Colonization of methicillin-resistant Staphylococcus aureus among healthcare students: an integrative review

Oliveira, Erika Morganna Neves de; Carvalho, Ana Raquel Batista de; Ferreira, Adriano Menis; Moura, Luana Kelle Batista; Valle, Andreia Rodrigues Moura da Costa; Freitas, Daniela Reis Joaquim de; Moura, Maria Eliete Batista

doi:10.1590/1516-3180.2020.0564.R2.22042021

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Sao Paulo Medical Journal

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Original Artical • Sao Paulo Med. J. 139 (6) • 2021 • https://doi.org/10.1590/1516-3180.2020.0564.R2.22042021 copy

Colonization of methicillin-resistant Staphylococcus aureus among healthcare students: an integrative review

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

BACKGROUND:

Methicillin-resistant Staphylococcus aureus (MRSA) infection is a worldwide concern given its presence even in non-hospitalized healthy individuals, such as university students.

OBJECTIVE:

To identify in the literature the prevalence of colonization by MRSA among healthcare students.

DESIGN AND SETTING:

Integrative review of the literature conducted in Universidade Federal do Piauí.

METHOD:

A search for primary studies was performed in the following databases: Medical Literature Analysis and Retrieval System on-line; Cumulative Index to Nursing and Allied Health Literature; Web of Science; Scopus; and LILACS.

RESULTS:

This review included 27 studies that demonstrated MRSA infection prevalence ranging from 0.0 to 15.3% among students.

CONCLUSION:

The prevalence of colonization of MRSA among healthcare students is high, and the nasal cavity was cited as an important reservoir location for these microorganisms.

KEY WORDS (MeSH terms):
Students, health occupations; Methicillin resistance; Methicillin-resistant Staphylococcus aureus; Staphylococcus aureus; Students

AUTHORS’ KEYWORDS:
Multiresistance; Healthcare students; Colonization; Microorganisms

Data Source
Descriptors and Keywords
BVS
	Estudantes OR Estudantes de Ciências da Saúde OR Estudantes de Enfermagem OR Estudantes de Farmácia OR Estudantes de Medicina OR Aluno OR Alunos OR Estudante OR Enfermeiras Estudantes OR Alunos de Enfermagem OR Estudante de Enfermagem OR Enfermeiros Estudantes
	Staphylococcus aureus
	Resistência à meticilina
PubMed/ WEB OF SCIENCE/ SCOPUS
	“Students” OR “Students, Health Occupations” OR “Students, Nursing” OR “Students, Pharmacy” OR “Students, Medical” OR Students, Dental” OR “Health Occupations Students” OR “Health Occupations Student” OR “Student, Nursing” OR “Nursing Student” OR “Nursing Students” OR “Pharmacy Students” OR “Student, Pharmacy” OR “Pharmacy Student” OR “Medical Students” OR “Student, Medical” OR “Medical Student” OR “Dental Students” OR “Student, Dental” OR “Dental Student”
	“Staphylococcus aureus”
	“Methicillin Resistance” OR “Resistance, Methicillin” OR “Methicillin-Resistant” OR “Methicillin Resistant”
CINAHL
	Students, Health Occupations
	Staphylococcus aureus
	Methicillin-Resistant Staphylococcus Aureus

