- Email: [email protected]
Outbreak of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae infection among renal transplant recipients
Letters to the Editor may have contributed to less stringent infection control practices. After these interventions, the outbreak was brought under control and no new clusters of A. baumannii cases were observed. This outbreak presented respiratory site predominance. A. baumannii was isolated from the respiratory tract in most cases, with very few isolates from other sites. Tracheostomy was the only factor associated with A. baumannii positivity among patients with respiratory tract involvement in the caseecontrol analysis. This is consistent with previous studies that identified risk factors such as tracheostomy and mechanical ventilation.3,4 The A. baumannii isolates involved in this outbreak were resistant to multiple antibiotics, including carbapenems, fully susceptible to gentamicin and colistin and partially susceptible to ampicillin/sulbactam. Outbreaks of carbapenemresistant A. baumannii have recently occurred in several countries, including Italy.5 In this outbreak, MICs for carbapenems were in a range indicating diminished susceptibility or low resistance, characteristic of isolates carrying the OXA-58 carbapenemase.6 OXA-58 has been identified in A. baumannii isolates causing recent outbreaks in other hospitals in Rome.7 In addition, meropenem exhibited a slightly greater activity than imipenem, although imipenem is generally considered to be more potent than meropenem against A. baumannii.8 In conclusion, this study found that, although considered to be of low virulence, A. baumannii can cause significant morbidity in ICUs. Invasive procedures, such as tracheostomy, were important factors in this outbreak caused by a multi-drugresistant strain.
References 1. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. 16th informational supplement. M100-S16. Wayne, PA: CLSI; 2006. 2. Gales AC, Reis OA, Jones RN. Contemporary assessment of antimicrobial susceptibility testing methods for polimyxin B and colistin: review of available interpretative criteria and quality control guidelines. J Clin Microbiol 2001;39:183e190. 3. Mah MW, Memish ZA, Cunningham G, Bannatyne RB. Outbreak of Acinetobacter baumannii in an intensive care unit associated with tracheostomy. Am J Infect Control 2001; 29:284e288. 4. Cefai C, Richards J, Gould FK, McPaeke P. An outbreak of Acinetobacter respiratory tract infection resulting from incomplete disinfection of ventilatory equipment. J Hosp Infect 1990;15:177e182. 5. Van Looveren M, Goossens H, ARPAC Steering Group. Antimicrobial resistance of Acinetobacter spp. in Europe. Clin Microbiol Infect 2004;10:684e704. 6. Coelho J, Woodford N, Afzal-Shah M, Livermore D. Occurrence of OXA-58-like carbapenemases in Acinetobacter spp.
305 collected over 10 years in three continents. Antimicrob Agents Chemother 2006;50:756e758. 7. Bertini A, Giordano A, Varesi P, Villa L, Mancini C, Carattoli A. First report of the carbapenem-hydrolyzing oxacillinase OXA-58 in Acinetobacter baumannii isolates in Italy. Antimicrob Agents Chemother 2006;50:2268e2269. 8. Rhomberg PR, Jones RN, MYSTIC Program (USA) Study Group. Antimicrobial spectrum of activity for meropenem and nine broad spectrum antimicrobials: report from the MYSTIC Program (2002) in North America. Diagn Microbiol Infect Dis 2003;47:365e372.
B. Longoa A. Pantostia I. Luzzia P. Placanicab S. Galloc A. Tarasic F. Di Sorac M. Monacoa A.M. Dionisia I. Volped F. Montellac A. Cassonea G. Rezzaa,* a Department of Infectious Diseases, National Institute of Health, Rome, Italy b Department of Microbiology, S. Giovanni Addolorata Hospital, Rome, Italy c Clinical Immunology - AIDS Care Unit, S. Giovanni Addolorata Hospital, Rome, Italy d Intensive Care Unit, S. Giovanni Addolorata Hospital, Rome, Italy E-mail address: [email protected] Available online 14 September 2006 * Corresponding author. Address: Reparto di Epidemiologia, Department of Infectious Diseases, National Institute of Health, Viale Regina Elena 299, 00161 Rome, Italy. Tel.: þ39 649903185; fax: þ39 649902755. ª 2006 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2006.07.010
Outbreak of extended-spectrum beta-lactamaseproducing Klebsiella pneumoniae infection among renal transplant recipients
Madam, The emergence of extended spectrum betalactamase (ESBL)-producing bacteria is a cause of
306
Letters to the Editor
concern.1 However, there are scarce data on infection or colonization with ESBL-producing bacteria in recipients of organ transplants.2e4 In this retrospective caseecontrol study performed in the nephrology unit of a teaching hospital in Rio de Janeiro, Brazil, we assessed the risk factors associated with an outbreak of ESBL-producing Klebsiella pneumoniae infection among renal transplant (RT) recipients. To our knowledge, this is the first report of an outbreak of ESBL K. pneumoniae infection in RT recipients. The nephrology unit includes four wards comprising 18 beds. Twelve beds are dedicated to RT recipients. The first case of ESBL K. pneumoniae infection in the nephrology unit occurred in 1999. Subsequently, the incidence of ESBL K. pneumoniae infections rose from 0.1/1000 patient-days in 1999 to 0.9/1000 patient-days in 2002, becoming the most frequent pathogen causing infection in the nephrology unit. Preliminary analyses showed that the rise in the incidence of ESBL K. pneumoniae infection occurred specifically among patients admitted recently for RT. A policy for antibiotic therapy with restriction of third-generation cephalosporins had been in place at the hospital since 2000.
