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The milk delivery chain and presence of Brucella spp. antibodies in bulk milk in Uganda

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Abstract

This study examined the influence of informal milk delivery chains on the risk of human exposure to Brucella spp. through milk consumption in two regions of Uganda (Gulu and Soroti Districts). The work involved describing milk delivery chains, investigating brucellosis awareness amongst milk deliverers and determining the presence of Brucella spp. antibodies in cattle milk on delivery to primary collection points (boiling points and dairies). Milk samples (n = 331) were collected from deliverers at primary collection points and from street vendors at point of sale and analysed using indirect enzyme-linked immunosorbent assay (I-ELISA). A written questionnaire was used to collect data from deliverers (n = 279) on their milk delivery chains and their brucellosis awareness. The most common delivery points in Gulu District were small dairies and in Soroti District boiling points. The presence of Brucella spp. antibodies in milk samples was higher in Soroti (40 %) than in Gulu (11 %) (P < 0.0001). There are possible public health risk consequences of this finding as 42 % of deliverers in Soroti District reported drinking raw milk, compared with 15 % in Gulu District (P < 0.0001). Awareness of brucellosis was low, with 70 % of all milk deliverers reporting not having heard of the disease or the bacterium. Application of quality controls for milk (colour and odour) along the delivery chain varied depending upon supply and demand. This study provides evidence of the diversity of informal milk markets in low-income countries and of the potential public health risks of consuming unpasteurised milk. These results can be useful to those planning interventions to reduce brucellosis.

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References

  • Adesokan, H.K., Alabi, P.I., Stack, J.A., Cadmus, S.I., 2013. Knowledge and practices related to bovine brucellosis transmission amongst livestock workers in Yewa, south-western Nigeria. Journal of the South African Veterinary Association 84, E1-5

  • Alarcon, P., Wieland, B., Mateus, A.L., Dewberry, C., 2014. Pig farmers’ perceptions, attitudes, influences and management of information in the decision-making process for disease control, Preventive Veterinary Medicine, 116, 223–242

    Article  PubMed  Google Scholar 

  • Balikowa, D., 2011. Dairy development in Uganda. A review of Uganda’s dairy industry. In: Ministry of Agriculture, Animal Industry and Fisheries, Uganda; Food and Agriculture Organization of the United Nations; Dairy Development Authority, Uganda

  • Benon, K.M., Owiny, D.O., Bage, R., Nassuna-Musoke, M.G., Humblot, P., Magnusson, U., 2015. Managerial practices and factors influencing reproductive performance of dairy cows in urban/peri-urban areas of Kampala and Gulu, Uganda, Acta Veterinaria Scandinavica, 57, 35

    Article  Google Scholar 

  • CDC (Centres of Disease Control and Prevention). http://www.cdc.gov/brucellosis/index.html. Accessed 15 Feb 2016

  • Diaz Aparicio, E., 2013. Epidemiology of brucellosis in domestic animals caused by Brucella melitensis, Brucella suis and Brucella abortus. Revue Scientifique et Technique, 32, 43–51, 53–60

    Article  Google Scholar 

  • Galinska, E.M., Zagorski, J., 2013. Brucellosis in humans—etiology, diagnostics, clinical forms, Annals of Agricultural and Environmental Medicine, 20, 233–238

    PubMed  Google Scholar 

  • Godfroid, J., Nielsen, K., Saegerman, C., 2010. Diagnosis of brucellosis in livestock and wildlife, Croatian Medical Journal, 51, 296–305

    Article  PubMed  PubMed Central  Google Scholar 

  • Grace, D., Dipeolu, M., Olawoye, J., Ojo, E., Odebode, S., Agbaje, M., Akindana, G., Randolph, T., 2012a. Evaluating a group-based intervention to improve the safety of meat in Bodija market, Ibadan, Nigeria, Tropical Animal Health and Production, 44 Suppl 1, S61-66

    Article  PubMed  Google Scholar 

  • Grace, D., Mutua, F., Ochungo, P., Kruska, R., Jones, K., Brierley, L., Lapar, L., Said, M., Herrero, M., Phuc, P.M., Thao, N.B., Akuku, I., Ogutu, F., 2012b. Mapping of poverty and likely zoonoses hotspots. Zoonoses Project 4. Report to the UK Department for International Development. International Livestock Research Institute, Nairobi, Kenya

