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Nasal decolonization of Staphylococcus aureus in orthopedic surgeons using mupirocin and chlorhexidine
ARTICLE IN PRESS American Journal of Infection Control 000 (2019) 1−2
Contents lists available at ScienceDirect
American Journal of Infection Control journal homepage: www.ajicjournal.org
Brief Report
Nasal decolonization of Staphylococcus aureus in orthopedic surgeons using mupirocin and chlorhexidine lez PhD, Víctor Pen ~ a-Martínez MD, Ana Gabriela Castro-Martínez MD, Elvira Garza-Gonza n Camacho-Ortiz MD, PhD * Juan Sebastian Gonzalez-Bracamonte MD, Adria lez, Facultad de Medicina, Universidad Auto noma de Nuevo Leo n Hospital Universitario Dr. Jose Eleuterio Gonza
Key Words: Orthopedics
Nasal mucosa colonization by Staphylococcus aureus is a risk factor for hospital-acquired infections. This study examined the effectiveness of a decolonization strategy on orthopedic surgeons in a teaching hospital. S aureus colonization was detected in 43.2% of the surgeons, 25% of which were methicillin-resistant S aureus strains. Eradication was documented in 61.53% of the subjects who completed the decolonization strategy. Among orthopedic surgeons, mupirocin with or without chlorhexidine decolonization strategies was effective in eradicating S aureus colonization. © 2019 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Staphylococcus aureus, a pathogen affecting humans, is associated with infections ranging from mild to severe and life-threatening and is ranked as the second most common cause of hospital-acquired infections (HAIs).1 Nasal colonization is a risk factor for HAIs, and nasal colonization in health care workers (HWs) has been demonstrated to cause nosocomial outbreaks.2 Nasal colonization by S aureus in patients has been shown to be an independent risk factor for the development of surgical site infections, and evidence demonstrates that a nasal decolonization strategy in surgical patients is effective in reducing surgical site infections.3 Nearly all available evidence on colonization and decolonization strategies is focused on patients,3-5 and studies on colonization and decolonization strategies on surgical physicians are scarce.6 Enforcing compliance by HWs can be difficult, but mupirocin seems to be a feasible method for decolonization in this population. We evaluated the effectiveness of this decolonization strategy on surgical residents and attending physicians in a teaching hospital. METHODS Ethics approval The study was approved by the institutional research board on ethics (IF17-00004). Written inform consent was required. n Camacho-Ortiz, MD, Servicio de Infectología, *Address correspondence to Adria Eleuterio Gonzalez, Universidad Auto noma de Nuevo Hospital Universitario Dr. Jose n, Madero y Gonzalitos S/N, Colonia Mitras Centro, 64460 Monterrey, Nuevo Leo n, Leo xico. Me E-mail address: [email protected] (A. Camacho-Ortiz). Conflicts of interest: None to report.
Population and selection criteria Residents and attending physicians from the Traumatology and Orthopedics program were invited to participate voluntarily in the study. Those with known active S aureus infection, recurrent epistaxis, nasal anatomical malformations, or hypersensitivity to mupirocin were excluded. Study population and cultures Study subjects underwent an initial nasal swabbing and a subsequent one at week 4 to evaluate eradication, persistence, or newly defined colonization by S aureus. Nasopharyngeal swabs were cultured onto 5% blood agar, and colonies were identified using a Bruker Microflex LT matrix-assisted laser desorption/ionization time-offlight system (Bruker Diagnostics; Bremen German) and Biotyper v3.0 software. Resistance to methicillin was detected using the cefoxitin disc test following Clinical & Laboratory Standards Institute guidelines. Subjects that were positive for S aureus in the initial nasopharyngeal swabbing were assigned to the decolonization strategy. Decolonization strategy and statistical analysis The decolonization strategy began after the initial swab and consisted of a daily topical nasal ointment of 2% mupirocin for 5 days straight then once weekly for 4 weeks, in addition to a once-a-week whole-body bath with 2% chlorhexidine gluconate towels.5,7 A repeated nasal swab for culture was drawn 1 month after completion of the decolonization strategy. Descriptive analyses with frequencies
https://doi.org/10.1016/j.ajic.2019.11.003 0196-6553/© 2019 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
ARTICLE IN PRESS A.G. Castro-Martínez et al. / American Journal of Infection Control 00 (2019) 1−2
2
