ORIGINAL_ARTICLE
Cystic Echinococcosis in slaughtered cattle and sheep from North Macedonia
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.
https://macvetrev.mk/Files/Article/2022/10.2478/macvetrev-2022-0011/macvetrev-2022-0011.pdf
2022-03-15T09:00:00
35
41
10.2478/macvetrev-2022-0011
Echinococcosis
North Macedonia
cattle
sheep
prevalence
Ljubica
Rashikj
false
1
Veterinary Institute, Faculty of Veterinary Medicine - Skopje, Ss. Cyril and Methodius University in Skopje, Lazar Pop-Trajkov 5-7, 1000 Skopje, North Macedonia
AUTHOR
Aleksandar
Cvetkovikj
acvetkovic@fvm.ukim.edu.mk
false
2
Veterinary Institute, Faculty of Veterinary Medicine - Skopje, Ss. Cyril and Methodius University in Skopje, Lazar Pop-Trajkov 5-7, 1000 Skopje, North Macedonia
LEAD_AUTHOR
Martin
Nikolovski
false
3
Institute for Reproduction and Biomedicine, Faculty of Veterinary Medicine - Skopje, Ss. Cyril and Methodius University in Skopje, Lazar Pop-Trajkov 5-7, 1000 Skopje, North Macedonia
AUTHOR
Iskra
Cvetkovikj
false
4
Veterinary Institute, Faculty of Veterinary Medicine - Skopje, Ss. Cyril and Methodius University in Skopje, Lazar Pop-Trajkov 5-7, 1000 Skopje, North Macedonia
AUTHOR
Jovana
Stefanovska
false
5
Veterinary Institute, Faculty of Veterinary Medicine - Skopje, Ss. Cyril and Methodius University in Skopje, Lazar Pop-Trajkov 5-7, 1000 Skopje, North Macedonia
AUTHOR
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. PMid:23755310 PMCid:PMC3674998
1
10.1371/journal.pntd.0002249
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. PMid:28426657 PMCid:PMC5398475
2
10.1371/journal.pntd.0005477
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. PMid:26895758 PMCid:PMC4759770
3
10.1186/s40249-016-0109-x
Eckert, J., Deplazes, P. (2004). Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clin Microbiol Rev. 17(1): 107-135. PMid:14726458 PMCid:PMC321468
4
10.1128/CMR.17.1.107-135.2004
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. PMid:28131364
5
10.1016/bs.apar.2016.11.002
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. PMid:20217864
6
10.1002/pmic.200900506
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. PMid:10831057
7
10.1017/S0022149X00000111
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. PMid:23084536
8
10.1016/j.vetpar.2012.09.027
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. PMid:20398435
9
10.1017/S0022149X10000234
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. PMid:19883622
10
10.1016/j.actatropica.2009.10.019
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. PMid:28870244 PMCid:PMC5583985
11
10.1186/s13071-017-2345-8
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. PMid:22509074 PMCid:PMC3319938
12
10.3748/wjg.v18.i13.1425
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. PMid:23075460
13
10.1089/fpd.2012.1237
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.
14
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. PMid:25102173 PMCid:PMC4125306
15
10.1371/journal.pntd.0003069
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. PMid:23271567 PMCid:PMC3597331
16
10.1007/s00436-012-3245-7
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. PMid:28799892
17
10.1017/S0031182017000750
Zuko, A., Obradović, Z. (2014). Echinococcosis in Bosnia and Herzegovina - an overview. ESCCAP Echinococcus meeting, Abstract booklet, October, 8-9, (p.21), Vilnius, Lithuania
18
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. PMid:20878182
19
10.1007/s00436-010-2067-8
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. PMid:26123192
20
10.1016/j.actatropica.2015.06.021
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. PMid:15127295
21
10.1007/s00436-004-1116-6
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. PMid:23113724
22
10.1089/fpd.2012.1227
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. PMid:19455399
23
10.1007/s11250-009-9368-x
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. PMid:26321135
24
10.1016/j.vetpar.2015.07.028
Abdulhameed, M.F. (2018). The epidemiology and impact of cystic echinococcosis in humans and domesticated animals in Basrah Province, Iraq. Doctoral dissertation, Murdoch University
25
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.
26
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. PMid:34264443
27
10.1007/s11686-021-00453-w
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. PMid:33794898 PMCid:PMC8015088
28
10.1186/s12917-021-02830-z
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. PMid:31749543 PMCid:PMC6841774
29
10.1007/s12639-019-01151-1
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. PMid:31193569 PMCid:PMC6536491
30
10.1016/j.parepi.2019.e00105
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. PMid:18234031
31
10.1111/j.1863-2378.2007.01101.x
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.
32
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.
33
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.
34
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. PMid:28053576 PMCid:PMC5198992
35
10.1016/j.sjbs.2016.05.007
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. PMid:19002598
36
10.1007/s11250-008-9264-9
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 PMid:22459831
37
10.3168/jds.2011-4767