Infectious Diseases

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Characteristics and outcomes of Klebsiella pneumoniae bacteraemia in Hong Kong Carrie K. Y. Pau, Florence F. T. Ma, Margaret Ip & Joyce H. S. You To cite this article: Carrie K. Y. Pau, Florence F. T. Ma, Margaret Ip & Joyce H. S. You (2015) Characteristics and outcomes of Klebsiella pneumoniae bacteraemia in Hong Kong, Infectious Diseases, 47:5, 283-288 To link to this article: http://dx.doi.org/10.3109/00365548.2014.985710

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Date: 05 November 2015, At: 13:47

Infectious Diseases, 2015; 47: 283–288

ORIGINAL ARTICLE

Characteristics and outcomes of Klebsiella pneumoniae bacteraemia in Hong Kong

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CARRIE K. Y. PAU1, FLORENCE F. T. MA1, MARGARET IP2 & JOYCE H. S. YOU1 From the 1School of Pharmacy and 2Department of Microbiology, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, NT, Hong Kong

Abstract Background: We compared clinical outcomes between patients with healthcare-associated and community-acquired Klebsiella pneumoniae bacteraemia and identified predictors associated with mortality and high treatment cost in Hong Kong. Methods: This was a retrospective cohort study of patients with K. pneumoniae bacteraemia in a teaching hospital. Adult patients with K. pneumoniae in blood cultures were included. Demographics and clinical data were retrieved from medical records. Results: The analysis included 208 patients. The mean age was 68.6 ⫾ 16.8 years. The Pitt bacteraemia score was 2.2 ⫾ 2.8. In all, 54.8% cases were healthcare-associated infections. The 30-day mortality rate was 32.7%. The mortality rate of patients with healthcare-associated bacteraemia was significantly higher than for community-acquired cases (p ⬍ 0.001). Extended-spectrum β-lactamase (ESBL)-producing K. pneumoniae accounted for 15.4% of cases. Intraabdominal infection was the most common infection (32.7%). Prior use of immunosuppressive agents and antimicrobial therapy were two major predisposing factors for infection. The treatment cost was USD12 282 ⫾ 11 751 and the length of hospitalization was 9.0 ⫾ 6.7 days. Multivariate analysis showed that liver disease (odds ratio (OR) ⫽ 3.06; 95% confidence interval (CI) ⫽ 1.38–6.78), malignancy (OR ⫽ 6.86; 95% CI ⫽ 3.25–14.48), pneumonia (OR ⫽ 5.25; 95% CI ⫽ 2.05–13.41) and Pitt score ⬎ 1 (OR ⫽ 2.50; 95% CI ⫽ 1.25–5.00) were associated with mortality. Malignancy (OR ⫽ 2.94; 95% CI ⫽ 1.33– 6.49), Pitt score ⬎ 1 (OR ⫽ 4.15; 95% CI ⫽ 1.87–9.24) and age ⬍ 72 years (OR ⫽ 2.86; 95% CI ⫽ 1.35–5.88) were associated with high treatment cost. Conclusions: The 30-day mortality and treatment cost of patients with K. pneumoniae bacteraemia were high in Hong Kong. Based upon the risk factors identified, infection control and treatment algorithms for K. pneumoniae bacteraemia in patients with malignancy or liver disease are highly warranted.

Keywords: Klebsiella pneumoniae, bacteraemia, mortality, cost, Hong Kong

Introduction Klebsiella pneumoniae is a common cause of nosocomial infections in the urinary tract, the respiratory tract and intra-abdominal sites [1,2]. High mortality rates ranging from 20% to 40% were reported in patients with K. pneumoniae bacteraemia, despite the lack of discrimination of attributable mortality of bacteraemia in most reports [2–4]. A worldwide collaborative study found that pneumonia was the major source of K. pneumoniae bacteraemia among patients in Taiwan and South Africa, whereas urinary tract infection was frequently reported to

be the origin of K. pneumoniae bacteraemia in other countries [1]. The study for Monitoring Antimicrobial Resistance Trends (SMART) found that the proportion of extended-spectrum β-lactamase (ESBL)-producing K. pneumoniae was 17% but varied geographically [5]. Despite the high mortality rate reported worldwide, data on characteristics, risk factors and outcomes of patients with K. pneumoniae bacteraemia in Hong Kong are lacking to facilitate the development of infection control guidelines and treatment strategies. The objectives of the present study were to

