Alexandria Journal of Veterinary Sciences www.alexjvs.com AJVS. Vol. 52: 1-5. January 2017 DOI: 10.5455/ajvs.246283 Detection of Mammary Tuberculosis in Slaughtered Cattle and Consequent Risk of Zoonosis to Human in Nigeria Ibrahim Ahmad 1, Caleb Ayuba Kudi 2, Nabila Dalhatu 3 1 Directorate of Animal Health and Livestock Development, Old Cabinet Office, Canteen Area Gusau, Zamfara State Nigeria. 2 Department of Veterinary Medicine, Faculty of Veterinary Medicine, Ahmadu Bello University Zaria, Nigeria. 3 National Agency for Food and Drug Administration and Control, Plot 2032, Olusegun Obasanjo Way, Wuse Zone 7, Abuja. Key words: Mammary tuberculosis; slaughtered cattle; zoonosis; Nigeria Correspondence to: Ibrahim Ahmad, ibrahimahmaad22@gmail.com Abstract Tuberculosis lesions are often more confined to thoracic region and associated lymph nodes than other body parts, as mostly documented in the surveillance studies of cattle tuberculosis in Nigeria. We report a detection of combined pulmonary and a rare extra-pulmonary (mammary) tuberculosis in two zebu cows slaughtered for human consumption. Tubercle bacilli may be disseminated to different anatomic locations in diseased animals, zoonotic transmission of these infective bacilli is predominantly acquired by consumption of unpasteurized milk and its products and poorly processed meat from diseased animals. The risks of intra-and-inter species exposure to tuberculosis as it relates to predominant livestock husbandry, eating habits and food preference in Nigeria were discussed. 1. INTRODUCTION Tuberculous mastitis is a chronic disease associated with granulomatous/caseous degeneration of the milk glands caused by Mycobacterium bovis or Mycobacterium tuberculosis, it is usually a reflection of tuberculosis of other organ(s) but can also occur independently, both posing a potential zoonotic threat (Shaheem et al., 2016). Once bovine tuberculosis (btb) is established, infection spreads between animals via aerosols, suckling, direct contact, and sharing of water and feeds (El-Sayed et al., 2016). While, man often acquires zoonotic tuberculosis through consumption of raw infected dairy products, ingestion of infected meat, and via aerosols by close and repeated contact with tuberculous cattle. Because mammary tuberculosis is rare and can be mistaken for pyogenic inflammatory disease or carcinoma of the mammary tissues, it requires a high index of suspicion to make a clinical diagnosis owing to its nonspecific ante-mortem symptoms in cattle until at the advanced stage. Post-mortem inspection at slaughterhouse turns out to be an effective tool for early detection of btb epidemics, evidence of btb infection at necropsy is more specific in comparisons to some weakness of prevalence by ante-mortem test(s) (Rossi et al., 2015; Broughan et al., 2016); hence, detection of gross TB pathology can be relied on for the diagnosis of bovine TB in developing countries where prevalence of the disease is high (Saidu et al., 2015; Elmonir and Ramadan, 2016). This report presents one of the rare detection of bovine TB infection that involves mammary tissues of cows in Nigeria, discuss the risk of zoonotic transmission as it regards the location of the observed pathology. 2. MATERIALS AND METHODS 2.1 Study area The study was conducted in Zamfara State (Northwest region of Nigeria) at a slaughterhouse. Zamfara State covers a land area of 39,762km 2, is located between latitudes 37 on to 12 42 N and longitudes 04 23 E to 5 52 E, and has an estimated 3,259,846 human population. A range of 32 to 55 head of cattle are being slaughtered daily according to an established record; cattle brought to this facility 1
for slaughter were drawn from different local herds and markets in the study area. 2.2 Necropsy and study animals On 12 th August 2016, slaughtered cow of estimated more than 6 years old White Fulani breed was observed to have bilaterally enlarged mammary glands at necropsy. Thorough postmortem inspection revealed multiple tubercles deeply seated in all of the mammary tissues along with scanty lesions in the lungs of the same animal (Fig. 1, 2, 3). By 2 nd September 2016, another cow older than 6 years of the same breed was observed to have similar but unilateral pathology of the mammary gland, and scores of tubercles in the lungs (Fig. 4, 5, 6). At inspection, the animals have a good body condition score, both have been purchased from one of the markets where cattle are being lifted from North to Southern Nigeria. Unfortunately, details of previous medical history or herd of origin for disease trace back could not be obtained from the butchers as such records are not filed up along with animal movement in Nigeria. Cattle production in Nigeria is largely by extensive and pastoral systems, predominantly being practiced in northern region by Hausa-Fulani ethnic communities; it is majorly focused on production of food animals raised for slaughter and dairy purposes nationwide, in which milk and meat yields are both consumed at homes and sold at the local markets. However, little or no attention is being given on routine vaccination and proper medication of the animals in the country. 