and percentages or central tendency and dispersion measures were used where appropriate, and x2 tests were used to compare proportions between groups. A P < .05 was considered statistically significant; SPSS Statistics 25.0 (IBM; Armonk, NY) was used for all analyses. RESULTS Of a total of 44 subjects, 84% (n = 37) were willing to participate. Of these, 59% (n = 22) were residents (4 first-year residents, 6 secondyear residents, 6 third-year residents, 5 fourth-year residents, 1 fifthyear resident), and 41% (n = 15) were attending physicians. S aureus colonization was detected in 16 out of 37 subjects (43.2%), and 4 of these samples were identified as methicillin-resistant S aureus (MRSA). Isolates detected in the first swabbing are shown in Table 1. Resident physicians were more likely to be colonized with S aureus than were attending physicians (81.3% vs 18.8%; P = .008). The year of residency was not different between those residents who were colonized and those who were not (P = .523). Subjects who had a negative culture at the beginning of the study were still negative at follow up. The bacterial load of Gram-negative rods in the subsequent cultures decreased; Acinetobacter johnsonii was isolated in only 1 subject. A total of 13 out of 16 subjects underwent decolonization. Eradication was documented in 61.53% (n = 8) of subjects who completed the decolonization strategy. Of those, 1 complied with the mupirocin and chlorhexidine regimen and 7 (85%) with the use of nasal mupirocin only. On long-term follow up, 3 subjects were lost due to completion of the residency program; 1 of these subjects had a negative culture, and methicillin-sensible strains were identified in the other 2 subjects. One of these subjects did not comply with the mupirocin and chlorhexidine regimen, and 1 complied with the use of mupirocin. No adverse events were reported during the study. DISCUSSION
CONCLUSION Among orthopedic surgeons with nasal colonization by S aureus, mupirocin with or without a chlorhexidine whole-body bath could be considered an effective strategy for decolonization. References
The majority of hospitals do not have S aureus detection or decolonization programs for their medical personnel. Given the importance of infections caused by this microorganism and its possible association with the colonization of medical personnel, we saw a need to study S aureus infections further. At the time of the study, there was no outbreak of infections related to S aureus. We achieved a S aureus eradication rate of 61.53%, in line with previous reports on patients.4 Adding chlorhexidine gluconate cleansing achieved a similar eradication rate when compared to mupirocin alone. Although chlorhexidine baths have been promoted as a standard of care,8 there is some debate regarding their effectiveness, as evidence is still of limited quality and there is no information Table 1 Bacterial isolates found in initial nasal swabbing Isolated agent
n
Staphylococcus epidermidis Staphylococcus aureus Corynebacterium pseudodiphtheriticum Acinetobacter johnsonii Moraxella sg Moraxella Neisseria subflava Staphylococcus lugdunensis Proteus mirabilis Other GNB Other GPB
24 16 4 3 3 3 2 2 6 11
GNB, Gram-negative bacilli; GPB, Gram-positive bacteria.
regarding the use of this strategy among physicians.8,9 Our results suggest that only nasal mupirocin alone is adequate for nasal eradication in health care personnel. We acknowledge possible resistance to mupirocin with indiscriminate use,9 but, although the risk exists, weekly use for a brief period is very unlikely to cause resistance. We found no MRSA strains during our follow-up of subjects who completed the decolonization strategy, which emphasizes the importance of decolonization strategies, as the eradication of nasal MRSA colonization can be highly efficacious and cost effective.10 The impact of these strategies on MRSA-associated infections, however, remains to be elucidated. Our follow-up loss rate was 8.1%, which can be explained by the nature of the personnel studied. Many of the subjects were residents, who, after completion of their program, returned to their home cities. Follow-up in health care personnel can be complicated by scheduling constraints or the fear of punitive measures. Only 16% of our population declined to participate in the study, and our evidence makes a strong case for institutional guidelines recommending generalized decolonization strategies. There are several limitations to our study, including the small sample size, which might limit generalization of our findings. Second, we have not yet measured the outcome that the strategies try to achieve—prevention of surgical site infections; however, our results are preliminary, and the impact on surgical site infections has yet to be determined.
1. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 2004;39:309-17. € den H, Behnke M, et al. 2. Vonberg RP, Stamm-Balderjahn S, Hansen S, Zuschneid I, Ru How often do asymptomatic healthcare workers cause methicillin-resistant Staphylococcus aureus outbreaks? A systematic evaluation. Infect Control Hosp Epidemiol 2006;27:1123-7. 3. Bode LGM, Kluytmans JAJW, Wertheim HF, Bogaers D, Vandenbroucke-Grauls CM, Roosendaal R, et al. Preventing surgical-site infections in nasal carriers of Staphylococcus aureus. N Engl J Med 2010;362:9-17. 4. Septimus EJ, Schweizer ML. Decolonization in prevention of health care-associated infections. Clin Microbiol Rev 2016;29:201-22. 5. George S, Leasure AR, Horstmanshof D. Effectiveness of decolonization with chlorhexidine and mupirocin in reducing surgical site infections: a systematic review. Dimens Crit Care Nurs 2016;35:204-22. 6. Fernandez C, Gaspar C, Torrellas A, Vindel A, Saez-Nieto JA, Cruzet F, et al. A double-blind, randomized, placebo-controlled clinical trial to evaluate the safety and efficacy of mupirocin calcium ointment for eliminating nasal carriage of Staphylococcus aureus among hospital personnel. J Antimicrob Chemother 1995;35:399408. 7. Roghmann MC, Lydecker AD, Langenberg P, Mongodin EF, Johnson JK. Microbiological effect of mupirocin and chlorhexidine for Staphylococcus aureus decolonization in community and nursing home based adults. Diagn Microbiol Infect Dis 2017;88:53-7. 8. Edmiston CE Jr, Leaper D. Should preoperative showering or cleansing with chlorhexidine gluconate (CHG) be part of the surgical care bundle to prevent surgical site infection? J Infect Prev 2017;18:311-4. 9. Poovelikunnel T, Gethin G, Humphreys H. Mupirocin resistance: clinical implications and potential alternatives for the eradication of MRSA. J Antimicrob Chemother 2015;70:2681-92. 10. Sai N, Laurent C, Strale H, Denis O, Byl B. Efficacy of the decolonization of methicillin-resistant Staphylococcus aureus carriers in clinical practice. Antimicrob Resist Infect Control 2015;4:56.
Contents lists available at ScienceDirect
American Journal of Infection Control journal homepage: www.ajicjournal.org
Brief Report
Nasal decolonization of Staphylococcus aureus in orthopedic surgeons using mupirocin and chlorhexidine lez PhD, Víctor Pen ~ a-Martínez MD, Ana Gabriela Castro-Martínez MD, Elvira Garza-Gonza n Camacho-Ortiz MD, PhD * Juan Sebastian Gonzalez-Bracamonte MD, Adria lez, Facultad de Medicina, Universidad Auto noma de Nuevo Leo n Hospital Universitario Dr. Jose Eleuterio Gonza
Key Words: Orthopedics
Nasal mucosa colonization by Staphylococcus aureus is a risk factor for hospital-acquired infections. This study examined the effectiveness of a decolonization strategy on orthopedic surgeons in a teaching hospital. S aureus colonization was detected in 43.2% of the surgeons, 25% of which were methicillin-resistant S aureus strains. Eradication was documented in 61.53% of the subjects who completed the decolonization strategy. Among orthopedic surgeons, mupirocin with or without chlorhexidine decolonization strategies was effective in eradicating S aureus colonization. © 2019 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Staphylococcus aureus, a pathogen affecting humans, is associated with infections ranging from mild to severe and life-threatening and is ranked as the second most common cause of hospital-acquired infections (HAIs).1 Nasal colonization is a risk factor for HAIs, and nasal colonization in health care workers (HWs) has been demonstrated to cause nosocomial outbreaks.2 Nasal colonization by S aureus in patients has been shown to be an independent risk factor for the development of surgical site infections, and evidence demonstrates that a nasal decolonization strategy in surgical patients is effective in reducing surgical site infections.3 Nearly all available evidence on colonization and decolonization strategies is focused on patients,3-5 and studies on colonization and decolonization strategies on surgical physicians are scarce.6 Enforcing compliance by HWs can be difficult, but mupirocin seems to be a feasible method for decolonization in this population. We evaluated the effectiveness of this decolonization strategy on surgical residents and attending physicians in a teaching hospital. METHODS Ethics approval The study was approved by the institutional research board on ethics (IF17-00004). Written inform consent was required. n Camacho-Ortiz, MD, Servicio de Infectología, *Address correspondence to Adria Eleuterio Gonzalez, Universidad Auto noma de Nuevo Hospital Universitario Dr. Jose n, Madero y Gonzalitos S/N, Colonia Mitras Centro, 64460 Monterrey, Nuevo Leo n, Leo xico. Me E-mail address: [email protected] (A. Camacho-Ortiz). Conflicts of interest: None to report.