Correspondence: Joyce H. S. You PharmD BCPS (Infectious Diseases), Associate Professor, School of Pharmacy, Faculty of Medicine, Chinese University of Hong Kong, Shatin, NT, Hong Kong. Tel: ⫹ 852 3943 6830. Fax: ⫹ 852 2603 5295. E-mail: [email protected] (Received 20 August 2014 ; accepted 28 October 2014 ) ISSN 2374-4235 print/ISSN 2374-4243 online © 2015 Informa Healthcare DOI: 10.3109/00365548.2014.985710

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describe patient characteristics, compare clinical outcomes between patients with healthcare-associated and community-acquired K. pneumoniae bacteraemia, and identify predictors associated with mortality and high treatment cost in a teaching hospital in Hong Kong.

Materials and methods

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Study design This was a retrospective study conducted at a 1300bed teaching hospital in Hong Kong. The study period was 1 June 2009 to 31 December 2011. Patients aged 18 years or above with K. pneumoniae in blood cultures were included. The study protocol was approved by the Joint Chinese University of Hong Kong and New Territories East Cluster Clinical Research Ethics Committee. Data were retrieved from electronic patient records and medical charts. Patient demographics, comorbidities and clinical and microbiologal data of the present infection as well as antimicrobial treatment were collected. Infection was classified as either healthcare-associated or community-acquired. Healthcare-associated infection was defined as: (1) infection occurred ⬎ 48 h after hospital admission, or (2) in a patient who was either hospitalized or living in a nursing home within 2 weeks before the present episode [6]. Empirical treatment was defined as the antimicrobial agents used before culture and sensitivity results were available [7]. Predisposing factors for bacteraemia were collected, including nursing home stay within 48 h, use of immunosuppressive agents (including chemotherapy and corticosteroids) within 30 days and invasive procedure within 48 h. Other predisposing factors were the presence of central venous catheter, urinary catheter, mechanical ventilation or nasogastric tube for more than 48 h, and use of antimicrobial agents for more than 72 h within 2 weeks before bacteraemia. Severity of bacteraemia was assessed by the Pitt score based on body temperature, blood pressure, mechanical ventilation, cardiac arrest and mental status within 48 h of blood sample collection. The highest point score within the duration was used [8]. Outcome measurements The primary outcomes were 30 day mortality rate and infection-related direct medical cost (IR-cost) for management of K. pneumoniae bacteraemia. The number of cases isolated with ESBL-producing K. pneumoniae was determined. The cost analysis was conducted from the perspective of healthcare provid-

