American Journal of Infection Control xxx (2014) 1-2
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
Outbreak of carbapenemase-producing Klebsiella pneumoniae neurosurgical site infections associated with a contaminated shaving razor used for preoperative scalp shaving Yuanyuan Dai MD a, Chengfang Zhang MD a, Xiaoling Ma MD a, *, Wenjiao Chang MD a, Shoukui Hu MD b, Hengmin Jia MD a, Jiaxiang Huang MD a, Huaiwei Lu MD a, Hua Li MD a, Shusheng Zhou MD a, Guangkuo Qiu MD a, Jiaqin Liu MD a a b
Affiliated Provincial Hospital of Anhui Medical University, Hefei, Anhui Province, China Anhui Provincial Center for Disease Control and Prevention, Hefei, Anhui Province, China
Key Words: Outbreak investigation Nosocomial transmission Surgical site infections
Between July 5 and 21, 2011, an outbreak of neurosurgical site infections with carbapenemase-producing Klebsiella pneumonia occurred in a tertiary care hospital. The outbreak affected 7 patients. The subsequent investigation revealed that a barber’s contaminated shaving razor may have caused the carbapenemase-producing Klebsiella pneumonia outbreak. Standardized skin preparation performed by registered nurses using sterilized instruments should be emphasized. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Surgical site infection (SSI), recognized as a serious complication of surgery, is associated with significant morbidity, mortality, and health care costs.1 Numerous patient- and procedure-related factors influence the risk of SSI. Procedure-related factors include inadequate sterilization of surgical instruments, quality of preoperative skin preparation, poor surgical technique, and duration of the operation.2,3 We report an outbreak of neurosurgical SSIs with carbapenemase-producing Klebsiella pneumonia (CPKP) in a tertiary care hospital. The subsequent investigation revealed that the contaminated razor reused for preoperative scalp shaving before neurosurgical procedures may have caused in this outbreak. METHODS The outbreak occurred in a 1000-bed tertiary care hospital in Hefei, Anhui Province, China. Between July 5 and 21, 2011, the Infectious Diseases Division was notified of 7 neurosurgical patients with persistent postoperative fever (temperature 39.6 C) and surgical wound purulent drainage on postoperative days 4-7. Wound effusion and cerebrospinal fluid cultures yielded CPKP. The infection control surveillance system was alerted of an unusually * Address correspondence to Xiaoling Ma, MD, Affiliated Provincial Hospital of Anhui Medical University China, Lujiang Rd 17, Hefei, Anhui Province 230001, China. E-mail address: [email protected] (X. Ma). Conflict of interest: None to report.
high incidence of CPKP, which prompted an epidemiologic investigation. Outbreak cases were defined when the surgical site samples of patients yielded CPKP. The c2 test was used for statistical analysis using SPSS version 11.0 (SPSS, Chicago, IL). An infection control team undertook active surveillance to detect the source of these infections. A total of 118 environmental samples were collected from the air, water sources, antiseptics, bedding surfaces, furniture in the neurosurgical wards, and operating rooms. Another 94 samples were collected from the shared equipment used for preoperative examination, skin preparation, anesthesia induction, and surgery. Finally, 190 samples were collected from the nose, throat, and hands of patients and medical, nursing, and ancillary staff (eg, cleaners, porters, the barber, kitchen staff) who were involved with these patients. All samples were cultured on blood plates. Identification and antibiotic susceptibility testing was performed using a Microscan WalkAway40 auto system (Siemens, West Sacramento, CA). All K pneumoniae isolates from clinical specimens and screening samples were detected for blakpc gene, as described previously.4 Pulsed-field gel electrophoresis (PFGE) and multilocus sequence typing were performed as the described by Mataseje et al.5
RESULTS Between January and June 2011, the neurosurgery medical staff admitted 1752 inpatients and performed a total of 1029
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.2014.03.023
2
Y. Dai et al. / American Journal of Infection Control xxx (2014) 1-2
Table 1 Characteristics of K pneumoniaeeinfected patients during the SSI outbreak in the neurosurgical ward Age, y/sex
Operation date
Isolate date
Invasive procedure
1
32/female
7/5/2011
7/11/2011
2 3 4 5 6 7
43/male 8/male 9/male 68/male 20/male 2/male
7/7/2011 7/8/2011 7/11/2011 7/11/2011 7/11/2011 7/13/2011
7/17/2011 7/17/2011 7/20/2011 7/20/2011 7/21/2011 7/21/2011
Craniotomy/ ventriculostomy Trauma/craniotomy Craniotomy Craniotomy Craniotomy Ventriculostomy Craniotomy/ ventriculostomy
Patient
Molecular typing of isolates
Sample source
Treatment received
Wound effusion
Amikacin and colistin IV
CSF Wound effusion Wound effusion CSF Wound effusion CSF
Amikacin Amikacin Amikacin Amikacin Amikacin Amikacin
and and and and and and
colistin colistin colistin colistin colistin colistin
IV þ amikacin IT IV IV IV þ amikacin IT IV IV
PFGE
ST
KPC
A
11
2
A A A A A A
11 11 11 11 11 11
2 2 2 2 2 2
CSF, cerebrospinal fluid; IT, intrathecal; IV, intravenous; KPC, Klebsiella pneumoniae carbapenemase; ST, sequence type.