Patients admitted to the nephrology unit for RT between March and September 2002 (outbreak period) were eligible for the study. A case was defined as an RT recipient who developed ESBL K. pneumoniae infection. All other RT recipients without ESBL K. pneumoniae infection were defined as controls. Only patients without a previous diagnosis of ESBL K. pneumoniae infection were included in the risk factor analyses. Antimicrobial susceptibility testing and detection of ESBL production was confirmed by disc diffusion according to The Clinical and Laboratory Standards Institute (CLSI) recommendations.5 Genotyping was performed by pulsed-field gel electrophoresis using XbaI. Plasmid profiles of ESBL K. pneumoniae isolates were also analysed. Six RT recipients had ESBL K. pneumoniae infections during the study period. There were three urinary infections, one pneumonia, one primary sepsis and one surgical site infection. The median time from transplantation to the diagnosis of ESBL K. pneumoniae infection was 12 days (range 4e25 days). The median length of hospital stay free from ESBL K. pneumoniae infection was not significantly different between cases (12 days) and controls (nine days, P ¼ 0.5). In bivariate analyses (Table I),
Table I Bivariate analysis of risk factors for infection with extended-spectrum beta-lactamase (ESBL) producing Klebsiella pneumoniae among renal transplant recipients Variable
With ESBL K. pneumoniae infection (N ¼ 6)
Patients without ESBL K. pneumoniae infection (N ¼ 55)
P value
Categorical variable, N (%) Age 30 years Female Cadaveric donor
3 (50) 6 (100) 3 (50)
6 (11) 31 (56) 14 (25)
0.034 0.073 0.33
Immunosuppressive drugs Corticosteroids Tacrolimus Mycophenolate mofetil OKT3 Cyclosporin Sirolimus Dual immunosuppressive drug therapy Acute graft rejection Graft thrombosis Previous use of two antibiotics or more Central venous catheter Nasogastric catheter Haemodialysis Haemotransfusion Re-operation
6 4 4 3 3 2 1 2 1 5 1 1 4 2 1
47 43 47 4 5 8 15 13 4 11 1 1 18 5 3
0.7 0.61 0.25 0.017 0.025 0.25 0.57 0.63 0.41 0.004 0.19 0.19 0.18 0.14 0.29
Continuous variable, median (range) Length of surgery (h) Days with urinary catheter
5 (4e6) 5 (4e11)
(100) (67) (67) (50) (50) (33) (16) (33) (16) (83) (16) (16) (66) (33) (16)
(85) (78) (85) (7) (9) (14) (27) (24) (7) (20) (2) (2) (33) (9) (5)
5 (2e8) 5 (2e36)
0.9 0.9
Letters to the Editor ESBL K. pneumoniae infections were significantly associated with age 30 years (P ¼ 0.034), use of cyclosporin (P ¼ 0.025), use of OKT3 (P ¼ 0.017), and use of two or more antimicrobial drugs for longer than 72 h (P ¼ 0.004). The antimicrobial drugs used for more than 72 h among cases were cefazolin (N ¼ 6), trimethoprim/sulphamethoxazole (N ¼ 5), fluoroquinolones (N ¼ 2) and imipenem (N ¼ 1). The median time of antibiotic use was 11 days. By multiple logistic regression analyses, the use of more than two different antibiotics [odds ratio (OR) 16.79, 95% confidence interval (CI) 1.64e 171.9, P ¼ 0.006] was the only variable independently associated with ESBL K. pneumoniae infection. There was also a trend for a higher incidence of ESBL K. pneumoniae infections in patients treated with cyclosporin (OR 7.44, 95% CI 0.88e63.1, P ¼ 0.065). Ten K. pneumoniae isolates were available for genotyping: five non-ESBL-producing K. pneumoniae isolates obtained from controls during the outbreak period, four isolates from four of the six patients with ESBL K. pneumoniae infection, and one isolate from a patient who was excluded from risk factor analyses due to a previous diagnosis of persistent ESBL K. pneumoniae bacteriuria. These five ESBL K. pneumoniae isolates and the other two isolates that were not available for genotyping had identical antibiogram