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Horizontal transmission of Streptococcus pneumoniae in the surgical ward: A rare source of nosocomial wound infection
American Journal of Infection Control 40 (2012) 71-2
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
Horizontal transmission of Streptococcus pneumoniae in the surgical ward: A rare source of nosocomial wound infection Marlène Guillet MD a, b, Jean-Ralph Zahar MD a, b, *, Marc-Olivier Timsit MD, PhD c, Laure Grandin MD d, Etienne Carbonnelle MD, PhD a, b, Olivier Join-Lambert MD, PhD a, b, Gilles Quesne BS a, Xavier Nassif MD, PhD a, b, Arnaud Mejean MD, PhD c, Anne Carbonne MD d a
Microbiology-Infection Control Unit, Necker Hospital, Assistance Public Hospital of Paris, Paris, France Faculty of Medicine, University of Paris Descartes, Paris, France Department of Urology, Necker Hospital, Assistance Public Hospital of Paris, Paris, France d CCLIN Coordinating Center for Nosocomial Infections Control, Paris, France b c
Key Words: Mask Surgical site infection Prostatic surgery Droplets transmission
Streptococcus pneumoniae is rarely isolated from nosocomial infections. We report an outbreak of 4 nosocomial-acquired surgical site infections due to S pneumoniae after retropubic simple prostatectomy. The likely source was detected in the rhinopharynx of the surgeon. After the implementation of recommendations, no new cases have been recorded. Copyright Ó 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Streptococcus pneumoniae is a major and well-known cause of community-acquired infections. It is the agent most frequently associated with sinusitis, pneumonia, and bacterial meningitis. S pneumoniae is part of the commensal flora of the upper respiratory tract, and carriage is an important source of horizontal spread of this pathogen within the community.1 The isolation of S pneumoniae from skin and soft tissues is an unusual finding, with a difficult clinical interpretation that can range from simple colonization to severe infection.2 To the best of our knowledge, published cases of cutaneous infection have not addressed the mode of S pneumoniae transmission in a surgical ward. Here we report an outbreak of pneumococcal surgical site infection and demonstrate the mode of contamination. The infection control unit was alerted of a nosocomial S pneumoniae bacteremia growing in the surgical ward. Investigation revealed that the affected patient had undergone retropubic simple prostatectomy for benign prostatic hyperplasia 1 day earlier. Physical examination revealed a surgical site abscess, with no other source of infection. A microbiological sampling of the surgical wound grew a pure culture of S pneumoniae with the same antibiotic susceptibility pattern. We concluded that bacteremia was secondary to surgical site infection. The patient underwent a 7-day * Address correspondence to Jean-Ralph Zahar, MD, Microbiology Infection Unit Control, Necker Hospital, Paris Descartes University, 149 rue de sèvres, 75015, Paris, France. E-mail address: [email protected] (J.-R. Zahar). Conflict of interest: None to report.
course of amoxicillin treatment and was discharged from the hospital. Six weeks later, another microbiological sample isolated from the same surgical ward grew S pneumoniae. Similarly, investigation revealed that the affected patient had undergone recent prostatic adenomectomy, and no other portal of entry was diagnosed. The 2 patients shared the same surgeon; however, the surgeon did not have a respiratory tract infection, and neither did any nurses and residents on the surgical ward. Because the 2 nosocomial infections were epidemiologically related and the strains isolated shared the same antibiotic susceptibility pattern and belonged to serogroup 3, we conducted a retrospective study of our database examining a 12-month period for positive microbiological samples to S pneumoniae in the same surgical ward. We identified 2 other cases of infection (1 blood culture and 1 local microbiological sample) due to serogroup 3 S pneumoniae with identical antibiotic susceptibility patterns. Like the first 2 cases, these 2 patients also had been hospitalized for prostatic surgery and shared the same surgeon. All infections occurred within the first 2 days after surgery. None of the patients had any signs of upper or lower respiratory tract infection. We hypothesized that the surgeon wore his mask inappropriately during surgery. A rhinopharyngeal sample was obtained from the surgeon, and a practice assessment was conducted in the operating theatre to determine the source of infection. The practice assessment revealed that the surgeon’s face mask was not tightly attached to his face and did not correctly cover his nose and mouth. A similar S pneumoniae isolate was cultured from
0196-6553/$36.00 - Copyright Ó 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. doi:10.1016/j.ajic.2011.02.012
72
M. Guillet et al. / American Journal of Infection Control 40 (2012) 71-2
Fig 1. PFGE patterns for 5 isolates of S pneumoniae from 3 surgical site infection isolates (1-3), 1 nasopharyngeal isolate (4), and 1 control (B).