ers. IR direct medical cost was determined for each study patient from antimicrobial usage, hospitalization and laboratory and diagnostic tests during the infection-related length of hospital stay (IR-LOS). IR-LOS in hospital was defined as the duration between onset of bacteraemia and end of antimicrobial therapy, discharge, or death, whichever occurred first. Unit cost of different hospital wards (such as medical and intensive care) and diagnostic and laboratory tests in public hospitals were calculated from the charges of public hospitals listed in the Hong Kong Government Gazette [9]. Costs of antimicrobial agents were obtained from the drug acquisition costs of the study hospital. All costs were adjusted to 2014 costs. Statistical analysis Data were analysed using SPSS 16.0 (SPSS Inc., Chicago, IL, USA). Categorical variables were presented as numbers and percentages, whereas continuous variables were presented as mean ⫾ standard deviation (SD). Categorical variables were tested with chi-squared test or Fisher’s exact test, as appropriate. To determine predictors of mortality and high IR-cost, univariate analysis was performed on demographic and clinical factors (age, Pitt score, concurrent infections, comorbidities, drug resistance and sensitivity of K. pneumoniae to empirical treatment) with a frequency of ⱖ 5%. Factors found to have correlations (p ⱕ 0.1) with mortality rate or IR-cost were further analysed by multiple logistic regression using a stepwise backward model. Factors with a two sided p value of ⱕ 0.05 were considered as significant predictors. Results Patient demographics The demographics of 208 patients with K. pneumoniae bacteraemia are shown in Table I. The mean age was 68.6 ⫾ 16.8 years and 51.9% (108/208) were male. The mean Pitt bacteraemia score was 2.2 ⫾ 2.8. Cardiovascular diseases were the most common underlying diseases in 52.4% (109/208) of patients. Healthcare-associated infections were identified in 54.8% (114/208) of cases and 45.2% (94/208) were community-acquired cases. Intra-abdominal infection was most common and was reported in 32.7% (68/208) of patients, followed by primary bacteraemia in 29.3% (61/208) and urinary tract infection in 20.2% (42/208). Before the onset of bacteraemia, 18.8% (39/208) of patients used immunosuppressive agents, 16.8% (35/208) received prior antimicrobial therapy and 14.4% (30/208) had a urinary catheter.

Klebsiella pneumoniae bacteraemia Table I. Patient demographics (n = 208).

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Characteristic Male Mean age (SD) (years) Mean Pitt bacteraemia score (SD) Comorbidities Cardiovascular disease Malignancy Diabetes mellitus Biliary disease Liver disease Renal disease Neurologic disease Respiratory disease Joint disease Infections Intra-abdominal infection Primary bacteraemia Urinary tract infection Pneumonia Neutropenic fever Skin or soft tissue infection Pancreatitis Healthcare-associated infections Community-acquired infections Predisposing factors for K. pneumoniae bacteraemia Immunosuppressive agents within 30 days Antimicrobials used for ⬎ 72 h within 2 weeks Urinary catheter presence for ⬎ 48 h within 2 weeks Old age home residence within 2 days Previous invasive procedure within 2 days Presence of Reye’s tube feeding for ⬎ 48 h within 2 weeks

No. of patients (%) 108 (51.9) 68.6 (16.8) 2.2 (2.8) 109 97 60 57 48 44 33 28 20

(52.4) (46.6) (28.8) (27.4) (23.1) (21.2) (15.9) (13.5) (9.6)

68 61 42 33 9 3 2 114 94

(32.7) (29.3) (20.2) (15.9) (4.3) (1.4) (1.0) (54.8) (45.2)

39 (18.8) 35 (16.8) 30 (14.4) 23 (11.1) 21 (10.1) 11 (5.3)

Drug resistance of Klebsiella isolates Overall, 15.4% (32/208) of patients were infected with ESBL-producing K. pneumoniae. The percentages of ESBL-producing K. pneumoniae infections in healthcare-associated versus community-acquired cases were 21% (24/114) and 8.5% (8/94), respectively (p ⫽ 0.013). Two (6.3%) of the ESBL-producing strains had multi-drug resistance, which was defined as resistance to cephalosporins, fluoroquinolones and aminoglycosides [10]. All K. pneumoniae isolates were susceptible to carbapenem. Empirical treatment Empirical antimicrobial therapy was administered to 98.1% (204/208; 4 patients did not receive antimicrobial therapy due to rapid death) of patients and isolated bacteria were sensitive to the empirical antibiotics in 87.1% (27/31) of cases with ESBL-producing bacteria and in 79.8% (138/173) of cases with non-ESBL-producers (p ⫽ 0.323). Amoxicillin/ clavulanate was the most commonly used empirical

