esbl infections in the united states 1213 Among device-related hospital-onset infections reported to
the National Healthcare Safety Network in 2006–2007, the incidence rates of extended-spectrum cephalosporin-resistant infections were 0.064 cases per 1,000 device days for ventilator- associated pneumonia, 0.061 cases per 1,000 device days for catheter-associated urinary tract infections, and 0.051 cases per 1,000 device days for catheter-associated bloodstream infec- tions.19 Soe et al23 used National Healthcare Safety Network data from 2011 to report incidence rates of central-line–asso- ciated bloodstream infections from intensive care units within 25 US states. The incidence by state ranged from 0 to 0.37 infections per 1,000 central-line days.23 Among patients from community hospitals in North Carolina, most of both the ESBL-E. coli (82.7%) and ESBL-Klebsiella (71.1%) infections were community-onset infections, and approximately half of the patients in each group were nursing home residents (ESBL- E. coli,51.9%; ESBL-Klebsiella, 50.0%).17 From 2005 to 2009, Han et al18 did not observe a significant difference in hospital- onset ESBL-E. coli and ESBL-Klebsiella infections (1.08–1.23 cases per 10,000 patient days; P=.51), even though this study focused on an intervention to reduce hospital-onset infection rates, perhaps the increased rate was due to the intense screening of the urine samples.18 Similarly, during that same period, Swami et al25 did not observe a significant difference in either hospital-onset (range, 0–1 per 100,00 person-years; P=.98) or hospital-associated (range, 4–7 per 100,00 person years; P=.14) ESBL-E. coli bacteriuria rates. However, a significant difference was observed for community-onset ESBL infections (range, 6–14 per 100,000 person years; P=.01).25
discussion
This systematic literature review examined the incidence of ESBL-E. coli and ESBL-Klebsiella infections among the US population. Even with an increasing trend, incidence rates varied among the included studies. The variation is potentially due to differences in defining ESBL-producing organisms. Identifying true ESBL incidence rates can be challenging because laboratories need to specifically test for ESBLs, which may not occur on all E. coli and Klebsiella isolates and may vary throughout the study period. Second, inconsistencies existed among the patient populations included in the studies. Some of the studies exam- ined neonates, while others included older adults. Furthermore, the populations included were from various regions throughout the United States. Castanheira et al26 also found differences in rates between US census regions when examining the proportion of ESBL-E. coli or ESBL-Klebsiella pneumonia over all E. coli or Klebsiella pneumonia isolates.26 For E. coli, ESBL rates ranged from 5.2% to 20.1%, and for Klebsiella pneumonia,rates ranged from 3.2% to 34.7%, with the lowest rates reported in the West North Central region and the highest rates in the Mid-Atlantic region.26 Many articles were excluded from our systematic literature
review because they did not report an appropriate denominator to calculate incidence rates. Instead, these studies reported the
proportion of isolates that were identified as ESBL-producing among the total number of isolates for that organism (eg, resistance rates). Thus, without uninfected population denominators, increases in ESBL might be due to increases in ESBL producers, all strains of that organism or both. Therefore, only estimates with population-level denominators that include uninfected patients accurately report incidence rates. In general, ESBL infections have increased from 1997 to
2011, with a slightly higher incidence rate for ESBL-Klebsiella infections compared with ESBL-E. coli infections. Other studies not included in this systematic literature review also reported increased ESBL infections when examining the proportion E. coli and Klebsiella that are ESBL producing. The SENTRY Antimicrobial Surveillance Program reported the ESBL phenotype in7%of the 2,768 Klebsiella isolates tested in 1997–2000 from 30 US hospitals.12 In 2011–2013, the proportion of Klebsiella isolates with an ESBL phenotype increased to 15% (840 of 5,580) among isolates collected from 79 US hospitals.13 Among E. coli isolates, 2 national surveil- lance programs (SENTRY Antimicrobial Surveillance Program and The Surveillance Network) reported a proportion of ESBL phenotype isolates around 1%–8% in 1997–2000, while in 2011–2013, the International Network for Optimal Resistance Monitoring program reported an increased proportion of 12% among isolates collected from US hospitals.13–15 Studies included in our analysis reported statistically significant
increasing incidence rates for community-onset ESBL infections, while this was not frequently observed among hospital-onset ESBL infections.18,25 A recent systematic review of the prevalence of ESBL fecal colonization among healthy individuals reported 14% colonization worldwide, with a 2% rate in the Americas.27 Therefore, ESBL infectionsmay be increasingmore rapidly within the community setting. However, the definitions of community- onset infections and hospital-onset infections differed throughout the studies, making direct comparisons difficult. This study had several limitations. First, the quality of any systematic literature review is reflected by the conditions of the studies included. Second, publication bias may be present because studies that reported an increase in ESBL infection rates may be more likely to be published compared with studies that found no change. In addition, we only included studies from the United States; therefore, our results may not be generalizable to other countries. In conclusion, the incidence rates of ESBL-E. coli and ESBL- Klebsiella infections are increasing throughout the United States. These findings may inform empiric antimicrobial treatment, and tracking the emergence of these infections is critically important for guiding antimicrobial stewardship and infection control programs. ESBL-containing bacteria are important targets for emerging state and national surveillance systems and multicenter or nationwide studies are needed to estimate current incidence rates. Without proper estimates for the burden of ESBL infections and other multidrug-resistant pathogens, it remains difficult to appropriately target research and prevention efforts.
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