3. RESULTS AND DISCUSSION This report presents an extremely rare and an uncommon occurrence of pulmonary (Fig. 1 and 4) and extra-pulmonary TB with severe lesions localized in the mammary tissues (Fig. 2, 3, 5 and 6). In-spite of the higher prevalence of btb in Nigeria, there were rarely reported cases that involved the lactating glands of cattle. From natural and experimental infection studies in cattle, btb characteristics lesions are well known as tuberculous granulomas most commonly noted in the lungs and lymph nodes (Waters and Palmer, 2015); thus, the diagnosis of these cases was based on the presence of tuberculous lesions, observed during postmortem meat inspection. The findings revealed btb infection in apparently healthy cows that appeared normal, but might had been infected and spread the disease for a period of time without any clinical manifestation. Figure 1: Lungs with tubercles (yellowish colored). Figure 2: Enlarged mammary gland with tuberculous lesions (cheese-like) on cut surface; before it was cut off from the carcass. Figure 3: Incised left and right mammary quarters with caseous necrosis typical of granulomatous reaction. Figure 4: Lungs with discreet tubercles (yellowish colored). 2
Figure 5: Enlarged tuberculous mammary gland with multiple tubercles (yellowish) in parenchymatous tissues. Figure 6: Cut opened mammary quarter (left) with yellowish cheese-like tuberculous lesions typical of granulomatous reaction. Localization and distribution of btb lesions are mostly observed higher in the organs associated with the thoracic region, less in the organs of abdominal cavity, but rarely in mammary tissues of the animals. Although infected cattle are the main reservoir hosts of M. bovis, TB lesions that might have been caused by M. tuberculosis or other members of Mycobacterium tuberculosis complex cannot be grossly distinguished. Mammary TB may be primary where lesions in lactating tissues are the only presentation of the disease, infection maybe when tubercle bacilli are transmitted direct to mammary glands via dilated ducts of the more susceptible pregnant and lactating cows, or it may also be secondary in which infection is being disseminated from primary foci through lymphatics and haematogenous routes by the migration of infected macrophages into the other parts of the body; consequence of either weak immunity on the part of the host inability to wall-off the primary infection or when very virulent tubercle bacilli is involved. In immuno-competent hosts, mycobacteria are phagocytosed and eliminated by the resident macrophages in the early phase of the infection or, tuberculoid granulomas are formed to prevent further spread of infection to the surrounding tissues consequence of interleukins-mediated cellular responses. However, replication of tubercle bacilli with reactivation and spread of infection, are enhanced by immuno-suppression that can disturb the balance between host control and agent dissemination leading to the spread of infection to all tissues (Fell et al., 2016); hence, mycobacteria will be shed via secretion/excretion of the diseased animal, becoming a point-source of infection to other susceptible hosts (man and animals). Previous study indicated that pregnant and lactating cows are most at risk of having btb, two times more compared to bulls (Ghebremariam et al., 2016); thus, hormonal shifts and stresses throughout production are the likely factors that affect susceptibility to btb infection in dairy cow (Broughan et al., 2016). Mammary TB of cattle is of grave concern to public health, due to the risk of milk borne zoonosis from M. bovis or M. tuberculosis that is enhanced by an increased level of raw milk consumption in Nigeria. M. bovis has been detected from the widely consumed fresh and fermented cattle milk sold in local markets in various parts of Nigeria (Ofukwu et al., 2008; Cadmus et al., 2010); nationwide, milk pooled from cows are consumed either as fresh or in soured form locally called Nono without any prior pasteurization, and the chances for zoonotic transmission to human are high. Similarly, M. bovis has been detected in 26.5% of unpasteurized milk samples in Burkina Faso (Sanou et al., 2014), and 8% incidence rate of M. bovis in raw cattle milk was reported in Iraq (Al-Sanjary et al., 2013). Recently, btb infection has been reported among dairy cows in India, the study suggested that tubercle bacilli are intermittently discharge in the milk of tuberculous cattle (Thakur et al., 2016). In some cases, M. bovis infection in cattle may involve udder lesions with the consequent tubercle bacilli being excreted in their milk, such milk from a single tuberculous cow when mixed can contaminate 100 gallons of milk from non-infected animals, all potentially infectious to animals and man if consumed unpasteurized (Hussein and Mahrous, 2016). Previous studies from different countries have shown that M. bovis is being shed in the milk of negative tuberculin tested cows (Zumarraga et al., 2012; Zarden et al., 2013). Bovine TB is endemic in cattle than in any other livestock population in Nigeria, in which the varying incidence rates of the disease from area to area continued to rise from 2.5% in 1976 to 15% in 2015. There is limited or no control of btb, only meat inspection is being used to detect outbreaks and it is 3