results. They were only susceptible to imipenem. Isolates obtained from three patients with ESBL K. pneumoniae infection and from the patient with persistent ESBL K. pneumoniae bacteriuria belonged to the same genotype. These isolates also clustered in time. All five available ESBL K. pneumoniae isolates harboured a plasmid of the same size. These data suggest that cross-transmission played an important role in ESBL K. pneumoniae dissemination among our patients. Exposure to third-generation cephalosporins has been recognized as a risk factor for acquisition of ESBL K. pneumoniae.6e8 No patient in this study was treated with these drugs. The independent association between ESBL K. pneumoniae infection and the use of more than two antimicrobial drugs suggests that exposure to other classes of antibiotics may also influence the risk of acquisition of ESBL K. pneumoniae. This finding emphasizes the importance of judicious use of antimicrobial therapy. We also observed a trend for an independent association between the use of cyclosporin and ESBL K. pneumoniae infection. However, further studies are needed to confirm this finding. The main limitation of this study was its small sample size, which may have precluded the
307 identification of additional risk factors for ESBL K. pneumoniae infection. Nevertheless, the small number of cases included in the study may reflect the timely implementation of infection control measures. Retraining in infection control practices, focusing on hand hygiene and appropriate urinary catheter manipulation, was undertaken after the first five cases were detected. In the five months following retraining, there was just one case of ESBL K. pneumoniae infection. These results emphasize the importance of providing periodic retraining to healthcare workers for the prevention of nosocomial transmission of ESBL K. pneumoniae.
Acknowledgements ~o de This study was supported by Coordenac ¸a Aperfeic ¸oamento de Pessoal de Nı´vel Superior, ~o de Conselho Nacional de Pesquisa and Fundac ¸a Amparo a ` Pesquisa do Estado do Rio de Janeiro of Brazil, and the Fogarty International Center Program in Global Infectious Diseases Research Training Program (TW006563) of the National Institutes of Health in the USA.
References 1. Karlowsky JA, Sahm DF. The impact of Gram-negative organisms with extended-spectrum b-lactamases. In: Wenzel RP, editor. Prevention and control of nosocomial infections. 4th edn. Philadelphia: Lippincott, Williams & Wilkins; 2003. p. 186e214. 2. Paterson DL, Singh N, Rihs R, Squier C, Rihs B, Muder RR. Control of an outbreak of infection due to extended-spectrum b-lactamase-producing Escherichia coli in a liver transplantation unit. Clin Infect Dis 2001;33:126e128. 3. Rebuck JA, Olsen KM, Fey PD, Langnas AN, Rupp ME. Characterization of an outbreak due to extended-spectrum b-lactamase-producing Klebsiella pneumoniae in a pediatric intensive care unit transplant population. Clin Infect Dis 2000;31:1368e1372. 4. Green M, Barbadora K. Recovery of ceftazidime-resistant Klebsiella pneumoniae from pediatric liver and intestinal transplant recipients. Pediatr Transplant 1998;2:224e230. 5. National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial susceptibility testing. NCCLS document M100-S10 (M2). Philadelphia: NCCLS; 2000. 6. Lee SO, Lee ES, Park SY, Kim SY, Seo YH, Cho YK. Reduced use of third-generation cephalosporins decreases the acquisition of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae. Infect Control Hosp Epidemiol 2004;25: 832e837. 7. Lin MF, Huangy ML, Laiy SH. Risk factors in the acquisition of extended-spectrum b-lactamase Klebsiella pneumoniae: a caseecontrol study in a district teaching hospital in Taiwan. J Hosp Infect 2003;53:39e45.