Article	Authors/Year	Location	Objective	Site
A1	Prates et al.¹¹11 Prates KA, Torres AM, Garcia LB, et al. Nasal carriage of methicillin-resistant Staphylococcus aureus in university students. Braz J Infect Dis. 2010;14(3):316-8. PMID: 20835520. 2010	Brazil	To determine the prevalence of nasal transportation of S. aureus in university students.	Nostrils
A2	Syafinaz et al.¹²12 Syafinaz AM, Nur Ain NZ, Nadzirahi SN, et al. Staphylococcus aureus Nasal Carriers Among Medical Students in A Medical School. Med J Malaysia. 2012;67(6):636-8. PMID: 23770966. 2012	Malaysia	To determine the prevalence of S. aureus nasal carriers among medical students.	Nostrils
A3	Bettin et al.¹³13 Bettin A, Causil C, Reyes N. Molecular identification and antimicrobial susceptibility of Staphylococcus aureus nasal isolates from medical students in Cartagena, Colombia. Braz J Infect Dis. 2012;16(4):329-34. PMID: 22846119; https://doi.org/10.1016/j.bjid.2012.06.017. https://doi.org/10.1016/j.bjid.2012.06.0... 2012	Colombia	To investigate the nasal transportation of Panton-Valentin leukocidin-positive S. aureus strains, categories of transportation and risk factors associated with colonization, in medical students.	Nostrils
A4	Chen et al.¹⁴14 Chen CS, Chen CY, Huang YC. Nasal carriage rate and molecular epidemiology of methicillin-resistant Staphylococcus aureus among medical students at a Taiwanese university. Int J Infect Dis. 2012;16(11):e799-803. PMID: 2287817; https://doi.org/10.1016/j.ijid.2012.07.004. https://doi.org/10.1016/j.ijid.2012.07.0... 2012	China	To investigate whether clinical exposure in the hospital affects MRSA nasal transportation among medical students.	Nostrils
A5	Sabri et al.¹⁶16 Sabri I, Adwan K, Essawi TA, Farraj MA. Molecular characterization of methicillin-resistant Staphylococcus aureus isolates in three different Arab world countries. Eur J Microbiol Immunol (Bp). 2013;3(3):183-7. PMID: 24265936; https://doi.org/10.1556/EuJMI.3.2013.3.5. https://doi.org/10.1556/EuJMI.3.2013.3.5... 2013	Palestine	To investigate the prevalence of nasal transportation of S. aureus and MRSA.	Nostrils
A6	López-Aguilera et al.¹⁵15 López-Aguilera S, Goñi-Yeste M del M, Barrado L, et al. Colonización nasal por Staphylococcus aureus en estudiantes de medicina: importancia en la transmisión hospitalaria [Staphylococcus aureus nasal colonization in medical students: importance in nosocomial transmission]. Enferm Infecc Microbiol Clin. 2013;31(8):500-5. PMID: 23352260; https://doi.org/10.1016/j.eimc.2012.12.005. https://doi.org/10.1016/j.eimc.2012.12.0... 2013	Spain	To determine the prevalence of nasal carriers of sensitive and methicillin-resistant S. aureus and evaluate knowledge of and adherence to hand hygiene among students.	Nostrils
A7	Mat Azis et al.¹⁷17 Mat Azis N, Hamid AAB, Pung HP, et al. Staphylococcus aureus infection risk in a population of health sciences students at a public university. Iranian J Publ Health 2014;43(Suppl 12):112-6. Available from: https://ijph.tums.ac.ir/index.php/ijph/article/view/4887. Accessed in 2021 (May 10). https://ijph.tums.ac.ir/index.php/ijph/a... 2014	Malaysia	To evaluate the transportation of S. aureus and its persistence in students of health sciences.	Nostrils
A8	Malik et al.¹⁸18 Malik NFA, Muharram SH, Abiola O. Staphylococcus aureus nasal carriage in young healthy adults in Brunei Darussalam. Brunei Int Med J. 2014;10(2):78-84. 2014	Brunei	To determine the prevalence of the status of nasal carrier of S. aureus and MRSA among healthy young people.	Nostrils
A9	Krishnamurthy et al.¹⁹19 Krishnamurthy V, Saha A, Renushri BV, Nagaraj ER. Methicillin Resistant Staphylococcus aureus Carriage, Antibiotic Resistance and Molecular Pathogenicity among Healthy Individuals Exposed and Not Exposed to Hospital Environment. J Clin Diagn Res. 2014;8(7):DC04-8. PMID: 25177563; https://doi.org/10.7860/JCDR/2014/8409.4638. https://doi.org/10.7860/JCDR/2014/8409.4... 2014	India	To examine the influence of exposure to the hospital environment on MRSA transportation, MRSA antimicrobial resistance patterns and presence of genes that encode five determinants of extracellular pathogenicity.	Nostrils, throat and hand palms
A10	Demirel et al.²⁰20 Demirel G, Findik D, Dagi HT, Arslan U. Community-acquired methicillin-resistant Staphylococcus aureus and genotypes among university students in Turkey. Southeast Asian J Trop Med Public Health. 2014;45(6):1401-9. PMID: 26466426. 2014	Turkey	To investigate the prevalence of methicillin-sensitive (CA-MSSA) and resistant (CA-MRSA) S. aureus, including inducible sleepers (ID-MRSA), in S. aureus and MRSA strain genotypes from nasal cultures.	Nostrils
A11	Renushri et al.²¹21 Renushri BV, Saha A, Nagaraj ER, et al. Screening for methicillin-resistant Staphylococcus aureus carriers among individuals exposed and not exposed to the hospital environment and their antimicrobial sensitivity pattern. Annals of Tropical Medicine and Public Health. 2014;7(1):19-24. Available from: https://cyberleninka.org/article/n/503731. Accessed in 2021 (May 10). https://cyberleninka.org/article/n/50373... 2014	India	To assess the influence of exposure to the hospital environment on MRSA transportation.	Nostrils and throat
