bs_bs_banner
SCIENTIFIC LETTER
Pleural empyema caused by Klebsiella oxytoca: A case series ELIZABETH SUTHERS,1 ANDREW ROSENSTENGEL,1 JULIE HART,2 JOSHUA R. LEWIS,3,4 IAN KAY,2 GRANT WATERER,3,5 Y.C. GARY LEE1,6 AND FRASER BRIMS1,3,7 1
Department of Respiratory Medicine and 4Department of Endocrinology and Diabetes, Sir Charles Gairdner Hospital, and Microbiology, PathWest Laboratory Medicine and 5Department of Respiratory Medicine, Royal Perth Hospital, 3School of Medicine and Pharmacology and 6Centre for Asthma Allergy & Respiratory Research, School of Medicine & Pharmacology, University of Western Australia, Perth, Western Australia, and 7Occupational & Respiratory Health Unit, Lung Institute of Western Australia, Perth, Australia 2
We report on 19 patients from Western Australia of pleural empyema with Klebsiella oxytoca, an organism never before reported in association with this condition. Median age was 65 years, 14/17 (83%) had been in hospital within 30 days prior to diagnosis, 12/18 (67%) had active cancer, 9/17 (53%) had been in intensive care and 7/17 (41%) had prior surgery. Nine patients died at the time of censure, five within 90 days of infection. Key words: empyema, Klebsiella oxytoca, nosocomial infection, pleural.
Empyema thoracis was described more than 2000 years ago by Hippocrates, and the incidence of pleural infection continues to rise in many developed countries.1 Up to 30% of adult patients with pleural infection either die or require surgery, with those most at risk being over 65 years old with comorbid conditions.2,3 There are a wide range of pathogenic organisms reported to cause pleural infection, although up to 44% of patients are culture negative using conventional techniques.4,5 There are notable differences between the bacteriology and outcome of community-acquired and hospital-acquired infections,4,5 with nosocomial infection associated with a higher than 1-year mortality.4 There is marked geographical variation in microbiological isolates with pleural infection and, therefore, recognition of the variation in local epidemiological data is of vital importance to clinicians as local knowledge may inform the use of appropriate antibiotic therapy and microbiological surveillance.6 Klebsiella oxytoca is a ubiquitous, facultatively anaerobic, Gram-negative bacillus, routinely distinguished from K. pneumoniae by its production of indole. In humans, K. oxytoca colonizes mucosal Correspondence: Fraser J.H. Brims, Respiratory Department, Ground Floor B-block, Sir Charles Gairdner Hospital, Hospital Avenue, Nedlands, Western Australia. Email: fraserbrims @uwa.edu.au Received 15 October 2014; invited to revised 16 November 2014; revised 17 November 2014; accepted 24 November 2014 (Associate Editor: Ioannis Kalomenidis). Article first published online: 11 February 2015 © 2015 Asian Pacific Society of Respirology
membranes, particularly the gastrointestinal tract.7 K. oxytoca produces chromosomal β-lactamases, which confer resistance to penicillins. Many infections are polymicrobial, hospital-associated and several neonatal and intensive care unit (ICU) outbreaks have been reported.8,9 To our knowledge K. oxytoca has not previously been reported as an organism causing pleural infection. Having observed a number of patients of pleural infection associated with K. oxytoca within our institution, we performed a retrospective database, case note and electronic health record review of cases reported to have K. oxytoca isolated from pleural fluid samples. The Sir Charles Gairdner Hospital Research Ethics Committee approved the study, reference number 2012-038 dated 26 April 2012. Hospital-associated infection was defined as those developing a de-novo pleural infection following more than 7 days stay in hospital, or in individuals who have had a hospital admission and/or surgery (including pleural intervention) within 30 days of the date of positive culture. Survival was censured (alive/ dead) at 01 August 2013 with dates of death confirmed with the statewide electronic hospital records system. K. oxytoca were identified using standard biochemical methods, including analytical profile index (bioMérieux), Vitek (bioMérieux) and agar dilution antimicrobial susceptibility testing, performed using US Clinical and Laboratory Standards Institute breakpoints. In addition to the routine microbiology reporting checks, for this study, confirmation of the correct identification of K. oxytoca was undertaken with re-examination of the original isolate (where available) and/or review of the biochemical profile report on electronic lab record by a senior scientist. Twenty-four individuals with K. oxytoca isolated from pleural fluid samples were identified, with 19 patients having case notes with adequate information (between the years 2001 and 2011). All isolates were confirmed to be K. oxytoca upon review, and all cases had confirmed physician-diagnosed pleural infection. The demographics and background description Respirology (2015) 20, 507–509 doi: 10.1111/resp.12476
508
E Suthers et al.
