Prevalence, virulence genes, antimicrobial susceptibility, and genetic diversity ofStaphylococcus aureusfrom young people from 18 to 25-year-old age in Ho Chi Minh City, Vietnam

Abstract

Objective: To investigate the prevalence, antimicrobial resistance and genetic diversity of Staphylococcus (S.) aureus among healthy young adults of 18 to 25 years in Ho Chi Minh City, Vietnam.

Methods: A cross-sectional, descriptive study was conducted between December 2023 and December 2024. Nasal swabs were processed for S. aureus isolation, antibiotic susceptibility testing, and PCR-based detection of spa, pvl, and mecA genes. Genetic similarity was assessed using the unweighted pair group method with arithmetic mean cluster analysis. Statistical significance was determined by Chi-square test.

Results: In this cross-sectional study of 428 students, the S. aureus carriage rate was 33.9%. Methicillin-resistant S. aureus (MRSA) prevalence was 54.5% (79/145). 10%-17% of MRSA isolates exhibited resistance to three to ten antibiotics, with two strains demonstrating resistance to 11 and 12 drugs, respectively. The pvl gene was detected in 5.8% of isolates. 55.17% S. aureus strains belonged to ten distinct spa types with 300-bp amplicons.

Conclusions: These findings provide valuable insights into S. aureus carriage patterns among youth in Ho Chi Minh City, informing public health strategies for prevention and treatment.

Keywords

Antibiotic resistance

Conflict of interest statement

The authors declare that there are no conflicts of interest.

Funding

This study was supported by Nguyen Tat Thanh University, Ho Chi Minh city, Viet Nam, grant number 2023.01.18/KHCN; University of Medicine and Pharmacy at Ho Chi Minh City, Vietnam, project number 214/2023/HD-DHYD.

Authors’ contributions

P.H.N., A.N.T.T. performed the data collection, data management. P.H.N, L.L.T., T.N.T.X., H.V.Q. performed data and statistical analysis. P.H.N, L.L.T. and H.V.Q. finalized the data and result writing. H.V.Q. provided overall supervision and finalized the final version of the manuscript for submission.

Publisher’s note

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Edited by Zhang Q, Lei Y, Pan Y

Acknowledgments

The authors sincerely thank NTT Hi-Tech Institute, Nguyen Tat Thanh University, for providing the experimental facilities, and acknowledge technicians Ngo Nguyen Vu, Bao Tran, and My Duyen for their professional microbiological technical support.

References

[1] Chen YH, Huang KYA, Huang YC, Chi H, Lu CY, Chang LY, et al. Prevalence and molecular characterizations of Staphylococcus aureus nasal colonization among patients in pediatric intensive care units in Taiwan. Antimicrob Resist Infect Control 2020; 9(1): 41.

[2] Sadauki AH, Olorukooba AA, Balogun MS, Dalhat MM, Waziri H, Abdulaziz MM, et al. Nasal carriage of meticillin-resistant Staphylococcus aureus among children living with HIV attending Infectious Diseases Clinics in Kano, Nigeria. Infect Prev Pract 2022; 4(2): 100213.

[3] Aires-de-Sousa M. Methicillin-resistant Staphylococcus aureus among animals: Current overview. Clin Microbiol Infect 2017; 23(6): 373-380.

[4] David MZ, Daum RS. Treatment of Staphylococcus aureus infections. Curr Top Microbiol Immunol 2017; 409: 325-383.

[5] Nair N, Kourbatova E, Poole K, Huckabee CM, Murray P, Huskins WC, et al. Molecular epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) among patients admitted to adult intensive care units: The STAR*ICU Trial. Infect Control Hosp Epidemiol 2011; 32(11): 1057-1063. doi: 10.1086/662178.

[6] Otto M. Community-associated MRSA: What makes them special? Int J Med Microbiol 2013; 303(6-7): 324-330. doi: 10.1016/j.ijmm.2013.02.007.

[7] Turner NA, Sharma-Kuinkel BK, Maskarinec SA, Eichenberger EM, Shah PP, Carugati M, et al. Methicillin-resistant Staphylococcus aureus: An overview of basic and clinical research. Nat Rev Microbiol 2019; 17(4): 203-218.

