Food Is Reservoir of MDR Salmonella: Prevalence of ESBLs Profiles and Resistance Genes in Strains Isolated from Food
Open accessAbstract
Salmonella spp. are among the most frequent causes of foodborne diseases, and the increasing occurrence of MDR strains is an additional cause for concern. In the three-year period 2019–2021, we collected Salmonella spp. strains isolated from different food categories analysed in the context of Regulation (EC) No 2073/2005 in order to assess their antibiotic susceptibility profiles and ESBL production. To determine the susceptibility profiles and identify MDR strains, we used the Kirby–Bauer method to test 17 antibiotics. Double-disc and PCR testing then allowed us to assess the production of ESBLs and the presence of beta-lactamase resistance genes. Phenotypic tests showed that 36 out of 67 strains were MDR and 52.7% of these were ESBL producers. Finally, molecular investigations conducted on ESBL-producing strains revealed the presence of blaSHV, blaCTX-M and blaTEM genes. Our results confirmed the prevalence of S. Infantis, an MDR strain and ESBL producer, in chicken meat. This suggests that further research on the prevalence of antibiotic resistance genes (ARGs) in foodborne strains is needed, especially from a One Health perspective.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Studies have revealed the presence of MDR bacteria, including methicillin-resistant S. aureus (MRSA), ESBL-producing Enterobacteriaceae, and MDR-Salmonella, in meat products.
“Studies have revealed the presence of MDR bacteria, including methicillin-resistant S. aureus (MRSA), ESBL-producing Enterobacteriaceae, and MDR-Salmonella, in meat products [63,76,77,78,79].”
From A Systematic Review on Antimicrobial Resistance in Ghana from a One Health Perspective (2024) · cites this paper as [77]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The European Union One Health 2020 Zoonoses Report
Authority, E. F. S. (2021) · EFSA Journal · doi:10.2903/j.efsa.2021.6971 · Cited by 1,577 · see citing works
The CTX-M β-lactamase pandemic
Cantón, R., & Coque, T. M. (2006) · Current Opinion in Microbiology · doi:10.1016/j.mib.2006.08.011 · Cited by 1,149 · see citing works
Authority, E. F. S. (2021) · EFSA Journal · doi:10.2903/j.efsa.2021.6490 · Cited by 874 · see citing works
Salmonella : A review on pathogenesis, epidemiology and antibiotic resistance
Eng, S.-K., Pusparajah, P., Mutalib, N. A., Ser, H., Chan, K., & Lee, L. (2015) · Frontiers in Life Science · doi:10.1080/21553769.2015.1051243 · Cited by 861 · see citing works
Past and Present Perspectives on β-Lactamases
Bush, K. (2018) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01076-18 · Cited by 844 · see citing works
Salmonella, food safety and food handling practices
Ehuwa, O., Jaiswal, A. K., & Jaiswal, S. (2021) · Foods · doi:10.3390/foods10050907 · Cited by 551 · see citing works
Antibiotic resistance in Enterobacteriaceae: mechanisms and clinical implications
Iredell, J. R., Brown, J. C., & Tagg, K. A. (2016) · BMJ · doi:10.1136/bmj.h6420 · Cited by 392 · see citing works
Elevated rates of horizontal gene transfer in the industrialized human microbiome