Population and selection criteria Residents and attending physicians from the Traumatology and Orthopedics program were invited to participate voluntarily in the study. Those with known active S aureus infection, recurrent epistaxis, nasal anatomical malformations, or hypersensitivity to mupirocin were excluded. Study population and cultures Study subjects underwent an initial nasal swabbing and a subsequent one at week 4 to evaluate eradication, persistence, or newly defined colonization by S aureus. Nasopharyngeal swabs were cultured onto 5% blood agar, and colonies were identified using a Bruker Microflex LT matrix-assisted laser desorption/ionization time-offlight system (Bruker Diagnostics; Bremen German) and Biotyper v3.0 software. Resistance to methicillin was detected using the cefoxitin disc test following Clinical & Laboratory Standards Institute guidelines. Subjects that were positive for S aureus in the initial nasopharyngeal swabbing were assigned to the decolonization strategy. Decolonization strategy and statistical analysis The decolonization strategy began after the initial swab and consisted of a daily topical nasal ointment of 2% mupirocin for 5 days straight then once weekly for 4 weeks, in addition to a once-a-week whole-body bath with 2% chlorhexidine gluconate towels.5,7 A repeated nasal swab for culture was drawn 1 month after completion of the decolonization strategy. Descriptive analyses with frequencies
https://doi.org/10.1016/j.ajic.2019.11.003 0196-6553/© 2019 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
ARTICLE IN PRESS A.G. Castro-Martínez et al. / American Journal of Infection Control 00 (2019) 1−2
2
and percentages or central tendency and dispersion measures were used where appropriate, and x2 tests were used to compare proportions between groups. A P < .05 was considered statistically significant; SPSS Statistics 25.0 (IBM; Armonk, NY) was used for all analyses. RESULTS Of a total of 44 subjects, 84% (n = 37) were willing to participate. Of these, 59% (n = 22) were residents (4 first-year residents, 6 secondyear residents, 6 third-year residents, 5 fourth-year residents, 1 fifthyear resident), and 41% (n = 15) were attending physicians. S aureus colonization was detected in 16 out of 37 subjects (43.2%), and 4 of these samples were identified as methicillin-resistant S aureus (MRSA). Isolates detected in the first swabbing are shown in Table 1. Resident physicians were more likely to be colonized with S aureus than were attending physicians (81.3% vs 18.8%; P = .008). The year of residency was not different between those residents who were colonized and those who were not (P = .523). Subjects who had a negative culture at the beginning of the study were still negative at follow up. The bacterial load of Gram-negative rods in the subsequent cultures decreased; Acinetobacter johnsonii was isolated in only 1 subject. A total of 13 out of 16 subjects underwent decolonization. Eradication was documented in 61.53% (n = 8) of subjects who completed the decolonization strategy. Of those, 1 complied with the mupirocin and chlorhexidine regimen and 7 (85%) with the use of nasal mupirocin only. On long-term follow up, 3 subjects were lost due to completion of the residency program; 1 of these subjects had a negative culture, and methicillin-sensible strains were identified in the other 2 subjects. One of these subjects did not comply with the mupirocin and chlorhexidine regimen, and 1 complied with the use of mupirocin. No adverse events were reported during the study. DISCUSSION
CONCLUSION Among orthopedic surgeons with nasal colonization by S aureus, mupirocin with or without a chlorhexidine whole-body bath could be considered an effective strategy for decolonization. References
The majority of hospitals do not have S aureus detection or decolonization programs for their medical personnel. Given the importance of infections caused by this microorganism and its possible association with the colonization of medical personnel, we saw a need to study S aureus infections further. At the time of the study, there was no outbreak of infections related to S aureus. We achieved a S aureus eradication rate of 61.53%, in line with previous reports on patients.4 Adding chlorhexidine gluconate cleansing achieved a similar eradication rate when compared to mupirocin alone. Although chlorhexidine baths have been promoted as a standard of care,8 there is some debate regarding their effectiveness, as evidence is still of limited quality and there is no information Table 1 Bacterial isolates found in initial nasal swabbing Isolated agent
n
Staphylococcus epidermidis Staphylococcus aureus Corynebacterium pseudodiphtheriticum Acinetobacter johnsonii Moraxella sg Moraxella Neisseria subflava Staphylococcus lugdunensis Proteus mirabilis Other GNB Other GPB
24 16 4 3 3 3 2 2 6 11
GNB, Gram-negative bacilli; GPB, Gram-positive bacteria.