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agent (43.1%, 88/204) and 26.5% (54/204) of cases received cefuroxime. Antipseudomonal agents (including aminoglycosides, carbapenems, cefoperazone/sulbactam, ceftazidime, cefepime, ciprofloxacin and piperacillin/tazobactam) were used in 25.5% (52/204) of patients. Ceftriaxone and cefotaxime were administered to 9.8% (20/204). Outcome measures The clinical and economic outcomes are shown in Table II. The 30-day mortality rate was 32.7% (68/208). Of all deaths, 35.3% (24/68) occurred within 72 h after hospitalization and 14.7% (10/68) occurred in the intensive care unit. The mortality rate in patients with healthcare-associated bacteraemia was significantly higher than in cases with community-acquired infection (p ⬍ 0.001), while no significant difference in mortality rate was found between cases with ESBL- and non-ESBL-producing strains. The overall IR-LOS was 9.0 ⫾ 6.7 days, and patients who survived had a significantly longer IR-LOS than those who expired (p ⬍ 0.001). The mean IR-cost for treatment of K. pneumoniae bacteraemia was USD12 282 ⫾ 11 751 (USD1 ⫽ HKD7.8). The mean cost of cases with ESBL-producing K. pneumoniae was higher than the mean cost of cases with nonESBL-producing K. pneumoniae, but the difference was not statistically significant (p ⫽ 0.382). Predictors of mortality and high treatment cost Of 208 patients, 4 patients did not receive antimicrobial therapy due to rapid death after onset of bacteraemia and data were missing for Pitt score estimation in 1 patient. These five patients were excluded from the multiple regression analysis of mortality. The 30-day mortality rate was associated with eight factors in univariate analysis (p ⬍ 0.10). Multiple logistic regression analysis of these factors showed Table II. Outcomes of K. pneumoniae bacteraemia. Factor 30-day mortality Healthcare-associated Community-acquired ESBL-producing Non-ESBL-producing IR-LOS (days) Survived Death IR-cost (USD) ESBL-producing Non-ESBL-producing

n (%) 68/208 (32.7) 49/114 (43.0) 19/94 (20.2) 8/32 (25.0) 60/176 (34.1) 9.0 ⫾ 6.7 10.3 ⫾ 6.3 8.0 ⫾ 7.5 12 282 ⫾ 11 751 16 026 ⫾ 20 634 11 602 ⫾ 71 859

p value

⬍ 0.001 0.322

⬍ 0.001

0.382

ESBL, extended spectrum β-lactamase; IR-cost, infection-related cost (USD1 ⫽ HKD7.8); IR-LOS, infection-related length of stay.

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C. K. Y. Pau et al. Table III. Factors associated with 30-day mortality ratea.

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Univariate analysisb Concurrent infections Pneumonia Urinary tract infection Comorbidities Cardiovascular disease Liver disease Malignancy Pitt score ⬎ 1 Primary empirical antibiotic Antipseudomonal antibiotic ESBL-producing K. pneumoniae Multiple logistic regression analysis

Death (n ⫽ 64)

Survival (n ⫽ 139)

17 (26.6%) 6 (9.4%)

13 (9.4%) 36 (25.9%)

27 20 45 34

79 28 48 50

(42.2%) (31.3%) (70.3%) (53.1%)

23 (35.9%) 14 (21.9%)

0.001 0.007

(56.8%) (20.1%) (34.5%) (36.0%)

0.052 0.084 ⬍ 0.001 0.021

28 (20.1%) 18 (12.9%)

0.016 0.105

OR (95% CI) 2.50 (1.25–5.00) 3.06 (1.38–6.78) 5.25 (2.05–13.41) 6.86 (3.25–14.48)

