Salmonella in Chicken and Pork Meat as a Likely Major Contributor to Foodborne Illness in Peru

Ana Cecilia Ho-Palma Department of Human Medicine, School of Human Medicine, Universidad Nacional del Centro del Peru, Huancayo, Peru;

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Eloy Gonzales-Gustavson Department of Animal and Public Health, School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru;
Tropical and Highlands Veterinary Research Institute, Universidad Nacional Mayor de San Marcos, Jauja, Peru;

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Enrique Quispe School of Engineering on Food Industries, Universidad Nacional del Centro del Peru, Huancayo, Peru;

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Matteo Crotta Veterinary Epidemiology, Economics and Public Health Group, WOAH Collaborating Centre for Risk Analysis and Modelling, Department of Pathobiology and Population Sciences, The Royal Veterinary College, Hertfordshire, United Kingdom;

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Erica Nunney Veterinary Epidemiology, Economics and Public Health Group, WOAH Collaborating Centre for Risk Analysis and Modelling, Department of Pathobiology and Population Sciences, The Royal Veterinary College, Hertfordshire, United Kingdom;

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Georgina Limon Veterinary Epidemiology, Economics and Public Health Group, WOAH Collaborating Centre for Risk Analysis and Modelling, Department of Pathobiology and Population Sciences, The Royal Veterinary College, Hertfordshire, United Kingdom;

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Daniel Andrade-Mogrovejo Department of Animal and Public Health, School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru;

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Jorge Pastor Subdirección de Inocuidad Agroalimentaria, Servicio Nacional de Sanidad Agraria del Peru, Lima, Peru;

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Emilio Yabar School of Engineering on Food Industries, Universidad Nacional del Centro del Peru, Huancayo, Peru;

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José Solis School of Engineering on Food Industries, Universidad Nacional del Centro del Peru, Huancayo, Peru;

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Luis Ordoñez Centro Nacional de Epidemiología, Prevención y Control de Enfermedades, Ministerio de Salud, Lima, Peru;

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Armando Gonzalez Department of Animal and Public Health, School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru;
School of Public Health and Administration, Universidad Peruana Cayetano Heredia, Lima, Peru

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Javier Guitian Veterinary Epidemiology, Economics and Public Health Group, WOAH Collaborating Centre for Risk Analysis and Modelling, Department of Pathobiology and Population Sciences, The Royal Veterinary College, Hertfordshire, United Kingdom;

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Nontyphoidal Salmonella is one of the major causes of self-limiting diarrheal disease and the most common foodborne pathogen worldwide. It is an important contributor to the burden of foodborne illness in South America, including Peru, where chicken and pork are important vehicles for Salmonella infection. Salmonella infections are underreported, particularly in low- and middle-income countries where concerted action tackling Salmonella along the chicken and pork chains, from primary production to retail, is urgently needed. To support and inform the implementation of new strategies to reduce Salmonella contamination of chicken and pork, this study describes the frequency and distribution of foodborne outbreaks attributed to Salmonella in Peru and evaluates the level of Salmonella in chicken and pork meat sold in markets of three regions of Peru. To that end, we analyzed historical reports of foodborne outbreaks, levels of Salmonella in chicken and pork sold in markets, and the number of mesophiles in the collected meat samples. As a result, the microbiological analysis reveals a widespread contamination of chicken (77.1%) and pork (26.8%) with Salmonella. It also pinpoints Salmonella as the causative agent in nearly half of the outbreaks (47.0%) where the potential origin is identified over a 11-year period with chicken, mayonnaise, and pork being the most likely food vehicles. These results suggest that Salmonella is a major contributor to foodborne illness in Peru and that the monitoring of mesophiles could be a good strategy for surveillance, generating data to support source attribution studies and ultimately evidence-informed policies.

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Author Notes

Financial support: This work was supported by the Medical Research Council (grant no. MR/S025049/1) and PROCIENCIA/FONDECYT (grant no. 0247-2019-FONDECYT).

