American Journal of Infection Control 42 (2014) 918-20
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
Risk factors for Staphylococcus aureus and methicillin-resistant S aureus colonization among health care workers in pediatrics departments Ivete Martins Gomes MD, MSc a, Mariel Asbury Marlow PhD, MPH b, Marcos Gabriel Pinheiro MSc c, d, Maria de Fátima Nogueira de Freitas BS c, Fernanda Fernandes Fonseca MD a, Claudete Aparecida Araújo Cardoso MD, PhD a, e, Fábio Aguiar-Alves PhD c, d, * a
Department of Maternal and Child Care, School of Medicine, Fluminense Federal University, Niterói, Rio de Janeiro, Brazil Division of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, CA c Laboratory of Molecular Epidemiology and Biotechnology, Rodolfo Albino University Laboratory, Fluminense Federal University, Niterói, Rio de Janeiro, Brazil d Graduate Program in Pathology, Fluminense Federal University, Niterói, Rio de Janeiro, Brazil e Graduate Program in Medical Science, Fluminense Federal University, Niterói, Rio de Janeiro, Brazil b
Key Words: Occupational health
Risk factors for Staphylococcus aureus and methicillin-resistant S aureus (MRSA) were evaluated for 178 health care workers from a public hospital pediatrics department in Brazil. Colonization rates were 33.1% for S aureus and 5.1% for MRSA. Risk factors for S aureus colonization differed from those for MRSA. Results suggest nurses with prolonged pediatric patient contact in inpatient units are at higher risk for MRSA colonization. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Staphylococcus aureus is a gram-positive bacteria that can act as a human commensal or as a potentially deadly opportunistic pathogen1 causing illnesses ranging from skin and soft tissue and respiratory infections to life-threatening conditions.2 Methicillin-resistant S aureus (MRSA) is a main cause of health care-associated disease burden, with an even more evident epidemiologic significance in developing countries.3 Health care worker colonization is recognized as an important risk factor for infection in health care institutions.4,5 Although less studied, children have been shown to be central reservoirs of these bacteria as well as a risk factor for adult infection.6 For this, we suspected health care professionals working in a pediatrics department in a Brazilian public hospital would have higher colonization rates than other health care workers. Additionally, to improve hospital infection and antibiotic resistance control programs in pediatrics departments, we investigated risk factors for colonization among this population. * Address correspondence to Fábio Aguiar-Alves, PhD, Laboratório de Epidemiologia Molecular e Biotecnologia, Laboratório Universitário Rodolfo Albino, Universidade Federal Fluminense, Rua Mário Viana, 523, Santa Rosa, Niterói, RJ CEP 24200-002, Brazil. E-mail address: [email protected] (F. Aguiar-Alves). Conflicts of interest: None to report.
MATERIALS AND METHODS For our cross-sectional study, a structured questionnaire was administered to 178 actively employed health care professionals (out of 189 total employees) of the Pediatrics Department of Antonio Pedro University Hospital of the Fluminense Federal University in Niterói, Rio de Janeiro State, Brazil, from January 2012eDecember 2012. Following the questionnaire, we collected swabs rotated in the anterior of the nares for all personnel. Swabs were streaked onto mannitol salt agar and cultured at 37 C for 24 hours. S aureus colonies were identified by catalase and coagulase tests followed by antimicrobial resistance test against cefoxitin and oxacillin with 30 mg and 1 mg antimicrobial embedded discs, respectively.7 Resistance was confirmed by identifying the mecA gene by polymerase chain reaction.8 In the statistical analysis, variables with c2 test P value < .15 and variables predetermined as potential confounding factors were included in the logistic regression analysis. First, we evaluated potential risk factors for S aureus colonization and MRSA colonization by bivariate logistic regression. The final multivariate logistic model was determined by backward elimination, maintaining significant and confounding variables. The Hosmer and Lemeshow goodness of fit test was used to assess if there was evidence for lack of fit in the logistic
0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2014.05.009
