Occurrence and distribution of Salmonella serovars associated with human infection isolated from irrigation waters and food-producing animals in southern Italy: eleven-year monitoring (2011-2021)


Submitted: 23 June 2023
Accepted: 3 August 2023
Published: 26 October 2023
Abstract Views: 727
PDF: 151
HTML: 11
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

Salmonella is one of the main zoonotic agents causing foodborne diseases in Europe. The main reservoirs of the infection are represented by domestic and wild animals, and the infection occurs by direct contact or following the consumption of contaminated food or water. The study aimed to evaluate the presence of Salmonella spp. in food-producing animals and irrigation waters in southern Italy and the serovar distribution. From 2011 to 2021, a total of 473 samples from 6 different animal species (bovine, buffalo, goat, ovine, swine, poultry, and wild boars) and 313 irrigation water samples were collected and analyzed. The overall percentage of positive samples was 56.87% in organs, 50.85% in feces, and 20.45% in irrigation waters. By animal species, the most frequently detected serovar was Salmonella Typhimurium in bovine (17.39%), in buffalo (13.10%) and swine (28.21%), and S. Kentucky (24.78%) in poultry. The subspecies diarizonaeIIIb was frequently detected in goats (40.00%) and ovine (83.33%), while salamaeII (14.12%) and diarizonaeIIIb (11.76%) were frequently isolated in wild boars. In the irrigation water samples, the most frequently detected serovar was S. Napoli (25%). Results revealed that, although in Europe, control strategies aimed at preventing the spread of Salmonella have been implemented, the prevalence of this pathogen in food-producing animals and irrigation waters is high. Considering the risk to public health associated with the contamination of products or foods, more stringent control interventions are needed at primary production and along the food chain.


Abd-Elghany SM, Fathy TM, Zakaria AI, Imre K, Morar A, Herman V, Pașcalău R, Șmuleac L, Morar D, Imre M, Sallam KI, 2022. Prevalence of multidrug-resistant Salmonella enterica serovars in buffalo meat in Egypt. Foods 11:2924.

Aung KT, Khor WC, Octavia S, Ye A, Leo J, Chan PP, Lim G, Wong WK, Tan BZY, Schlundt J, Dalsgaard A, Ng LC, Lin YN, 2020. Distribution of Salmonella serovars in humans, foods, farm animals and environment, companion and wildlife animals in Singapore. Int J Environ Res Public Health 17:5774.

Bonardi S, Bruini I, Alpigiani I, Vismarra A, Barilli E, Brindani F, Morganti M, Bellotti P, Bolzoni L, Pongolini S, 2016. Influence of pigskin on salmonella contamination of pig carcasses and cutting lines in an Italian slaughterhouse. Ital J Food Saf 5:5654.

Borriello G, Lucibelli MG, Pesciaroli M, Carullo MR, Graziani C, Ammendola S, Battistoni A, Ercolini D, Pasquali P, Galiero G, 2012. Diversity of Salmonella spp. serovars isolated from the intestines of water buffalo calves with gastroenteritis. BMC Vet Res 8:201.

Burjaq SZ, Abu-Romman SM, 2020. Prevalence and antimicrobial resistance of Salmonella spp. from irrigation water in two major sources in Jordan. Curr Microbiol 177:3760-6.

Chalias A, Grispoldi L, Cenci Goga B, 2022. A risk assessment model for Salmonella spp. in swine carcasses. EFSA J 20:e200405.

Cristiano D, Peruzy MF, Aponte M, Mancusi A, Proroga YTR, Capuano F, Murru N, 2021. Comparison of droplet digital PCR vs real-time PCR for Yersinia enterocolitica detection in vegetables. Int J Food Microbiol 354:109321.

D’angelo L, Vecchio D, Cozza D, La Tela I, Carullo MR, Menozzi I, Scaltriti E, Pongolini S, Galiero G, De Carlo E, 2022. Identification of a new serovar of Salmonella enterica in mediterranean buffalo calves (Bubalus bubalis). Animals 12:161.

D’Incau M, Salogni C, Giovannini S, Ruggeri J, Scali F, Tonni M, Formenti N, Guarneri F, Pasquali P, Alborali GL, 2021. Occurrence of Salmonella Typhimurium and its monophasic variant (4, [5],12:i:-) in healthy and clinically ill pigs in northern Italy. Porcine Health Manag 7:34.