    Google Scholar 

  • Grace, D., Makita, K., Kang’ethe, E., Bonfoh, B., Roesel, K., 2015. Taking food safety to informal markets. In: K. Roesel and D. Grace (eds), Food safety and informal markets—animal products in sub-Saharan Africa, (Routledge, Abingdon, UK9), 11–22

  • Grimaud, P., Sserunjogi, M., Wesuta, M., Grillet, N., Kato, M., Faye, B., 2009. Effects of season and agro-ecological zone on the microbial quality of raw milk along the various levels of the value chain in Uganda, Tropical Animal Health and Production, 41, 883–890

    Article  PubMed  Google Scholar 

  • Havelaar, A.H., Kirk, M.D., Torgerson, P.R., Gibb, H.J., Hald, T., Lake, R.J., Praet, N., Bellinger, D.C., de Silva, N.R., Gargouri, N., Speybroeck, N., Cawthorne, A., Mathers, C., Stein, C., Angulo, F.J., Devleesschauwer, B., World Health Organization Foodborne Disease Burden Epidemiology Reference, G., 2015. World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010, PLoS medicine, 12, e1001923

    Article  PubMed  PubMed Central  Google Scholar 

  • Herrero, M., Grace, D., Njuki, J., Johnson, N., Enahoro, D., Silvestri, S., Rufino, M.C., 2013. The roles of livestock in developing countries. Animal: an International Journal of Animal Bioscience, 7 Suppl 1, 3–18

    Article  Google Scholar 

  • HI 2015. East Africa Dairy Development, Heifer International. http://www.heifer.org/eadd/index.html. Accessed 4 Dec 2015

  • MAAIF. 2009. The national livestock census report 2008. Ministry of Agriculture, Animal Industry and Fisheries (MAAIF), Entebbe/Uganda Bureau of Statistics, Kampala, Uganda

  • Makita, K., Fevre, E.M., Waiswa, C., Eisler, M.C., Welburn, S.C., 2010. How human brucellosis incidence in urban Kampala can be reduced most efficiently? A stochastic risk assessment of informally-marketed milk, Plos One 5, doi: 10.1371/journal.pone.0014188

    PubMed  PubMed Central  Google Scholar 

  • Makita, K., Fevre, E.M., Waiswa, C., Kaboyo, W., Eisler, M.C., Welburn, S.C., 2011. Evidence-based identification of the most important livestock related zoonotic diseases in Kampala, Uganda, Journal of Veterinary Medical Science, 73, 991–1000

    Article  Google Scholar 

  • McDermott, J., Grace, D., Zinsstag, J., 2013. Economics of brucellosis impact and control in low-income countries, Revue Scientifique et Technique, 32, 249–261

    Article  CAS  PubMed  Google Scholar 

  • Miller, R., Nakavuma, J.L., Ssajjakambwe, P., Vudriko, P., Musisi, N., Kaneene, J.B., 2015. The prevalence of brucellosis in cattle, goats and humans in rural Uganda: a comparative study, Transboundary and Emerging Diseases, doi: 10.1111/tbed.12332

    Google Scholar 

  • Mugizi, D.R., Boqvist, S., Nasinyama, G.W., Waiswa, C., Ikwap, K., Rock, K., Lindahl, E., Magnusson, U., Erume, J., 2015. Prevalence of and factors associated with Brucella sero-positivity in cattle in urban and peri-urban Gulu and Soroti towns of Uganda, Journal of Veterinary Medical Science, 77, 557–564

    Article  PubMed  PubMed Central  Google Scholar 

  • Mugizi, D.R., Muradrasoli, S., Boqvist, S., Erume, J., Nasinyama, G.W., Waiswa, C., Mboowa, G., Klint, M., Magnusson, U., 2015. Isolation and molecular characterization of Brucella isolates in cattle milk in Uganda, BioMed Research International, doi: 10.1155/2015/720413

    PubMed  PubMed Central  Google Scholar 

  • OIE, 2009. Bovine brucellosis. Chapter 2.4.3. In: OIE Terrestrial Manual 2009 (Paris, France)

  • Osoro, E.M., Munyua, P., Omulo, S., Ogola, E., Ade, F., Mbatha, P., Mbabu, M., Ng’ang’a, Z., Kairu, S., Maritim, M., Thumbi, S.M., Bitek, A., Gaichugi, S., Rubin, C., Njenga, K., Guerra, M., 2015. Strong association between human and animal Brucella seropositivity in a linked study in Kenya, 2012–2013, American Journal of Tropical Medicine and Hygiene, 93, 224–231