a rhinopharyngeal sample obtained from the surgeon. Molecular typing of the strains from 3 patients and the surgeon was performed by pulsed-field gel electrophoresis (PFGE) using smaI as the restriction enzyme. All strains had the same PFGE profile (100% similarity), supporting the hypothesis of droplet infection transmitted during surgery (Fig 1). Even though it is a common pathogen, S pneumoniae is a rarely responsible for soft tissue infection. Of the overall number isolates of S pneumoniae recovered in general institutions, only 2.2% involve skin and soft tissues. In a 12-year study conducted in Spain, GarciaLechuz et al2 identified 36 cases of skin and soft tissue S pneumoniae infection. Surgical site infections were the most frequent (11 cases); others included burn infection, cellulitis, pyomyositis, and perineal abcess. Unlike in the present study, in that study most of the surgical site infections involved multiple pathogens and occurred in patients with underlying morbid conditions, such as diabetes mellitus, HIV infection, or cancer.2 Nosocomial outbreaks of pneumococcal infections are rare. Those reported in the literature occurred in geriatric and adult oncology wards3 and presumably resulted from patient-to-patient transmission. In intensive care units, S pneumoniae is responsible
for 5%-20% of early-onset ventilator-acquired pneumonia, occurring within the first 4 days of hospitalization. Patients’ own flora is the usual source of respiratory tract contamination. Some authors have reported central catheter colonization and catheterrelated bacteremia due to S pneumoniae.4 Although surgical site infection secondary to S pneumoniae has been reported previously,5 the precise sources of contamination have rarely been identified. To the best of our knowledge, this article is the first to link a surgical site infection outbreak to a specific surgeon as the identified source for S pneumoniae carriage. Indeed, S oralis or S pyogenes surgical site infections are well known, as are meningitis postelumbar puncture, soft tissue infections, and postpartum endometritis.6 In our case there is much evidence to support the direct horizontal transmission of S pneumoniae originating from the surgeon’s oropharyngeal secretions. The use of surgical masks to prevent contamination during surgical procedures was first mentioned by Mikuliez in 1897,7 and the efficacy of this technique has been demonstrated, but the literature in this area is controversial.8 Indeed, a case-control study designed to assess the incidence of infectious events according to the use of a surgical mask would not be ethically acceptable. Earlier studies investigated mechanisms by which S pneumoniae is transmitted within a family. The presence of a child in daycare has been identified as a significant risk factor of invasive pneumococcal disease in adults. Such interfamily transmission of pneumococcal serotypes is well described and has been investigated using molecular analysis tools able to discriminate among pneumococcal strains belonging to a single serotype.9 In the present case, it is critical to note that the surgeon did not respect current standards of practice and did not comply with his institution’s hygiene guidelines. Because his mask did not cover his face appropriately, droplets likely contaminated the surgical site whenever he spoke or coughed. Our identification of the bacterial strain demonstrates that horizontal transmission of S pneumoniae may cause surgical wound infection, and highlights the crucial importance of adherence to basic hygiene measures. Despite this case, however, we should emphasize that violations of such rudimentary principles of patient safety are uncommon, and those that occur may be related to an obsolete surgical practice. As stated by René Küss in his speech accepting the 2002 Medawar Prize: “Surgeons of my generation in France had two peculiarities: they did not take courses of foreign languages, and they used to operate ‘nude nose’ (nose outside of the mask)!”10 References 1. Bogaert D, De Groot R, Hermans PW. Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect Dis 2004;4:144-54. 