I.M. Gomes et al. / American Journal of Infection Control 42 (2014) 918-20 Table 1 Risk factors for Staphylococcus aureus and methicillin-resistant S aureus (MRSA) colonization of health care workers from a public hospital pediatrics department in Niterói, Rio de Janeiro, Brazil (N ¼ 178)
Risk factor Risk factor for S aureus colonization Age (y) 18-30 31-40 41-50 51 or older Length of employment (y) 0-5 6-10 11-20 21 or more Surgery within the past year* No Yes Risk factor for MRSA colonization Occupation Physician Nurse Nurse technician Type of patient care Outpatient Inpatient
Unadjusted odds ratio
95% Confidence interval
Adjusted odds ratio
95% Confidence interval
919
Nurses were found to have 11.6 higher odds of MRSA colonization (95% CI, 1.2-110.7), even after adjusting for the type of care they provide (outpatient vs inpatient) (Table 1). Four of 9 MRSAcolonized health care workers were nurses working in inpatient units in pediatrics departments. DISCUSSION
1.00 2.90 4.30 3.68
d 0.84-10.06 1.31-14.08 1.12-12.10
1.00 2.95 6.82 6.25
d 0.80-10.84 1.43-32.45 1.05-37.18
1.00 2.00 1.56 1.78
d 0.73-5.27 0.68-3.57 0.77-4.13
1.00 1.04 0.52 0.60
d 0.34-3.19 0.14-1.88 0.13-2.68
1.00 2.22
d 0.870-5.69
1.00 15.60 3.84
d 1.74-139.92 0.39-37.80
1.00 11.61 2.94
d 1.22-110.65 0.28-30.47
1.00 4.64
d 0.57-37.94
1.00 2.66
d 0.30-23.70
*Not included in the final logistic regression model.
regression model. All data analysis was performed in SAS version 9.3 (SAS Institute Inc, Cary, NC). Our study was approved by the Antonio Pedro University Hospital of the Fluminense Federal University Ethics Committee. Written consent was received from all patients before the initiation of data and sample collection. RESULTS Mean age of the pediatrics department health care workers was 43.6 10.1 years with the majority being women (87.6%). A majority of health care workers had worked at the hospital for more than 10 years (52.8%). Colonization rates among all health care workers were 33.1% (n ¼ 59) for S aureus and 5.1% (n ¼ 9) for MRSA. None of the health care workers’ demographic, household, and clinical characteristics investigated, including income, number of household members, using antibiotic agents during the past 30 days, being hospitalized during the past year, or having surgery during the past year, were found to be associated with S aureus or MRSA colonization in the c2 analyses. The only variable found to have a significant association was type of health care professional with MRSA colonization (P ¼ .022), with 16.7% (n ¼ 5) of nurses being colonized. After adjusting for length of employment, health care workers aged 41-50 years had 6.8 higher odds (95% confidence interval [CI], 1.4-32.5), and those aged 51 years or older had 6.3 higher odds of S aureus colonization (95% CI, 1.1-37.2) (Table 1). Although length of employment was not found to be an individual risk factor, it was a confounding factor with age. Health care workers having had surgery within the past year had 2.2 higher odds for S aureus colonization (95% CI, 0.9-5.7), but this was not significant nor a confounder in the multivariate analysis and was not included in the final model.
S aureus and MRSA colonization rates found in our study suggest Brazilian health care workers in pediatrics departments experience relatively high S aureus and MRSA colonization rates in comparison to health care workers from other countries and departments. In studies published during the past 5 years with a sample size of at least 100 health care workers (nonoutbreak situations), mean S aureus nasal colonization was 24% 8.9%.9-24 In these studies, the mean nasal MRSA colonization was 3.5% 2.5% for developed and 6.8% 4.7% for developing nations, excluding a study from Libya that found 36.8% MRSA colonization. Rates found here were higher than in other studies on health care worker nasal colonization conducted in Brazil (18.7% for S aureus25 and 1.5% and 3% for MRSA25,26). On the other hand, these rates are lower than what we observed in children attending public daycare centers in the same city, in which 48% and 6.2% were colonized with S aureus and MRSA, respectively (unpublished results). Our results suggest nurses with prolonged pediatric patient contact in inpatient units are at higher risk of MRSA colonization than other professionals in the same department. Three previous studies conducted in Ethiopia and