southern Italy. Zoonoses Public Health 55(2): 119-123. https://doi.org/10.1111/j.1863-2378.2007.01101.x PMid:18234031
  32. Zelalem, F., Tadele, T., Nigussie, Z., Macias, C., Kebede, N. (2012). Prevalence and characterization of hydatidosis in animals slaughtered at Addis Ababa abattoir, Ethiopia. J Parasitol Vector Biol. 4(1): 1-6.
  33. Founta, A., Chliounakis, S., Antoniadou Sotiriadou, K., Koidou, M., Bampidis, V. (2016). Prevalence of hydatidosis and fertility of hydatid cysts in food animals in Northern Greece. Vet Ital. 52(2): 123-27.
  34. Kouidri, M., Benchaib-Khoudja, F., Boulkaboul, A., Selles, S.M.A. (2013). Cystic echinococcosis in small ruminants in Tiaret (Algeria). Glob Vet. 11(6): 753-758.
  35. Almalki, E., Al-Shaebi, E.M., Al-Quarishy, S., El-Matbouli, M., Abdel-Baki, A.S. (2017). In vitro effectiveness of Curcuma longa and Zingiber officinale extracts on Echinococcus protoscoleces. Saudi J Biol Sci. 24(1): 90-94. https://doi.org/10.1016/j.sjbs.2016.05.007 PMid:28053576 PMCid:PMC5198992
  36. Kebede, W., Hagos, A., Girma, Z., Lobago, F. (2009). Echinococcosis/hydatidosis: its prevalence, economic and public health significance in Tigray region, North Ethiopia. Trop Anim Health Prod. 41(6): 865-871. https://doi.org/10.1007/s11250-008-9264-9 PMid:19002598
  37. Thompson, R.C.A. (1995). Biology and systematics of Echinococcus. In R.C.A. Thompson, A.J. Lymbery (Eds.), The biology of Echinococcus and hydatid disease (pp. 1-50). Wallingford: CAB International https://doi.org/10.3168/jds.2011-4767 PMid:22459831

Copyright

© 2022 Rashikj Lj. This is an open-access article published under the terms of the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Conflict of Interest Statement

The authors have declared that no competing interests exist.

Citation Information

Macedonian Veterinary Review. Volume 45, Issue 1, Pages 35-41, e-ISSN 1857-7415, p-ISSN 1409-7621, DOI: 10.2478/macvetrev-2022-0011, 2022

The all content of the Macedonian Veterinary Review, except where otherwise noted, is licensed under a Creative Commons Attribution License.