EFSA, ECDC, 2022. The European Union One Health 2021 zoonoses report. EFSA J 20:7666.

Falardeau J, Johnson RP, Pagotto F, Wang S, 2017. Occurrence, characterization, and potential predictors of verotoxigenic Escherichia coli, Listeria monocytogenes, and Salmonella in surface water used for produce irrigation in the lower mainland of British Columbia, Canada. PLoS One 12:e0185437.

Farahani RK, Meskini M, Langeroudi AG, Gharibzadeh S, Ghosh S, Farahani AHK, 2022. Evaluation of the different methods to detect Salmonella in poultry feces samples. Arch Microbiol 204:269.

Ferrari RG, Rosario DKA, Cunha-Neto A, Mano SB, Figueiredo EES, Conte-Juniora CA, 2019. Worldwide epidemiology of Salmonella serovars in animal-based foods: a meta-analysis. Appl Environ Microbiol 85:e00591-19.

Gil Molino M, Garcia Sanchez A, Risco Perez D, Goncalves Blanco P, Quesada Molina A, Rey Pérez J, Cano FEM, Cerrato Horrillo R, Hermoso-de-Mendoza Salcedo J, Fernandez Llario P, 2019. Prevalence of Salmonella spp. in tonsils, mandibular lymph nodes and faeces of wild boar from Spain and genetic relationship between isolates. Transbound Emerg Dis 66:1218-26.

Giner-Lamia J, Vinuesa P, Betancor L, Silva C, Bisio J, Soleto L, Chabalgoity JA, Puente JL, Soncini FC, García-Vescovi E, Flores G, Pedraza J, Yim L, García C, Astocondor L, Ochoa T, Hinostroza N, Graciela Pucciarelli M, Hernández-Alvarez A, Del Moral V, García-Del Portillo F, 2019. Genome analysis of Salmonella enterica subsp. diarizonae isolates from invasive human infections reveals enrichment of virulence-related functions in lineage ST1256. BMC Genomics 20:99.

Gong B, Li H, Feng Y, Zeng S, Zhuo Z, Luo J,Chen X, Li X, 2022. Prevalence, serotype distribution and antimicrobial resistance of non-typhoidal Salmonella in hospitalized patients in Conghua District of Guangzhou, China. Front Cell Infect Microbiol 12:805384.

ISO, 2006. Water quality. Sampling for microbiological analysis. ISO 19458:2006. International Standardization Organization ed., Geneva, Switzerland.

ISO, 2010. Water quality. Detection of Salmonella spp. ISO 19250:2010. International Standardization Organization ed., Geneva, Switzerland.

ISO, 2017. Microbiology of the food chain. Horizontal method for the detection, enumeration and serotyping of Salmonella. Part 1: detection of Salmonella spp. ISO 6579-1:2017. International Standardization Organization ed., Geneva, Switzerland.

Kagambèga A, Thibodeau A, Trinetta V, Soro D K, Sama F N, Bako É, Bouda CS, N’Diaye AW, Fravalo P, Barro N, 2018. Salmonella spp. and Campylobacter spp. in poultry feces and carcasses in Ouagadougou, Burkina Faso. Food Sci Nutr 6:1601-6.

La Tela I, Peruzy MF, D’Alessio N, Di Nocera F, Casalinuovo F, Carullo, MR, Cardinale D, Cristiano D, Capuano F, 2021. Serotyping and evaluation of antimicrobial resistance of salmonella strains detected in wildlife and natural environments in southern Italy. Antibiotics 10:353.

Leati M, Busani L, Zaccherini A, Ruocco L, Amato SD, Villa L, Barco L, Ricci A, Cibin V, 2021. The challenging task to select Salmonella target serovars in poultry: the Italian point of view. Epidemiol Infect 149:e160.

Liu H, Whitehouse CA, Li B, 2018. Presence and persistence of Salmonella in water: the impact on microbial quality of water and food safety. Front Public Health 6:159.

Methner U, Moog U, 2018. Occurrence and characterisation of Salmonella enterica subspecies diarizonae serovar 61: K: 1, 5, (7) in sheep in the federal state of Thuringia, Germany. BMC Vet Res 14:401.