the United States also found nurses to be at increased risk for MRSA colonization.13,19,21 In Ethiopia, 21.2% of nurses, compared with 12.7% for all health care workers, had nasal MRSA colonization.13 One study from Atlanta found 4 of 7 MRSA-colonized health care workers to be nurses, 2 of whom worked in pediatrics departments.21 The type of care these nurses provide to pediatric patients, such as holding and feeding, may result in increased exposure to the bacteria. The difference in risk factors for S aureus and MRSA colonization suggests MRSA may have different transmission patterns and could be related to the carriage of community-associated MRSA by children into the hospital setting. Interventions for control of antibiotic resistant bacteria in pediatrics departments should be targeted in this population of nurses. Acknowledgment The authors thank the staff of the Pediatrics Department, Antonio Pedro University Hospital of the Fluminense Federal University, for providing support. This study received financial support from Programa de Fomento à Pesquisa (FOPESQ-UFF Grant), Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ - APQ1 Grant) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq Grant). References 1. Brown AF, Leech JM, Rogers TR, McLoughlin RM. Colonization: modulation of host immune response and impact on human vaccine design. Front Immunol 2014;4:507. 2. Lowy FD. Staphylococcus aureus infections. N Engl J Med 1998;339:520-32. 3. Allegranzi B, Bagheri Nejad S, Combescure C, Graafmans W, Attar H, Donaldson L, et al. Burden of endemic health-care-associated infection in developing countries: systematic review and meta-analysis. Lancet 2011;377: 228-41. 4. Peacock SJ, de Silva I, Lowy FD. What determines nasal carriage of Staphylococcus aureus? Trends Microbiol 2001;9:605-10. 5. Cimolai N. The role of healthcare personnel in the maintenance and spread of methicillin-resistant Staphylococcus aureus. J Infect Public Health 2008;1:78-100.
920
I.M. Gomes et al. / American Journal of Infection Control 42 (2014) 918-20
6. Wang JT, Liao CH, Fang CT, Chie WC, Lai MS, Lauderdale TL, et al. Prevalence of and risk factors for colonization by methicillin-resistant Staphylococcus aureus among adults in community settings in Taiwan. J Clin Microbiol 2009;47:2957-63. 7. Performance standards for antimicrobial disk susceptibility tests; approved standard. 11th ed. Wayne, [PA]: Clinical and Laboratory Standards Institute; 2012. 8. Oliveira DC, de Lencastre H. Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2002;46:2155-61. 9. Akhtar N. Staphylococcal nasal carriage of health care workers. J Coll Physicians Surgeons Pakistan 2010;20:439-43. 10. D’Souza M, Kotigadde S, Saralaya KV, Kotian MS. Prevalence of methicillinresistant Staphylococcus aureus carriage amongst health care workers of critical care units in Kasturba Medical College Hospital, Mangalore, India. J Clin Diagn Res 2013;7:2697-700. 11. Ruiz A, Mora M, Zurita C, Larco D, Toapanta Y, Zurita J. Prevalence of methicillin-resistant Staphylococcus aureus among health care workers of intensive care units in Ecuador. J Infect Dev Ctries 2014;8:116-9. 12. Huang YC, Su LH, Lin TY. Nasal carriage of methicillin-resistant Staphylococcus aureus among pediatricians in Taiwan. PLoS One 2013;8:e82472. 13. Shibabaw A, Abebe T, Mihret A. Nasal carriage rate of methicillin resistant Staphylococcus aureus among Dessie Referral Hospital health care workers; Dessie, Northeast Ethiopia. Antimicrob Resist Infect Control 2013;2:25. 14. Jannati E, Arzanlou M, Habibzadeh S, Mohammadi S, Ahadi P, MohammadiGhalehbin B, et al. Nasal colonization of mecA-positive, oxacillin-susceptible, methicillin-resistant Staphylococcus aureus isolates among nursing staff in an Iranian teaching hospital. Am J Infect Control 2013;41:1122-4. 15. Rongpharpi SR, Hazarika NK, Kalita H. The prevalence of nasal carriage of Staphylococcus aureus among healthcare workers at a tertiary care hospital in Assam with special reference to MRSA. J Clin Diagn Res 2013;7:257-60. 16. Tsering DC, Pal R, Kar S. Methicillin-resistant Staphylococcus aureus: prevalence and current susceptibility pattern in Sikkim. J Glob Infect Dis 2011;3:9-13. 17. Askarian M, Zeinalzadeh A, Japoni A, Alborzi A, Memish ZA. Prevalence of nasal carriage of methicillin-resistant Staphylococcus aureus and its antibiotic
18.
19.
20.
21.
22.
23.
24.
25.
