Epidemiology of Methicillin-Resistant Staphylococcus aureus with a “One Health” Approach
Main Article Content
Abstract
Introduction. Methicillin-resistant Staphylococcus aureus (MRSA) represents a significant threat to public health due to its capacity for dissemination, colonization, and resistance to multiple antibiotics. Its distribution among humans, animals, food, and environment emphasizes the need to address it from a “One Health” approach. Objective. To analyze the epidemiology of methicillin-resistant Staphylococcus aureus, including its virulence profile, distribution in different reservoirs, frequency of resistance genes and evaluation of the susceptibility profile. Methodology. A literature review was performed in PubMed, Scopus, and BVS databases, using MeSH terms and Boolean operators, applying the PRISMA method for article selection. Results. Analysis of 26 MRSA-focused studies identified the most prevalent virulence factors as: nuc, hla, hlb, clfA, clfB, coa, ica, and icaD, in addition to enterotoxins seb, sel, seo, and immunomodulatory genes scn, sak, and chp. The highest MRSA prevalence was identified in animal reservoirs (22.8%), followed by human (18.8%), food (7.7%), and environmental samples (4.6%). A high prevalence of the mecA (57.1%) and blaZ (70.7%) genes was observed, whereas the mecC gene was detected at a lower frequency (2.5%). Resistance to cefoxitin, oxacillin, penicillin, and ampicillin was consistently high across all reservoirs. Notably, resistance to vancomycin was detected in animal-derived isolates, representing a significant concern. Nevertheless, linezolid remained highly effective, with negligible resistance observed in the studied reservoirs. Conclusion. Methicillin-resistant Staphylococcus aureus exhibits a broad range of virulence factors and resistance determinants, with considerable prevalence across multiple reservoirs, highlighting its zoonotic potential and the importance of integrated surveillance within a One Health framework. General Area of Study: Health. Specific area of study: Microbiology. Type of study: Systematic bibliographic review.
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Sangucho Suntasig, J. L., Burgos Mayorga, A. R., Cruz Quintana, S. M., & Jaramillo Ruales, E. K. (2025). Epidemiology of Methicillin-Resistant Staphylococcus aureus with a “One Health” Approach. Anatomía Digital, 8(3), 6-28. https://doi.org/10.33262/anatomiadigital.v8i3.3421
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Articulos de revisión bibliográfica
References
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2. Adeyemi FM, Oyedara OO, Yusuf-Omoloye NA, Ajigbewu OH, Ndaji OL, Adegbite-Badmus MK, et al. Guardians of resistance and virulence: detection of mec, femA, Van, pvl, hlg and spa genes in methicillin and vancomycin-resistant Staphylococcus aureus from clinical and food samples in Southwestern Nigeria. BioMed Central Microbiology [Internet]. 2024 [cited 2025 April 22];24(1):498. Available from: https://pubmed.ncbi.nlm.nih.gov/39592938/
3. Sieber RN, Skov RL, Nielsen J, Schulz J, Price LB, Aarestrup FM, et al. Drivers and dynamics of methicillin-resistant livestock-associated staphylococcus aureus CC398 in pigs and humans in Denmark. American Society for Microbiology [Internet]. 2018 [cited 2025 April 22];9(6). Available from: https://journals.asm.org/doi/10.1128/mbio.02142-18
