Molecular profiling of methicillin‑resistant Staphylococcus aureus isolated from healthy pet dogs and their owners in western Iran
,
Abstract
Background and Objectives: Growing apprehension surrounds methicillin-resistant Staphylococcus aureus (MRSA) strains. The objective of this investigation was to molecularly profile MRSA strains recovered from asymptomatic companion dogs and their human caretakers in Kermanshah, located in western Iran, marking the inaugural research of its kind within the country.
Materials and Methods: During a six-month period, specimens were obtained from the oral cavities and nasal passages of 200 clinically normal pet dogs, as well as their owners. MRSA isolates were identified, DNA was extracted, and characterized via staphylococcal cassette chromosome mec (SCCmec), accessory gene regulator (agr), and staphylococcal protein A (spa) typing, plus detection of mecA and Panton-Valentine leukocidin (PVL) genes.
Results: Eighteen MRSA isolates were identified (12 from dogs, six from owners). All carried mecA. Most had SCCmec type III. Human isolates included one agr II and two agr IV; no dog isolates were agr-positive. Isolates belonged to four spa types: t690 (dogs) and t325, t037, t030 (owners). PVL genes were absent. Isolates from dogs and owners showed type diversity.
Conclusion: This study reveals MRSA epidemiology in healthy dogs and owners in Iran, with low colonization rates. Continuous monitoring is essential to track MRSA circulation, as colonization raises infection risk.
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2. Shoaib M, Aqib AI, Ashfaq K, Naveed A, Kulyar MF-e-A, Bhutta ZA, et al. Diversified epidemiological pattern and antibiogram of mecA gene in Staphylococcus aureus isolates of pets, pet owners and environment. Pak Vet J 2020; 40: 331-336.
3. Bilyk BL, Panchal VV, Tinajero-Trejo M, Hobbs JK, Foster SJ. An interplay of multiple positive and negative factors governs methicillin resistance in Staphylococcus aureus. Microbiol Mol Biol Rev 2022; 86(2): e00159-21.
4. Turlej A, Hryniewicz W, Empel J. Staphylococcal cassette chromosome mec (Sccmec) classification and typing methods: an overview. Pol J Microbiol 2011; 60: 95-103.
5. Crespo-Piazuelo D, Lawlor PG. Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) prevalence in humans in close contact with animals and measures to reduce on-farm colonisation. Ir Vet J 2021; 74: 21.
6. Suepaul S, Georges K, Unakal C, Boyen F, Sookhoo J, Ashraph K, et al. Determination of the frequency, species distribution and antimicrobial resistance of staphylococci isolated from dogs and their owners in Trinidad. PloS One 2021; 16(7): e0254048.
7. Hanitsch LG, Krüger R, Hoppe P-A, Humme D, Pokrywka A, Niebank M, et al. Outpatient decolonization after recurrent skin infection with Panton-Valentine leukocidin (PVL)-producing S. aureus—The importance of treatment repetition. PloS One 2020; 15(4): e0231772.
8. Jenul C, Horswill AR. Regulation of Staphylococcus aureus virulence. Microbiol Spectr 2019; 7(2): 10.1128/microbiolspec. gpp3-0031-2018.
9. Boero E, Pansegrau W, Giovani C, Rooijakkers SH, van Kessel KP, van Strijp JA, et al. Natural human immunity against staphylococcal protein A relies on effector functions triggered by IgG3. Front Immunol 2022; 13: 834711.
10. Hoffman CL, Thibault M, Hong J. Characterizing pet acquisition and retention during the COVID-19 pandemic. Front Vet Sci 2021; 8: 781403.
11. Hesari Y, Sohrabi N, Abiri R, Babaei S, Amiri Z. Staphylococcal cassette chromosome mec typing of meticillin-resistant Staphylococcus aureus in Kermanshah Province, West of Iran. Jundishapur J Microbiol 2020; 13: 1-7.
12. Davis MF, Misic AM, Morris DO, Moss JT, Tolomeo P, Beiting DP, et al. Genome sequencing reveals strain dynamics of methicillin-resistant Staphylococcus aureus in the same household in the context of clinical disease in a person and a dog. Vet Microbiol 2015; 180: 304-307.
13. Algammal AM, Hetta HF, Elkelish A, Alkhalifah DHH, Hozzein WN, Batiha GE-S, et al. Methicillin-Resistant Staphylococcus aureus (MRSA): one health perspective approach to the bacterium epidemiology, virulence factors, antibiotic-resistance, and zoonotic impact. Infect Drug Resist 2020; 13: 3255-3265.
