Abstract
Fascioliasis, a prevalent disease in livestock globally, is primarily caused by the trematode parasites Fasciola hepatica and Fasciola gigantica. This parasitic infection leads to significant economic repercussions. In this study, our objective was to gain insight into the pathophysiological consequences of Fascioliasis in cattle through the evaluation of metabolic, oxidative stress, and histological parameters. A thorough investigation was carried out on the liver of 197 bovines after their slaughter, which unveiled the occurrence of Fascioliasis, with a prevalence rate of 13.2% observed. The bovine that were infected exhibited notable increase in serum transaminases (ALT, AST, and ALP) and malondialdehyde (MDA) and catalase (CAT) while the decrease in glutathione (GSH) and superoxide dismutase (SOD) levels. The lipid profile analysis of infected cattle revealed alterations in the cholesterol and triglyceride levels. Moreover, the histopathological examination revealed a range of hepatic lesions associated with Fascioliasis, including necrosis, inflammation, fibrosis, and proliferative alterations. The bile ducts also displayed distinct pathological changes, including hyperplasia, thickening, and edema, and harbored various developmental stages of Fasciola spp. highlighting the parasitic infestation’s effects on the biliary system. These results highlight the serious effects of Fascioliasis on lipid metabolism and the oxidative damage that is induced in the livers of cattle. Thus, Fasciola infestation in bovine causes alteration in biochemical and antioxidant activities, which are considered as important factors in the diagnosis of Fascioliasis.
Similar content being viewed by others
Availability of data and materials
All data generated or analyzed during this study are included in this published article.
References
Abdel-Fatah, O.R., Arafa, W.M., Wahba, A.A., and El-Dakhly, K.M., 2022. Economic losses, morpho-molecular identification, and identity of Fasciola species recovered from Egypt, J Parasit Dis, 46, 1036-1046
Abraham, J.T., and Jude, I.B., 2014. Fascioliasis in cattle and goat slaughtered at Calabar abattoirs., Journal of Biology, Agriculture and Healthcare, 14, 34-40
Addy, F., Gyan, K., Arhin, E., and Wassermann, M., 2020. Prevalence of bovine fasciolosis from the Bolgatanga abattoir, Ghana, Scientific African, 8, e00469
Alcalá-Canto, Y., Ibarra-Velarde, F., Gracia-Mora, J., and Sumano-López, H., 2005. Fasciola hepatica proteolytic activity in liver revealed by in situ zymography, Parasitol Res, 96, 308-311
Alfaia, C.M., Alves, S.P., Lopes, A.F., Fernandes, M.J., Costa, A.S., Fontes, C.M., Castro, M.L., Bessa, R.J., and Prates, J.A., 2010. Effect of cooking methods on fatty acids, conjugated isomers of linoleic acid and nutritional quality of beef intramuscular fat, Meat Science, 84, 769-777
Al-Mahmood, S.S., and Al-sabaawy, H.B., 2019. Fasciolosis: grading the histopathological lesions in naturally infected bovine liver in Mosul city, Iraqi Journal of Veterinary Sciences,
Al-Sabaawy, H.B., Mustafa, E., Rahawi, A.M., Jaber, M., Al-Hamdany, E.K., and Al-Hmdany, S.M., 2022. Histopathological study of sheep lung roaming in dump zones, Iraqi Journal of Veterinary Sciences, 36, 151-160
Alshammari, A., Gattan, H.S., Marzok, M., Salem, M., Al-Jabr, O.A., and Selim, A., 2023. Fasciola hepatica infection in horses in three governorates in Northern Egypt: prevalence and risk factors, J Equine Vet Sci, 130, 104915
AS, D.A.S., Baldissera, M.D., Bottari, N.B., Gabriel, M.E., Rhoden, L.A., Piva, M.M., Christ, R., Stedille, F.A., Gris, A., Morsch, V.M., Schetinger, M.R., and Mendes, R.E., 2017. Oxidative stress and changes in adenosine deaminase activity of cattle experimentally infected by Fasciola hepatica, Parasitology, 144, 520-526
Bahrami, S., Esmaeilzadeh, S., and Oryan, A., 2014. Role of oxidative stress in concomitant occurrence of Fasciola gigantica and leiomyoma in cattle, Vet Parasitol, 203, 43-50