308
Letters to the Editor
8. Kanafani ZA, Mehio-Sibai A, Araj GF, Kanaan M, Kanj SS. Epidemiology and risk factors for extended-spectrum beta-lactamaseproducing organisms: a caseecontrol study at a tertiary care center in Lebanon. Am J Infect Control 2005;33:326e332.
c
School of Public Health, UC Berkeley, Berkeley, CA, USA E-mail address: [email protected] Available online 14 September 2006
a,
I. Souto Martins * B. Meurer Moreirab L.W. Rileyc G. Santoro-Lopesa a Departamento de Medicina Preventiva, Faculdade de Medicina, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil b Instituto de Microbiologia Prof. Paulo de Go´es, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
* Corresponding author. Address: Rua Gaspar Magalhaes 89/102 Ilha do Governador, CEP 21940-120, Rio de Janeiro, Brazil. Tel.: þ55 21 246330034; fax: þ55 21 22542694.
ª 2006 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2006.07.011
References 1. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. 16th informational supplement. M100-S16. Wayne, PA: CLSI; 2006. 2. Gales AC, Reis OA, Jones RN. Contemporary assessment of antimicrobial susceptibility testing methods for polimyxin B and colistin: review of available interpretative criteria and quality control guidelines. J Clin Microbiol 2001;39:183e190. 3. Mah MW, Memish ZA, Cunningham G, Bannatyne RB. Outbreak of Acinetobacter baumannii in an intensive care unit associated with tracheostomy. Am J Infect Control 2001; 29:284e288. 4. Cefai C, Richards J, Gould FK, McPaeke P. An outbreak of Acinetobacter respiratory tract infection resulting from incomplete disinfection of ventilatory equipment. J Hosp Infect 1990;15:177e182. 5. Van Looveren M, Goossens H, ARPAC Steering Group. Antimicrobial resistance of Acinetobacter spp. in Europe. Clin Microbiol Infect 2004;10:684e704. 6. Coelho J, Woodford N, Afzal-Shah M, Livermore D. Occurrence of OXA-58-like carbapenemases in Acinetobacter spp.
305 collected over 10 years in three continents. Antimicrob Agents Chemother 2006;50:756e758. 7. Bertini A, Giordano A, Varesi P, Villa L, Mancini C, Carattoli A. First report of the carbapenem-hydrolyzing oxacillinase OXA-58 in Acinetobacter baumannii isolates in Italy. Antimicrob Agents Chemother 2006;50:2268e2269. 8. Rhomberg PR, Jones RN, MYSTIC Program (USA) Study Group. Antimicrobial spectrum of activity for meropenem and nine broad spectrum antimicrobials: report from the MYSTIC Program (2002) in North America. Diagn Microbiol Infect Dis 2003;47:365e372.
B. Longoa A. Pantostia I. Luzzia P. Placanicab S. Galloc A. Tarasic F. Di Sorac M. Monacoa A.M. Dionisia I. Volped F. Montellac A. Cassonea G. Rezzaa,* a Department of Infectious Diseases, National Institute of Health, Rome, Italy b Department of Microbiology, S. Giovanni Addolorata Hospital, Rome, Italy c Clinical Immunology - AIDS Care Unit, S. Giovanni Addolorata Hospital, Rome, Italy d Intensive Care Unit, S. Giovanni Addolorata Hospital, Rome, Italy E-mail address: [email protected] Available online 14 September 2006 * Corresponding author. Address: Reparto di Epidemiologia, Department of Infectious Diseases, National Institute of Health, Viale Regina Elena 299, 00161 Rome, Italy. Tel.: þ39 649903185; fax: þ39 649902755. ª 2006 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2006.07.010
Outbreak of extended-spectrum beta-lactamaseproducing Klebsiella pneumoniae infection among renal transplant recipients
Madam, The emergence of extended spectrum betalactamase (ESBL)-producing bacteria is a cause of
306
Letters to the Editor
concern.1 However, there are scarce data on infection or colonization with ESBL-producing bacteria in recipients of organ transplants.2e4 In this retrospective caseecontrol study performed in the nephrology unit of a teaching hospital in Rio de Janeiro, Brazil, we assessed the risk factors associated with an outbreak of ESBL-producing Klebsiella pneumoniae infection among renal transplant (RT) recipients. To our knowledge, this is the first report of an outbreak of ESBL K. pneumoniae infection in RT recipients. The nephrology unit includes four wards comprising 18 beds. Twelve beds are dedicated to RT recipients. The first case of ESBL K. pneumoniae infection in the nephrology unit occurred in 1999. Subsequently, the incidence of ESBL K. pneumoniae infections rose from 0.1/1000 patient-days in 1999 to 0.9/1000 patient-days in 2002, becoming the most frequent pathogen causing infection in the nephrology unit. Preliminary analyses showed that the rise in the incidence of ESBL K. pneumoniae infection occurred specifically among patients admitted recently for RT. A policy for antibiotic therapy with restriction of third-generation cephalosporins had been in place at the hospital since 2000.