14. Tadesse S. Antimicrobial resistance profile of Staphylococcus aureus isolated from clinical specimens and nasal swabs of patients at Tikur Anbessa specialized hospital, Addis Ababa, Ethiopia. BMC Pharmacol Toxicol 2018; 19: 24.
15. Tille PM (2021). Bailey & Scott's Diagnostic Microbiology. 15th ed. Elsevier Health Sciences. St. Louis, Missouri.
16. Zhang K, Sparling J, Chow BL, Elsayed S, Hussain Z, Church DL, et al. New quadriplex PCR assay for detection of methicillin and mupirocin resistance and simultaneous discrimination of Staphylococcus aureus from coagulase-negative staphylococci. J Clin Microbiol 2004; 42: 4947-4955.
17. Clinical and Laboratory Standards Institute (2024). Performance Standards for Antimicrobial Susceptibility Testing, 33 rd ed. Available online: www.clsi.org (accessed on 20 September 2024).
18. Brakstad OG, Aasbakk K, Maeland JA. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J Clin Microbiol 1992; 30: 1654-1660.
19. Zhang K, McClure J-A, Elsayed S, Louie T, Conly JM. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J Clin Microbiol 2005; 43: 5026-5033.
20. Shopsin B, Mathema B, Alcabes P, Said-Salim B, Lina G, Matsuka A, et al. Prevalence of agr specificity groups among Staphylococcus aureus strains colonizing children and their guardians. J Clin Microbiol 2003; 41: 456-459.
21. Lina G, Piémont Y, Godail-Gamot F, Bes M, Peter M-O, Gauduchon V, et al. Involvement of Panton-Valentine leukocidin—producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 1999; 29: 1128-1132.
22. Pomba C, Rantala M, Greko C, Baptiste KE, Catry B, Van Duijkeren E, et al. Public health risk of antimicrobial resistance transfer from companion animals. J Antimicrob Chemother 2017; 72: 957-968.
23. Harmsen D, Claus H, Witte W, Rothganger J, Claus H, Turnwald D, et al. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 2003; 41: 5442-5448.
24. Duquette R, Nuttall T. Methicillin‐resistant Staphylococcus aureus in dogs and cats: an emerging problem? J Small Anim Pract 2004; 45: 591-597.
25. Cuny C, Layer-Nicolaou F, Weber R, Köck R, Witte W. Colonization of dogs and their owners with Staphylococcus aureus and Staphylococcus pseudintermedius in households, veterinary practices, and healthcare facilities. Microorganisms 2022; 10: 677.
26. Van Balen J, Landers T, Nutt E, Dent A, Hoet A. Molecular epidemiological analysis to assess the influence of pet-ownership in the biodiversity of Staphylococcus aureus and MRSA in dog-and non-dog-owning healthy households. Epidemiol Infect 2017; 145: 1135-1147.
27. Sakr A, Brégeon F, Mège J-L, Rolain J-M, Blin O. Staphylococcus aureus nasal colonization: an update on mechanisms, epidemiology, risk factors, and subsequent infections. Front Microbiol 2018; 9: 2419.
28. Funaki T, Yasuhara T, Kugawa S, Yamazaki Y, Sugano E, Nagakura Y, et al. SCCmec typing of PVL-positive community-acquired Staphylococcus aureus (CA-MRSA) at a Japanese hospital. Heliyon 2019; 5(3): e01415.
29. Abdullahi IN, Zarazaga M, Campaña‐Burguet A, Eguizábal P, Lozano C, Torres C. Nasal Staphylococcus aureus and S. pseudintermedius carriage in healthy dogs and cats: a systematic review of their antibiotic resistance, virulence and genetic lineages of zoonotic relevance. J Appl Microbiol 2022; 133: 3368-3390.
30. Oh J-Y, Chae J-C, Han J-I, Song W-K, Lee C-M, Park H-M. Distribution and epidemiological relatedness of methicillin-resistant Staphylococcus aureus isolated from companion dogs, owners, and environments. J Vet Med 2020; 82: 1379-1386.
31. Fabri FV, Pinto NB, de Mattos MdSF, Rodrigues RF, Shinohara DR, Pereira PM, et al. First report of oxacillin-susceptible mecA-positive Staphylococcus aureus in healthy dogs and their owners in southern Brazil. Prev Vet Med 2021; 189: 105286.