neurosurgical operations. Among these patients, 32 (1.83%) developed nosocomial infections but no SSIs. Between July 5 and 21, 2011, the neurosurgery medical staff admitted 146 inpatients and performed 98 neurosurgical operations. Seven of these patients developed an SSI with CPKP. The CPKP infection rate was 4.79%, and the SSI rate was 7.14%. The CPKP infection rate increased significantly from the preoutbreak period to the outbreak period (P < .05). These patients were located in different wards, and their operations were performed by different surgeons. Patient characteristics and epidemiologic patterns of CPKP are summarized in Table 1. Among the 402 surveillance samples, CPKP was detected only on a razor that had been used to shave multiple patients’ hair before surgery. The isolates from infected patients and the razor shared the same resistance pattern, with susceptibility only to amikacin and resistance to all other antibiotic classes. Molecular biological analysis identified the isolates as belonging to the same PFGE-defined strain, blakpc-2 and sequence type 11 (ST11). As soon as the outbreak was suspected in the neurosurgical wards, the infected patients were isolated in single-bed side rooms with cohort nursing. Strict contact precautions and deep cleaning were maintained in the operating room, patient room, and nurses’ station, with particular attention given to equipment and surfaces. The latter were cleaned with chlorine-based or 75% alcohol disinfectant. Preoperative skin preparation procedures were revised. A trained registered nurse shaved scalps using disposable razors. The institution’s infection preventionist performed daily rounds to enforce standardized skin preparation procedures. After institution of infection control measures, no further patients were infected with CPKP. All 7 infected patients underwent external ventricular drainage and were treated with intravenous amikacin and colistin. Two patients also received intrathecal injections of amikacin. After receiving surgical and medical treatment, none of the patients relapsed with persistent or recurrent CPKP. DISCUSSION CPKP isolates are often resistant to multiple antimicrobial classes, including all available b-lactams, fluoroquinolones, and aminoglycosides. Some CPKP strains have reduced susceptibility to chlorhexidine.6 It is possible that extremely drug-resistant K pneumoniae contributes to its ability to persist in the hospital environment and has become a major pathogen for nosocomial pathogens. In China, traditionally scalp shaving was performed by a barber with no infection control training. They generally reuse a same razor without any disinfection. In this report, these isolates from infected patients and the shaving razor shared the same molecular typing pattern, all belonging to the same PFGE-defined strain, blakpc-2 and
ST11. After removal of the contaminated razor and implementation of appropriate infection control measures, no further cases occurred. Thus, the contaminated shaving razor was identified as the likely source of the outbreak. This report has important implications for front-line clinicians, managers, and infection control preventionists. Inadequate skin preparation may cause severe SSIs. Standardizing the skin preparation procedure is important. It is imperative that all perioperative activities be performed by infection controletrained nurses using sterilized instruments. K pneumoniae normally colonizes in the human nasal cavity, intestinal tract, and the hands of hospital staff members, and thus can spread through person-to-person contact.7,8 A limitation of this study is that rectal screening swabs were not obtained, and so it is unclear whether these patients were already colonized with CPKP or perhaps transmission itself was directly associated with a single patient with CPKP.