Patients admitted to the nephrology unit for RT between March and September 2002 (outbreak period) were eligible for the study. A case was defined as an RT recipient who developed ESBL K. pneumoniae infection. All other RT recipients without ESBL K. pneumoniae infection were defined as controls. Only patients without a previous diagnosis of ESBL K. pneumoniae infection were included in the risk factor analyses. Antimicrobial susceptibility testing and detection of ESBL production was confirmed by disc diffusion according to The Clinical and Laboratory Standards Institute (CLSI) recommendations.5 Genotyping was performed by pulsed-field gel electrophoresis using XbaI. Plasmid profiles of ESBL K. pneumoniae isolates were also analysed. Six RT recipients had ESBL K. pneumoniae infections during the study period. There were three urinary infections, one pneumonia, one primary sepsis and one surgical site infection. The median time from transplantation to the diagnosis of ESBL K. pneumoniae infection was 12 days (range 4e25 days). The median length of hospital stay free from ESBL K. pneumoniae infection was not significantly different between cases (12 days) and controls (nine days, P ¼ 0.5). In bivariate analyses (Table I),
Table I Bivariate analysis of risk factors for infection with extended-spectrum beta-lactamase (ESBL) producing Klebsiella pneumoniae among renal transplant recipients Variable
With ESBL K. pneumoniae infection (N ¼ 6)
Patients without ESBL K. pneumoniae infection (N ¼ 55)
P value
Categorical variable, N (%) Age 30 years Female Cadaveric donor
3 (50) 6 (100) 3 (50)
6 (11) 31 (56) 14 (25)
0.034 0.073 0.33
Immunosuppressive drugs Corticosteroids Tacrolimus Mycophenolate mofetil OKT3 Cyclosporin Sirolimus Dual immunosuppressive drug therapy Acute graft rejection Graft thrombosis Previous use of two antibiotics or more Central venous catheter Nasogastric catheter Haemodialysis Haemotransfusion Re-operation
6 4 4 3 3 2 1 2 1 5 1 1 4 2 1
47 43 47 4 5 8 15 13 4 11 1 1 18 5 3
0.7 0.61 0.25 0.017 0.025 0.25 0.57 0.63 0.41 0.004 0.19 0.19 0.18 0.14 0.29
Continuous variable, median (range) Length of surgery (h) Days with urinary catheter
5 (4e6) 5 (4e11)
(100) (67) (67) (50) (50) (33) (16) (33) (16) (83) (16) (16) (66) (33) (16)
(85) (78) (85) (7) (9) (14) (27) (24) (7) (20) (2) (2) (33) (9) (5)
5 (2e8) 5 (2e36)
0.9 0.9
Letters to the Editor ESBL K. pneumoniae infections were significantly associated with age 30 years (P ¼ 0.034), use of cyclosporin (P ¼ 0.025), use of OKT3 (P ¼ 0.017), and use of two or more antimicrobial drugs for longer than 72 h (P ¼ 0.004). The antimicrobial drugs used for more than 72 h among cases were cefazolin (N ¼ 6), trimethoprim/sulphamethoxazole (N ¼ 5), fluoroquinolones (N ¼ 2) and imipenem (N ¼ 1). The median time of antibiotic use was 11 days. By multiple logistic regression analyses, the use of more than two different antibiotics [odds ratio (OR) 16.79, 95% confidence interval (CI) 1.64e 171.9, P ¼ 0.006] was the only variable independently associated with ESBL K. pneumoniae infection. There was also a trend for a higher incidence of ESBL K. pneumoniae infections in patients treated with cyclosporin (OR 7.44, 95% CI 0.88e63.1, P ¼ 0.065). Ten K. pneumoniae isolates were available for genotyping: five non-ESBL-producing K. pneumoniae isolates obtained from controls during the outbreak period, four isolates from four of the six patients with ESBL K. pneumoniae infection, and one isolate from a patient who was excluded from risk factor analyses due to a previous diagnosis of persistent ESBL K. pneumoniae bacteriuria. These five ESBL K. pneumoniae isolates and the other two isolates that were not available for genotyping had identical antibiogram results. They were only susceptible to imipenem. Isolates obtained from three patients with ESBL K. pneumoniae infection and from the patient with persistent ESBL K. pneumoniae bacteriuria belonged to the same genotype. These isolates also clustered in time. All five available ESBL K. pneumoniae isolates harboured a plasmid of the same size. These data suggest that cross-transmission played an important role in ESBL K. pneumoniae dissemination among our