26.
susceptibility pattern in healthcare workers at Namazi Hospital, Shiraz, Iran. Int J Infect Dis 2009;13:e241-7. Zorgani A, Elahmer O, Franka E, Grera A, Abudher A, Ghenghesh KS. Detection of meticillin-resistant Staphylococcus aureus among healthcare workers in Libyan hospitals. J Hosp Infect 2009;73:91-2. Elie-Turenne MC, Fernandes H, Mediavilla JR, Rosenthal M, Mathema B, Singh A, et al. Prevalence and characteristics of Staphylococcus aureus colonization among healthcare professionals in an urban teaching hospital. Infect Control Hosp Epidemiol 2010;31:574-80. Rijnders MIA, Nys S, Driessen C, Hoebe C, Hopstaken RM, Oudhuis GJ, et al. Staphylococcus aureus carriage among GPs in the Netherlands. Br J Gen Pract 2010;60:902-6. Immergluck LC, Satola SW, Jain S, McCracken C, Watson JR, Chan T, et al. Methicillin-resistant Staphylococcus aureus colonization among pediatric health care workers from different outpatient settings. Am J Infect Control 2013;41:841-3. Kottler S, Middleton JR, Perry J, Weese JS, Cohn LA. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus carriage in three populations. J Vet Intern Med 2010;24:132-9. Verwer PE, Robinson JO, Coombs GW, Wijesuriya T, Murray RJ, Verbrugh HA, et al. Prevalence of nasal methicillin-resistant Staphylococcus aureus colonization in healthcare workers in a Western Australian acute care hospital. Eur J Clin Microbiol Infect Dis 2012;31:1067-72. Vinodhkumaradithyaa A, Uma A, Srinivasan M, Ananthalakshmi I, Nallasivam P, Thirumalaikolundusubramanian P. Nasal carriage of methicillinresistant Staphylococcus aureus among surgical unit staff. Jpn J Infect Dis 2009; 62:228-9. Silva EC, Antas M, Monteiro BNA, Rabelo MA, Melo FL, Maciel MA. Prevalence and risk factors for Staphylococcus aureus in health care workers at a university hospital of Recife-PE. Braz J Infect Dis 2008;12:504-8. Senna JP, Pinto CA, Bernardon DR, Francisco AG, Epztein E, Ritt CB, et al. Identification of methicillin-resistant Staphylococcus aureus among careworkers and patients in an emergency hospital. J Hosp Infect 2003;54: 167-8.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
Risk factors for Staphylococcus aureus and methicillin-resistant S aureus colonization among health care workers in pediatrics departments Ivete Martins Gomes MD, MSc a, Mariel Asbury Marlow PhD, MPH b, Marcos Gabriel Pinheiro MSc c, d, Maria de Fátima Nogueira de Freitas BS c, Fernanda Fernandes Fonseca MD a, Claudete Aparecida Araújo Cardoso MD, PhD a, e, Fábio Aguiar-Alves PhD c, d, * a
Department of Maternal and Child Care, School of Medicine, Fluminense Federal University, Niterói, Rio de Janeiro, Brazil Division of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, CA c Laboratory of Molecular Epidemiology and Biotechnology, Rodolfo Albino University Laboratory, Fluminense Federal University, Niterói, Rio de Janeiro, Brazil d Graduate Program in Pathology, Fluminense Federal University, Niterói, Rio de Janeiro, Brazil e Graduate Program in Medical Science, Fluminense Federal University, Niterói, Rio de Janeiro, Brazil b
Key Words: Occupational health
Risk factors for Staphylococcus aureus and methicillin-resistant S aureus (MRSA) were evaluated for 178 health care workers from a public hospital pediatrics department in Brazil. Colonization rates were 33.1% for S aureus and 5.1% for MRSA. Risk factors for S aureus colonization differed from those for MRSA. Results suggest nurses with prolonged pediatric patient contact in inpatient units are at higher risk for MRSA colonization. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Staphylococcus aureus is a gram-positive bacteria that can act as a human commensal or as a potentially deadly opportunistic pathogen1 causing illnesses ranging from skin and soft tissue and respiratory infections to life-threatening conditions.2 Methicillin-resistant S aureus (MRSA) is a main cause of health care-associated disease burden, with an even more evident epidemiologic significance in developing countries.3 Health care worker colonization is recognized as an important risk factor for infection in health care institutions.4,5 Although less studied, children have been shown to be central reservoirs of these bacteria as well as a risk factor for adult infection.6 For this, we suspected health care professionals working in a pediatrics department in a Brazilian public hospital would have higher colonization rates than other health care workers. Additionally, to improve hospital infection and antibiotic resistance control programs in pediatrics departments, we investigated risk factors for colonization among this population. * Address correspondence to Fábio Aguiar-Alves, PhD, Laboratório de Epidemiologia Molecular e Biotecnologia, Laboratório Universitário Rodolfo Albino, Universidade Federal Fluminense, Rua Mário Viana, 523, Santa Rosa, Niterói, RJ CEP 24200-002, Brazil. E-mail address: [email protected] (F. Aguiar-Alves). Conflicts of interest: None to report.