Table 1 Descriptive factors of patients with pleural infection from Klebsiella oxytoca Variable Male Age (years) Length of hospital stay (days) Time to culture‡ from admission (days) Right-sided infection Resident in care home Hospital admission < 30 days prior Surgery < 30 days prior Pleural intervention < 30 days prior ICU admission prior to culture Number of days chest tube inserted prior to positive culture Died as inpatient Survival† (days)
n=
n = (%) / median (IQR)
19 19 14 14
16 (84.2%) 65 (47–73) 35 (26.0–71.3) 5 (0.0–15)
17 18 17 17 17 17 14
12 (70.5%) 1 (5.5%) 14 (82.5%) 7 (41.1%) 9 (52.9%) 9 (52.9%) 8.5 (3–26)
16 8
2 (12.5%) 291 (32–511)
†
From date of positive culture of K. oxytoca. Date of positive culture of K. oxytoca. Numbers for the denominator (n) vary due to availability of complete data. ICU, intensive care unit; IQR, interquartile range. ‡
of the cases are provided in Table 1. Hospital length of stay following positive culture was a median of 14 days (interquartile range 0.0–33.5). Twelve out of 18 (66%) patients had a history of cancer; four patients with thoracic cancer. Four patients had a diagnosis of diabetes mellitus and two of oral corticosteroid use prior to development of infection (one for chronic obstructive pulmonary disease, one for ulcerative colitis). One patient had an indwelling pleural catheter in-situ for mesothelioma for 8 months before the isolate. Records of antibiotic susceptibility were available for 17 patients. All isolates were resistant to amoxicillin/ampicillin, one additionally resistant to amoxicillin/clavulanic acid and piperacillin/tazobactam and one further resistant to cefazolin. Intravenous antibiotics were administered for a median of 10 days following diagnosis of pleural infection. K. oxytoca empyema commonly occurred as part of a polymicrobial infection (12 of 17 patients, 70%). Additional isolates tended to be associated with either skin, oral or gastrointestinal tract colonization, with other organisms commonly found in the environment and associated with nosocomial infection. Nine patients had died at the time of censure; two patients within 30 days and three within 90 days, of positive culture. Median survival from date of positive culture was 291 days. The cause of death was unknown in three, progression of underlying disease in five, and one died as a direct result of sepsis from bilateral pneumonia and oesophageal rupture. One patient had surgery as part of the treatment for pleural infection, and one had local fibrinolysis administered via chest tube. In this study, empyema caused by K. oxytoca was associated with current, or recent, inpatient hospital Respirology (2015) 20, 507–509
stay which is consistent with previous reports of Klebsiella species causing nosocomial urinary tract and wound infections, pneumonia and septicaemia.7,10,11 Just two of our patients were found to be community acquired. K. oxytoca was the sole isolate in five patients of empyema, supporting the notion that it may be a true pathogen; all these patients had all been in hospital within 30 days of infection. Interestingly, despite being a nosocomial pathogen, there was only limited antibiotic resistance patterns in this report, and this is consistent with other microbiology reports of K. oxytoca.11 The presence of five patients of solitary K. oxytoca empyema suggests that the organism is likely to be pathogenic and not a contaminant or benign co-isolate. These novel findings highlight the importance of local knowledge with respect to the bacteriology of pleural infection and understanding antibiotic susceptibility profiles. The Australian therapeutic guidelines12 recommend piperacillin/ tazobactam as empirical therapy for empyema. Although one of the 17 isolates tested resistant, in our institution we recommend piperacillin/tazobactam should still be used empirically until susceptibility results are available. Cases had a broad range of comorbidities and a high incidence of malignancy with 12/18 patients with solid organ cancer. Patients with active cancer are likely to have relative immune suppression and will frequently undergo invasive procedures and thus may be more susceptible to such infections. In this series, no patients developed infection associated with cytotoxic chemotherapy. Five of nine patients died within 90 days of positive culture, although the median survival of 291 days following K. oxytoca-associated pleural infection suggests that with adequate treatment, the infection itself may not be directly associated with mortality. This observation is important as it differs from previous reports identifying those with hospital-acquired pleural infection to have a high mortality.4,5 Our finding of comorbidities, high