Groussin, M., Poyet, M., Sistiaga, A., Kearney, S. M., Moniz, K., Noel, M., Hooker, J., Gibbons, S. M., Ségurel, L., Froment, A., et al. (2021) · Cell · doi:10.1016/j.cell.2021.02.052 · Cited by 331 · see citing works
(BIOHAZ), E. P. O. B. H., Koutsoumanis, K. P., Allende, A., Álvarez‐Ordóñez, A., Bolton, D., Bover‐Cid, S., Chemaly, M., Davies, R., Cesare, A. D., Herman, L., et al. (2021) · EFSA Journal · doi:10.2903/j.efsa.2021.6651 · Cited by 329 · see citing works
Liu, H., Whitehouse, C. A., & Li, B. (2018) · Frontiers in Public Health · doi:10.3389/fpubh.2018.00159 · Cited by 285 · see citing works
Antibiotic resistance in Salmonella spp. isolated from poultry: A global overview
Castro-Vargas, R. E., Herrera‐Sánchez, M. P., Rodríguez‐Hernández, R., & Rondón‐Barragán, I. S. (2020) · Veterinary World · doi:10.14202/vetworld.2020.2070-2084 · Cited by 254 · see citing works
A Review of SHV Extended-Spectrum β-Lactamases: Neglected Yet Ubiquitous
Liakopoulos, A., Mevius, D. J., & Ceccarelli, D. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01374 · Cited by 241 · see citing works
Campos, J., Mourão, J., Peixe, L. M. S. V., & Antunes, P. (2019) · Pathogens · doi:10.3390/pathogens8010019 · Cited by 157 · see citing works
A Structure-Based Classification of Class A β-Lactamases, a Broadly Diverse Family of Enzymes
Philippon, A., Slama, P. S., Dény, P., & Labia, R. (2015) · Clinical Microbiology Reviews · doi:10.1128/cmr.00019-15 · Cited by 150 · see citing works
Nguyen, D. T. A., Kanki, M., Nguyen, P., Le, H. T., Thanh, P. N., Tran, D. N. M., Le, N. H., Dang, C. V., Kawai, T., Kawahara, R., et al. (2016) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2016.07.017 · Cited by 113 · see citing works
Alcalá, L., Alonso, C. A., Simón, C., González, C., Espinosa, J. O., Rezusta, A., Ortega, C., & Torres, C. (2015) · Microbial Ecology · doi:10.1007/s00248-015-0718-0 · Cited by 105 · see citing works
Kim, H.-S., Chon, J., Kim, Y., Kim, D., Kim, M.-S., & Seo, K. (2015) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2015.04.049 · Cited by 97 · see citing works
Ye, Q., Wu, Q., Zhang, S., Zhang, J., Yang, G., Wang, J., Xue, L., & Chen, M. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01709 · Cited by 91 · see citing works
Dhanani, A. S., Block, G., Dewar, K., Forgetta, V., Topp, E., Beiko, R. G., & Diarra, M. S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0128773 · Cited by 68 · see citing works
Zhao, X., Hu, M., Zhang, Q., Zhao, C., Zhang, Y., Li, L., Qi, J., Luo, Y., Zhou, D., & Liu, Y. (2020) · Poultry Science · doi:10.1016/j.psj.2020.09.071 · Cited by 56 · see citing works
Dhanani, A. S., Block, G., Dewar, K., Forgetta, V., Topp, E., Beiko, R. G., & Diarra, M. S. (2016) · PLoS ONE · doi:10.1371/journal.pone.0148706 · Cited by 55 · see citing works
Gargano, V., Sciortino, S., Gambino, D., Costa, A., Agozzino, V., Reale, S., Alduina, R., & Vicari, D. (2021) · Antibiotics · doi:10.3390/antibiotics10070809 · Cited by 45 · see citing works
Self-citationColosi, I. A., Baciu, A. M., Opriș, R. V., Peca, L., Gudat, T., Simon, L. M., Colosi, H. A., & Costache, C. (2020) · Foods · doi:10.3390/foods9121726 · Cited by 35 · see citing works
Proietti, P. C., Stefanetti, V., Musa, L., Zicavo, A., Dionisi, A. M., Bellucci, S., Mensa, A. L., Menchetti, L., Branciari, R., Ortenzi, R., et al. (2020) · Antibiotics · doi:10.3390/antibiotics9110814 · Cited by 32 · see citing works