solemnly relied upon to limit public health risks of the disease in Nigeria. However, about 3.1% of all human TB cases worldwide are caused by M. bovis (El-Sayed et al., 2016); out of which approximately 2.8% rates are reported for continental Africa (Muller et al., 2013), and ~5% rate was estimated in Nigeria (Cadmus et al., 2006). 4. CONCLUSIONS This study reports a rare form of btb in cattle, which highlighted the risk of exposure to infection in human and animal population in Nigeria. General public should be strongly cautioned against the consumption of raw dairy products, and meat processed from unauthorized slaughterhouses; hence, policy needs to be adopted at a large scale with respect to pasteurization of milk and its products in Nigeria. 5. CONFLICT OF INTEREST There is no conflict of interests in respect to authorship and publication of this article. 6. ACKNOWLEDGEMENTS We are grateful to Dr Fatima Bello (Director Public Health), Dr Munzir Abbas and Dr Umar Muhammad of the Directorate of Animal Health and Livestock Development Zamfara State Nigeria, for the logistic support. 7. Funding None. 8. Ethical approval Not required. 9. REFERENCES Al-Sanjary, R.A., Sheet, O.H., Jwher, Dh.M.T. 2013. Direct detection of Mycobacterium tuberculosis and Mycobacterium bovis in cattle raw milk by using species-specific PCR technique. Assiut Vet. Med. J. 59(136): 1-4. Broughan, J.M., Judge, J., Ely, E., Delahay, R.J., Wilson, G., Clifton-Hadley, R.S., Goodchild, A.V., Bishop, H., Parry, J.E., Downs, S.H., 2016. A review of risk factors for bovine tuberculosis infection in cattle in the UK and Ireland. Epidemiology and Infection. Cadmus, S., Palmer, S., Okker, M., Dale, J., Gover, K., Smith, N., Jahans, K., Hewinson, R.G., Gordon, S.V. 2006. Molecular analysis of human and bovine tubercle bacilli from a local setting in Nigeria. Journal of Clinical Microbiology 44: 29-34. Cadmus, S.I.B., Yakubu, M.K., Magaji, A.A., Jenkins, A.O., van Soolingen, D. 2010. Mycobacterium bovis, but also Mycobacterium africanum present in raw milk of pastoral cattle in North-Central Nigeria [Brief communication]. Tropical Animal Health and Production. http://dx.doi:10.1007/s11250-010-9533-2. Elmonir, W., Ramadan, H. 2016. Abattoir based prevalence, economic losses and veterinarians high-risk practices survey of bovine tuberculosis in Mid-Delta of Egypt. Alexandria Journal of Veterinary Sciences 49(2): 24-30. El-Sayed, A., El-Shannat, S., Kamel, M., Castaneda- Vazquez, M.A., Castaneda- Vazquez, H. 2016. Molecular epidemiology of Mycobacterium bovis in humans and cattle: a review. Zoonoses and Public Health 63: 251-264. Fell, S., Brockl, S., Buttner, M., Rettinger, A., Zimmermann, P., Straubinger, K. 2016. Two alternative DNA extraction methods to improve the detection of Mycobacterium tuberculosis complex members in cattle and red deer tissue samples. BMC Microbiology 16: 213. Doi:10.1186/s12866-016- 0816-2 Ghebremariam, M.K., Rutten, V.P.M., Vernooij, J.C.M., Uqbazghi, K., Tesfaalem, T., Butsuamlak, T., Idris, A.M., Nielen, M., Michel, A.L. 2016. Prevalence and risk factors of bovine tuberculosis in dairy cattle in Eritrea. BMC Veterinary Research 12: 80. Doi:10.1186/s12917-016-0705-9. Hussein, H., Mahrous, E. 2016. Isolation and molecular characterization of Mycobacterium tuberculosis complex isolated from raw milk in some dairy farms in Egypt. International Journal of Basic and Applied Science 5(2): 105-109. Muller, B., Durr, S., Alonso, S., Hattendorf, J., Laisse, C.J., Parsons, S.D., van Helden, P.D., Zinsstag, J. 2013. Zoonotic Mycobacterium bovis-induced tuberculosis in humans. Emerging Infectious Diseases 19: 899-908. Ofukwu, R.A. 2008. Zoonotic Mycobacterium species in fresh cow milk and fresh skimmed, unpasteurized market milk (nono) in Makurdi, Nigeria: implications for public health. Journal of Animal and Plant Sciences 1(1): 21-25. Rossi, G., De Leo, G.A., Pongolini, S., Natalini, S., Vincenzi, S., Bolzoni, S. 2015. Epidemiological modelling for the assessment of bovine tuberculosis surveillance in the dairy farm network in Emilia- Romana (Italy). Epidemics 11: 62-70. Saidu, A.S., Okolocha, E.C., Gamawa, A.A., Babashani, M., 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(3): 432-437. Sanou, A., Tarnagda, Z., Kanyala, E., Zingue, D., Nouctara, M., Ganame, Z., Combary, A., Hien, H., Dembele, M., Kabore, A., Meda, N., Van de Perre, P., Neveu, D., Banuls, A.L., Godreuil, S. 2014. Mycobacterium bovis in Burkina Faso: epidemiologic and genetic links between human and cattle isolates. PLoS Neglected Tropical Diseases 8: e3142. 4
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