MATERIALS AND METHODS For our cross-sectional study, a structured questionnaire was administered to 178 actively employed health care professionals (out of 189 total employees) of the Pediatrics Department of Antonio Pedro University Hospital of the Fluminense Federal University in Niterói, Rio de Janeiro State, Brazil, from January 2012eDecember 2012. Following the questionnaire, we collected swabs rotated in the anterior of the nares for all personnel. Swabs were streaked onto mannitol salt agar and cultured at 37 C for 24 hours. S aureus colonies were identified by catalase and coagulase tests followed by antimicrobial resistance test against cefoxitin and oxacillin with 30 mg and 1 mg antimicrobial embedded discs, respectively.7 Resistance was confirmed by identifying the mecA gene by polymerase chain reaction.8 In the statistical analysis, variables with c2 test P value < .15 and variables predetermined as potential confounding factors were included in the logistic regression analysis. First, we evaluated potential risk factors for S aureus colonization and MRSA colonization by bivariate logistic regression. The final multivariate logistic model was determined by backward elimination, maintaining significant and confounding variables. The Hosmer and Lemeshow goodness of fit test was used to assess if there was evidence for lack of fit in the logistic
0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2014.05.009
I.M. Gomes et al. / American Journal of Infection Control 42 (2014) 918-20 Table 1 Risk factors for Staphylococcus aureus and methicillin-resistant S aureus (MRSA) colonization of health care workers from a public hospital pediatrics department in Niterói, Rio de Janeiro, Brazil (N ¼ 178)
Risk factor Risk factor for S aureus colonization Age (y) 18-30 31-40 41-50 51 or older Length of employment (y) 0-5 6-10 11-20 21 or more Surgery within the past year* No Yes Risk factor for MRSA colonization Occupation Physician Nurse Nurse technician Type of patient care Outpatient Inpatient
Unadjusted odds ratio
95% Confidence interval
Adjusted odds ratio
95% Confidence interval
919
Nurses were found to have 11.6 higher odds of MRSA colonization (95% CI, 1.2-110.7), even after adjusting for the type of care they provide (outpatient vs inpatient) (Table 1). Four of 9 MRSAcolonized health care workers were nurses working in inpatient units in pediatrics departments. DISCUSSION
1.00 2.90 4.30 3.68
d 0.84-10.06 1.31-14.08 1.12-12.10
1.00 2.95 6.82 6.25
d 0.80-10.84 1.43-32.45 1.05-37.18
1.00 2.00 1.56 1.78
d 0.73-5.27 0.68-3.57 0.77-4.13
1.00 1.04 0.52 0.60
d 0.34-3.19 0.14-1.88 0.13-2.68
1.00 2.22
d 0.870-5.69
1.00 15.60 3.84
d 1.74-139.92 0.39-37.80
1.00 11.61 2.94
d 1.22-110.65 0.28-30.47
1.00 4.64
d 0.57-37.94
1.00 2.66
d 0.30-23.70
*Not included in the final logistic regression model.
regression model. All data analysis was performed in SAS version 9.3 (SAS Institute Inc, Cary, NC). Our study was approved by the Antonio Pedro University Hospital of the Fluminense Federal University Ethics Committee. Written consent was received from all patients before the initiation of data and sample collection. RESULTS Mean age of the pediatrics department health care workers was 43.6 10.1 years with the majority being women (87.6%). A majority of health care workers had worked at the hospital for more than 10 years (52.8%). Colonization rates among all health care workers were 33.1% (n ¼ 59) for S aureus and 5.1% (n ¼ 9) for MRSA. None of the health care workers’ demographic, household, and clinical characteristics investigated, including income, number of household members, using antibiotic agents during the past 30 days, being hospitalized during the past year, or having surgery during the past year, were found to be associated with S aureus or MRSA colonization in the c2 analyses. The only variable found to have a significant association was type of health care professional with MRSA colonization (P ¼ .022), with 16.7% (n ¼ 5) of nurses being colonized. After adjusting for length of employment, health care workers aged 41-50 years had 6.8 higher odds (95% confidence interval [CI], 1.4-32.5), and those aged 51 years or older had 6.3 higher odds of S aureus colonization (95% CI, 1.1-37.2) (Table 1). Although length of employment was not found to be an individual risk factor, it was a confounding factor with age. Health care workers having had surgery within the past year had 2.2 higher odds for S aureus colonization (95% CI, 0.9-5.7), but this was not significant nor a confounder in the multivariate analysis and was not included in the final model.