Acknowledgment We thank the infection control teams for their assistance in investigating the outbreak. We also thank the staff of the Anhui Provincial Center for Disease Control and Prevention for their work in typing the isolates, without whom this study would not have been possible.
References 1. Plowman R, Graves N, Griffin M, Roberts JA, Swan A. The socioeconomic burden of hospital-acquired infection. London, UK: Public Health Laboratory Service; 1999. 2. Owens CD, Stoessel K. Surgical site infections: epidemiology, microbiology and prevention. J Hosp Infect 2008;70:3-10. 3. Shahane V, Bhawal S, Lele U. Surgical site infections: a one-year prospective study in a tertiary care center. Int J Health Sci (Qassim) 2012;6:79-84. 4. Woodford N, Zhang J, Warner M, Kaufmann ME, Matos J, Macdonald A, et al. Arrival of Klebsiella pneumoniaeeproducing KPC carbapenemase in the United Kingdom. J Antimicrob Chemother 2008;62:1261-4. 5. Mataseje LF, Boyd DA, Willey BM, Prayitno N, Kreiswirth N, Gelosia A, et al. Plasmid comparison and molecular analysis of Klebsiella pneumoniae habouring bla(KPC) from New York City and Toronto. J Antimicrob Chemother 2011;66: 1273-7. 6. Naparstek L, Carmeli Y, Chmelnitsky I, Banin E, Navon-Venezia S. Reduced susceptibility to chlorhexidine among extremely-drug-resistant strains of Klebsiella pneumoniae. J Hosp Infect 2012;81:15-9. 7. Coudeyras S, Nakusi L, Charbonnel N, Forestier C. A tripartite efflux pump involved in gastrointestinal colonization by Klebsiella pneumoniae confers a tolerance response to inorganic acid. Infect Immun 2008;76:4633-41. 8. Seid J, Asrat D. Occurrence of extended spectrum beta-lactamase enzymes in clinical isolates of Klebsiella species from Harar region, eastern Ethiopia. Acta Trop 2005;95:143-8.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
Outbreak of carbapenemase-producing Klebsiella pneumoniae neurosurgical site infections associated with a contaminated shaving razor used for preoperative scalp shaving Yuanyuan Dai MD a, Chengfang Zhang MD a, Xiaoling Ma MD a, *, Wenjiao Chang MD a, Shoukui Hu MD b, Hengmin Jia MD a, Jiaxiang Huang MD a, Huaiwei Lu MD a, Hua Li MD a, Shusheng Zhou MD a, Guangkuo Qiu MD a, Jiaqin Liu MD a a b
Affiliated Provincial Hospital of Anhui Medical University, Hefei, Anhui Province, China Anhui Provincial Center for Disease Control and Prevention, Hefei, Anhui Province, China
Key Words: Outbreak investigation Nosocomial transmission Surgical site infections
Between July 5 and 21, 2011, an outbreak of neurosurgical site infections with carbapenemase-producing Klebsiella pneumonia occurred in a tertiary care hospital. The outbreak affected 7 patients. The subsequent investigation revealed that a barber’s contaminated shaving razor may have caused the carbapenemase-producing Klebsiella pneumonia outbreak. Standardized skin preparation performed by registered nurses using sterilized instruments should be emphasized. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Surgical site infection (SSI), recognized as a serious complication of surgery, is associated with significant morbidity, mortality, and health care costs.1 Numerous patient- and procedure-related factors influence the risk of SSI. Procedure-related factors include inadequate sterilization of surgical instruments, quality of preoperative skin preparation, poor surgical technique, and duration of the operation.2,3 We report an outbreak of neurosurgical SSIs with carbapenemase-producing Klebsiella pneumonia (CPKP) in a tertiary care hospital. The subsequent investigation revealed that the contaminated razor reused for preoperative scalp shaving before neurosurgical procedures may have caused in this outbreak. METHODS The outbreak occurred in a 1000-bed tertiary care hospital in Hefei, Anhui Province, China. Between July 5 and 21, 2011, the Infectious Diseases Division was notified of 7 neurosurgical patients with persistent postoperative fever (temperature 39.6 C) and surgical wound purulent drainage on postoperative days 4-7. Wound effusion and cerebrospinal fluid cultures yielded CPKP. The infection control surveillance system was alerted of an unusually * Address correspondence to Xiaoling Ma, MD, Affiliated Provincial Hospital of Anhui Medical University China, Lujiang Rd 17, Hefei, Anhui Province 230001, China. E-mail address: [email protected] (X. Ma). Conflict of interest: None to report.