4. Sasaki Y, Aoki K, Ishii Y, Tamura Y, Asai T. First isolation of ST398 methicillin-resistant Staphylococcus aureus carrying staphylococcal cassette chromosome mec type IVd from pig ears in Japan. The Journal of Veterinary Medical Science [Internet]. 2022 [cited 2025 April 22];84(9):1211-1215. Available from: https://pmc.ncbi.nlm.nih.gov/articles/PMC9523295/
5. Back SH, Eom HS, Lee HH, Lee GY, Park KT, Yang SJ. Livestock-associated methicillin-resistant Staphylococcus aureus in Korea: antimicrobial resistance and molecular characteristics of LA-MRSA strains isolated from pigs, pig farmers, and farm environment. Journal of Veterinary Science [Internet]. 2020 [cited 2025 April 22]; 21(1): e2. Available from: https://doi.org/10.4142/jvs.2020.21.e2
6. Rafif Khairullah A, Rehman S, Agus SS, Helmi Effendi M, Chasyer Ramandinianto S, Aega Gololodo M, et al. Detection of mecA gene and methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and risk factors from farms in Probolinggo, Indonesia. Faculty1000Research [Internet]. 2022 [cited 2025 April 22]; 11:722. Available from: https://f1000research.com/articles/11-722
7. Giacinti G, Carfora V, Caprioli A, Sagrafoli D, Marri N, Giangolini G, et al. Prevalence and characterization of methicillin-resistant Staphylococcus aureus carrying mecA or mecC and methicillin-susceptible Staphylococcus aureus in dairy sheep farms in central Italy. Journal of Dairy Science [Internet]. 2017 [cited 2025 April 22]; 100(10):7857–7863. Available from: https://www.journalofdairyscience.org/action/showFullText?pii=S002203021730735X
8. Oliveira R, Pinho E, Almeida G, Azevedo NF, Almeida C. Prevalence and diversity of staphylococcus aureus and staphylococcal enterotoxins in raw milk from northern portugal. Frontiers in Microbiology [Internet]. 2022 [cited 2025 April 22]; 13:846653. Available from: https://doi.org/10.3389/FMICB.2022.846653/BIBTEX
9. Beshiru A, Igbinosa IH, Akinnibosun O, Ogofure AG, Dunkwu-Okafor A, Uwhuba KE, et al. Characterization of resistance and virulence factors in livestock-associated methicillin-resistant Staphylococcus aureus. Scientific Reports [Internet]. 2024 [cited 2025 April 22];14(13235). Available from: https://www.nature.com/articles/s41598-024-63963-3
10. Shahzad MA, Yousaf A, Ahsan A, Irshad H, Riaz A, Khan A, et al. Virulence and resistance profiling of Staphylococcus aureus isolated from subclinical bovine mastitis in the Pakistani Pothohar region. Scientific Reports [Internet]. 2024 [cited 2025 April 22]; 14(1):14569. Available from: https://pubmed.ncbi.nlm.nih.gov/38914650/
11. Zhang Z, Wang J, Wang H, Zhang L, Shang W, Li Z, et al. Molecular Surveillance of MRSA in Raw Milk Provides Insight into MRSA Cross Species Evolution. Microbiology Spectrum [Internet]. 2023 [cited 2025 April 22];11(4). Available from: https://journals.asm.org/doi/10.1128/spectrum.00311-23
12. Okorie-Kanu OJ, Anyanwu MU, Ezenduka EV, Mgbeahuruike AC, Thapaliya D, Gerbig G, et al. Molecular epidemiology, genetic diversity, and antimicrobial resistance of Staphylococcus aureus isolated from chicken and pig carcasses, and carcass handlers. Public Library of Science One [Internet]. 2020 [cited 2025 April 22]; 15(5): e0232913. Available from: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0232913
13. Deepak SJ, Kannan P, Savariraj WR, Ayyasamy E, Tuticorin Maragatham Alagesan SK, Ravindran NB, et al. Characterization of Staphylococcus aureus isolated from milk samples for their virulence, biofilm, and antimicrobial resistance. Scientific Reports [Internet]. 2024 [cited 2025 April 22];14(25635):1–12. Available from: https://www.nature.com/articles/s41598-024-75076-y