Beck, M.A., Goater, C.P., and Colwell, D.D., 2015. Comparative recruitment, morphology and reproduction of a generalist trematode, Dicrocoelium dendriticum, in three species of host, Parasitology, 142, 1297-1305
Brahmbhatt, N.N., Kumar, B., Thakre, B.J., and Bilwal, A.K., 2021. Haemato-biochemical characterization of fasciolosis in Gir cattle and Jaffrabadi buffaloes, J Parasit Dis, 45, 683-688
Cancela, M., Acosta, D., Rinaldi, G., Silva, E., Durán, R., Roche, L., Zaha, A., Carmona, C., and Tort, J.F., 2008. A distinctive repertoire of cathepsins is expressed by juvenile invasive Fasciola hepatica, Biochimie, 90, 1461-1475
Charlier, J., Rinaldi, L., Musella, V., Ploeger, H.W., Chartier, C., Vineer, H.R., Hinney, B., von Samson-Himmelstjerna, G., Băcescu, B., Mickiewicz, M., Mateus, T.L., Martinez-Valladares, M., Quealy, S., Azaizeh, H., Sekovska, B., Akkari, H., Petkevicius, S., Hektoen, L., Höglund, J., Morgan, E.R., Bartley, D.J., and Claerebout, E., 2020. Initial assessment of the economic burden of major parasitic helminth infections to the ruminant livestock industry in Europe, Preventive Veterinary Medicine, 182, 105103
Córsico, B., and Falomir-Lockhart, L.J., 2009. Signals from the adipose tissue alter systemic metabolism, Clinical Lipidology, 4, 13-16
Dharmayudha, A.A.G.O., Kusumadarma, I.B.D., Ardana, I.B.K., Anthara, M.S., Gunawan, I.W.N.F., Sudimartini, L.M., and Agustina, K.K., 2018. Aktivitas Alanin Aminotransferase Dan Aspartat Aminotransferase Sapi Bali Terinfeksi Fasciola Gigantica, Buletin Veteriner Udayana, 10, 87-92
Dyab, A.K., Ahmed, H.A., Hefnawy, Y.A., Abdelaziz, A.R., and Gomaa, M.M., 2019. Revalence of tissue parasites in cattle and buffaloes slaughtered in El-Minia Governorate Abattoirs, Egypt., PSM Veterinary Research, 4, 49-58
Elshahawy, II, Elshanat, S., Arab, M.M., Nayel, M., Salama, A., El-Sify, A., and Aly, M., 2021. Hepatic biomarkers and coprology as indicators of clinical bovine fasciolosis in Chad, Vet World, 14, 1153-1157
Grünwaldt, E., Guevara, J., Estevez, O., Vicente, A., Rousselle, H., Alcuten, N., Aguerregaray, D., and Stasi, C., 2005. Biochemical and haematological measurements in beef cattle in Mendoza plain rangelands (Argentina), Trop Anim Health Prod, 37, 527-540
Guemouri, L., Artur, Y., Herbeth, B., Jeandel, C., Cuny, G., and Siest, G., 1991. Biological variability of superoxide dismutase, glutathione peroxidase, and catalase in blood, Clin Chem, 37, 1932-1937
Hernández-Guzmán, K., Molina-Mendoza, P., Olivares-Pérez, J., Alcalá-Canto, Y., Olmedo-Juárez, A., Córdova-Izquierdo, A., and Villa-Mancera, A., 2021. Prevalence and seasonal variation of Fasciola hepatica in slaughtered cattle: the role of climate and environmental factors in Mexico, J Helminthol, 95, e46
Howell, A., Mugisha, L., Davies, J., LaCourse, E.J., Claridge, J., Williams, D.J., Kelly-Hope, L., Betson, M., Kabatereine, N.B., and Stothard, J.R., 2012. Bovine fasciolosis at increasing altitudes: parasitological and malacological sampling on the slopes of Mount Elgon, Uganda, Parasit Vectors, 5, 196
Ibrahim, I.E., Sherif, K.E., Mayo, M.A., Mohamed, N., Akram, S., Ahmed, E., and Mahmoud, A., 2021. Hepatic biomarkers and coprology as indicators of clinical bovine fasciolosis in Chad., Vet World, 14, 1153–1157
Ikeda, I., Tomari, Y., Sugano, M., Watanabe, S., and Nagata, J., 1991. Lymphatic absorption of structured glycerolipids containing medium-chain fatty acids and linoleic acid, and their effect on cholesterol absorption in rats, Lipids, 26, 369-373
Jahed Khaniki, G.R., Kia, E.B., and Raei, M., 2013. Liver condemnation and economic losses due to parasitic infections in slaughtered animals in Iran, J Parasit Dis, 37, 240-244
Jaja, I.F., Mushonga, B., Green, E., and Muchenje, V., 2017a. A quantitative assessment of causes of bovine liver condemnation and its implication for food security in the Eastern Cape Province South Africa, Sustainability, 9, 736
