Advancing meat safety diverse approaches for bovine tuberculosis detection and control in abattoirs
Main Article Content
Keywords
Egypt, livestock, Mycobacterium bovis, postmortem lesions, RT-PCR, tuberculosis
Abstract
Bovine tuberculosis (BTB) still represents a significant public health concern and economic issue for livestock breeders in Egypt. This research investigates the incidence of bovine tuberculosis in cattle slaughtered at the central abattoir in Aswan, Egypt, in 2023. A total of 720 cattle were checked antemortem and postmortem at the abattoir. The suspected lesions were analyzed with acid-fast staining, microscopy, histology, ELISA, and RT-PCR. Based on gross tubercle lesions, the overall occurrence of bovine tuberculosis in cattle slaughtered at Aswan abattoirs was 3.2% (23/720), with thoracic lymph nodes and lungs exhibiting the highest frequency of tubercle lesions compared to other organs. According to employed diagnostic tests, the prevalence of tuberculosis was estimated as 68.6, 61, 56.5, and 78.3% for microscopy, histopathology, ELISA, and RT-PCR, respectively. These findings highlight the incidence of bovine tuberculosis and the dissemination of tuberculous lesions among cattle slaughtered at Aswan abattoirs. Furthermore, such prevalence emphasizes the urgent need for a practical disease control approach and an organized surveillance system in the cattle population. One Health strategy is strongly advised to mitigate the zoonotic transmission to people and economic losses in the cattle industry.
References
Algammal, A.M., Wahdan, A., and Elhaig, M.M., 2019. Potential efficiency of conventional and advanced approaches used to detect Mycobacterium bovis in cattle. Microbial Pathogenesis. 134: 103574. 10.1016/j.micpath.2019.103574
Amin, R.A, Nasr, E.A., El-Gaml, A.M., and Saafan, E.M., 2015. Detection of tuberculosis in slaughtered food animals by using recent technique. Benha Veterinary Medical Journal. 2: 129–134. 10.21608/bvmj.2015.32488
Araujo, C.P., Leite, C.Q., Prince, K.A., Jorge, K.S., and Osorio, A.L., 2005. Mycobacterium bovis identification by a molecular method from postmortem inspected cattle obtained in abattoirs of Mato Grosso do Sul, Brazil. Memorias do Instituto Oswaldo Cruz. 100: 749–752. 10.1590/s0074-02762005000700013
Aylate, A., Shah, S.N., Aleme, H., and Gizaw, T.T., 2013. Bovine tuberculosis: Prevalence and diagnostic efficacy of routine meat inspection procedure in Woldiya municipality abattoir north Wollo zone, Ethiopia. Tropical Animal Health and Production. 45: 855–64. 10.1007/s11250-012-0298-7
Belakehal, F., Moser, I., Naim, M., Zenia, S., and Hamdi, T.M., 2021. Tuberculosis lesions of bovine carcasses in Algerian municipal abattoirs and associated risk factors. Journal of Animal Health and Production. 9: 479–486. 10.17582/journal.jahp/2021/9.4.479.486
Belete, A., Tilahun, S., Hail, A.B., Demessie, Y., Nigatu, S., and Getachew, A., 2021. Prevalence of bovine tuberculosis and distribution of tuberculous lesions in cattle slaughtered at Gondar, Northwest Ethiopia. Infection Ecology & Epidemiology. 11: 1986919. 10.1080/20008686.2021.1986919
Benhathat, Y., and Aggad, H., 2017. Occurrence and severity of major gross pulmonary lesions in cattle slaughtered at Tiaret (Western Algeria). Journal of Applied Environmental and Biological Sciences. 7: 48–53. https://api.semanticscholar.org/CorpusID:212480912
Boko, C.K., Zoclanclounon, A.R., Adoligbe, C.M., Dedehouanou, H., M’Po, M., Mantip, S., et al., 2022. Molecular diagnosis of bovine tuberculosis on postmortem carcasses during routine meat inspection in Benin: GeneXpert® testing to improve diagnostic scheme. Veterinary World. 15: 2506–2510. 10.14202/vetworld.2022.2506-2510
Branger, B., 2013. Valeur diagnostique et prédictive d’un test de diagnostic ou de dépistage. 11. In: Test Diagnostique. Réseau de Périnatalité des Pays de la Loire. Nantes, France. Available from: https://www.reseau-naissance.fr/data/mediashare/zy/5lort-2g2ifme9q429gvnfgmoh0xctd-org.pdf.