Montone AMI, Cutarelli A, Peruzy MF, La Tela I, Brunetti R, Pirofalo MG, Folliero V, Balestrieri A, Murru N, Capuano F, 2023. Antimicrobial resistance and genomic characterization of salmonella infantis from different sources. Int J Mol Sci 24:5492.

Nguyen DTA, Awasthi SP, Hoang PH, Nguyen PD, Jayedul H, Hatanaka N. Hinenoya A, Van Dang C, Faruque SM, Yamasaki S, 2021. Prevalence, serovar, and antimicrobial resistance of Nontyphoidal salmonella in vegetable, fruit, and water samples in Ho Chi Minh City, Vietnam. Foodborne Pathog Dis18:354-63.

Peruzy MF, Capuano F, Proroga YTR, Cristiano D, Carullo MR, Murru N, 2020. Antimicrobial susceptibility testing for salmonella serovars isolated from food samples: five-year monitoring (2015-2019). Antibiotics 9:365.

Peruzy MF, Cristiano D, Delibato E, D’alessio N, Proroga YTR, Capozza RL, Rippa A, Murru N, 2022. Presence of enteric bacterial pathogens in meat samples of wild boar hunted in Campania region, southern Italy. Ital J Food Saf 11:9967.

Peruzy MF, Murru N, Yu Z, Kerkhof P, Neola B, Joossens M, Proroga YTR, Houf K, 2019. Assessment of microbial communities on freshly killed wild boar meat by MALDI-TOF MS and 16S rRNA amplicon sequencing. Int J Food Microbiol 301:51-60.

Peruzy MF, Proroga YTR, Capuano F, Mancusi A, Montone AMI, Cristiano D, Balestrieri A, Murru N, 2022. Occurrence and distribution of Salmonella serovars in carcasses and foods in southern Italy: eleven-year monitoring (2011–2021). Front Microbiol 13:1005035.

Piras F, Spanu V, Siddi G, Gymoese P, Spanu C, Cibin V, Schjørring S., De Santis EPL, Scarano C 2021. Whole-genome sequencing analysis of highly prevalent Salmonella serovars in wild boars from a national park in Sardinia. Food Control 130:108247.

Roasto M, Bonardi S, Mäesaar M, Alban L, Gomes-Neves E, Vieira-Pinto M, Vågsholm I, Elias T, Lindegaard LL, Blagojevic B 2023. Salmonella enterica prevalence, serotype diversity, antimicrobial resistance and control in the European pork production chain. Trends Food Sci Tech 131:210-9.

Silva DG, Santana AM, Maluta RP, Pizauro LJL, Bernardes PA, Aquino GV, Benincasa NC, Rodrigues DP, Fagliari JJ, 2018. Prevalence and identification of Salmonella spp. in water buffaloes from São Paulo State, Brazil. Arq Bras Med Vet Zootec 70:1645-8.

Silveira L, Pinto M, Isidro J, Pista Â, Themudo P, Vieira L, Machado J, Gomes JP, 2019. Multidrug-resistant Salmonella enterica serovar rissen clusters detected in Azores archipelago, Portugal. Int J Genomics 2019:1860275.

Stevens MP, Kingsley RA, 2021. Salmonella pathogenesis and host-adaptation in farmed animals. Curr Opin Microbiol 63:52-8.

Sychanh T, Chaunchom S, Pulsrikarn C, Pornreongwong S, Chaichana P, Boonmar S, 2013. Salmonella prevalence in slaughtered buffaloes and cattle in Champasak province, Lao People’s Democratic Republic. Kasetsart J - Nat Sci 47:561-70.

Tegegne FM, 2019. Epidemiology of Salmonella and its serotypes in human, food animals, foods of animal origin, animal feed and environment. J Food Nutr Health 2:7-14.

1.
Peruzy MF, La Tela I, Carullo MR, Ioele S, Proroga YTR, Balestrieri A, Murru N. Occurrence and distribution of <i>Salmonella</i> serovars associated with human infection isolated from irrigation waters and food-producing animals in southern Italy: eleven-year monitoring (2011-2021). Ital J Food Safety [Internet]. 2023 Oct. 26 [cited 2024 Jun. 15];12(4). Available from: https://www.pagepressjournals.org/ijfs/article/view/11538

Downloads

Download data is not yet available.

Citations