Although mobile phones as a rapid communication vehicle can lead to improved quality of healthcare, they can also facilitate the transmission of pathogens to patients. This current research focuses on genetic diversity, and genes involved in resistance and biofilm production of Staphylococcus aureus isolates from mobile phones of medical students. Antibiotic resistance profiling and polymerase chain reaction (PCR) amplification of antibiotic resistance and biofilm-related genes were investigated and statistically analyzed. Staphylococcal cassette chromosome mec (SCCmec) types were analyzed by multiplex PCR, and S. aureus protein A gene typing (spa typing) was done using PCR and sequencing. Sixty-four S. aureus isolates (16.8%) were obtained from 380 medical students' mobile phones who were working in hospitals. The findings showed that 71.9% of the isolates were MRSA and 78.1% were classified as MDR. All isolates exhibited sensitivity to vancomycin and linezolid. Overall, 7.8% of the isolates displayed an inducible clindamycin resistance phenotype, while 26.7% showed resistance to mupirocin. The results indicated that 68.8% of the isolates were biofilm producers, with 7 isolates (15.9%) classified as strong producers, 22 isolates (50%) as moderate producers, and 15 isolates (34.1%) as weak producers. The most prevalent type was CC8-MRSA III/t030 (18.7%), followed by CC8-MRSA III/t037 (12.5%), CC/ST22-MSSA/t790 (10.9%), CC1-MRSA IV-t114 (9.4%), CC1-MRSA IV-t127 (7.8%), CC8-MRSA V/t064 (7.8%), CC/ST15-MSSA-t360 (7.8%), CC30-MSSA/t021(6.3%), MRSA V-t355 (6.3%), CC8-MRSA III/t421 (4.7%), CC1-MRSA V-t267 (4.7%), and CC/ST15-MSSA-t084 (3.1%). The genetic diversity and prevalent multidrug resistance indicate that the resistance situation of S. aureus recovered from mobile phones in Tehran is severe, posing a potential threat to patients, the community, and healthcare settings.
De Groote P, Blot K, Conoscenti E, Labeau S, Blot S. Mobile phones as a vector for Healthcare-Associated Infection: a systematic review. Intensive Crit Care Nurs 2022; 72: 103266. https://doi.org/10.1016/j.iccn.2022.103266.
Oluduro AO, Adesiyan YM, Omoboye OO, Odeyemi AT. Phenotypic and molecular characterization of Staphylococcus aureus from mobile phones in Nigeria. AIMS Microbiol 2023; 9: 402–18. https://doi.org/10.3934/microbiol.2023021.
Simmonds-Cavanagh R. Viability of hospital pathogens on mobile phone. Am J Infect Control 2022; 50: 787–91. https://doi.org/10.1016/j.ajic.2021.11.003.
Hamdan-Partida A, González-García S, Martínez-Ruíz FJ, Zavala-Sánchez MÁ, Bustos-Hamdan A, Bustos-Martínez J. Molecular characterization of staphylococcus aureus strains isolated from mobile phones. Microorganisms 2022; 10: 669. https://doi.org/10.3390/microorganisms10030669.
Furuhata K, Ishizaki N, Sogawa K, Kawakami Y, Lee S-I, Sato M, et al. Isolation, identification and antibacterial susceptibility of Staphylococcus spp. Associated with the mobile phones of university students. Biocontrol Sci 2016; 21: 91–8. https://doi.org/10.4265/bio.21.91.
Jansen AS, Balbinot GC, Daur AV, Silva ACFd, Nogueira KS, Fernandes T, et al. Detection of potentially pathogenic bacteria on cell phones of hospital and university-based populations in Curitiba, southern Brazil. A cross-sectional study. Sao Paulo Med J 2019; 137: 343–8. https://doi.org/10.1590/1516-3180.2018.044305072019.
Al-Masri MY, Abu-Hasan NS. Staphylococcus aureus carriage and contamination of mobile phones among students of An-Najah National University in Palestine (P. 247). Chula Med J 2020; 64: 247–57.
Jalalmanesh S, Darvishi M, Rahimi M, Akhlaghdoust M. Contamination of senior medical students' cell phones by nosocomial infections: a survey in a university-affiliated Hospital in Tehran. Shiraz E-med J 2017; 18. https://doi.org/10.5812/semj.43920.