Chauhan, R.S., and Agarwal, D.K., 2008. Textbook of veterinary, clinical and laboratory diagnosis. 2nd ed. New Delhi, India: Jaypee Brothers Medical Publishers. pp. 1–364.
Cleaveland, S., Shaw, D.J., Mfinanga, S.G., Shirima, G., Kazwala, R.R., Eblate, E., et al., 2007. Mycobacterium bovis in rural Tanzania: Risk factors for infection in human and cattle populations. Tuberculosis. 87: 30–43. 10.1016/j.tube.2006.03.001
Corner, L.A., 1994. Postmortem diagnosis of Mycobacterium bovis infection in cattle. Veterinary Microbiology. 40: 53–63. 10.1016/0378-1135(94)90046-9
Courcoul, A., Moyen, J.L., Brugère, L., Faye, S., Hénault, S., and Gares, H., 2014. Estimation of sensitivity and specificity of bacteriology, histopathology and PCR for the confirmatory diagnosis of bovine tuberculosis using latent class analysis. PLoS One. 9: e90334. 10.1371/journal.pone.0090334
Cousins, D.V., Huchzermeyer, H.F.K., Griffin, J.F.T., Bruckner, G.K., Van Ransburg, I.B.J., and Kriek, N.P.J., 2004. Tuberculosis. In: Coetzer, A.W., and Tustin, R.C., editors. Infectious diseases of livestock. Cape Town: Oxford University Press. 2: 1973–1993.
Da Silva, E.B., De Souza, B.D., Leon, J.R., Kipnis, A., De Miranda, I.K., and Junqueira-Kipnis, A.P., 2011. Using BCG, MPT-51 and Ag85 as antigens in an indirect ELISA for the diagnosis of bovine tuberculosis. The Veterinary Journal. 187: 276–278. 10.1016/j.tvjl.2009.11.017
Damene, H., Tahir, D., Diels, M., Berber, A., Sahraoui, N., and Rigouts, L., 2020. Broad diversity of Mycobacterium tuberculosis complex strains isolated from humans and cattle in Northern Algeria suggests a zoonotic transmission cycle. PLoS Neglected Tropical Diseases. 14: e0008894. 10.1371/journal.pntd.0008894
Damina, M.S., Barnes, D.A., Inuwa, B., Ularamu, H.G., Bello, M., and Okaiyeto, S.O., 2023. Molecular characterisation of Mycobacterium bovis isolates from cattle slaughtered in Adamawa and Gombe states, North-Eastern Nigeria. Current Issues in Molecular Biology. 45: 6055–6066. 10.3390/cimb45070382
De la Rua-Domenech, R., Goodchild, A.T., Vordermeier, H.M., Hewinson, R.G., Christiansen, K.H., and Clifton-Hadley, R.S., 2006. Ante mortem diagnosis of tuberculosis in cattle: A review of tuberculin tests g-interferon assay and other ancillary diagnostic techniques. Research in Veterinary Science. 83: 190–210. 10.1016/j.rvsc.2005.11.005
Dergal, N.B., Ghermi, M., Imre, K., Morar, A., Acaroz, U., and Arslan-Acaroz, D., 2021. Estimated prevalence of tuberculosis in ruminants from slaughterhouses in Constantine Province (Northeastern Algeria): A 10-year retrospective survey (2011–2020). Life. 13: 817. 10.3390/life13030817