ICU stay numbers and a high prevalence of cancer in this study population, suggests that K. oxytoca-associated pleural infection affects those with inherent increased susceptibility to infection and may simply be a marker of frailty. This observation is in keeping with previous reports examining pleural infection that have also identified a subset with significant comorbidities within their populations.2,3,5 Certain limitations of these data must be acknowledged. The study is retrospective, and it is possible that further cases of K. oxytoca infection may have been missed. Without a baseline denominator for all pleural cultures, the incidence of K. oxytoca infection cannot be estimated. Similarly, without knowing the denominator of all infections of K. oxytoca, we are unable to estimate the proportion with pleural infection. While these findings from Western Australia are representative of a very large geographical area, this is not necessarily generalizable to the Australian population as a whole. An improved understanding of local and national bacteriology profiles is therefore desirable. Improvements in microbiological testing platforms such as organism-specific polymerase chain © 2015 Asian Pacific Society of Respirology
509
K. oxytoca empyema
reaction or matrix-assisted laser desorption/ ionisation-time of flight mass spectrometry performed directly on pleural fluid may improve identification of organisms in pleural fluid; however, this is not routine practice at present. In summary, to our knowledge, this report is the first description of K. oxytoca contributing to pleural empyema. Cases are predominantly nosocomial and polymicrobial in a population with comorbidities and high prevalence of cancer. This series demonstrates that K. oxytoca is an important organism to recognize and treat in the context of pleural infection, particularly in a susceptible population.
REFERENCES 1 Brims FJ, Lansley SM, Waterer GW, Lee YC. Empyema thoracis: new insights into an old disease. Eur. Respir. Rev. 2010; 19: 220–8. 2 Maskell NA, Davies CW, Nunn AJ, Hedley EL, Gleeson FV, Miller R, Gabe R, Rees GL, Peto TE, Woodhead MA et al. Controlled trial of intrapleural streptokinase for pleural infection. N. Engl. J. Med. 2005; 352: 865–74. 3 Rahman NM, Maskell NA, West A, Teoh R, Arnold A, Mackinlay C, Peckham D, Davies CW, Ali N, Kinnear W et al. Intrapleural use of tissue plasminogen activator and DNase in pleural infection. N. Engl. J. Med. 2011; 365: 518–26. 4 Maskell NA, Batt S, Hedley EL, Davies CW, Gillespie SH, Davies RJ. The bacteriology of pleural infection by genetic and standard
© 2015 Asian Pacific Society of Respirology
5
6 7
8
9
10
11
12
methods and its mortality significance. Am. J. Respir. Crit. Care Med. 2006; 174: 817–23. Marks DJ, Fisk MD, Koo CY, Pavlou M, Peck L, Lee SF, Lawrence D, Macrae MB, Wilson AP, Brown JS et al. Thoracic empyema: a 12-year study from a UK tertiary cardiothoracic referral centre. PLoS ONE 2012; 7: e30074. Lisboa T, Waterer GW, Lee YC. Pleural infection: changing bacteriology and its implications. Respirology 2011; 16: 598–603. Podschun R, Ullmann U. Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin. Microbiol. Rev. 1998; 11: 589–603. Lowe C, Willey B, O’Shaughnessy A, Lee W, Lum M, Pike K, Larocque C, Dedier H, Dales L, Moore C et al. Outbreak of extended-spectrum beta-lactamase-producing Klebsiella oxytoca infections associated with contaminated handwashing sinks(1). Emerg. Infect. Dis. 2012; 18: 1242–7. Kim BN, Ryu J, Kim YS, Woo JH. Retrospective analysis of clinical and microbiological aspects of Klebsiella oxytoca bacteremia over a 10-year period. Eur J Clin Microbiol Infect Dis 2002; 21: 419–26. Sahly H, Podschun R. Clinical, bacteriological, and serological aspects of Klebsiella infections and their spondylarthropathic sequelae. Clin. Diagn. Lab. Immunol. 1997; 4: 393–9. Stock I, Wiedemann B. Natural antibiotic susceptibility of Klebsiella pneumoniae, K. oxytoca, K. planticola, K. ornithinolytica and K. terrigena strains. J. Med. Microbiol. 2001; 50: 396–406. eTG. Antibiotic Expert Groups. Therapeutic Guidelines: Antibiotic. Version 15. Therapeutic Guidelines Limited, Melbourne, 2014. [Accessed 17 November 2014]. Available from URL: http:// www.tg.org.au/?sectionid=41
Respirology (2015) 20, 507–509
Copyright of Respirology is the property of Wiley-Blackwell and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
SCIENTIFIC LETTER
Pleural empyema caused by Klebsiella oxytoca: A case series ELIZABETH SUTHERS,1 ANDREW ROSENSTENGEL,1 JULIE HART,2 JOSHUA R. LEWIS,3,4 IAN KAY,2 GRANT WATERER,3,5 Y.C. GARY LEE1,6 AND FRASER BRIMS1,3,7 1