Pitt score ⬎ 1 Liver disease Pneumonia Malignancy

p value

0.010 0.006 0.001 ⬍ 0.001

CI, confidence interval; ESBL, extended spectrum β-lactamase; OR, odds ratio. mortality rate of 203 patients who received antimicrobial therapy and had data for Pitt score calculation. bFactors correlating with 30-day mortality rate with p ⬍ 0.10. a30-day

that liver disease (odds ratio (OR) ⫽ 3.06; 95% confidence interval (CI) ⫽ 1.38–6.78), malignancy (OR ⫽ 6.86; 95% CI ⫽ 3.25–14.48), pneumonia (OR ⫽ 5.25; 95% CI ⫽ 2.05–13.41) and Pitt score ⬎ 1 (OR ⫽ 2.50; 95% CI ⫽ 1.25–5.00) were significant predictors of mortality (Table III). Univariate and multiple analyses were conducted on data from 139 patients who survived (1 surviving

patient without data for Pitt score was excluded) to identify predictors associated with high IR-cost (Table IV). High IR-cost was defined as ⬎ USD9117 (the median IR-cost of the surviving cohort). Malignancy (OR ⫽ 2.94; 95% CI ⫽ 1.33–6.49), Pitt score ⬎ 1 (OR ⫽ 4.15; 95% CI ⫽ 1.87–9.24) and age ⬍ 72 years (median age) (OR ⫽ 2.86; 95% CI ⫽ 1.35–5.88) were predictors of high IR-cost.

Table IV. Factors associated with infection-related costa.

Univariate

analysisb

Neurological disease Malignancy Pitt score ⬎ 1 Age ⬎ 72 years Choice of empirical antimicrobial therapy Antimicrobials with antipseudomonal activityd ⬎ 90% K. pneumoniae isolates were sensitivee Multiple logistic regression analysis Age ⬍ 72 years Malignancy Pitt score ⬎ 1 aIR-cost

High IR-cost (n ⫽ 69) 8 31 34 24

(11.6%) (44.9%) (49.3%) (34.8%)

19 (27.5%) 10 (14.5%) OR (95% CI) 2.86 (1.35–5.88) 2.94 (1.33–6.49) 4.15 (1.87–9.24)

Low IR-costc (n ⫽ 70) 16 17 16 40

p value

(22.9%) (24.3%) (22.9%) (57.1%)

0.079 0.010 0.001 0.008

9 (12.9%) 4 (5.7%)

0.031 0.086

0.006 0.008 ⬍ 0.001

(infection-related cost) of 139 surviving patients who received antimicrobial therapy and had data for Pitt score calculation. bFactors correlating with IR-cost with p ⬍ 0.10 cHigh IR-cost was defined as ⬎ USD9 672; low IR-cost was defined as ⱕ USD9672. dAntimicrobials with antipseudomonal activity included aminoglycoside, carbapenem, cefoperazonesulbactam, ceftazidime, cefepime, ciprofloxacin, piperacillin-tazobactam. eAgents to which ⬎ 90% of K. pneumoniae isolates were sensitive (retrieved from antibiogram data of the study hospital).

Klebsiella pneumoniae bacteraemia

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Discussion High mortality rate was found in the present cohort of patients with K. pneumoniae bacteraemia. The 30-day mortality rate was 32.7% and 15.4% of the K. pneumoniae isolates were ESBL-producing strains. These results are consistent with the mortality rate of 33.2% and 16.7% for ESBL-producing K. pneumoniae reported by Kang et al. in Korea [4,11]. The most commonly documented infections in the present cohort were intra-abdominal infection, primary bacteraemia and urinary tract infection, similar to previously identified sources of K. pneumoniae bacteraemia [12]. The present study showed that liver disease, malignancy and pneumonia were positive predictors of mortality in patients with K. pneumoniae bacteraemia, similar to reports from Canada, Taiwan and Korea [2,4,12]. Patients with a Pitt score ⬎ 1 had higher mortality, in accordance with data from Taiwan (OR ⫽ 1.07; 95% CI ⫽ 1.01–1.14) [13]. The mortality rate in healthcare-associated cases was significantly higher than in community-acquired bacteraemia, while ESBL bacteraemia was not significantly associated with mortality in the present study. Previous studies were inconclusive regarding the impact of ESBL-producing strains on mortality. ESBL bacteraemia had a significant association with higher mortality in some [3,5,14,15] but not in all settings [2,11,14–18].The lack of association between ESBL-producing K. pneumoniae bacteraemia and mortality in the present cohort could possibly be due to the relatively high percentage of ESBL-producing isolates (⬎ 87%) being susceptible to empirical treatment. Blot et al. suggested that the difference in mortality of ESBL infection reported by different studies could be related to the confounding effect of appropriateness of therapy. They suggested that if the appropriateness of therapy was controlled, ESBL infection did not have excess mortality [19]. The use of antipseudomonal antimicrobials as empirical treatment was associated with mortality in univariate analysis, but was not a significant factor in the multiple logistic analysis. The impact of using an empirical agent to which ⬎ 90% of K. pneumoniae isolates were sensitive (according to hospital antibiogram) as initial empirical therapy was also examined against mortality and no significant association was found in univariate analysis. The selection of empirical treatment is usually influenced by underlying diseases and severity of the present infection. Prescribers tend to use broad-spectrum (including antipseudomonal) antimicrobials empirically in patients with malignancy or signs of sepsis [20]. Our multiple logistic analysis further showed that the selection of antipseudomonal agents for empirical treatment was not an independent factor associated