Dibaba, A.B., Daborn, C.J., Cadmus, S., and Michel, A., 2019. The current status of bovine tuberculosis in Africa. In: Tuberculosis in animals: An African perspective. Cham: Springer. pp. 15–30. 10.1007/978-3-030-18690-6_2
Elagdar, A., Edris, A., Moustafa, S., and Heikal, G., 2022. Prevalence of tuberculosis in bovine slaughtered animals and suspected patients in Gharbia governorate. Benha Veterinary Medical Journal. 43: 95–99. 10.21608/bvmj.2022.160378.1586
Elbarbary, N.K., Darwish, W.S., Fotouh, A., and Mohamed K.D., 2024. Unveiling the mix-up: investigating species and unauthorized tissues in beef-based meat products. BMC Veterinary Research. 20: 380. 10.1186/s12917-024-04223-4
El-Gedawy, A., El Shazly, Y., and El sheikh, H., 2022. A comparative study between some diagnostic techniques in diagnosis of bovine tuberculosis. New Valley Veterinary Journal. 2: 1–8. 10.21608/nvvj.2022.224022
Elsohaby, I., Alahadeb, J.I., Mahmmod, Y.S., Mweu, M.M., Ahmed, H.A., and El-Diasty, M.M., 2021. Bayesian estimation of diagnostic accuracy of three diagnostic tests for bovine tuberculosis in Egyptian dairy cattle using latent class models. Veterinary Science. 8: 246. 10.3390/vetsci8110246
FAOLEX, 2012. Food and Agriculture Organisation of the United Nations. Female Cattle (Prohibition of Slaughter and Spaying) Regulations (Cap. 103), Rome. Available from: https://faolex.fao.org/docs/pdf/van51577.pdf
GOVS, 1986. General Organization for Veterinary Services, Law (517).
Habitu, T., Demelash, A., Adrian, M., Girum, T., Eystein, S., and Tadesse, G., 2019. Prevalence and risk factors analysis of bovine tuberculosis in cattle raised in mixed crop-livestock farming system in Tigray region, Ethiopia. Transboundary and Emerging Diseases. 66: 488–496. 10.1111/tbed.13050
Hamed, Y., Nasr, E., Azooz, M., and Youssef, H., 2021. Prevalence and risk factors of bovine tuberculosis in dairy cattle farms in Egypt. Iraqi Journal of Veterinary Sciences. 35: 351–359. 10.33899/ijvs.2020.126850.1399
Hasanen, F.S., Hassan, M.A., and Moawad, E., 2017. Studies on Tuberculosis in Slaughtered Animals at Menufia Governorate. Benha Journal of Applied Sciences. 2: 99–102. 10.21608/bjas.2017.165726
Heidi, B., 2017. Body Condition Scoring Resource Center. [cited 2020 Sep 09]. Available from: https://nagonline.net/3877/bodycondition-scoring/
Hekal, S.H.A., Al-Gaabary, M.H., El-Sayed, M.M., Sobhy, H.M., and Fayed, A.A., 2019. Seroprevalence of some Infectious transboundary diseases in cattle imported from Sudan to Egypt. Journal of Advanced Veterinary and Animal Research. 6: 92–99. 10.5455/javar.2019.f318
Herenda, D.C., Chambers, P.G., and Ettriqui, A., 1994. Manual on meat inspection for developing countries. Rome, Italy: Food & Agriculture Org., FAO. pp. 1–357.