Banawas S, Abdel-Hadi A, Alaidarous M, Alshehri B, Bin Dukhyil AA, Alsaweed M, et al. Multidrug-resistant bacteria associated with cell phones of healthcare professionals in selected hospitals in Saudi Arabia. Can J Infect Dis Med Microbiol 2018; 2018. https://doi.org/10.1155/2018/6598918.
Mushabati N, Samutela M, Yamba K, Ngulube J, Nakazwe R, Nkhoma P, et al. Bacterial contamination of mobile phones of healthcare workers at the University Teaching Hospital, Lusaka, Zambia. J Infect Prev 2021; 3: 100126. https://doi.org/10.1016/j.infpip.2021.100126.
Cicciarella Modica D, Maurici M, D'Alò GL, Mozzetti C, Messina A, Distefano A, et al. Taking screenshots of the invisible: a study on bacterial contamination of mobile phones from university students of healthcare professions in Rome, Italy. Microorganisms 2020; 8: 1075. https://doi.org/10.3390/microorganisms8071075.
Silva V, Capelo JL, Igrejas G, Poeta P. Molecular mechanisms of antimicrobial resistance in Staphylococcus aureus biofilms. Emerging Modalities Mitigation Antimicrob Resist 2022: 291–314. https://doi.org/10.1007/978-3-030-84126-3_12.
Noumi E, Merghni A, Alreshidi M, Del Campo R, Adnan M, Haddad O, et al. Phenotypic and genotypic characterization with MALDI-TOF-MS based identification of Staphylococcus spp. isolated from Mobile phones with their antibiotic susceptibility, biofilm formation, and adhesion properties. Int J Environ Res Public Health 2020; 17: 3761. https://doi.org/10.3390/ijerph17113761.
Goudarzi M, Kobayashi N, Dadashi M, Pantůček R, Nasiri MJ, Fazeli M, et al. Prevalence, genetic diversity, and temporary shifts of inducible clindamycin resistance Staphylococcus aureus clones in Tehran, Iran: a molecular-epidemiological analysis from 2013 to 2018. Front Microbiol 2020; 11: 663. https://doi.org/10.3389/fmicb.2020.00663.
Goudarzi M, Goudarzi H, Sá Figueiredo AM, Udo EE, Fazeli M, Asadzadeh M, et al. Molecular characterization of methicillin resistant Staphylococcus aureus strains isolated from intensive care units in Iran: ST22-SCC mec IV/t790 emerges as the major clone. PLoS One 2016; 11: e0155529. https://doi.org/10.1371/journal.pone.0155529.
Yousefi M, Pourmand MR, Fallah F, Hashemi A, Mashhadi R, Nazari-Alam A. Characterization of Staphylococcus aureus biofilm formation in urinary tract infection. Iran J Public Health 2016; 45: 485.
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: 5442–8. https://doi.org/10.1128/JCM.41.12.5442-5448.2003.
Goh Z, Chung P. Incidence of meticillin-resistant Staphylococcus aureus contamination on mobile phones of medical students. J Hosp Infect 2019; 101: 482–3. https://doi.org/10.1016/j.jhin.2019.01.022.
Zakai S, Mashat A, Abumohssin A, Samarkandi A, Almaghrabi B, Barradah H, et al. Bacterial contamination of cell phones of medical students at King Abdulaziz University, Jeddah, Saudi Arabia. J Microsc Ultrastruct 2016; 4: 143–6. https://doi.org/10.1016/j.jmau.2015.12.004.
Kanayama AK, Takahashi H, Yoshizawa S, Tateda K, Kaneko A, Kobayashi I. Staphylococcus aureus surface contamination of mobile phones and presence of genetically identical strains on the hands of nursing personnel. Am J Infect Control 2017; 45: 929–31. https://doi:10.1016/j.ajic.2017.02.011.
Taher N. Pathogenic bacteria isolated from personal cell phones of health care staff in Iraqi hospitals. J Pure Appl Microbiol 2019; 13: 1145–50. https://dx.doi.org/10.22207/JPAM.13.2.53.
Dadashi M, Hajikhani B, Darban-Sarokhalil D, van Belkum A, Goudarzi M. Mupirocin resistance in Staphylococcus aureus: a systematic review and meta-analysis. J Glob Antimicrob Resist 2020; 20: 238–47. https://doi.org/10.1016/j.jgar.2019.07.032.