high incidence of CPKP, which prompted an epidemiologic investigation. Outbreak cases were defined when the surgical site samples of patients yielded CPKP. The c2 test was used for statistical analysis using SPSS version 11.0 (SPSS, Chicago, IL). An infection control team undertook active surveillance to detect the source of these infections. A total of 118 environmental samples were collected from the air, water sources, antiseptics, bedding surfaces, furniture in the neurosurgical wards, and operating rooms. Another 94 samples were collected from the shared equipment used for preoperative examination, skin preparation, anesthesia induction, and surgery. Finally, 190 samples were collected from the nose, throat, and hands of patients and medical, nursing, and ancillary staff (eg, cleaners, porters, the barber, kitchen staff) who were involved with these patients. All samples were cultured on blood plates. Identification and antibiotic susceptibility testing was performed using a Microscan WalkAway40 auto system (Siemens, West Sacramento, CA). All K pneumoniae isolates from clinical specimens and screening samples were detected for blakpc gene, as described previously.4 Pulsed-field gel electrophoresis (PFGE) and multilocus sequence typing were performed as the described by Mataseje et al.5
RESULTS Between January and June 2011, the neurosurgery medical staff admitted 1752 inpatients and performed a total of 1029
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.2014.03.023
2
Y. Dai et al. / American Journal of Infection Control xxx (2014) 1-2
Table 1 Characteristics of K pneumoniaeeinfected patients during the SSI outbreak in the neurosurgical ward Age, y/sex
Operation date
Isolate date
Invasive procedure
1
32/female
7/5/2011
7/11/2011
2 3 4 5 6 7
43/male 8/male 9/male 68/male 20/male 2/male
7/7/2011 7/8/2011 7/11/2011 7/11/2011 7/11/2011 7/13/2011
7/17/2011 7/17/2011 7/20/2011 7/20/2011 7/21/2011 7/21/2011
Craniotomy/ ventriculostomy Trauma/craniotomy Craniotomy Craniotomy Craniotomy Ventriculostomy Craniotomy/ ventriculostomy
Patient
Molecular typing of isolates
Sample source
Treatment received
Wound effusion
Amikacin and colistin IV
CSF Wound effusion Wound effusion CSF Wound effusion CSF
Amikacin Amikacin Amikacin Amikacin Amikacin Amikacin
and and and and and and
colistin colistin colistin colistin colistin colistin
IV þ amikacin IT IV IV IV þ amikacin IT IV IV
PFGE
ST
KPC
A
11
2
A A A A A A
11 11 11 11 11 11
2 2 2 2 2 2
CSF, cerebrospinal fluid; IT, intrathecal; IV, intravenous; KPC, Klebsiella pneumoniae carbapenemase; ST, sequence type.