Department of Respiratory Medicine and 4Department of Endocrinology and Diabetes, Sir Charles Gairdner Hospital, and Microbiology, PathWest Laboratory Medicine and 5Department of Respiratory Medicine, Royal Perth Hospital, 3School of Medicine and Pharmacology and 6Centre for Asthma Allergy & Respiratory Research, School of Medicine & Pharmacology, University of Western Australia, Perth, Western Australia, and 7Occupational & Respiratory Health Unit, Lung Institute of Western Australia, Perth, Australia 2
We report on 19 patients from Western Australia of pleural empyema with Klebsiella oxytoca, an organism never before reported in association with this condition. Median age was 65 years, 14/17 (83%) had been in hospital within 30 days prior to diagnosis, 12/18 (67%) had active cancer, 9/17 (53%) had been in intensive care and 7/17 (41%) had prior surgery. Nine patients died at the time of censure, five within 90 days of infection. Key words: empyema, Klebsiella oxytoca, nosocomial infection, pleural.
Empyema thoracis was described more than 2000 years ago by Hippocrates, and the incidence of pleural infection continues to rise in many developed countries.1 Up to 30% of adult patients with pleural infection either die or require surgery, with those most at risk being over 65 years old with comorbid conditions.2,3 There are a wide range of pathogenic organisms reported to cause pleural infection, although up to 44% of patients are culture negative using conventional techniques.4,5 There are notable differences between the bacteriology and outcome of community-acquired and hospital-acquired infections,4,5 with nosocomial infection associated with a higher than 1-year mortality.4 There is marked geographical variation in microbiological isolates with pleural infection and, therefore, recognition of the variation in local epidemiological data is of vital importance to clinicians as local knowledge may inform the use of appropriate antibiotic therapy and microbiological surveillance.6 Klebsiella oxytoca is a ubiquitous, facultatively anaerobic, Gram-negative bacillus, routinely distinguished from K. pneumoniae by its production of indole. In humans, K. oxytoca colonizes mucosal Correspondence: Fraser J.H. Brims, Respiratory Department, Ground Floor B-block, Sir Charles Gairdner Hospital, Hospital Avenue, Nedlands, Western Australia. Email: fraserbrims @uwa.edu.au Received 15 October 2014; invited to revised 16 November 2014; revised 17 November 2014; accepted 24 November 2014 (Associate Editor: Ioannis Kalomenidis). Article first published online: 11 February 2015 © 2015 Asian Pacific Society of Respirology
membranes, particularly the gastrointestinal tract.7 K. oxytoca produces chromosomal β-lactamases, which confer resistance to penicillins. Many infections are polymicrobial, hospital-associated and several neonatal and intensive care unit (ICU) outbreaks have been reported.8,9 To our knowledge K. oxytoca has not previously been reported as an organism causing pleural infection. Having observed a number of patients of pleural infection associated with K. oxytoca within our institution, we performed a retrospective database, case note and electronic health record review of cases reported to have K. oxytoca isolated from pleural fluid samples. The Sir Charles Gairdner Hospital Research Ethics Committee approved the study, reference number 2012-038 dated 26 April 2012. Hospital-associated infection was defined as those developing a de-novo pleural infection following more than 7 days stay in hospital, or in individuals who have had a hospital admission and/or surgery (including pleural intervention) within 30 days of the date of positive culture. Survival was censured (alive/ dead) at 01 August 2013 with dates of death confirmed with the statewide electronic hospital records system. K. oxytoca were identified using standard biochemical methods, including analytical profile index (bioMérieux), Vitek (bioMérieux) and agar dilution antimicrobial susceptibility testing, performed using US Clinical and Laboratory Standards Institute breakpoints. In addition to the routine microbiology reporting checks, for this study, confirmation of the correct identification of K. oxytoca was undertaken with re-examination of the original isolate (where available) and/or review of the biochemical profile report on electronic lab record by a senior scientist. Twenty-four individuals with K. oxytoca isolated from pleural fluid samples were identified, with 19 patients having case notes with adequate information (between the years 2001 and 2011). All isolates were confirmed to be K. oxytoca upon review, and all cases had confirmed physician-diagnosed pleural infection. The demographics and background description Respirology (2015) 20, 507–509 doi: 10.1111/resp.12476
508
E Suthers et al.