Babu T, Rekasius V, Parada JP, Schreckenberger P, Challapalli M. Mupirocin resistance among methicillin-resistant Staphylococcus aureus-colonized patients at admission to a tertiary care medical center. J Clin Microbiol 2009; 47: 2279–80. https://doi.org/10.1128/JCM.01834-08.
Desroches M, Potier J, Laurent F, Bourrel A-S, Doucet-Populaire F, Decousser J-W, et al. Prevalence of mupirocin resistance among invasive coagulase-negative staphylococci and methicillin-resistant Staphylococcus aureus (MRSA) in France: emergence of a mupirocin-resistant MRSA clone harbouring mupA. J Antimicrob Chemother 2013; 68: 1714–7. https://doi.org/10.1093/jac/dkt085.
Liu Q-Z, Wu Q, Zhang Y-B, Liu M-N, Hu F-P, Xu X-G, et al. Prevalence of clinical meticillin-resistant Staphylococcus aureus (MRSA) with high-level mupirocin resistance in Shanghai and Wenzhou, China. Int J Antimicrob Agents 2010; 35: 114–8. https://doi.org/10.1016/j.ijantimicag.2009.09.018.
Goudarzi M, Mohammadi A, Amirpour A, Fazeli M, Nasiri MJ, Hashemi A, et al. Genetic diversity and biofilm formation analysis of Staphylococcus aureus causing urinary tract infections in Tehran, Iran. J Infect Dev Ctries 2019; 13: 777–85. https://doi.org/10.3855/jidc.11329.
Prakash PH, Rajan V, Gopal S. Predominance of SCCmec types IV and V among biofilm producing device-associated Staphylococcus aureus strains isolated from tertiary care hospitals in Mysuru, India. Enferm Infecc Microbiol Clin 2017; 35: 229–35. https://doi.org/10.1016/j.eimc.2016.09.005.
Navidinia M, Zamani S, Mohammadi A, Araghi S, Amini C, Pourhossein B, et al. Hospital-related lineage of USA300 methicillin-resistant Staphylococcus aureus (MRSA) to cause bacteremia in Iran. Biomed Res Int 2023; 2023. https://doi.org/10.1155/2023/8335385.
Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, et al. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One 2011; 6: e17936. https://doi.org/10.1371/journal.pone.0017936.
Boswihi SS, Udo EE, Al-Sweih N. Shifts in the clonal distribution of methicillin-resistant Staphylococcus aureus in Kuwait hospitals: 1992-2010. PLoS One 2016; 11: e0162744. https://doi.org/10.1371/journal.pone.0162744.
Boswihi SS, Udo EE, AlFouzan W. Antibiotic resistance and typing of the methicillin-resistant Staphylococcus aureus clones in Kuwait hospitals, 2016-2017. BMC Microbiol 2020; 20: 1–9. https://doi.org/10.1186/s12866-020-02009-w.
Li J, Wang L, Ip M, Sun M, Sun J, Huang G, et al. Molecular and clinical characteristics of clonal complex 59 methicillin-resistant Staphylococcus aureus infections in Mainland China. PLoS One 2013; 8: e70602. https://doi.org/10.1371/journal.pone.0070602.
Goudarzi M, Bahramian M, Tabrizi MS, Udo EE, Figueiredo AMS, Fazeli M, et al. Genetic diversity of methicillin resistant Staphylococcus aureus strains isolated from burn patients in Iran: ST239-SCCmec III/t037 emerges as the major clone. Microb Pathog 2017; 105: 1–7. https://doi.org/10.1016/j.micpath.2017.02.004.
Qin Y, Wen F, Zheng Y, Zhao R, Hu Q, Zhang R. Antimicrobial resistance and molecular characteristics of methicillin-resistant Staphylococcus aureus isolates from child patients of high-risk wards in Shenzhen, China. Jpn J Infect Dis 2017; 70: 479–84. https://doi.org/10.7883/yoken.JJID.2016.328.
Mora-Hernández Y, Vera Murguía E, Stinenbosch J, Hernández Jauregui P, van Dijl JM, Buist G. Molecular typing and antimicrobial resistance profiling of 33 mastitis-related Staphylococcus aureus isolates from cows in the Comarca Lagunera region of Mexico. Sci Rep 2021; 11: 6912. https://doi.org/10.1038/s41598-021-86453-2.