S aureus and MRSA colonization rates found in our study suggest Brazilian health care workers in pediatrics departments experience relatively high S aureus and MRSA colonization rates in comparison to health care workers from other countries and departments. In studies published during the past 5 years with a sample size of at least 100 health care workers (nonoutbreak situations), mean S aureus nasal colonization was 24% 8.9%.9-24 In these studies, the mean nasal MRSA colonization was 3.5% 2.5% for developed and 6.8% 4.7% for developing nations, excluding a study from Libya that found 36.8% MRSA colonization. Rates found here were higher than in other studies on health care worker nasal colonization conducted in Brazil (18.7% for S aureus25 and 1.5% and 3% for MRSA25,26). On the other hand, these rates are lower than what we observed in children attending public daycare centers in the same city, in which 48% and 6.2% were colonized with S aureus and MRSA, respectively (unpublished results). Our results suggest nurses with prolonged pediatric patient contact in inpatient units are at higher risk of MRSA colonization than other professionals in the same department. Three previous studies conducted in Ethiopia and the United States also found nurses to be at increased risk for MRSA colonization.13,19,21 In Ethiopia, 21.2% of nurses, compared with 12.7% for all health care workers, had nasal MRSA colonization.13 One study from Atlanta found 4 of 7 MRSA-colonized health care workers to be nurses, 2 of whom worked in pediatrics departments.21 The type of care these nurses provide to pediatric patients, such as holding and feeding, may result in increased exposure to the bacteria. The difference in risk factors for S aureus and MRSA colonization suggests MRSA may have different transmission patterns and could be related to the carriage of community-associated MRSA by children into the hospital setting. Interventions for control of antibiotic resistant bacteria in pediatrics departments should be targeted in this population of nurses. Acknowledgment The authors thank the staff of the Pediatrics Department, Antonio Pedro University Hospital of the Fluminense Federal University, for providing support. This study received financial support from Programa de Fomento à Pesquisa (FOPESQ-UFF Grant), Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ - APQ1 Grant) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq Grant). References 1. Brown AF, Leech JM, Rogers TR, McLoughlin RM. Colonization: modulation of host immune response and impact on human vaccine design. Front Immunol 2014;4:507. 2. Lowy FD. Staphylococcus aureus infections. N Engl J Med 1998;339:520-32. 3. Allegranzi B, Bagheri Nejad S, Combescure C, Graafmans W, Attar H, Donaldson L, et al. Burden of endemic health-care-associated infection in developing countries: systematic review and meta-analysis. Lancet 2011;377: 228-41. 4. Peacock SJ, de Silva I, Lowy FD. What determines nasal carriage of Staphylococcus aureus? Trends Microbiol 2001;9:605-10. 5. Cimolai N. The role of healthcare personnel in the maintenance and spread of methicillin-resistant Staphylococcus aureus. J Infect Public Health 2008;1:78-100.