Isihak, F.A., Hassan, S.M., Shaker, B.Z., and Salih, Y.A., 2020. Follow up the antibodies titer against Newcastle disease virus in broiler breeders using ELISA test. Iraqi Journal of Veterinary Sciences. 34: 295–299. 10.33899/ijvs.2019.125931.1189
Kanyala, E., Shuaib, Y.A., Schwarz, N.G., Andres, S., Richter, E., and Sawadogo, B., 2022. Prevalence and molecular characterization of Mycobacterium bovis in slaughtered cattle carcasses in Burkina Faso; West Africa. Microorganisms. 10: 1378. 10.3390/microorganisms10071378
Kapalamula, T.F., Kawonga, F., Shawa, M., Chizimu, J., Thapa, J., and Nyenje, M., 2023. Prevalence and risk factors of bovine tuberculosis in slaughtered cattle, Malawi. Heliyon. 9: e13647. 10.1016/j.heliyon.2023.e13647
Kazwala, R.R., D.M. Kambarage, C.J, Daborn, J, Nyange, S.F.H., and Jiwa, J.M., 2001. Sharp, Risk factors associated with the occurrence of bovine tuberculosis in cattle in the Southern Highlands of Tanzania. Veterinary Research Communications. 25: 609–614. 10.1023/A:1012757011524
Kemal, J., Sibhat, B., Abraham, A., Terefe, Y., Tulu, K.T., Welay, K., et al., 2019. Bovine tuberculosis in eastern Ethiopia: Prevalence, risk factors and its public health importance. BMC Infectious Diseases. 19: 1–9. 10.1186/s12879-018-3628-1
Kuria, J.K., 2019. Diseases caused by bacteria in cattle: Tuberculosis. In: El-Sayed Kaoud, H.A., editor. Bacterial cattle diseases; London, UK: IntechOpen.
Lawan, F.A., Ejeh, E.F., Waziri, A., Kwanashie, C.N., Kadima, K.B., and Kazeem, H.M., 2020. Prevalence of tuberculosis in cattle slaughtered at Maiduguri Central aAbattoir, Nigeria. Sahel Journal of Veterinary Sciences. 17: 14–21. 10.54058/saheljvs.v17i3.167
Mekonnen, G.A., Conlan, A.J., Berg, S., Ayele, B.T., Alemu, A., and Guta, S., 2019. Prevalence of bovine tuberculosis and its associated risk factors in the emerging dairy belts of regional cities in Ethiopia. Preventive Veterinary Medicine. 168: 81–89. 10.1016/j.prevetmed.2019.04.010
Mekonnen, G.A., Mihret, A., Tamiru, M., Hailu, E., Olani, A., and Aliy, A., 2020. Genotype diversity of Mycobacterium bovis and pathology of bovine tuberculosis in selected emerging dairy regions of Ethiopia. Frontiers in Veterinary Science. 7: 553940. 10.3389/fvets.2020.553940
Michel, A.L., Müller, B., and van Helden, P.D., 2010. Mycobacterium bovis at the animal-human interface: A problem, or not? Journal of Veterinary Microbiology. 140: 371–381. 10.1016/j.vetmic.2009.08.029
Ministry of Egyptian Agriculture: Law 53 for 1966 and 207 for 1980. https://api.worldanimalprotection.org/country/egypt
Moiane, I.A., Machado, N., Santos, A., Nhambir, O., Inlamea, J., and Hattendorf, G., 2014. Prevalence of bovine tuberculosis and risk factor assessment in cattle in rural livestock areas of Govuro District in the southeast of Mozambique, PLoS One. 9: e91527. 10.1371/journal.pone.0091527
Munyeme, M.L., Rigouts, I.C., Shamputa, J.B., Muma, M., Tryland, E., and Skjerve, B., 2009. Isolation and characterization of Mycobacterium bovis strains from indigenous Zambian cattle using spacer oligonucleotide typing technique. BMC Microbiology. 9: 1–8. 10.1186/1471-2180-9-144.
Nasr, E.A., Marwah, M., Abdel Rahman, M., and Shafeek, H., 2016. Comparison of modified decontamination methods with culture systems for primary isolation of Mycobacterium bovis from bovine tissues. Benha Veterinary Medical Journal. 30: 59–67. 10.21608/bvmj.2016.31346
OIE, 2015. Office International des Epizooties (OIE) Terrestrial manual: Bovine tuberculosis, World Health Organization for Animal Health URL, https://www.oie.int/en/animal-health-in-the-world/animal-diseases/Bovine-tuberculosis/.