32. Wolska-Gębarzewska M, Międzobrodzki J, Kosecka-Strojek M. Current types of staphylococcal cassette chromosome mec (SCC mec) in clinically relevant coagulase-negative staphylococcal (CoNS) species. Crit Rev Microbiol 2024; 50: 1020-1036.
33. Ma GC, Worthing KA, Gottlieb T, Ward MP, Norris JM. Molecular characterization of community‐associated methicillin‐resistant Staphylococcus aureus from pet dogs. Zoonoses Public Health 2020; 67: 222-
230.
34. Sakoulas G, Eliopoulos GM, Fowler Jr VG, Moellering Jr RC, Novick RP, Lucindo N, et al. Reduced susceptibility of Staphylococcus aureus to vancomycin and platelet microbicidal protein correlates with defective autolysis and loss of accessory gene regulator (agr) function. Antimicrob Agents Chemother 2005; 49: 2687-2692.
35. Khermouche F, Heleili N, Merradi M, Hachemi A, Drapeau A, Murri S, et al. Methicillin-resistant S. aureus carrying the PVL and Toxic Shock Syndrome toxin in healthy dogs in Algeria. Antibiotics 2024; 13: 1090.
36. Tabatabaei S, Najafifar A, Badouei MA, Salehi TZ, Tamai IA, Khaksar E, et al. Genetic characterisation of methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in pets and veterinary personnel in Iran: new insights into emerging methicillin-resistant S. pseudintermedius (MRSP). J Glob Antimicrob Resist 2019; 16:6-10.
37. Gómez-Sanz E, Torres C, Lozano C, Zarazaga M. High diversity of Staphylococcus aureus and Staphylococcus pseudintermedius lineages and toxigenic traits in healthy pet-owning household members. Underestimating normal household contact? Comp Immunol Microbiol Infect Dis 2013; 36: 83-94.
38. Goudarzi M, Fazeli M, Eslami G, Pouriran R, Hajikhani B, Dadashi M. Genetic diversity analysis of methicillin-resistant Staphylococcus aureus strains isolated from intensive care unit in Iran. Oman Med J 2019; 34: 118.
39. Ho W-Y, Choo Q-C, Chew C-H. Predominance of three closely related methicillin-resistant Staphylococcus aureus clones carrying a unique ccrC-positive SCCmec type III and the emergence of spa t304 and t690 SCCmec type IV pvl+ MRSA Isolates in Kinta Valley, Malaysia. Microbial Drug Resistance 2017; 23: 215-223.
40. Weese JS. Methicillin-resistant Staphylococcus aureus in animals. ILAR J 2010; 51: 233-244.
2. Shoaib M, Aqib AI, Ashfaq K, Naveed A, Kulyar MF-e-A, Bhutta ZA, et al. Diversified epidemiological pattern and antibiogram of mecA gene in Staphylococcus aureus isolates of pets, pet owners and environment. Pak Vet J 2020; 40: 331-336.
3. Bilyk BL, Panchal VV, Tinajero-Trejo M, Hobbs JK, Foster SJ. An interplay of multiple positive and negative factors governs methicillin resistance in Staphylococcus aureus. Microbiol Mol Biol Rev 2022; 86(2): e00159-21.
4. Turlej A, Hryniewicz W, Empel J. Staphylococcal cassette chromosome mec (Sccmec) classification and typing methods: an overview. Pol J Microbiol 2011; 60: 95-103.
5. Crespo-Piazuelo D, Lawlor PG. Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) prevalence in humans in close contact with animals and measures to reduce on-farm colonisation. Ir Vet J 2021; 74: 21.
6. Suepaul S, Georges K, Unakal C, Boyen F, Sookhoo J, Ashraph K, et al. Determination of the frequency, species distribution and antimicrobial resistance of staphylococci isolated from dogs and their owners in Trinidad. PloS One 2021; 16(7): e0254048.
7. Hanitsch LG, Krüger R, Hoppe P-A, Humme D, Pokrywka A, Niebank M, et al. Outpatient decolonization after recurrent skin infection with Panton-Valentine leukocidin (PVL)-producing S. aureus—The importance of treatment repetition. PloS One 2020; 15(4): e0231772.
8. Jenul C, Horswill AR. Regulation of Staphylococcus aureus virulence. Microbiol Spectr 2019; 7(2): 10.1128/microbiolspec. gpp3-0031-2018.