neurosurgical operations. Among these patients, 32 (1.83%) developed nosocomial infections but no SSIs. Between July 5 and 21, 2011, the neurosurgery medical staff admitted 146 inpatients and performed 98 neurosurgical operations. Seven of these patients developed an SSI with CPKP. The CPKP infection rate was 4.79%, and the SSI rate was 7.14%. The CPKP infection rate increased significantly from the preoutbreak period to the outbreak period (P < .05). These patients were located in different wards, and their operations were performed by different surgeons. Patient characteristics and epidemiologic patterns of CPKP are summarized in Table 1. Among the 402 surveillance samples, CPKP was detected only on a razor that had been used to shave multiple patients’ hair before surgery. The isolates from infected patients and the razor shared the same resistance pattern, with susceptibility only to amikacin and resistance to all other antibiotic classes. Molecular biological analysis identified the isolates as belonging to the same PFGE-defined strain, blakpc-2 and sequence type 11 (ST11). As soon as the outbreak was suspected in the neurosurgical wards, the infected patients were isolated in single-bed side rooms with cohort nursing. Strict contact precautions and deep cleaning were maintained in the operating room, patient room, and nurses’ station, with particular attention given to equipment and surfaces. The latter were cleaned with chlorine-based or 75% alcohol disinfectant. Preoperative skin preparation procedures were revised. A trained registered nurse shaved scalps using disposable razors. The institution’s infection preventionist performed daily rounds to enforce standardized skin preparation procedures. After institution of infection control measures, no further patients were infected with CPKP. All 7 infected patients underwent external ventricular drainage and were treated with intravenous amikacin and colistin. Two patients also received intrathecal injections of amikacin. After receiving surgical and medical treatment, none of the patients relapsed with persistent or recurrent CPKP. DISCUSSION CPKP isolates are often resistant to multiple antimicrobial classes, including all available b-lactams, fluoroquinolones, and aminoglycosides. Some CPKP strains have reduced susceptibility to chlorhexidine.6 It is possible that extremely drug-resistant K pneumoniae contributes to its ability to persist in the hospital environment and has become a major pathogen for nosocomial pathogens. In China, traditionally scalp shaving was performed by a barber with no infection control training. They generally reuse a same razor without any disinfection. In this report, these isolates from infected patients and the shaving razor shared the same molecular typing pattern, all belonging to the same PFGE-defined strain, blakpc-2 and
ST11. After removal of the contaminated razor and implementation of appropriate infection control measures, no further cases occurred. Thus, the contaminated shaving razor was identified as the likely source of the outbreak. This report has important implications for front-line clinicians, managers, and infection control preventionists. Inadequate skin preparation may cause severe SSIs. Standardizing the skin preparation procedure is important. It is imperative that all perioperative activities be performed by infection controletrained nurses using sterilized instruments. K pneumoniae normally colonizes in the human nasal cavity, intestinal tract, and the hands of hospital staff members, and thus can spread through person-to-person contact.7,8 A limitation of this study is that rectal screening swabs were not obtained, and so it is unclear whether these patients were already colonized with CPKP or perhaps transmission itself was directly associated with a single patient with CPKP.
Acknowledgment We thank the infection control teams for their assistance in investigating the outbreak. We also thank the staff of the Anhui Provincial Center for Disease Control and Prevention for their work in typing the isolates, without whom this study would not have been possible.
References 1. Plowman R, Graves N, Griffin M, Roberts JA, Swan A. The socioeconomic burden of hospital-acquired infection. London, UK: Public Health Laboratory Service; 1999. 2. Owens CD, Stoessel K. Surgical site infections: epidemiology, microbiology and prevention. J Hosp Infect 2008;70:3-10. 3. Shahane V, Bhawal S, Lele U. Surgical site infections: a one-year prospective study in a tertiary care center. Int J Health Sci (Qassim) 2012;6:79-84. 4. Woodford N, Zhang J, Warner M, Kaufmann ME, Matos J, Macdonald A, et al. Arrival of Klebsiella pneumoniaeeproducing KPC carbapenemase in the United Kingdom. J Antimicrob Chemother 2008;62:1261-4. 5. Mataseje LF, Boyd DA, Willey BM, Prayitno N, Kreiswirth N, Gelosia A, et al. Plasmid comparison and molecular analysis of Klebsiella pneumoniae habouring bla(KPC) from New York City and Toronto. J Antimicrob Chemother 2011;66: 1273-7. 6. Naparstek L, Carmeli Y, Chmelnitsky I, Banin E, Navon-Venezia S. Reduced susceptibility to chlorhexidine among extremely-drug-resistant strains of Klebsiella pneumoniae. J Hosp Infect 2012;81:15-9. 7. Coudeyras S, Nakusi L, Charbonnel N, Forestier C. A tripartite efflux pump involved in gastrointestinal colonization by Klebsiella pneumoniae confers a tolerance response to inorganic acid. Infect Immun 2008;76:4633-41. 8. Seid J, Asrat D. Occurrence of extended spectrum beta-lactamase enzymes in clinical isolates of Klebsiella species from Harar region, eastern Ethiopia. Acta Trop 2005;95:143-8.