Pollock, J.M., McNair, J., Welsh, M.D., Girvin, R.M., Kennedy, H.E., Mackie, D.P., and Neill, S.D., 2001. Immune responses in bovine tuberculosis. Tuberculosis. 81: 103–107. 10.1054/tube.2000.0258
Reddington, J., Siobhan, S., Dick, V., and Thomas, B., 2011. A novel multiplex real-time PCR for the identification of mycobacteria associated with zoonotic tuberculosis. PLoS One. 6: 23481. 10.1371/journal.pone.0023481
Sabry, M., and Elkerdasy, A., 2014. polymerase chain reaction and enzyme linked immunosorbent assay-based approach for diagnosis and differentiation between vaccinated and infected cattle with Mycobacterium bovis. Journal of Pharmacy and Bioallied Sciences. 6: 115–121. 10.4103/0975-7406.126584
Saidu, A.S., Okolocha, E.C., Gamawa, A.A., Babashani, M., and Bakari, N.A., 2015. Occurrence and distribution of bovine tuberculosis (Mycobacterium bovis) in slaughtered cattle in the abattoirs of Bauchi State, Nigeria. Veterinary World. 8: 432–437. 10.14202/vetworld.2015.432-437
Sallam, K.I., Abd-Elghany, S.M., Hussein, M.A., Imre, K., Morar, A., Morshdy, A.E., et al., 2020. Microbial decontamination of beef carcass surfaces by lactic acid, acetic acid, and trisodium phosphate sprays. BioMed Research International. 2020: 2324358. 10.1155/2020/2324358
Shang, X., and Tonsor, G.T., 2017. Food safety recall effects across meat products and regions. Food Policy. 69: 145–153. 10.1016/j.foodpol.2017.04.002
Singhla, T., and Boonyayatra, S., 2022. Prevalence, risk factors, and diagnostic efficacy of bovine tuberculosis in slaughtered animals at the Chiang Mai Municipal abattoir, Thailand. Frontiers in Veterinary Science. 9: 846423. 10.3389/fvets.2022.846423
Thrusfield, M., Christley, R., and Brown, H., 2017. Veterinary epidemiology. 4th ed. Edinburgh, UK: Wiley-Blackwell; pp. 1–861.
Van Soolingen, D., Hermans, P.W.M., De Haas, P.E., Soll, D.R., and Van Embden, J.D.A., 1991. Occurrence and stability of insertion sequences in Mycobacterium tuberculosis complex strains: Evaluation of an insertion sequence-dependent DNA polymorphism as a tool in the epidemiology of tuberculosis. Journal of Clinical Microbiology. 29: 2578–2586. 10.1128/jcm.29.11.2578-2586.1991
Wadhwa, A., Hickling, G.J., and Eda, S., 2012. Opportunities for improved serodiagnosis of human tuberculosis, bovine tuberculosis, and paratuberculosis. Veterinary Medicine International. 2012: 674238. 10.1155/2012/674238
Wards, B.J., Collins, D.M., and De Lisle, G.W., 1995. Detection of Mycobacterium bovis in tissues by polymerase chain reaction. Veterinary Microbiology. 43: 227–240. 10.1016/0378-1135(94)00096-f
WHO, 1998. World Health Organization. Laboratory services in tuberculosis control. Geneva Switzerland: Part II: Microscopy. World Health Organization; pp. 1–63.
WHO, 2017. Roadmap for zoonotic tuberculosis. © World Heal Organ (WHO), Food Agric Organ United Nations & World Organ Anim Heal; 2017. Geneva, 1–20. https://apps.who.int/iris/handle/10665/259229
Willeberg, P.W., McAloon, C.G., Houtsma, E., Higgins, I., Clegg, T.A., and More, S.J., 2018. The herd-level sensitivity of abattoir surveillance for bovine tuberculosis: Simulating the effects of current and potentially modified meat inspection procedures in Irish cattle. Frontiers in Veterinary Science. 5: 82. 10.3389/fvets.2018.00082
Woldemariyam, F.T., Markos, T., Shegu, D., Abdi, K.D., and Paeshuyse, J., 2021. Evaluation of postmortem inspection procedures to diagnose bovine tuberculosis at Debre Birhan Municipal abattoir. Animals. 11: 2620. 10.3390/ani11092620