Elnekave, E., Hong, S. L., Lim, S., Boxrud, D. J., Rovira, A., Mather, A. E., Perez, A., & Álvarez, J. (2020) · Emerging infectious diseases · doi:10.3201/eid2612.200336 · Cited by 28 · see citing works
Gargano, V., Gambino, D., Migliore, S., Vitale, M., Sciortino, S., Costa, A., & Vicari, D. (2021) · Microorganisms · doi:10.3390/microorganisms9102018 · Cited by 12 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
A Systematic Review on Antimicrobial Resistance in Ghana from a One Health Perspective
Donkor, E. S., Odoom, A., Osman, A.-H., Darkwah, S., & Kotey, F. C. N. (2024) · Antibiotics · doi:10.3390/antibiotics13070662 · Cited by 52 · see citing works
Akshay, S. D., Deekshit, V. K., Raj, J. R. M., & Maiti, B. (2023) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.3c00408 · Cited by 41 · see citing works
Krüger, G. I., Pardo-Esté, C., Zepeda, P., Olivares‐Pacheco, J., Galleguillos, N., Suarez, M., Castro‐Severyn, J., Alvarez‐Thon, L., Tello, M., Valdés, J., et al. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1072793 · Cited by 27 · see citing works
Chavan, P., & Vashishth, R. (2025) · Discover Applied Sciences · doi:10.1007/s42452-025-07015-z · Cited by 25 · see citing works
Damianos, A., Tsitsos, A., Economou, V., Gioula, G., & Haidich, A. (2024) · Food Control · doi:10.1016/j.foodcont.2024.111127 · Cited by 15 · see citing works
Kang, H., Kim, H., Kim, H., Jeon, J. H., Kim, S. H., Park, Y., & Kim, S. H. (2024) · Journal of Microbiology and Biotechnology · doi:10.4014/jmb.2312.12018 · Cited by 11 · see citing works
Parzygnat, J. L., Crespo, R., Fosnaught, M., Muyyarrikkandy, M., Hull, D. M., Harden, L., & Thakur, S. (2024) · Foodborne Pathogens and Disease · doi:10.1089/fpd.2023.0181 · Cited by 9 · see citing works
Custodio, M., Peñaloza, R., Ordinola‐Zapata, A., Ortiz, T. P., Suárez, H., Vieyra-Peña, E. G., la Cruz, H. D., & Alvarado-Ibáñez, J. C. (2023) · Toxicology Reports · doi:10.1016/j.toxrep.2023.02.002 · Cited by 8 · see citing works
Wang, W., Liu, F., Li, H., Li, M., Hu, Y., Li, F., Xiao, J., & Dong, Y. (2024) · Microbial Genomics · doi:10.1099/mgen.0.001164 · Cited by 7 · see citing works
Gonçalves, C., Silveira, L., Rodrigues, J., Furtado, R., Ramos, S., Nunes, A., & Pista, Â. (2024) · Antibiotics · doi:10.3390/antibiotics13100957 · Cited by 10 · see citing works
Prevalence and antimicrobial resistance profiles of Salmonella spp. in poultry meat
Castello, A., Piraino, C., Butera, G., Alio, V., Cardamone, C., Oliveri, G., Cascone, G., Ciravolo, C., & Costa, A. (2023) · Italian Journal of Food Safety · doi:10.4081/ijfs.2023.11135 · Cited by 7 · see citing works
Self-citationBu, X., Wu, Y., Hong, Y., Shi, J., Shao, J., Jia, K., Dong, Q., & Wang, X. (2024) · BMC Microbiology · doi:10.1186/s12866-024-03651-4 · Cited by 8 · see citing works
Fraccalvieri, R., Castellana, S., Bianco, A., Difato, L. M., Capozzi, L., Sambro, L. D., Donatiello, A., Pugliese, D., Tempesta, M., Parisi, A., et al. (2025) · Microorganisms · doi:10.3390/microorganisms13081770 · Cited by 4 · see citing works