[8] Lee AS, De Lencastre H, Garau J, Kluytmans J, Malhotra-Kumar S, Peschel A, et al. Methicillin-resistant Staphylococcus aureus. Nat Rev Dis Primers 2018; 4: 18033. doi: 10.1038/nrdp.2018.33.

[9] Hamzah AMC, Yeo CC, Puah SM, Chua KH, Chew CH, Hamzah AMC, et al. Staphylococcus aureus infections in Malaysia: A review of antimicrobial resistance and characteristics of the clinical isolates, 1990-2017. Antibiotics (Basel) 2019; 8(3): 128. doi: 10.3390/antibiotics8030128.

[10] Jevons M, Coe A, Parker M. Methicillin resistance in staphylococci. Lancet 1963; 281: 904-907.

[11] Hayakawa K, Marchaim D, Palla M, Gudur UM, Pulluru H, Bathina P, et al. Epidemiology of vancomycin-resistant Enterococcus faecalis: A case-case-control study. Antimicrob Agents Chemother 2012; 57(1): 49-55.

[12] Tenover FC, Weigel LM, Appelbaum PC, McDougal LK, Chaitram J, McAllister S, et al. Vancomycin-resistant Staphylococcus aureus isolate from a patient in Pennsylvania. Antimicrob Agents Chemother 2004; 48(1): 275-280.

[13] Doan DA, Nguyen AD, Le GB, Nguyen TTX, Nguyen PL, Dinh DX. Prevalence and associated factors of antibiotic self-medication and home storage among antibiotic users: A cross-sectional study in Vietnam. BMC Public Health 2025; 25(1): 1940.

[14] Shallcross LJ, Fragaszy E, Johnson AM, Hayward AC. The role of the Panton-Valentine leucocidin toxin in staphylococcal disease: A systematic review and meta-analysis. Lancet Infect Dis 2013; 13(1): 4354.

[15] Amdan NAN, Zamri HF, Ali MRM, Dahalan NA, Maling DRA, Hamdan WAFW, et al. Predominance of SCCmec type IV in community-acquired meticillin-resistant Staphylococcus aureus (MRSA) in multi-centre Malaysian hospitals. J Hosp Infect 2024; 143: 113-114.

[16] Tang CT, Nguyen DT, Hoa NT, Nguyen TMP, Le VT, To SD, et al. An outbreak of severe infections with community-acquired MRSA carrying the panton-valentine leukocidin following vaccination. PLoS One 2007; 2(9): e822. doi: 10.1371/journal.pone.0000822.

[17] Junaidi NSSA, Shakrin NNSM, Desa MNM, Yunus WMZW. Dissemination pattern of hospital-acquired methicillin-resistant Staphylococcus aureus and community-acquired MRSA isolates from Malaysian hospitals: A review from a molecular perspective. Malays J Med Sci 2023; 30(2): 26-41.

[18] Shume T, Urgesa K, Mekonnen S, Ayele F, Tesfa T, Tebeje F, et al. Nasal carriage of MRSA among clinically affiliated undergraduate students at the College of Health and Medical Sciences, Haramaya University, Ethiopia. Sci Rep 2024; 14(1): 29977.

[19] Congdon ST, Guaglione JA, Ricketts OMA, Murphy KV, Anderson MG, Trowbridge DA, et al. Prevalence and antibiotic resistance of Staphylococcus aureus associated with a college-aged cohort: Life-style factors that contribute to nasal carriage. Front Cell Infect Microbiol 2023; 13: 1195758. doi: 10.3389/fcimb.2023.1195758.

[20] Van Nguyen K, Zhang T, Vu BNT, Dao TT, Tran TK, Nguyen DNT, et al. Staphylococcus aureus nasopharyngeal carriage in rural and urban northern Vietnam. Trans R Soc Trop Med Hyg 2014; 108(12): 783-790. doi: 10.1093/trstmh/tru132.