Disclosure: Ethics clearance was obtained from the institutional research ethics committee of the Universidad Peruana Cayetano Heredia (Constancia 516-22-19). Matteo Crotta is now employed by the European Food Safety Authority (EFSA). However, the present article is published under the sole responsibility of the authors and may not be considered as an EFSA scientific output. positions and opinions presented in this article are those of the authors alone and do not necessarily represent the views/any official position or scientific works of EFSA. To know about the views or scientific outputs of EFSA, please consult its website www.efsa.europa.eu.

Authors’ contributions: A. C. Ho-Palma: conceptualization, methodology, validation, investigation, resources, writing—original draft, writing—review and editing, visualization. E. Gonzales-Gustavson: conceptualization, methodology, validation, data analysis, investigation, resources, data curation, writing—original draft, writing—review and editing, visualization, supervision, project administration, funding acquisition. E. Quispe: methodology, validation, investigation, data curation, writing—review and editing, visualization. G. Limon: conceptualization, methodology, writing—original draft, writing—review and editing, supervision, data analysis. M. Crotta: conceptualization, methodology, writing—original draft, writing—review and editing, supervision, data analysis. E. Nunney: data analysis, data curation, writing—original draft, writing—review and editing. J. Pastor: conceptualization, resources, writing—review and editing. D. Andrade-Mogrovejo: data analysis, data curation, writing—review and editing. E. Yabar: conceptualization, resources, writing—review and editing. J. Solis: conceptualization, resources, writing—review and editing. L. Ordoñez: resources, writing—review and editing. A. Gonzalez: conceptualization, methodology, resources, writing—review and editing, funding acquisition. J. Guitian: conceptualization, methodology, data analysis, resources, writing—original draft, writing—review and editing, supervision, project administration, funding acquisition.

Authors’ addresses: Ana Cecilia Ho-Palma, Department of Human Medicine, School of Human Medicine, Universidad Nacional del Centro del Peru, Huancayo, Peru, E-mail: ahopalma@uncp.edu.pe. Eloy Gonzales-Gustavson, Department of Animal and Public Health, School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru; and Tropical and Highlands Veterinary Research Institute, Universidad Nacional Mayor de San Marcos, Jauja, Peru, E-mail: egonzalesg@unmsm.edu.pe. Enrique Quispe, School of engineering on food industries, Universidad Nacional del Centro del Peru, Huancayo, Peru, E-mail: enrique.quispe@upch.pe. Matteo Crotta, Erica Nunney, and Georgina Limon, Veterinary Epidemiology, Economics and Public Health Group, WOAH Collaborating Centre for Risk Analysis and Modelling, Department of Pathobiology and Population Sciences, The Royal Veterinary College, Hertfordshire, United Kingdom, E-mails: glimon@rvc.ac.uk, mcrotta4@rvc.ac.uk, and Enunney18@rvc.ac.uk. Daniel Andrade-Mogrovejo, Department of Animal and Public Health, School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru, E-mail: daniel.andrade@unmsm.edu.pe. Jorge Pastor, Subdirección de Inocuidad Agroalimentaria, Servicio Nacional de Sanidad Agraria del Peru, Lima, Peru, E-mail: jpastor@senasa.gob.pe. Emilio Yabar and Jose Solis, School of Engineering on Food Industries, Universidad Nacional del Centro del Peru, Huancayo, Peru, E-mails: eyabar@uncp.edu.pe and jsolis@uncp.edu.pe. Luis Ordoñez, Centro Nacional de Epidemiología, Prevención y Control de Enfermedades, Ministerio de Salud, Lima, Peru, E-mail: lordonez@dge.gob.pe. Armando Gonzalez, School of Public Health and Administration, Universidad Peruana Cayetano Heredia, Lima, Peru, and Department of Animal and Public Health, School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru, E-mail: armando.gonzalez@upch.pe. Javier Guitian, Veterinary Epidemiology, Economics and Public Health Group, WOAH Collaborating Centre for Risk Analysis and Modelling, Department of Pathobiology and Population Sciences, The Royal Veterinary College, Hertfordshire, United Kingdom, E-mail: Jguitian@rvc.ac.uk.

Address correspondence to Eloy Gonzales-Gustavson, Tropical and Highlands Veterinary Research Institute, Universidad Nacional Mayor de San Marcos, Av. 28 de Julio s/n, El Mantaro—Jauja (Junin), Peru. E-mail: egonzalesg@unmsm.edu.pe
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