14. Lee GY, Lee SI, Kim S Do, Park JH, Kim GB, Yang SJ. Clonal distribution and antimicrobial resistance of methicillin-susceptible and -resistant Staphylococcus aureus strains isolated from broiler farms, slaughterhouses, and retail chicken meat. Poultry Science [Internet]. 2022 [cited 2025 April 22];101(10):102070. Available from: https://www.sciencedirect.com/science/article/pii/S0032579122003613
15. Zou G, Matuszewska M, Jia M, Zhou J, Ba X, Duan J, et al. A Survey of Chinese Pig Farms and Human Healthcare Isolates Reveals Separate Human and Animal Methicillin-Resistant Staphylococcus aureus Populations. Advanced Science [Internet]. 2022 [cited 2025 April 22]; 9(4):2103388. Available from: https://onlinelibrary.wiley.com/doi/full/10.1002/advs.202103388
16. El-Deeb W, Cave R, Fayez M, Alhumam N, Quadri S, Mkrtchyan HV. Methicillin Resistant Staphylococci Isolated from Goats and Their Farm Environments in Saudi Arabia Genotypically Linked to Known Human Clinical Isolates: a Pilot Study. Microbiology Spectrum [Internet]. 2022 [cited 2025 April 22];10(4). Available from: https://journals.asm.org/doi/10.1128/spectrum.00387-22
17. Krukowski H, Bakuła Z, Iskra M, Olender A, Bis-Wencel H, Jagielski T. The first outbreak of methicillin-resistant Staphylococcus aureus in dairy cattle in Poland with evidence of on-farm and intrahousehold transmission. Journal of Dairy Science [Internet]. 2020 [cited 2025 April 22];103(11):10577-10584. Available from: https://www.journalofdairyscience.org/action/showFullText?pii=S0022030220306536
18. Lee JB, Lim JH, Park JH, Lee GY, Park KT, Yang SJ. Genetic characteristics and antimicrobial resistance of Staphylococcus aureus isolates from pig farms in Korea: emergence of cfr-positive CC398 lineage. BioMed Central Veterinary Research [Internet]. 2024 [cited 2025 April 22]; 20(1):503. Available from: https://pmc.ncbi.nlm.nih.gov/articles/PMC11529005/
19. Merve Bayrakal G, Aydin A. Investigation of various toxigenic genes and antibiotic and disinfectant resistance profiles of staphylococcus aureus originating from raw milk. Foods [Internet]. 2024 [cited 2025 April 22];13(21):3448. Available from: https://www.mdpi.com/2304-8158/13/21/3448/htm
20. Cavalcante FS, Saintive S, Ferreira DC, Rocha Silva AB, Guimarães LC, Braga BS, et al. Methicillin-resistant Staphylococcus aureus from infected skin lesions presents several virulence genes and are associated with the CC30 in Brazilian children with atopic dermatitis. Virulence [Internet]. 2021 [cited 2025 April 22]; 12(1):260–269. Available from: https://pubmed.ncbi.nlm.nih.gov/33356835/
21. Kurukulasooriya MRP, Tillekeratne LG, Wijayaratne WMDGB, Bodinayake CK, Dilshan UHBY, De Silva AD, et al. Prevalence and molecular epidemiology of methicillin-resistant Staphylococcus aureus in livestock farmers, livestock, and livestock products in southern Sri Lanka: A one health approach. Infection, Genetics and Evolution [Internet]. 2024 [cited 2025 April 22]; 126:105693. Available from: https://doi.org/10.1016/J.MEEGID.2024.105693
22. Cranmer KD, Pant MD, Quesnel S, Sharp JA. Clonal Diversity, Antibiotic resistance, and virulence factor prevalence of community associated staphylococcus aureus in southeastern Virginia. Pathogens [Internet]. 2024 [cited 2025 April 22]; 13(1):25. Available from: https://pmc.ncbi.nlm.nih.gov/articles/PMC10821353/