Table 1 Descriptive factors of patients with pleural infection from Klebsiella oxytoca Variable Male Age (years) Length of hospital stay (days) Time to culture‡ from admission (days) Right-sided infection Resident in care home Hospital admission < 30 days prior Surgery < 30 days prior Pleural intervention < 30 days prior ICU admission prior to culture Number of days chest tube inserted prior to positive culture Died as inpatient Survival† (days)
n=
n = (%) / median (IQR)
19 19 14 14
16 (84.2%) 65 (47–73) 35 (26.0–71.3) 5 (0.0–15)
17 18 17 17 17 17 14
12 (70.5%) 1 (5.5%) 14 (82.5%) 7 (41.1%) 9 (52.9%) 9 (52.9%) 8.5 (3–26)
16 8
2 (12.5%) 291 (32–511)
†
From date of positive culture of K. oxytoca. Date of positive culture of K. oxytoca. Numbers for the denominator (n) vary due to availability of complete data. ICU, intensive care unit; IQR, interquartile range. ‡
of the cases are provided in Table 1. Hospital length of stay following positive culture was a median of 14 days (interquartile range 0.0–33.5). Twelve out of 18 (66%) patients had a history of cancer; four patients with thoracic cancer. Four patients had a diagnosis of diabetes mellitus and two of oral corticosteroid use prior to development of infection (one for chronic obstructive pulmonary disease, one for ulcerative colitis). One patient had an indwelling pleural catheter in-situ for mesothelioma for 8 months before the isolate. Records of antibiotic susceptibility were available for 17 patients. All isolates were resistant to amoxicillin/ampicillin, one additionally resistant to amoxicillin/clavulanic acid and piperacillin/tazobactam and one further resistant to cefazolin. Intravenous antibiotics were administered for a median of 10 days following diagnosis of pleural infection. K. oxytoca empyema commonly occurred as part of a polymicrobial infection (12 of 17 patients, 70%). Additional isolates tended to be associated with either skin, oral or gastrointestinal tract colonization, with other organisms commonly found in the environment and associated with nosocomial infection. Nine patients had died at the time of censure; two patients within 30 days and three within 90 days, of positive culture. Median survival from date of positive culture was 291 days. The cause of death was unknown in three, progression of underlying disease in five, and one died as a direct result of sepsis from bilateral pneumonia and oesophageal rupture. One patient had surgery as part of the treatment for pleural infection, and one had local fibrinolysis administered via chest tube. In this study, empyema caused by K. oxytoca was associated with current, or recent, inpatient hospital Respirology (2015) 20, 507–509
stay which is consistent with previous reports of Klebsiella species causing nosocomial urinary tract and wound infections, pneumonia and septicaemia.7,10,11 Just two of our patients were found to be community acquired. K. oxytoca was the sole isolate in five patients of empyema, supporting the notion that it may be a true pathogen; all these patients had all been in hospital within 30 days of infection. Interestingly, despite being a nosocomial pathogen, there was only limited antibiotic resistance patterns in this report, and this is consistent with other microbiology reports of K. oxytoca.11 The presence of five patients of solitary K. oxytoca empyema suggests that the organism is likely to be pathogenic and not a contaminant or benign co-isolate. These novel findings highlight the importance of local knowledge with respect to the bacteriology of pleural infection and understanding antibiotic susceptibility profiles. The Australian therapeutic guidelines12 recommend piperacillin/ tazobactam as empirical therapy for empyema. Although one of the 17 isolates tested resistant, in our institution we recommend piperacillin/tazobactam should still be used empirically until susceptibility results are available. Cases had a broad range of comorbidities and a high incidence of malignancy with 12/18 patients with solid organ cancer. Patients with active cancer are likely to have relative immune suppression and will frequently undergo invasive procedures and thus may be more susceptible to such infections. In this series, no patients developed infection associated with cytotoxic chemotherapy. Five of nine patients died within 90 days of positive culture, although the median survival of 291 days following K. oxytoca-associated pleural infection suggests that with adequate treatment, the infection itself may not be directly associated with mortality. This observation is important