Non-typhoidal Salmonella among slaughterhouse workers and in the pork value chain in selected districts of Uganda

Velma Kivali; Kristina Roesel; Ian Dohoo; Lordrick Alinaitwe; James Katamba Bugeza; Jolly Justine Hoona; Denis Rwabiita Mugizi; Clovice Kankya; Sinh Dang-Xuan; Istvan Szabo; Uwe Rösler; Anika Friese; Elizabeth A J Cook

doi:10.3389/fvets.2024.1427773

Non-typhoidal Salmonella among slaughterhouse workers and in the pork value chain in selected districts of Uganda

Front Vet Sci. 2024 Sep 17:11:1427773. doi: 10.3389/fvets.2024.1427773. eCollection 2024.

Authors

Velma Kivali^{1

2

3}, Kristina Roesel^{1

2}, Ian Dohoo⁴, Lordrick Alinaitwe^{1

2

5

6}, James Katamba Bugeza^{1

2}, Jolly Justine Hoona⁷, Denis Rwabiita Mugizi^{1

2}, Clovice Kankya⁸, Sinh Dang-Xuan^{1

2}, Istvan Szabo⁹, Uwe Rösler³, Anika Friese³, Elizabeth A J Cook^{1

2}

Affiliations

¹ Animal and Human Health Program, International Livestock Research Institute, Kampala, Uganda.
² Animal and Human Health Program, International Livestock Research Institute, Nairobi, Kenya.
³ Institute for Animal Hygiene and Environmental Health, Freie University of Berlin, Berlin, Germany.
⁴ Department of Health Management, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, PE, Canada.
⁵ Veterinary Public Health Institute, University of Bern, Bern, Switzerland.
⁶ Graduate School for Cellular and Biomedical Sciences, University of Bern, Bern, Switzerland.
⁷ Department of Animal Production, Ministry of Agriculture, Animal Industry and Fisheries, Entebbe, Uganda.
⁸ College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University, Kampala, Uganda.
⁹ Department for Biological Safety, German Federal Institute for Risk Assessment, BfR, Berlin, Germany.

Abstract

Introduction: Non-typhoidal Salmonella (NTS) is a major cause of gastroenteritis worldwide, often associated with meat consumption and meat processing. Research on NTS infection and circulating serovars in meat value chains in Uganda is limited. We aimed to establish NTS prevalence, antimicrobial resistance, and risk factors among slaughterhouse workers, and to identify potentially zoonotic serovars in the pork value chain.

Material and methods: We conducted a nationwide cross-sectional survey, collecting 364 stool samples from livestock slaughterhouse workers and 1,535 samples from the pork value chain: mesenteric lymph nodes, fecal samples, swabs of carcass splitting floor, cleaning water, meat handlers hand swabs, carcass swabs, raw pork, cooked pork, and mixed raw vegetables. Samples were cultured for isolation of NTS, and subsequently serotyped according to White-Kauffmann-Le Minor scheme. Antimicrobial resistance profiles were determined using tube microdilution and Sensititre^® EUVSEC3^® plates. Semi- structured questionnaires with 35 questions were used to collect data on demographics, work related risk factors and activities outside the slaughterhouse.

Results and discussion: Overall NTS prevalence was 19.2% (365/1899). Proportions at slaughter were; 46.7% in floor swabs, 30.5% in carcass swabs, 20.5% in pig faeces,19.2% in mesenteric lymph nodes,18.4% in hand swabs, 9.5% in water and 5.2% in slaughterhouse workers. At retail, proportions were 33.8% in pork chopping surface, 33.1% in raw pork, 18.9% in hand swabs, 4.0% in cooked pork and 0.7% in vegetables. Sixty-one serovars were identified, with significant overlap between humans and the pork value chain. Overall, zoonotic S. Zanzibar, monophasic serovars of S. subspecies salamae (II) and subspecies enterica (I), S. Typhimurium and S. Newport, were the most prevalent. S. Typhimurium was predominant in humans and exhibited multi-drug resistance. NTS infection was significantly associated with eating, drinking, or smoking while working (OR = 1.95, 95% CI: 0.67-2.90%, p = 0.004). The detected NTS serovars in slaughterhouse workers could be a potential indicator of circulating serovars in the general population. The persistent presence of NTS along the pork value chain highlights occurrence of cross-contamination and the potential for transmission to consumers and slaughterhouse workers. This emphasizes the need to reduce Salmonella prevalence on pig farms and improve hygiene and pork handling practices at slaughter and retail points.

Keywords: NTS serovars; Uganda; non-typhoidal Salmonella; pork value chain; slaughterhouse workers.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was funded by the German Federal Ministry of Economic Cooperation and Development (BMZ) through the project Boosting Uganda’s Investment in Livestock Development (BUILD) (Grant number BMZ001). Additional support was received from the CGIAR Research Programs on Livestock and Agriculture for Nutrition and Health. We also acknowledge the CGIAR Initiative on One Health (Protecting human health through a One Health approach) and the CGIAR Fund Donors (https://www.cgiar.org/funders).