23. Esemu SN, Nya’Nying SF, Ndip LM, Bessong PO, Tanih NF, Smith SI, et al. Isolation and characterization of methicillin-resistant Staphylococcus aureus from bovine mastitis in Northwest Cameroon: public health implications. BioMed Central Research Notes [Internet]. 2024 [cited 2025 April 22]; 17(1):389. Available from: https://pmc.ncbi.nlm.nih.gov/articles/PMC11673689/
24. Silva V, Silva A, Barbero R, Romero M, del Campo R, Caniça M, et al. Resistome, Virulome, and Clonal Variation in Methicillin-Resistant Staphylococcus aureus (MRSA) in healthy swine populations: a cross-sectional study. Genes [Internet]. 2024 [cited 2025 April 22];15(5):532. Available from: https://pmc.ncbi.nlm.nih.gov/articles/PMC11121583/
25. Aravena C, Cáceres J, Bastías AA, Opazo JF, Magna Y, Saralegui C, et al. Nasal carriage, antibiotype and genotype of isolated Staphylococcus aureus from Medicine and Nursing students of Campus San Felipe, University of Valparaiso, Chile, during 2017. Revista Chilena de Infectología [Internet]. 2021 [cited 2025 April 22];38(6):774–782. Available from: http://www.scielo.cl/scielo.php?script=sci_arttext&pid=S0716-10182021000600774&lng=en&nrm=iso&tlng=en
26. Goes ICRDS, Romero LC, Turra AJ, Gotardi MA, Rodríguez TFS de O, Santos L de O, et al. Prevalence of nasal carriers of methicillin-resistant Staphylococcus aureus in primary health care units in Brazil. Revista do Instituto de Medicina Tropical de São Paulo [Internet]. 2021 [cited 2025 April 22]; 63: e14. Available from: https://pmc.ncbi.nlm.nih.gov/articles/PMC7924983/
27. Tenezaca Lliguin NM, Orellana Bravo PP, Andrade Tacuri CF, Ortiz Tejedor JG. Staphylococcus aureus resistentes a meticilina aislados de teléfonos móviles de estudiantes de Enfermería en Cuenca, Ecuador. Revista Argentina de Microbiología [Internet]. 2025 [cited 2025 April 22];57(1):54–58. Available from: https://www.sciencedirect.com/science/article/pii/S0325754124001585?via%3Dihub
28. Zuo H, Uehara Y, Lu Y, Sasaki T, Hiramatsu K. Genetic and phenotypic diversity of methicillin-resistant Staphylococcus aureus among Japanese inpatients in the early 1980s. Scientific Reports [Internet]. 2021 [cited 2025 April 22];11(1):5447. Available from: https://pmc.ncbi.nlm.nih.gov/articles/PMC7940613/
29. Patel K, Godden SM, Royster EE, Crooker BA, Johnson TJ, Smith EA, et al. Prevalence, antibiotic resistance, virulence, and genetic diversity of Staphylococcus aureus isolated from bulk tank milk samples of U.S. dairy herds. BioMed Central Genomics [Internet]. 2021 [cited 2025 April 22]; 22(1):367. Available from: https://pmc.ncbi.nlm.nih.gov/articles/PMC8135151/
30. Ribeiro LF, Sato RA, Pollo A de S, Rossi GAM, Do Amaral LA. Occurrence of methicillin-resistant staphylococcus spp. on Brazilian dairy farms that produce unpasteurized cheese. Toxins [Internet]. 2020 [cited 2025 April 22]; 12(12):779. Available from: https://pmc.ncbi.nlm.nih.gov/articles/PMC7762534/
31. Inagawa T, Hisatsune J, Kutsuno S, Iwao Y, Koba Y, Kashiyama S, et al. Genomic characterization of Staphylococcus aureus isolated from patients admitted to intensive care units of a tertiary care hospital: epidemiological risk of nasal carriage of virulent clone during admission. Microbiology Spectrum [Internet]. 2024 [cited 2025 April 22];12(6): e0295023. Available from: https://pubmed.ncbi.nlm.nih.gov/38709078/
32. Gerardo Ortiz J, Parra Bernal OF, Segovia Clavijo EP. Susceptibilidad de cepas de Staphylococcus aureus presente en superficies inertes del Hospital José Félix Valdivieso. Anatomía Digital [Internet]. 2023 [citado 22 de abril de 2025]; 6(3.1):44-58. Disponible en: https://doi.org/10.33262/anatomiadigital.v6i3.1.2647