920
I.M. Gomes et al. / American Journal of Infection Control 42 (2014) 918-20
6. Wang JT, Liao CH, Fang CT, Chie WC, Lai MS, Lauderdale TL, et al. Prevalence of and risk factors for colonization by methicillin-resistant Staphylococcus aureus among adults in community settings in Taiwan. J Clin Microbiol 2009;47:2957-63. 7. Performance standards for antimicrobial disk susceptibility tests; approved standard. 11th ed. Wayne, [PA]: Clinical and Laboratory Standards Institute; 2012. 8. Oliveira DC, de Lencastre H. Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2002;46:2155-61. 9. Akhtar N. Staphylococcal nasal carriage of health care workers. J Coll Physicians Surgeons Pakistan 2010;20:439-43. 10. D’Souza M, Kotigadde S, Saralaya KV, Kotian MS. Prevalence of methicillinresistant Staphylococcus aureus carriage amongst health care workers of critical care units in Kasturba Medical College Hospital, Mangalore, India. J Clin Diagn Res 2013;7:2697-700. 11. Ruiz A, Mora M, Zurita C, Larco D, Toapanta Y, Zurita J. Prevalence of methicillin-resistant Staphylococcus aureus among health care workers of intensive care units in Ecuador. J Infect Dev Ctries 2014;8:116-9. 12. Huang YC, Su LH, Lin TY. Nasal carriage of methicillin-resistant Staphylococcus aureus among pediatricians in Taiwan. PLoS One 2013;8:e82472. 13. Shibabaw A, Abebe T, Mihret A. Nasal carriage rate of methicillin resistant Staphylococcus aureus among Dessie Referral Hospital health care workers; Dessie, Northeast Ethiopia. Antimicrob Resist Infect Control 2013;2:25. 14. Jannati E, Arzanlou M, Habibzadeh S, Mohammadi S, Ahadi P, MohammadiGhalehbin B, et al. Nasal colonization of mecA-positive, oxacillin-susceptible, methicillin-resistant Staphylococcus aureus isolates among nursing staff in an Iranian teaching hospital. Am J Infect Control 2013;41:1122-4. 15. Rongpharpi SR, Hazarika NK, Kalita H. The prevalence of nasal carriage of Staphylococcus aureus among healthcare workers at a tertiary care hospital in Assam with special reference to MRSA. J Clin Diagn Res 2013;7:257-60. 16. Tsering DC, Pal R, Kar S. Methicillin-resistant Staphylococcus aureus: prevalence and current susceptibility pattern in Sikkim. J Glob Infect Dis 2011;3:9-13. 17. Askarian M, Zeinalzadeh A, Japoni A, Alborzi A, Memish ZA. Prevalence of nasal carriage of methicillin-resistant Staphylococcus aureus and its antibiotic
18.
19.
20.
21.
22.
23.
24.
25.
26.
susceptibility pattern in healthcare workers at Namazi Hospital, Shiraz, Iran. Int J Infect Dis 2009;13:e241-7. Zorgani A, Elahmer O, Franka E, Grera A, Abudher A, Ghenghesh KS. Detection of meticillin-resistant Staphylococcus aureus among healthcare workers in Libyan hospitals. J Hosp Infect 2009;73:91-2. Elie-Turenne MC, Fernandes H, Mediavilla JR, Rosenthal M, Mathema B, Singh A, et al. Prevalence and characteristics of Staphylococcus aureus colonization among healthcare professionals in an urban teaching hospital. Infect Control Hosp Epidemiol 2010;31:574-80. Rijnders MIA, Nys S, Driessen C, Hoebe C, Hopstaken RM, Oudhuis GJ, et al. Staphylococcus aureus carriage among GPs in the Netherlands. Br J Gen Pract 2010;60:902-6. Immergluck LC, Satola SW, Jain S, McCracken C, Watson JR, Chan T, et al. Methicillin-resistant Staphylococcus aureus colonization among pediatric health care workers from different outpatient settings. Am J Infect Control 2013;41:841-3. Kottler S, Middleton JR, Perry J, Weese JS, Cohn LA. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus carriage in three populations. J Vet Intern Med 2010;24:132-9. Verwer PE, Robinson JO, Coombs GW, Wijesuriya T, Murray RJ, Verbrugh HA, et al. Prevalence of nasal methicillin-resistant Staphylococcus aureus colonization in healthcare workers in a Western Australian acute care hospital. Eur J Clin Microbiol Infect Dis 2012;31:1067-72. Vinodhkumaradithyaa A, Uma A, Srinivasan M, Ananthalakshmi I, Nallasivam P, Thirumalaikolundusubramanian P. Nasal carriage of methicillinresistant Staphylococcus aureus among surgical unit staff. Jpn J Infect Dis 2009; 62:228-9. Silva EC, Antas M, Monteiro BNA, Rabelo MA, Melo FL, Maciel MA. Prevalence and risk factors for Staphylococcus aureus in health care workers at a university hospital of Recife-PE. Braz J Infect Dis 2008;12:504-8. Senna JP, Pinto CA, Bernardon DR, Francisco AG, Epztein E, Ritt CB, et al. Identification of methicillin-resistant Staphylococcus aureus among careworkers and patients in an emergency hospital. J Hosp Infect 2003;54: 167-8.