A12	Ribeiro et al.²²22 Ribeiro IF, Silva SFR, Silva SL, et al. Identificação de Staphylococcus aureus e Staphylococcus aureus resistente à meticilina em estudantes universitários. Rev Ciênc Farm Básica Apl. 2014;35(2):299-302. Available from: https://rcfba.fcfar.unesp.br/index.php/ojs/article/view/145/143. Accessed in 2021 (May 10). https://rcfba.fcfar.unesp.br/index.php/o... 2014	Brazil	To identify S. aureus and MRSA in university students.	Nostrils and palm hands
A13	Holý et al.²⁴24 Holý O, Vlčková J, Matoušková I, Kolář M. Prevalence výskytu nosního nosičství kmenů Staphylococcus aureus a meticilin rezistentních kmenů S. aureus (MRSA) u studentů všeobecného lékařství LF UP v Olomouci [The prevalence of nasal carriage of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) among general medicine students of the Palacky University Olomouc]. Epidemiol Mikrobiol Imunol. 2015;64(2):98-101. PMID: 26099614. 2015	Czech Republic	To investigate the prevalence of nasal transportation of S. aureus and MRSA in healthy people aged 18–26 years. To find out whether the prevalence of nasal transportation strains of S. aureus and MRSA varies over the years of studies. To compare general medical students from year 1 and year 5 for nasal transportation of S. aureus and MRSA strains.	Nostrils
A14	Zakai et al.²³23 Zakai SA. Prevalence of methicillin-resistant Staphylococcus aureus nasal colonization among medical students in Jeddah, Saudi Arabia. Saudi Med J. 2015;36(7):807-12. PMID: 26108584; https://doi.org/10.15537/smj.2015.7.11609. https://doi.org/10.15537/smj.2015.7.1160... 2015	Saudi Arabia	To identify MRSA nasal carrier status among medical students during their clinical rotations.	Nostrils
A15	Collazos Marín et al.²⁵25 Collazos Marín LF, Estupiñan Arciniegas G, Chavez Vivas M. Characterization of Staphylococcus aureus Isolates That Colonize Medical Students in a Hospital of the City of Cali, Colombia. Int J Microbiol. 2015;2015:358489. PMID: 26495001; https://doi.org/10.1155/2015/358489. https://doi.org/10.1155/2015/358489... 2015	Colombia	To establish the genetic diversity of S. aureus isolates and detect the presence of mecA gene in isolated strains in asymptomatic medical students who were in their clinical rotation phase in a hospital.	Nostrils
A16	Petti et al.²⁶26 Petti S, Kakisina N, Volgenant CM, et al. Low methicillin-resistant Staphylococcus aureus carriage rate among Italian dental students. Am J Infect Control. 2015;43(12):e89-91. PMID: 26384585; https://doi.org/10.1016/j.ajic.2015.08.008. https://doi.org/10.1016/j.ajic.2015.08.0... 2015	Italy	To evaluate the MRSA carrier rate in a sample of dental students.	Nostrils, throat and palm hands
A17	Hogan et al.³3 Hogan B, Rakotozandrindrainy R, Al-Emran H, et al. Prevalence of nasal colonisation by methicillin-sensitive and methicillin-resistant Staphylococcus aureus among healthcare workers and students in Madagascar. BMC Infect Dis. 2016;16(1):420. PMID: 27526771; https://doi.org/10.1186/s12879-016-1733-6. https://doi.org/10.1186/s12879-016-1733-... 2016	Madagascar	To examine the prevalence and clonal epidemiology of nasal S. aureus and MRSA among healthcare professionals and non-medical university students.	Nostrils
A18	Javaeed et al.²⁷27 Javaeed A, Khan S, Haqsubhani RU, Ghauri SK, Jahan S. Methicillin Resistant Staphylococcus Aureus Prevalence of Nasal Carriage among Healthy MBBS Students of Continental Medical College, Lahore. P J M H S. 2016;10(3): 1057-9. Available from: https://pjmhsonline.com/2016/july_sep/pdf/1057.pdf. Accessed in 2021 (May 10). https://pjmhsonline.com/2016/july_sep/pd... 2016	Pakistan	To assess the prevalence of MRSA transportation in healthy medical students.	Nostrils
A19	Subri et al.²⁸28 Subri NIBM, Hlaing SS, Myint, T, et al. Nasal Carriage of Staphylococcus aureus and Its Antibiotic Susceptibility Pattern among Medical and Nursing Students. Asian J Pharm. 2016;10(4):736-40. https://dx.doi.org/10.22377/ajp.v10i04.917. https://dx.doi.org/10.22377/ajp.v10i04.9... 2016	Malaysia	To determine the prevalence of nasal colonization of S. aureus and its susceptibility to antibiotics among pre-clinical and clinical physicians and nursing students.	Nostrils
A20	Ansari et al.²⁹29 Ansari S, Gautam R, Shrestha S, et al. Risk factors assessment for nasal colonization of Staphylococcus aureus and its methicillin resistant strains among pre-clinical medical students of Nepal. BMC Res Notes. 2016;9:214. PMID: 27068121; https://doi.org/10.1186/s13104-016-2021-7. https://doi.org/10.1186/s13104-016-2021-... 2016	Nepal	To evaluate the rate of nasal colonization of S. aureus, its methicillin-resistant strains and risk factors in medical students before clinical exposure.	Nostrils
A21	Okamo et al.³⁰30 Okamo B, Moremi N, Seni J, et al. Prevalence and antimicrobial susceptibility profiles of Staphylococcus aureus nasal carriage among pre-clinical and clinical medical students in a Tanzanian University. BMC Res Notes. 2016;9:47. PMID: 26817605; https://doi.org/10.1186/s13104-016-1858-0. https://doi.org/10.1186/s13104-016-1858-... 2016	Tanzania	To determine the prevalence of S. aureus and MRSA nasal transportation among medical students, and the antimicrobial susceptibility of isolated profiles of S. aureus, and to verify the association of S. aureus nasal transportation with demographic and clinical characteristics.	Nostrils