2. Garcia-Lechuz JM, Cuevas O, Castellares C, Perez-Fernandez C, Cercenado E, Bouza E. Streptococcus pneumoniae skin and soft tissue infections: characterization of causative strains and clinical illness. Eur J Clin Microbiol Infect Dis 2007;26:247-53. 3. Denton M, Hawkey PM, Hoy CM, Porter C. Co-existent cross-infection with Streptococcus pneumoniae and group B streptococci on an adult oncology unit. J Hosp Infect 1993;23:271-8. 4. Dhillon SS, Watanakunakorn C. Pneumococcal bacteremia associated with an infected central venous catheter. Chest 2000;117:1515-6. 5. Cuenca-Estrella M, Ramos JM, Esteban J, Soriano F. Pneumococcal soft-tissue infections. Clin Infect Dis 1995;21:697-8. 6. Daneman N, Green KA, Low DE, Simor AE, Willey B, Schwartz B, et al. Surveillance for hospital outbreaks of invasive group a streptococcal infections in Ontario, Canada, 1992 to 2000. Ann Intern Med 2007;147:234-41. 7. Romney MG. Surgical face masks in the operating theatre: re-examining the evidence. J Hosp Infect 2001;47:251-6. 8. Tunevall TG. Postoperative wound infections and surgical face masks: a controlled study. World J Surg 1991;15:383-7. 9. Regev-Yochay G, Raz M, Dagan R, Porat N, Shainberg B, Pinco E, et al. Nasopharyngeal carriage of Streptococcus pneumoniae by adults and children in community and family settings. Clin Infect Dis 2004;38:632-9. 10. Morris PJ. René Kuss (1913e2006). Transplantation 2006;82:1410 [letter].
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
Horizontal transmission of Streptococcus pneumoniae in the surgical ward: A rare source of nosocomial wound infection Marlène Guillet MD a, b, Jean-Ralph Zahar MD a, b, *, Marc-Olivier Timsit MD, PhD c, Laure Grandin MD d, Etienne Carbonnelle MD, PhD a, b, Olivier Join-Lambert MD, PhD a, b, Gilles Quesne BS a, Xavier Nassif MD, PhD a, b, Arnaud Mejean MD, PhD c, Anne Carbonne MD d a
Microbiology-Infection Control Unit, Necker Hospital, Assistance Public Hospital of Paris, Paris, France Faculty of Medicine, University of Paris Descartes, Paris, France Department of Urology, Necker Hospital, Assistance Public Hospital of Paris, Paris, France d CCLIN Coordinating Center for Nosocomial Infections Control, Paris, France b c
Key Words: Mask Surgical site infection Prostatic surgery Droplets transmission
Streptococcus pneumoniae is rarely isolated from nosocomial infections. We report an outbreak of 4 nosocomial-acquired surgical site infections due to S pneumoniae after retropubic simple prostatectomy. The likely source was detected in the rhinopharynx of the surgeon. After the implementation of recommendations, no new cases have been recorded. Copyright Ó 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Streptococcus pneumoniae is a major and well-known cause of community-acquired infections. It is the agent most frequently associated with sinusitis, pneumonia, and bacterial meningitis. S pneumoniae is part of the commensal flora of the upper respiratory tract, and carriage is an important source of horizontal spread of this pathogen within the community.1 The isolation of S pneumoniae from skin and soft tissues is an unusual finding, with a difficult clinical interpretation that can range from simple colonization to severe infection.2 To the best of our knowledge, published cases of cutaneous infection have not addressed the mode of S pneumoniae transmission in a surgical ward. Here we report an outbreak of pneumococcal surgical site infection and demonstrate the mode of contamination. The infection control unit was alerted of a nosocomial S pneumoniae bacteremia growing in the surgical ward. Investigation revealed that the affected patient had undergone retropubic simple prostatectomy for benign prostatic hyperplasia 1 day earlier. Physical examination revealed a surgical site abscess, with no other source of infection. A microbiological sampling of the surgical wound grew a pure culture of S pneumoniae with the same antibiotic susceptibility pattern. We concluded that bacteremia was secondary to surgical site infection. The patient underwent a 7-day * Address correspondence to Jean-Ralph Zahar, MD, Microbiology Infection Unit Control, Necker Hospital, Paris Descartes University, 149 rue de sèvres, 75015, Paris, France. E-mail address: [email protected] (J.-R. Zahar). Conflict of interest: None to report.