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with mortality. Isolation of multidrug-resistant gramnegative bacteria was reported to be associated with increased mortality in hospital-acquired bloodstream infections in a multicentre cohort study in intensive care units [21]. The risk of multidrug resistance was not significant in our cohort, owing to the low incidence (2/208) of multidrug-resistant K. pneumoniae. This is the first study to report the treatment cost of K. pneumoniae bacteraemia in a hospital setting in Hong Kong. The mean IR-cost for management of K. pneumoniae bacteraemia was USD12 282 ⫾ 11 751. It was comparable to the IR-cost of Acinetobacter baumanii bacteraemia (USD11 660 ⫾ 10 493 adjusted to year 2014 cost with discounted rate of 3%) in Hong Kong [22]. A case-control study in Hong Kong reported that the IR-cost for bacteraemia caused by ESBL-producing Escherichia coli (USD6551 ⫾ 5678) was significantly higher than for cases with non-ESBLproducing bacteria (USD3885 ⫾ 2491) (p ⫽ 0.003) [23]. Higher cost was observed in the subgroup with ESBL-producing K. pneumoniae in the present cohort, yet the difference in cost between ESBL-producing and non-ESBL-producing subgroups did not achieve statistical significance. The IR-cost of survivors was examined for predictors of higher treatment cost. The patients who did not survive the infection were excluded from the univariate and multivariate analyses to avoid the confounding effect of mortality. Malignancy, Pitt score ⬎ 1 and age ⬍ 72 years were predictors of high IR-cost. Severity of bacteraemia indicated by a high Pitt score and presence of malignancy would contribute to higher consumption of healthcare resources. Being younger than median age (⬍ 72 years) was associated with higher cost and seems to be related to a more aggressive management approach used by clinicians in the younger cohort, resulting in a higher resource utilization [20]. The present study was limited by the retrospective study design and small sample size. A multiple logistic regression method was used to control potential confounding effects on the outcome analyses. Despite the high mortality rate reported for patients with Klebsiella bacteraemia in the literature, the attributable mortality was low [24]. The present study only included patients with K. pneumoniae bacteraemia and did not include a matching control group (patients without K. pneumoniae bacteraemia). Excess mortality of K. pneumoniae bacteraemia was therefore not determined in the present analysis. In conclusion, the 30-day mortality and treatment costs of patients with K. pneumoniae bacteraemia were high in Hong Kong. Malignancy, liver disease, Pitt score ⬎ 1 and pneumonia were predictors of mortality. High treatment cost was associated with malignancy, Pitt score ⬎ 1 and age ⬍ 72 years.

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Our findings support the implementation of infection control and treatment algorithms for K. pneumoniae bacteraemia in patients with malignancy or liver disease. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

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Characteristics and outcomes of Klebsiella pneumoniae bacteraemia in Hong Kong.

We compared clinical outcomes between patients with healthcare-associated and community-acquired Klebsiella pneumoniae bacteraemia and identified pred...
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