9. Boero E, Pansegrau W, Giovani C, Rooijakkers SH, van Kessel KP, van Strijp JA, et al. Natural human immunity against staphylococcal protein A relies on effector functions triggered by IgG3. Front Immunol 2022; 13: 834711.
10. Hoffman CL, Thibault M, Hong J. Characterizing pet acquisition and retention during the COVID-19 pandemic. Front Vet Sci 2021; 8: 781403.
11. Hesari Y, Sohrabi N, Abiri R, Babaei S, Amiri Z. Staphylococcal cassette chromosome mec typing of meticillin-resistant Staphylococcus aureus in Kermanshah Province, West of Iran. Jundishapur J Microbiol 2020; 13: 1-7.
12. Davis MF, Misic AM, Morris DO, Moss JT, Tolomeo P, Beiting DP, et al. Genome sequencing reveals strain dynamics of methicillin-resistant Staphylococcus aureus in the same household in the context of clinical disease in a person and a dog. Vet Microbiol 2015; 180: 304-307.
13. Algammal AM, Hetta HF, Elkelish A, Alkhalifah DHH, Hozzein WN, Batiha GE-S, et al. Methicillin-Resistant Staphylococcus aureus (MRSA): one health perspective approach to the bacterium epidemiology, virulence factors, antibiotic-resistance, and zoonotic impact. Infect Drug Resist 2020; 13: 3255-3265.
14. Tadesse S. Antimicrobial resistance profile of Staphylococcus aureus isolated from clinical specimens and nasal swabs of patients at Tikur Anbessa specialized hospital, Addis Ababa, Ethiopia. BMC Pharmacol Toxicol 2018; 19: 24.
15. Tille PM (2021). Bailey & Scott's Diagnostic Microbiology. 15th ed. Elsevier Health Sciences. St. Louis, Missouri.
16. Zhang K, Sparling J, Chow BL, Elsayed S, Hussain Z, Church DL, et al. New quadriplex PCR assay for detection of methicillin and mupirocin resistance and simultaneous discrimination of Staphylococcus aureus from coagulase-negative staphylococci. J Clin Microbiol 2004; 42: 4947-4955.
17. Clinical and Laboratory Standards Institute (2024). Performance Standards for Antimicrobial Susceptibility Testing, 33 rd ed. Available online: www.clsi.org (accessed on 20 September 2024).
18. Brakstad OG, Aasbakk K, Maeland JA. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J Clin Microbiol 1992; 30: 1654-1660.
19. Zhang K, McClure J-A, Elsayed S, Louie T, Conly JM. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J Clin Microbiol 2005; 43: 5026-5033.
20. Shopsin B, Mathema B, Alcabes P, Said-Salim B, Lina G, Matsuka A, et al. Prevalence of agr specificity groups among Staphylococcus aureus strains colonizing children and their guardians. J Clin Microbiol 2003; 41: 456-459.
21. Lina G, Piémont Y, Godail-Gamot F, Bes M, Peter M-O, Gauduchon V, et al. Involvement of Panton-Valentine leukocidin—producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 1999; 29: 1128-1132.
22. Pomba C, Rantala M, Greko C, Baptiste KE, Catry B, Van Duijkeren E, et al. Public health risk of antimicrobial resistance transfer from companion animals. J Antimicrob Chemother 2017; 72: 957-968.
23. Harmsen D, Claus H, Witte W, Rothganger J, Claus H, Turnwald D, et al. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 2003; 41: 5442-5448.
24. Duquette R, Nuttall T. Methicillin‐resistant Staphylococcus aureus in dogs and cats: an emerging problem? J Small Anim Pract 2004; 45: 591-597.
25. Cuny C, Layer-Nicolaou F, Weber R, Köck R, Witte W. Colonization of dogs and their owners with Staphylococcus aureus and Staphylococcus pseudintermedius in households, veterinary practices, and healthcare facilities. Microorganisms 2022; 10: 677.
26. Van Balen J, Landers T, Nutt E, Dent A, Hoet A. Molecular epidemiological analysis to assess the influence of pet-ownership in the biodiversity of Staphylococcus aureus and MRSA in dog-and non-dog-owning healthy households. Epidemiol Infect 2017; 145: 1135-1147.
27. Sakr A, Brégeon F, Mège J-L, Rolain J-M, Blin O. Staphylococcus aureus nasal colonization: an update on mechanisms, epidemiology, risk factors, and subsequent infections. Front Microbiol 2018; 9: 2419.