course of amoxicillin treatment and was discharged from the hospital. Six weeks later, another microbiological sample isolated from the same surgical ward grew S pneumoniae. Similarly, investigation revealed that the affected patient had undergone recent prostatic adenomectomy, and no other portal of entry was diagnosed. The 2 patients shared the same surgeon; however, the surgeon did not have a respiratory tract infection, and neither did any nurses and residents on the surgical ward. Because the 2 nosocomial infections were epidemiologically related and the strains isolated shared the same antibiotic susceptibility pattern and belonged to serogroup 3, we conducted a retrospective study of our database examining a 12-month period for positive microbiological samples to S pneumoniae in the same surgical ward. We identified 2 other cases of infection (1 blood culture and 1 local microbiological sample) due to serogroup 3 S pneumoniae with identical antibiotic susceptibility patterns. Like the first 2 cases, these 2 patients also had been hospitalized for prostatic surgery and shared the same surgeon. All infections occurred within the first 2 days after surgery. None of the patients had any signs of upper or lower respiratory tract infection. We hypothesized that the surgeon wore his mask inappropriately during surgery. A rhinopharyngeal sample was obtained from the surgeon, and a practice assessment was conducted in the operating theatre to determine the source of infection. The practice assessment revealed that the surgeon’s face mask was not tightly attached to his face and did not correctly cover his nose and mouth. A similar S pneumoniae isolate was cultured from
0196-6553/$36.00 - Copyright Ó 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. doi:10.1016/j.ajic.2011.02.012
72
M. Guillet et al. / American Journal of Infection Control 40 (2012) 71-2
Fig 1. PFGE patterns for 5 isolates of S pneumoniae from 3 surgical site infection isolates (1-3), 1 nasopharyngeal isolate (4), and 1 control (B).
a rhinopharyngeal sample obtained from the surgeon. Molecular typing of the strains from 3 patients and the surgeon was performed by pulsed-field gel electrophoresis (PFGE) using smaI as the restriction enzyme. All strains had the same PFGE profile (100% similarity), supporting the hypothesis of droplet infection transmitted during surgery (Fig 1). Even though it is a common pathogen, S pneumoniae is a rarely responsible for soft tissue infection. Of the overall number isolates of S pneumoniae recovered in general institutions, only 2.2% involve skin and soft tissues. In a 12-year study conducted in Spain, GarciaLechuz et al2 identified 36 cases of skin and soft tissue S pneumoniae infection. Surgical site infections were the most frequent (11 cases); others included burn infection, cellulitis, pyomyositis, and perineal abcess. Unlike in the present study, in that study most of the surgical site infections involved multiple pathogens and occurred in patients with underlying morbid conditions, such as diabetes mellitus, HIV infection, or cancer.2 Nosocomial outbreaks of pneumococcal infections are rare. Those reported in the literature occurred in geriatric and adult oncology wards3 and presumably resulted from patient-to-patient transmission. In intensive care units, S pneumoniae is responsible