    Article  PubMed  PubMed Central  Google Scholar 

  • Roesel, K., Grace, D., Toyomaki, H., Mwai, C., Desissa., F. 2015. Informal markets are not necessarily dangerous and formal markets are not necessarily safe. In: K. Roesel and D. Grace (eds), Food safety and informal markets—animal products in sub-Saharan Africa, (Routledge, Abingdon, UK9), 23–30

  • Smits, H.L., 2013. Brucellosis in pastoral and confined livestock: prevention and vaccination. Revue Scientifique et Technique 32, 219–228

    Article  CAS  PubMed  Google Scholar 

  • Svanova 2009. SVANOVIR Brucella-Ab I-ELISA—summary of evaluation data. http://www.svanova.com/content/dam/internet/ah/svanova/dk_EN/documents/Performance%20reviews/Scientific%20folder%20Brucella%2009-04.pdf. Accessed 6 Dec 2015.

  • Swai, E.S., Schoonman, L., 2011. Microbial quality and associated health risks of raw milk marketed in the Tanga region of Tanzania, Asian Pacific Journal of Tropical Biomedicine, 1, 217–222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tschopp, R., Abera, B., Sourou, S.Y., Guerne-Bleich, E., Aseffa, A., Wubete, A., Zinsstag, J., Young, D., 2013. Bovine tuberculosis and brucellosis prevalence in cattle from selected milk cooperatives in Arsi zone, Oromia region, Ethiopia, BMC Veterinary Research, 9, doi: 10.1186/1746-6148-9-163

  • Tumwine, G., Matovu, E., Kabasa, J.D., Owiny, D.O., Majalija, S., 2015. Human brucellosis: sero-prevalence and associated risk factors in agro-pastoral communities of Kiboga District, central Uganda, BMC public health, 15, 900

  • UBOS 2014. Statistical abstract 2014. Entebbe/Uganda Bureau of Statistics, Kampala, Uganda

    Google Scholar 

  • Wamalwa, K., Castiello, M., Ombui, J.N., Gathuma, J., 2012. Capacity building: benchmark for production of meat with low levels of bacterial contamination in local slaughterhouses in Somaliland, Tropical Animal Health and Production, 44, 427–433

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was financially supported by the SLU Global Food Security Research and Education Programme 2010–2013 (UD40), the Ministry for Foreign Affairs. We would like to thank Makerere University Institute of Environment and Natural Resources in Kampala, Uganda, for their assistance in laboratory analyses. We also gratefully acknowledge the essential participation of Tonny Kidega, Tony Aliro, Charles Ariko, Patrick Eyudu, and Kokais Ikwap for the assistance and translation. The management and staff of Gulu Women’s Dairy, Gulu Progressive Dairy (Milk Matters), Patiko-Bardege Gulu and Soroti Dairy and Aarapoo Dairy Farmers Association, Soroti, are thanked for their cooperation as are farmers and street vendors of Gulu and Soroti.

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Authors and Affiliations

  1. Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences, SE-750 07, Uppsala, Sweden

    Kim Toeroek Rock & Sofia Boqvist

  2. Department of Biomolecular Resources and Biolab Sciences, College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University, P.O. Box 7062, Kampala, Uganda

    Denis Rwabiita Mugizi

  3. Department of Disease Control and Epidemiology, National Veterinary Institute, 751 89, Uppsala, Sweden

    Karl Ståhl

  4. Department of Clinical Sciences, Swedish University of Agricultural Sciences, SE-750 07, Uppsala, Sweden

    Ulf Magnusson

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  1. Kim Toeroek Rock
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  2. Denis Rwabiita Mugizi
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  4. Ulf Magnusson
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  5. Sofia Boqvist
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Correspondence to Sofia Boqvist.

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The authors of this study state they have no conflict of interest.

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No animals were involved in this study.

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Informed consent was obtained from all individual participants included in the study.

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Rock, K.T., Mugizi, D.R., Ståhl, K. et al. The milk delivery chain and presence of Brucella spp. antibodies in bulk milk in Uganda. Trop Anim Health Prod 48, 985–994 (2016). https://doi.org/10.1007/s11250-016-1052-3

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