A22	Baek et al.³¹31 Baek YS, Baek SH, Yoo YJ. Higher nasal carriage rate of methicillin-resistant Staphylococcus aureus among dental students who have clinical experience. J Am Dent Assoc. 2016 May;147(5):348-53. PMID: 26778005; https://doi.org/10.1016/j.adaj.2015.12.004. https://doi.org/10.1016/j.adaj.2015.12.0... 2016	South Korea	To determine the prevalence rate of nasal colonization by MRSA among dental students and identify the characteristics of the strains isolated.	Nostrils
A23	Radhakrishna et al.³²32 Radhakrishna M, Taneja A, Rao P. Nasal carriage of Staphylococcus aureus with special emphasis on methicillin-resistant Staphylococcus aureus among students of a south Indian medical college - prevalence and antibiogram pattern. Asian J Pharm Clin Res. 2016;9(8):129-32. https://doi.org/10.22159/ajpcr.2016.v9s2.13274. https://doi.org/10.22159/ajpcr.2016.v9s2... 2016	India	To establish the prevalence and pattern of S. aureus antibiograms, with special emphasis on MRSA among students of the second year.	Nostrils
A24	Abroo et al.⁷7 Abroo S, Hosseini Jazani N, Sharifi Y. Methicillin-resistant Staphylococcus aureus nasal carriage between healthy students of medical and nonmedical universities. Am J Infect Control. 2017;45(7):709-12. PMID: 28359610; https://doi.org/10.1016/j.ajic.2017.02.034. https://doi.org/10.1016/j.ajic.2017.02.0... 2017	Iran	To investigate the prevalence, antimicrobial susceptibility and molecular factors characteristic of CA (community acquired) MRSA among two groups of college students (medical and non-medical).	Nostrils
A25	Budri et al.³³33 Budri PE, Shore AC, Coleman DC, et al. Observational cross-sectional study of nasal staphylococcal species of medical students of diverse geographical origin, prior to healthcare exposure: prevalence of SCCmec, fusC, fusB and the arginine catabolite mobile element (ACME) in the absence of selective antibiotic pressure. BMJ Open. 2018 Apr 20;8(4):e020391. PMID: 29678979; http://dx.doi.org/10.1136/bmjopen-2017-020391. http://dx.doi.org/10.1136/bmjopen-2017-0... 2018	Ireland	To investigate co-located nasal Staphylococcus aureus and coagulase-negative staphylococci (CoNS), recovered from healthy medical students in a preclinical year and the transportation of genes and common elements to both species that may contribute to the evolution of S. aureus and MRSA.	Nostrils
A26	Al-Tamimi et al.³⁴34 Al-Tamimi M, Himsawi N, Abu-Raideh J, Jazar DA, Al-jawaldeh H, Mahmoud SAH. Nasal colonization by methicillin-sensitive and methicillin-resistant Staphylococcus aureus among medical students. J Infect Dev Ctries 2018; 12(5):326-35. https://doi.org/10.3855/jidc.9908 https://doi.org/10.3855/jidc.9908... 2018	Jordan	To investigate the prevalence, standard antimicrobial susceptibility, antibiotic resistance genes and risk factors of medical students with MRSA.	Nostrils
A27	Suhaili et al.³⁵35 Suhaili Z, Rafee P’, Mat Azis N, et al. Characterization of resistance to selected antibiotics and Panton-Valentine leukocidin-positive Staphylococcus aureus in a healthy student population at a Malaysian University. Germs. 2018;8(1):21-30. PMID: 29564245; https://doi.org/10.18683/germs.2018.1129. https://doi.org/10.18683/germs.2018.1129... 2018	Malaysia	To evaluate the antimicrobial susceptibility profile of S. aureus strains isolated from university students and to determine the prevalence of resistance to constitutive and inducible clindamycin, in which the latter would be capable of causing therapeutic failure due to false in vitro susceptibility to clindamycin.	Nostrils
A28	Onanuga et al.³⁶36 Onanuga A, Eboh DD, Okou GT. Antibiogram and Virulence Characteristics of Multi-drug Resistant Staphylococcus aureus from Nasal Cavity of Healthy Students of Niger Delta University, Amassoma, Bayelsa State, Nigeria. Journal of Clinical and Diagnostic Research. 2019;13(7):24-9. https://doi.org/10.7860/JCDR/2019/41396.13031. https://doi.org/10.7860/JCDR/2019/41396.... 2019	Nigeria	To determine the antibiogram and the virulent characteristics of nasal S. aureus, accessing its profile of resistance to antibiotics and potential pathogens in healthy students at the University of the Niger Delta, Bayelsa State, Nigeria.	Nostrils
A29	Szymanek-Majchrzak et al.³⁷37 Szymanek-Majchrzak K, Kosiński J, Żak K, et al. Prevalence of methicillin resistant and mupirocin-resistant Staphylococcus aureus strains among medical students of Medical University in Warsaw. Przegl Epidemiol. 2019;73(1):39-48. PMID: 31134773; https://doi.org/10.32394/pe.73.05. https://doi.org/10.32394/pe.73.05... 2019	Poland	To evaluate and compare the level of colonization of S. aureus (MRSA or MSSA) among medical students and evaluate the sensitivity of the strains.	Nostrils
A30	Efa et al.⁵5 Efa F, Alemu Y, Beyene G, Gudina EK, Kebede W. Methicillin-resistant Staphylococcus aureus carriage among medical students of Jimma University, Southwest Ethiopia. Heliyon. 2019;5(1):e01191. PMID: 30775580; https://doi.org/10.1016/j.heliyon.2019.e01191. https://doi.org/10.1016/j.heliyon.2019.e... 2019	Ethiopia	To determine the nasal transportation of MRSA and its antimicrobial susceptibility patterns among medical students at the Jimma University Medical Center (JUMC), southwestern Ethiopia.	Nostrils