for 5%-20% of early-onset ventilator-acquired pneumonia, occurring within the first 4 days of hospitalization. Patients’ own flora is the usual source of respiratory tract contamination. Some authors have reported central catheter colonization and catheterrelated bacteremia due to S pneumoniae.4 Although surgical site infection secondary to S pneumoniae has been reported previously,5 the precise sources of contamination have rarely been identified. To the best of our knowledge, this article is the first to link a surgical site infection outbreak to a specific surgeon as the identified source for S pneumoniae carriage. Indeed, S oralis or S pyogenes surgical site infections are well known, as are meningitis postelumbar puncture, soft tissue infections, and postpartum endometritis.6 In our case there is much evidence to support the direct horizontal transmission of S pneumoniae originating from the surgeon’s oropharyngeal secretions. The use of surgical masks to prevent contamination during surgical procedures was first mentioned by Mikuliez in 1897,7 and the efficacy of this technique has been demonstrated, but the literature in this area is controversial.8 Indeed, a case-control study designed to assess the incidence of infectious events according to the use of a surgical mask would not be ethically acceptable. Earlier studies investigated mechanisms by which S pneumoniae is transmitted within a family. The presence of a child in daycare has been identified as a significant risk factor of invasive pneumococcal disease in adults. Such interfamily transmission of pneumococcal serotypes is well described and has been investigated using molecular analysis tools able to discriminate among pneumococcal strains belonging to a single serotype.9 In the present case, it is critical to note that the surgeon did not respect current standards of practice and did not comply with his institution’s hygiene guidelines. Because his mask did not cover his face appropriately, droplets likely contaminated the surgical site whenever he spoke or coughed. Our identification of the bacterial strain demonstrates that horizontal transmission of S pneumoniae may cause surgical wound infection, and highlights the crucial importance of adherence to basic hygiene measures. Despite this case, however, we should emphasize that violations of such rudimentary principles of patient safety are uncommon, and those that occur may be related to an obsolete surgical practice. As stated by René Küss in his speech accepting the 2002 Medawar Prize: “Surgeons of my generation in France had two peculiarities: they did not take courses of foreign languages, and they used to operate ‘nude nose’ (nose outside of the mask)!”10 References 1. Bogaert D, De Groot R, Hermans PW. Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect Dis 2004;4:144-54. 2. Garcia-Lechuz JM, Cuevas O, Castellares C, Perez-Fernandez C, Cercenado E, Bouza E. Streptococcus pneumoniae skin and soft tissue infections: characterization of causative strains and clinical illness. Eur J Clin Microbiol Infect Dis 2007;26:247-53. 3. Denton M, Hawkey PM, Hoy CM, Porter C. Co-existent cross-infection with Streptococcus pneumoniae and group B streptococci on an adult oncology unit. J Hosp Infect 1993;23:271-8. 4. Dhillon SS, Watanakunakorn C. Pneumococcal bacteremia associated with an infected central venous catheter. Chest 2000;117:1515-6. 5. Cuenca-Estrella M, Ramos JM, Esteban J, Soriano F. Pneumococcal soft-tissue infections. Clin Infect Dis 1995;21:697-8. 6. Daneman N, Green KA, Low DE, Simor AE, Willey B, Schwartz B, et al. Surveillance for hospital outbreaks of invasive group a streptococcal infections in Ontario, Canada, 1992 to 2000. Ann Intern Med 2007;147:234-41. 7. Romney MG. Surgical face masks in the operating theatre: re-examining the evidence. J Hosp Infect 2001;47:251-6. 8. Tunevall TG. Postoperative wound infections and surgical face masks: a controlled study. World J Surg 1991;15:383-7. 9. Regev-Yochay G, Raz M, Dagan R, Porat N, Shainberg B, Pinco E, et al. Nasopharyngeal carriage of Streptococcus pneumoniae by adults and children in community and family settings. Clin Infect Dis 2004;38:632-9. 10. Morris PJ. René Kuss (1913e2006). Transplantation 2006;82:1410 [letter].