as it differs from previous reports identifying those with hospital-acquired pleural infection to have a high mortality.4,5 Our finding of comorbidities, high ICU stay numbers and a high prevalence of cancer in this study population, suggests that K. oxytoca-associated pleural infection affects those with inherent increased susceptibility to infection and may simply be a marker of frailty. This observation is in keeping with previous reports examining pleural infection that have also identified a subset with significant comorbidities within their populations.2,3,5 Certain limitations of these data must be acknowledged. The study is retrospective, and it is possible that further cases of K. oxytoca infection may have been missed. Without a baseline denominator for all pleural cultures, the incidence of K. oxytoca infection cannot be estimated. Similarly, without knowing the denominator of all infections of K. oxytoca, we are unable to estimate the proportion with pleural infection. While these findings from Western Australia are representative of a very large geographical area, this is not necessarily generalizable to the Australian population as a whole. An improved understanding of local and national bacteriology profiles is therefore desirable. Improvements in microbiological testing platforms such as organism-specific polymerase chain © 2015 Asian Pacific Society of Respirology
509
K. oxytoca empyema
reaction or matrix-assisted laser desorption/ ionisation-time of flight mass spectrometry performed directly on pleural fluid may improve identification of organisms in pleural fluid; however, this is not routine practice at present. In summary, to our knowledge, this report is the first description of K. oxytoca contributing to pleural empyema. Cases are predominantly nosocomial and polymicrobial in a population with comorbidities and high prevalence of cancer. This series demonstrates that K. oxytoca is an important organism to recognize and treat in the context of pleural infection, particularly in a susceptible population.
REFERENCES 1 Brims FJ, Lansley SM, Waterer GW, Lee YC. Empyema thoracis: new insights into an old disease. Eur. Respir. Rev. 2010; 19: 220–8. 2 Maskell NA, Davies CW, Nunn AJ, Hedley EL, Gleeson FV, Miller R, Gabe R, Rees GL, Peto TE, Woodhead MA et al. Controlled trial of intrapleural streptokinase for pleural infection. N. Engl. J. Med. 2005; 352: 865–74. 3 Rahman NM, Maskell NA, West A, Teoh R, Arnold A, Mackinlay C, Peckham D, Davies CW, Ali N, Kinnear W et al. Intrapleural use of tissue plasminogen activator and DNase in pleural infection. N. Engl. J. Med. 2011; 365: 518–26. 4 Maskell NA, Batt S, Hedley EL, Davies CW, Gillespie SH, Davies RJ. The bacteriology of pleural infection by genetic and standard
© 2015 Asian Pacific Society of Respirology
5
6 7
8
9
10
11
12
methods and its mortality significance. Am. J. Respir. Crit. Care Med. 2006; 174: 817–23. Marks DJ, Fisk MD, Koo CY, Pavlou M, Peck L, Lee SF, Lawrence D, Macrae MB, Wilson AP, Brown JS et al. Thoracic empyema: a 12-year study from a UK tertiary cardiothoracic referral centre. PLoS ONE 2012; 7: e30074. Lisboa T, Waterer GW, Lee YC. Pleural infection: changing bacteriology and its implications. Respirology 2011; 16: 598–603. Podschun R, Ullmann U. Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin. Microbiol. Rev. 1998; 11: 589–603. Lowe C, Willey B, O’Shaughnessy A, Lee W, Lum M, Pike K, Larocque C, Dedier H, Dales L, Moore C et al. Outbreak of extended-spectrum beta-lactamase-producing Klebsiella oxytoca infections associated with contaminated handwashing sinks(1). Emerg. Infect. Dis. 2012; 18: 1242–7. Kim BN, Ryu J, Kim YS, Woo JH. Retrospective analysis of clinical and microbiological aspects of Klebsiella oxytoca bacteremia over a 10-year period. Eur J Clin Microbiol Infect Dis 2002; 21: 419–26. Sahly H, Podschun R. Clinical, bacteriological, and serological aspects of Klebsiella infections and their spondylarthropathic sequelae. Clin. Diagn. Lab. Immunol. 1997; 4: 393–9. Stock I, Wiedemann B. Natural antibiotic susceptibility of Klebsiella pneumoniae, K. oxytoca, K. planticola, K. ornithinolytica and K. terrigena strains. J. Med. Microbiol. 2001; 50: 396–406. eTG. Antibiotic Expert Groups. Therapeutic Guidelines: Antibiotic. Version 15. Therapeutic Guidelines Limited, Melbourne, 2014. [Accessed 17 November 2014]. Available from URL: http:// www.tg.org.au/?sectionid=41
Respirology (2015) 20, 507–509
Copyright of Respirology is the property of Wiley-Blackwell and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