regarding the use of this strategy among physicians.8,9 Our results suggest that only nasal mupirocin alone is adequate for nasal eradication in health care personnel. We acknowledge possible resistance to mupirocin with indiscriminate use,9 but, although the risk exists, weekly use for a brief period is very unlikely to cause resistance. We found no MRSA strains during our follow-up of subjects who completed the decolonization strategy, which emphasizes the importance of decolonization strategies, as the eradication of nasal MRSA colonization can be highly efficacious and cost effective.10 The impact of these strategies on MRSA-associated infections, however, remains to be elucidated. Our follow-up loss rate was 8.1%, which can be explained by the nature of the personnel studied. Many of the subjects were residents, who, after completion of their program, returned to their home cities. Follow-up in health care personnel can be complicated by scheduling constraints or the fear of punitive measures. Only 16% of our population declined to participate in the study, and our evidence makes a strong case for institutional guidelines recommending generalized decolonization strategies. There are several limitations to our study, including the small sample size, which might limit generalization of our findings. Second, we have not yet measured the outcome that the strategies try to achieve—prevention of surgical site infections; however, our results are preliminary, and the impact on surgical site infections has yet to be determined.
1. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 2004;39:309-17. € den H, Behnke M, et al. 2. Vonberg RP, Stamm-Balderjahn S, Hansen S, Zuschneid I, Ru How often do asymptomatic healthcare workers cause methicillin-resistant Staphylococcus aureus outbreaks? A systematic evaluation. Infect Control Hosp Epidemiol 2006;27:1123-7. 3. Bode LGM, Kluytmans JAJW, Wertheim HF, Bogaers D, Vandenbroucke-Grauls CM, Roosendaal R, et al. Preventing surgical-site infections in nasal carriers of Staphylococcus aureus. N Engl J Med 2010;362:9-17. 4. Septimus EJ, Schweizer ML. Decolonization in prevention of health care-associated infections. Clin Microbiol Rev 2016;29:201-22. 5. George S, Leasure AR, Horstmanshof D. Effectiveness of decolonization with chlorhexidine and mupirocin in reducing surgical site infections: a systematic review. Dimens Crit Care Nurs 2016;35:204-22. 6. Fernandez C, Gaspar C, Torrellas A, Vindel A, Saez-Nieto JA, Cruzet F, et al. A double-blind, randomized, placebo-controlled clinical trial to evaluate the safety and efficacy of mupirocin calcium ointment for eliminating nasal carriage of Staphylococcus aureus among hospital personnel. J Antimicrob Chemother 1995;35:399408. 7. Roghmann MC, Lydecker AD, Langenberg P, Mongodin EF, Johnson JK. Microbiological effect of mupirocin and chlorhexidine for Staphylococcus aureus decolonization in community and nursing home based adults. Diagn Microbiol Infect Dis 2017;88:53-7. 8. Edmiston CE Jr, Leaper D. Should preoperative showering or cleansing with chlorhexidine gluconate (CHG) be part of the surgical care bundle to prevent surgical site infection? J Infect Prev 2017;18:311-4. 9. Poovelikunnel T, Gethin G, Humphreys H. Mupirocin resistance: clinical implications and potential alternatives for the eradication of MRSA. J Antimicrob Chemother 2015;70:2681-92. 10. Sai N, Laurent C, Strale H, Denis O, Byl B. Efficacy of the decolonization of methicillin-resistant Staphylococcus aureus carriers in clinical practice. Antimicrob Resist Infect Control 2015;4:56.