	General students	Students before clinical exposure	Students after clinical exposure
A1	2.4%	–	–
A2	0.0%	–	–
A3	1.61%	–	–
A4	2.2%	1.9%	2.4%
A5	9.0%	–	–
A6	2.1%	–	–
A7	3.3%	–	–
A8	–	0.0%	–
A9	6.8 %	4.0%	9.0%
A10	3.0%	–	–
A11	8.2%	4.0%	11.8%
A12	1.9%	–	–
A13	0.0%	–	–
A14	15.3%	0.0%	6.7%
A15	14.3%	–	–
A16	3.2%	3.1%	0.0%
A17	1.3%	–	–
A18	5.5%	–	–
A19	0.0%	–	–
A20	–	4.0%	–
A21	0.3%	0.0%	0.3%
A22	3.1%	–	3.1%
A23	6.1%	–	–
A24	13.1%	–	–
A25	2.1%	2.1%	–
A26	4.1%	–	–
A27	8%	–	–
A28	7.1%	–	–
A29	0.1%	–	–
A30	8.4%	–	–

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[1] Address for correspondence: Erika Morganna Neves de Oliveira Universidade Federal do Piauí (UFPI), Campus Universitário Ministro Petrônio Portella Ininga —Teresina (PI) — Brasil CEP 64049-550 Tel. (+55 86) 3215-5513 E-mail: morgannaneves@hotmail.com