Jaja, I.F., Mushonga, B., Green, E., and Muchenje, V., 2017b. Seasonal prevalence, body condition score and risk factors of bovine fasciolosis in South Africa, Vet Anim Sci, 4, 1-7
Khovidhunkit, W., Memon, R.A., Feingold, K.R., and Grunfeld, C., 2000. Infection and inflammation-induced proatherogenic changes of lipoproteins, J Infect Dis, 181 Suppl 3, S462-472
Kwon, J., Lee, C., Heo, S., Kim, B., and Hyun, C.K., 2021. DSS-induced colitis is associated with adipose tissue dysfunction and disrupted hepatic lipid metabolism leading to hepatosteatosis and dyslipidemia in mice, Sci Rep, 11, 5283
Lalor, R., Cwiklinski, K., Calvani, N.E.D., Dorey, A., Hamon, S., Corrales, J.L., Dalton, J.P., and De Marco Verissimo, C., 2021. Pathogenicity and virulence of the liver flukes Fasciola hepatica and FasciolaGigantica that cause the zoonosis Fasciolosis, Virulence, 12, 2839-2867
Hassanabadi Mahmoud, Abdelrouf Ali, Yahia A. Amin, and Alsagher O. Ali, 2022. The infection rate of Fasciola and Anaplasma in cattle and buffaloes in Qena, Egypt., Int. J. Vet. Sci., 308–314
Mazeri, S., Rydevik, G., Handel, I., Bronsvoort, B.M.D., and Sargison, N., 2017. Estimation of the impact of Fasciola hepatica infection on time taken for UK beef cattle to reach slaughter weight, Sci Rep, 7, 7319
Mehmood, K., Zhang, H., Sabir, A.J., Abbas, R.Z., Ijaz, M., Durrani, A.Z., Saleem, M.H., Ur Rehman, M., Iqbal, M.K., Wang, Y., Ahmad, H.I., Abbas, T., Hussain, R., Ghori, M.T., Ali, S., Khan, A.U., and Li, J., 2017. A review on epidemiology, global prevalence and economical losses of fasciolosis in ruminants, Microb Pathog, 109, 253-262
Mellau, L.S.B., Nonga, H.E., and Karimuribo, E.D., 2010. A slaughterhouse survey of liver lesions in slaughtered cattle, sheep and goats at Arusha, Tanzania, Research Journal of Veterinary Sciences, 3, 179-188
Molina, E.C., Gonzaga, E.A., and Lumbao, L.A., 2005. Prevalence of infection with Fasciola gigantica and its relationship to carcase and liver weights, and fluke and egg counts in slaughter cattle and buffaloes in southern Mindanao, Philippines, Trop Anim Health Prod, 37, 215-221
Mungube, E.O., Bauni, S.M., Tenhagen, B.A., Wamae, L.W., Nginyi, J.M., and Mugambi, J.M., 2006. The prevalence and economic significance of Fasciola gigantica and Stilesia hepatica in slaughtered animals in the semi-arid coastal Kenya, Trop Anim Health Prod, 38, 475-483
Nasreldin, N., and Zaki, R.S., 2020. Biochemical and immunological investigation of fascioliasis in cattle in Egypt, Vet World, 13, 923-930
Olsen, A., Frankena, K., Bødker, R., Toft, N., Thamsborg, S.M., Enemark, H.L., and Halasa, T., 2015. Prevalence, risk factors and spatial analysis of liver fluke infections in Danish cattle herds, Parasit Vectors, 8, 160
Opio, L.G., Abdelfattah, E.M., Terry, J., Odongo, S., and Okello, E., 2021. Prevalence of Fascioliasis and associated economic losses in cattle slaughtered at Lira Municipality Abattoir in Northern Uganda, Animals (Basel), 11,
Park, B.-K., Hong, E.-J., Ryu, S.-Y., Jung, B.-D., Kim, J.-M., and Kim, H.-C., 2015. Prevalence of Fasciola spp. from cattle in slaughterhouse by macroscopic examination., Korean J. Vet. Serv., 38, 227-232
Pereira, A.L.F., and Abreu, V.K.G., 2018. Lipid peroxidation in meat and meat products, Lipid peroxidation research, 29,
Pfukenyi, D.M., and Mukaratirwa, S., 2004. A retrospective study of the prevalence and seasonal variation of Fasciola gigantica in cattle slaughtered in the major abattoirs of Zimbabwe between 1990 and 1999, Onderstepoort J Vet Res, 71, 181-187
Prasetyo, D.A., Nurlaelasari, A., Wulandari, A.R., Cahyadi, M., Wardhana, A.H., Kurnianto, H., Kurniawan, W., Kristianingrum, Y.P., Muñoz-Caro, T., and Hamid, P.H., 2023. High prevalence of liver fluke infestation, Fasciola gigantica, among slaughtered cattle in Boyolali District, Central Java, Open Vet J, 13, 654-662
Rana, M., Roohi, N., and Khan, M., 2014. Fascioliasis in cattle-a review, JAPS: Journal of Animal & Plant Sciences, 24,