[21] Stegger M, Andersen PS, Kearns A, Pichon B, Holmes MA, Edwards G, et al. Rapid detection, differentiation and typing of methicillin-resistant Staphylococcus aureus harbouring either mecA or the new mecA homologue mecALGA251. Clin Microbiol Infect 2012; 18(4): 395-400.

[22] Soe PE, Han WW, Sagili KD, Satyanarayana S, Shrestha P, Htoon TT, et al. High prevalence of methicillin-resistant Staphylococcus aureus among healthcare facilities and its related factors in Myanmar (2018-2019). Trop Med Infect Dis 2021; 6(2): 70.

[23] Valle DL, Paclibare PAP, Cabrera EC, Rivera WL. Molecular and phenotypic characterization of methicillin-resistant Staphylococcus aureus isolates from a tertiary hospital in the Philippines. Trop Med Health 2016; 44: 3.

[24] Xing A, Ng HM, Jiao H, Li K, Ye Q. The prevalence, epidemiological, and molecular characterization of methicillin-resistant Staphylococcus aureus (MRSA) in Macau (2017-2022). Microorganisms 2024; 12(1): 148. doi: 10.3390/microorganisms12010148.

[25] Al-Talib H, Samsudin S, Adnan A, Murugaiah C, Al-Talib H, Samsudin S, et al. Genetic diversity among methicillin-resistant Staphylococcus aureus in Malaysia (2002-2020). Trop Med Infect Dis 2022; 7(11): 360. doi: 10.3390/tropicalmed7110360.

[26] Waitayangkoon P, Thongkam A, Benjamungkalarak T, Rachayon M, Thongthaisin A, Chatsuwan T, et al. Hospital epidemiology and antimicrobial susceptibility of isolated methicillin-resistant Staphylococcus aureus: A one-year retrospective study at a tertiary care center in Thailand. Pathog Glob Health 2020; 114(4): 212-217.

[27] Santosaningsih D, Santoso S, Setijowati N, Rasyid HA, Budayanti NS, Suata K, et al. Prevalence and characterisation of Staphylococcus aureus causing community-acquired skin and soft tissue infections on Java and Bali, Indonesia. Trop Med Int Health 2018; 23(1): 34-44.

[28] Rio-Tinto A, Costa NS, Alvim DCSS, Oliveira LMA, De Oliveira TLR, Dos Santos KRN, et al. Increase in methicillin-resistant Staphylococcus spp. colonization among pregnant individuals during COVID-19 pandemic. Sci Rep 2024; 14(1): 14961.

[29] Farook NAM, Argimón S, Samat MNA, Salleh SA, Sulaiman S, Tan TL, et al. Diversity and dissemination of methicillin-resistant Staphylococcus aureus (MRSA) genotypes in Southeast Asia. Trop Med Infect Dis 2022; 7(12): 438. doi: 10.3390/tropicalmed7120438.

[30] Masim ML, Argimon S, Espiritu HO, Magbanua MA, Lagrada ML, Olorosa AM, et al. Genomic surveillance of methicillin-resistant Staphylococcus aureus in the Philippines, 2013-2014. Western Pac Surveill Response J 2021; 12(1): 6-16. doi: 10.5365/wpsar.2020.11.1.004.

[31] Saito N, Solante RM, Guzman FD, Telan EO, Umipig DV, Calayo JP, et al. A prospective observational study of community-acquired bacterial bloodstream infections in Metro Manila, the Philippines. PLoS Negl Trop Dis 2022; 16(5): e0010414.

[32] Abimannan N, Sumathi G, Krishnarajasekhar OR, Sinha B, Krishnan P. Clonal clusters and virulence factors of methicillin-resistant Staphylococcus aureus: Evidence for community-acquired methicillin-resistant Staphylococcus aureus infiltration into hospital settings in Chennai, South India. Indian J Med Microbiol 2019; 37(3): 326-336.

[33] Wang B, Xu Y, Zhao H, Wang X, Rao L, Guo Y, et al. Methicillin-resistant Staphylococcus aureus in China: A multicentre longitudinal study and whole-genome sequencing. Emerg Microbes Infect 2022; 11(1): 532-542.