patients. Exposure to third-generation cephalosporins has been recognized as a risk factor for acquisition of ESBL K. pneumoniae.6e8 No patient in this study was treated with these drugs. The independent association between ESBL K. pneumoniae infection and the use of more than two antimicrobial drugs suggests that exposure to other classes of antibiotics may also influence the risk of acquisition of ESBL K. pneumoniae. This finding emphasizes the importance of judicious use of antimicrobial therapy. We also observed a trend for an independent association between the use of cyclosporin and ESBL K. pneumoniae infection. However, further studies are needed to confirm this finding. The main limitation of this study was its small sample size, which may have precluded the
307 identification of additional risk factors for ESBL K. pneumoniae infection. Nevertheless, the small number of cases included in the study may reflect the timely implementation of infection control measures. Retraining in infection control practices, focusing on hand hygiene and appropriate urinary catheter manipulation, was undertaken after the first five cases were detected. In the five months following retraining, there was just one case of ESBL K. pneumoniae infection. These results emphasize the importance of providing periodic retraining to healthcare workers for the prevention of nosocomial transmission of ESBL K. pneumoniae.
Acknowledgements ~o de This study was supported by Coordenac ¸a Aperfeic ¸oamento de Pessoal de Nı´vel Superior, ~o de Conselho Nacional de Pesquisa and Fundac ¸a Amparo a ` Pesquisa do Estado do Rio de Janeiro of Brazil, and the Fogarty International Center Program in Global Infectious Diseases Research Training Program (TW006563) of the National Institutes of Health in the USA.
References 1. Karlowsky JA, Sahm DF. The impact of Gram-negative organisms with extended-spectrum b-lactamases. In: Wenzel RP, editor. Prevention and control of nosocomial infections. 4th edn. Philadelphia: Lippincott, Williams & Wilkins; 2003. p. 186e214. 2. Paterson DL, Singh N, Rihs R, Squier C, Rihs B, Muder RR. Control of an outbreak of infection due to extended-spectrum b-lactamase-producing Escherichia coli in a liver transplantation unit. Clin Infect Dis 2001;33:126e128. 3. Rebuck JA, Olsen KM, Fey PD, Langnas AN, Rupp ME. Characterization of an outbreak due to extended-spectrum b-lactamase-producing Klebsiella pneumoniae in a pediatric intensive care unit transplant population. Clin Infect Dis 2000;31:1368e1372. 4. Green M, Barbadora K. Recovery of ceftazidime-resistant Klebsiella pneumoniae from pediatric liver and intestinal transplant recipients. Pediatr Transplant 1998;2:224e230. 5. National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial susceptibility testing. NCCLS document M100-S10 (M2). Philadelphia: NCCLS; 2000. 6. Lee SO, Lee ES, Park SY, Kim SY, Seo YH, Cho YK. Reduced use of third-generation cephalosporins decreases the acquisition of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae. Infect Control Hosp Epidemiol 2004;25: 832e837. 7. Lin MF, Huangy ML, Laiy SH. Risk factors in the acquisition of extended-spectrum b-lactamase Klebsiella pneumoniae: a caseecontrol study in a district teaching hospital in Taiwan. J Hosp Infect 2003;53:39e45.
308
Letters to the Editor
8. Kanafani ZA, Mehio-Sibai A, Araj GF, Kanaan M, Kanj SS. Epidemiology and risk factors for extended-spectrum beta-lactamaseproducing organisms: a caseecontrol study at a tertiary care center in Lebanon. Am J Infect Control 2005;33:326e332.
c
School of Public Health, UC Berkeley, Berkeley, CA, USA E-mail address: [email protected] Available online 14 September 2006
a,
I. Souto Martins * B. Meurer Moreirab L.W. Rileyc G. Santoro-Lopesa a Departamento de Medicina Preventiva, Faculdade de Medicina, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil b Instituto de Microbiologia Prof. Paulo de Go´es, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
* Corresponding author. Address: Rua Gaspar Magalhaes 89/102 Ilha do Governador, CEP 21940-120, Rio de Janeiro, Brazil. Tel.: þ55 21 246330034; fax: þ55 21 22542694.
ª 2006 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2006.07.011