Richmond, W., 1973. Preparation and properties of a cholesterol oxidase from Nocardia sp. and its application to the enzymatic assay of total cholesterol in serum, Clin Chem, 19, 1350-1356
Rizwan, H., Usman, M., Naeem, M., Farid, M., Younus, M., Sajid, M., Tahir, U., Luqman, N., Abbas, H., and Ateeq, M., 2022. Prevalence of ruminant paramphistomosis and comparative histopathology of the infected rumens in Narowal district, Punjab, Pakistan, Helminthologia, 59, 377-384
Royer, M., 1969. Determination of triglycerides, Anal. Biochem, 29, 405
Samadieh, H., Mohammadi, G.R., Maleki, M., Borji, H., Azizzadeh, M., and Heidarpour, M., 2017. Relationships between oxidative stress, liver, and erythrocyte injury, trace elements and parasite burden in sheep naturally infected with Dicrocoelium dendriticum, Iran J Parasitol, 12, 46-55
Selim, A., Khater, H., and Almohammed, H.I., 2021a. A recent update about seroprevalence of ovine neosporosis in Northern Egypt and its associated risk factors, Sci Rep, 11, 14043
Selim, A., Manaa, E.A., Alanazi, A.D., and Alyousif, M.S., 2021b. Seroprevalence, risk factors and molecular identification of bovine leukemia virus in Egyptian cattle, Animals, 11, 319
Selim, A., Attia, K.A., Alsubki, R.A., Kimiko, I., and Sayed-Ahmed, M.Z., 2022. Cross-sectional survey on Mycobacterium avium Subsp. paratuberculosis in Dromedary Camels: seroprevalence and risk factors, Acta Tropica, 226, 106261
Selim, A., Abdelrahman, A., Thiéry, R., and Sidi-Boumedine, K., 2019. Molecular typing of Coxiella burnetii from sheep in Egypt, comparative immunology, microbiology and infectious diseases, 67, 101353
Taibi, A., Aissi, M., Harhoura, K., Zenia, S., Zait, H., and Hamrioui, B., 2019. Evaluation of Fasciola hepatica infections in cattle in northeastern Algeria and the effects on both enzyme and hepatic damage, confirmed by scanning electron microscopy, Acta Parasitol, 64, 112-128
Ukam, U.A., Enogiomwan, I.E., Offiong, E.E., and Chinyere, O.-A., 2020. Prevalence and histopathological effects of Fascioliasis in cattle slaughtered in Ikot Eneobong Abattoir, Calabar, Nigeria, Microbiology Research Journal International,
Vannier, A.G., Shay, J.E., Fomin, V., Patel, S.J., Schaefer, E., Goodman, R.P., and Luther, J., 2022. Incidence and progression of alcohol-associated liver disease after medical therapy for alcohol use disorder, JAMA Network Open, 5, e2213014-e2213014
Vos, D.Y., Heida, A., Koster, M., Tissink, J., Kuentzel, K.B., Kloosterhuis, N.J., Smit, M., Huijkman, N., Reggiori, F., Mari, M., Scheja, L., Heeren, J., Kratky, D., Kuivenhoven, J., and Sluis, B.V.D., 2022. The endosomal sorting protein VPS35 controls lipid homeostasis through regulating hepatic lysosomal function., Atherosclerosis, 355, 19-20
Wiseman, H., and Halliwell, B., 1996. Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer, Biochem J, 313 ( Pt 1), 17-29
Yokus, B., and Cakir, U.D., 2006. Seasonal and physiological variations in serum chemistry and mineral concentrations in cattle, Biol Trace Elem Res, 109, 255-266
Author information
Authors and Affiliations
Contributions
Conceptualization, methodology, formal analysis, investigation, resources, data curation, writing – original draft preparation: Salma Shoulah, Mohamed Gaballa, Marwa Al-Assas, Abdelfattah Selim, and Sayed Saqr; writing – review and editing: Salma Shoulah, Mohamed Gaballa, Marwa Al-Assas, Abdelfattah Selim, Hattan Gattan, and Sayed Saqr; project administration: Abdelfattah Selim; funding acquisition: Salma Shoulah, Mohamed Gaballa, Marwa Al-Assas, Abdelfattah Selim, and Sayed Saqr. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Shoulah, S.A., Gaballa, M.M.S., Al-Assas, M.M. et al. Histopathological changes and oxidative stress associated with Fascioliasis in bovines. Trop Anim Health Prod 56, 48 (2024). https://doi.org/10.1007/s11250-024-03896-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11250-024-03896-1