Earls MR, Kinnevey PM, Brennan GI, Lazaris A, Skally M, O'Connell B, et al. The recent emergence in hospitals of multidrug-resistant community-associated sequence type 1 and spa type t127 methicillin-resistant Staphylococcus aureus investigated by whole-genome sequencing: implications for screening. PLoS One 2017; 12: e0175542. https://doi.org/10.1371/journal.pone.0175542.
Tsergouli K, Karampatakis T, Kontopoulou K, Pappa S, Kampouridou P, Kallasidou G, et al. Spa diversity and genetic characterization of t127 methicillin-resistant Staphylococcus aureus in a tertiary Greek hospital. Acta Microbiol Immunol Hung 2022; 69: 185–92. https://doi.org/10.1556/030.2022.01825.
Güven Gökmen T, Kalayci Y, Yaman A, Köksal F. Molecular characterization of methicillin-resistant Staphylococcus aureus strains by spa typing and pulsed field gel electrophoresis methods. BMC Microbiol 2018; 18: 1–7. https://doi.org/10.1186/s12866-018-1305-6.
Grundmann H, Schouls LM, Aanensen DM, Pluister GN, Tami A, Chlebowicz M, et al. The dynamic changes of dominant clones of Staphylococcus aureus causing bloodstream infections in the European region: results of a second structured survey. Eurosurveillance 2014; 19: 20987. https://doi.org/10.2807/1560-7917.ES2014.19.49.20987.
Rijnders M, Deurenberg R, Boumans M, Hoogkamp-Korstanje J, Beisser P, Stobberingh E. Population structure of Staphylococcus aureus strains isolated from intensive care unit patients in The Netherlands over an 11-year period (1996 to 2006). J Clin Microbiol 2009; 47: 4090–5. https://doi.org/10.1128/JCM.00820-09.
Skraamm I, Moen AEF, Bukholm G. Nasal carriage of Staphylococcus aureus: frequency and molecular diversity in a randomly sampled Norwegian community population. APMIS 2011; 119: 522–8. https://doi.org/10.1111/j.1600-0463.2011.02758.x.
Wurster JI, Bispo PJ, Van Tyne D, Cadorette JJ, Boody R, Gilmore MS. Staphylococcus aureus from ocular and otolaryngology infections are frequently resistant to clinically important antibiotics and are associated with lineages of community and hospital origins. PLoS One 2018; 13: e0208518. https://doi.org/10.1371/journal.pone.0208518.
Chamon RC, Iorio NLP, da Silva Ribeiro S, Cavalcante FS, Dos Santos KRN. Molecular characterization of Staphylococcus aureus isolates carrying the Panton-Valentine leukocidin genes from Rio de Janeiro hospitals. Diagn Microbiol Infect Dis 2015; 83: 331–4. https://doi.org/10.1016/j.diagmicrobio.2015.09.004.
Hashemizadeh Z, Hadi N, Mohebi S, Kalantar-Neyestanaki D, Bazargani A. Characterization of SCCmec, spa types and Multi Drug Resistant of methicillin-resistant Staphylococcus aureus isolates among inpatients and outpatients in a referral hospital in Shiraz, Iran. BMC Res Notes 2019; 12: 1–6. https://doi.org/10.1186/s13104-019-4627-z.
Aggarwal S, Jena S, Panda S, Sharma S, Dhawan B, Nath G, et al. Antibiotic susceptibility, virulence pattern, and typing of Staphylococcus aureus strains isolated from variety of infections in India. Front Microbiol 2019; 10: 2763. https://doi.org/10.3389/fmicb.2019.02763.
Egyir B, Bentum J, Attram N, Fox A, Obeng-Nkrumah N, Appiah-Korang L, et al. Whole genome sequencing and antimicrobial resistance of staphylococcus aureus from surgical site infections in Ghana. Pathogens 2021; 10: 196. https://doi.org/10.3390/pathogens10020196.
Kateete DP, Asiimwe BB, Mayanja R, Mujuni B, Bwanga F, Najjuka CF, et al. Nasopharyngeal carriage, spa types and antibiotic susceptibility profiles of Staphylococcus aureus from healthy children less than 5 years in Eastern Uganda. BMC Infect Dis 2019; 19: 1–10. https://doi.org/10.1186/s12879-019-4652-5.