Vinueza-Burgos, C., Hidalgo-Arellano, L., Gómez-Coronado, C., Medina-Santana, J. L., & Cevallos-Almeida, M. (2023) · F1000Research · doi:10.12688/f1000research.138671.1 · Cited by 4 · see citing works
Antimicrobial resistance in foodborne Salmonella enterica isolates in the Republic of Belarus
Kulikova, N. G., Chernyshkov, A., Mikhailova, Y. V., Zenkovich, A. L., Dovnar, D. A., Mareiko, A. M., Айткалиевна, Б. Л., Shelenkov, A. A., Egorova, A. E., Saenko, S., et al. (2023) · Journal of microbiology epidemiology immunobiology · doi:10.36233/0372-9311-343 · Cited by 3 · see citing works
Eryıldız, M., BİLGİC, V., Ekici, S., Yiğin, A., & Demırci, M. (2022) · Etlik Veteriner Mikrobiyoloji Dergisi · doi:10.35864/evmd.1145433 · Cited by 2 · see citing works
Vinueza-Burgos, C., Hidalgo-Arellano, L., Gómez-Coronado, C., Medina-Santana, J. L., & Cevallos-Almeida, M. (2024) · F1000Research · doi:10.12688/f1000research.138671.3 · Cited by 1 · see citing works
AHMAD, Y. A., & MUSTAFA, K. K. (2023) · Applied Ecology and Environmental Research · doi:10.15666/aeer/2105_40194033
Vinueza-Burgos, C., Hidalgo-Arellano, L., Gómez-Coronado, C., Medina-Santana, J. L., & Cevallos-Almeida, M. (2024) · F1000Research · doi:10.12688/f1000research.138671.2
Liu, R., & Huang, C. (2024) · IntechOpen eBooks · doi:10.5772/intechopen.1005294
Hardany, M. J., Al-Hmudi, H. A., & Abdul-Hussein, Z. R. (2024) · Basrah Researches Sciences · doi:10.56714/bjrs.50.2.6
Alhaj, A. A. O., & Alawed, A. A. M. (2025) · ARID International Journal for Science and Technology · doi:10.36772/arid.aijst.2025.8161
ESBL and carbapenemase-producing enteric pathogens in animal-origin foods: a one health perspective
Khan, S. A., Siddiqui, S. A., Samreen, Ahmad, I., Neyaz, L. A., & Abulreesh, H. H. (2026) · Folia Microbiologica · doi:10.1007/s12223-026-01505-2
Gupta, M. D., Sen, A., Ahad, A., Barua, P. K., Paul, P., Mya, U., Das, S., & Das, A. (2026) · Veterinary Medicine and Science · doi:10.1002/vms3.71071
Alsubaie, S., Alsufyani, A. T., Alotaibi, N. M., Alhamed, A. S., Alsalman, S. A., Almusa, M. A., Aljohani, A. M., Sabour, A. A. A., & Mukhtar, L. E. (2026) · Foods · doi:10.3390/foods15152585
Oyetade, J. A., & Fayemi, O. E. (2026) · Materials Today Communications · doi:10.1016/j.mtcomm.2026.115832
- Authors
- Gambino, D., Gargano, V., Butera, G., Sciortino, S., Pizzo, M., Oliveri, G., Cardamone, C., Piraino, C., Cassata, G., Vicari, D., & Costa, A.
- Affiliations
- Istituto Zooprofilattico Sperimentale Della Sicilia (IT)
- Corresponding author
- Gargano, Valeria
- ORCID
- Venue
- Microorganisms
- Publisher
- MDPI AG
- Published
- 2022-04-06
- Volume
- 10
- Issue
- 4
- Pages
- 780
- ISSN
- 2076-2607 (ISSN-L)
- PMC
- PMC9026803
- OpenAlex
- W4224271514
- Cited by
- 28
- References
- 26
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 11 · 2023: 8 · 2022: 1
- FWCI
- 3.19
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Microorganisms (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
- Health Sciences › Medicine › Infectious Diseases › Antimicrobial Resistance in Staphylococcus
- Keywords
- Salmonella, multidrug resistance, extended-spectrum beta-lactamase, antibiotic resistance genes, foodborne pathogens, chicken meat, Salmonella Infantis, blaSHV, blaCTX-M, blaTEM, food safety, One Health
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review