28. Funaki T, Yasuhara T, Kugawa S, Yamazaki Y, Sugano E, Nagakura Y, et al. SCCmec typing of PVL-positive community-acquired Staphylococcus aureus (CA-MRSA) at a Japanese hospital. Heliyon 2019; 5(3): e01415.
29. Abdullahi IN, Zarazaga M, Campaña‐Burguet A, Eguizábal P, Lozano C, Torres C. Nasal Staphylococcus aureus and S. pseudintermedius carriage in healthy dogs and cats: a systematic review of their antibiotic resistance, virulence and genetic lineages of zoonotic relevance. J Appl Microbiol 2022; 133: 3368-3390.
30. Oh J-Y, Chae J-C, Han J-I, Song W-K, Lee C-M, Park H-M. Distribution and epidemiological relatedness of methicillin-resistant Staphylococcus aureus isolated from companion dogs, owners, and environments. J Vet Med 2020; 82: 1379-1386.
31. Fabri FV, Pinto NB, de Mattos MdSF, Rodrigues RF, Shinohara DR, Pereira PM, et al. First report of oxacillin-susceptible mecA-positive Staphylococcus aureus in healthy dogs and their owners in southern Brazil. Prev Vet Med 2021; 189: 105286.
32. Wolska-Gębarzewska M, Międzobrodzki J, Kosecka-Strojek M. Current types of staphylococcal cassette chromosome mec (SCC mec) in clinically relevant coagulase-negative staphylococcal (CoNS) species. Crit Rev Microbiol 2024; 50: 1020-1036.
33. Ma GC, Worthing KA, Gottlieb T, Ward MP, Norris JM. Molecular characterization of community‐associated methicillin‐resistant Staphylococcus aureus from pet dogs. Zoonoses Public Health 2020; 67: 222-
230.
34. Sakoulas G, Eliopoulos GM, Fowler Jr VG, Moellering Jr RC, Novick RP, Lucindo N, et al. Reduced susceptibility of Staphylococcus aureus to vancomycin and platelet microbicidal protein correlates with defective autolysis and loss of accessory gene regulator (agr) function. Antimicrob Agents Chemother 2005; 49: 2687-2692.
35. Khermouche F, Heleili N, Merradi M, Hachemi A, Drapeau A, Murri S, et al. Methicillin-resistant S. aureus carrying the PVL and Toxic Shock Syndrome toxin in healthy dogs in Algeria. Antibiotics 2024; 13: 1090.
36. Tabatabaei S, Najafifar A, Badouei MA, Salehi TZ, Tamai IA, Khaksar E, et al. Genetic characterisation of methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in pets and veterinary personnel in Iran: new insights into emerging methicillin-resistant S. pseudintermedius (MRSP). J Glob Antimicrob Resist 2019; 16:6-10.
37. Gómez-Sanz E, Torres C, Lozano C, Zarazaga M. High diversity of Staphylococcus aureus and Staphylococcus pseudintermedius lineages and toxigenic traits in healthy pet-owning household members. Underestimating normal household contact? Comp Immunol Microbiol Infect Dis 2013; 36: 83-94.
38. Goudarzi M, Fazeli M, Eslami G, Pouriran R, Hajikhani B, Dadashi M. Genetic diversity analysis of methicillin-resistant Staphylococcus aureus strains isolated from intensive care unit in Iran. Oman Med J 2019; 34: 118.
39. Ho W-Y, Choo Q-C, Chew C-H. Predominance of three closely related methicillin-resistant Staphylococcus aureus clones carrying a unique ccrC-positive SCCmec type III and the emergence of spa t304 and t690 SCCmec type IV pvl+ MRSA Isolates in Kinta Valley, Malaysia. Microbial Drug Resistance 2017; 23: 215-223.
40. Weese JS. Methicillin-resistant Staphylococcus aureus in animals. ILAR J 2010; 51: 233-244.
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| Issue | Vol 18 No 2 (2026) | |
| Section | Original Article(s) | |
| Keywords | ||
| Genotyping Drug resistance Methicillin-resistant Staphylococcus aureus | ||
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How to Cite
1.
Korani AM, Ahmadi E, Derakhshan S. Molecular profiling of methicillin‑resistant Staphylococcus aureus isolated from healthy pet dogs and their owners in western Iran. Iran J Microbiol. 2026;18(2):251-261.
