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Vital Signs: Containment of Novel Multidrug-Resistant Organisms and Resistance Mechanisms — United States, 2006–2017

Vital Signs: Containment of Novel Multidrug-Resistant Organisms and Resistance Mechanisms —... Background: Approaches to controlling emerging antibiotic resistance in health care settings have evolved over time. When resistance to broad-spectrum antimicrobials mediated by extended-spectrum β-lactamases (ESBLs) arose in the 1980s, targeted interventions to slow spread were not widely promoted. However, when Enterobacteriaceae with carbapenemases that confer resistance to carbapenem antibiotics emerged, directed control efforts were recommended. These distinct approaches could have resulted in differences in spread of these two pathogens. CDC evaluated these possible changes along with initial findings of an enhanced antibiotic resistance detection and control strategy that builds on interventions developed to control carbapenem resistance. Methods: Infection data from the National Healthcare Safety Network from 2006–2015 were analyzed to calculate changes in the annual proportion of selected pathogens that were nonsusceptible to extended-spectrum cephalosporins (ESBL phenotype) or resistant to carbapenems (carbapenem-resistant Enterobacteriaceae [CRE]). Testing results for CRE and carbapenem-resistant Pseudomonas aeruginosa (CRPA) are also reported. Results: The percentage of ESBL phenotype Enterobacteriaceae decreased by 2% per year (risk ratio [RR] = 0.98, p<0.001); by comparison, the CRE percentage decreased by 15% per year (RR = 0.85, p<0.01). From January to September 2017, carbapenemase testing was performed for 4,442 CRE and 1,334 CRPA isolates; 32% and 1.9%, respectively, were carbapenemase producers. In response, 1,489 screening tests were performed to identify asymptomatic carriers; 171 (11%) were positive. Conclusions: The proportion of Enterobacteriaceae infections that were CRE remained lower and decreased more over time than the proportion that were ESBL phenotype. This difference might be explained by the more directed control efforts implemented to slow transmission of CRE than those applied for ESBL-producing strains. Increased detection and aggressive early response to emerging antibiotic resistance threats have the potential to slow further spread. Introduction remained susceptible to some first-line therapies, including The emergence and spread of antibiotic resistance threat- carbapenems. In general, facilities independently selected ens to outpace the development of new antimicrobials, and approaches to control spread, which often included core slowing the spread of these organisms has become a priority. infection control practices, such as hand hygiene, and placing Among Enterobacteriaceae, the family of pathogens most patients with ESBL-producing strains in single rooms under frequently associated with health care–associated infec- Contact Precautions. tions (1), resistance to the broad-spectrum antimicrobials Enterobacteriaceae resistance to even broader spectrum extended-spectrum cephalosporins and carbapenems has been antimicrobials, including carbapenems, was reported with driven largely by the spread of plasmid-mediated resistance increasing frequency beginning in 2001 (3). Rapid spread of genes encoding extended-spectrum β-lactamases (ESBLs) these carbapenem-resistant Enterobacteriaceae (CRE) in parts and carbapenemases, respectively. In the United States, of the United States and other countries (4,5) highlighted a ESBL-producing Enterobacteriaceae were first reported in need to more aggressively control CRE transmission. In 2009, 1988 (2). The emergence of these ESBL-producing isolates CDC created CRE-specific guidance, which was endorsed limited the options available for treatment, but these organisms by the Healthcare Infection Control Practices Advisory 396 MMWR / April 6, 2018 / Vol. 67 / No. 13 US Department of Health and Human Services/Centers for Disease Control and Prevention Morbidity and Mortality Weekly Report Committee (6). This guidance included recommendations bloodstream infections (CLABSIs) and catheter-associated for additional interventions when CRE was identified at a urinary tract infections (CAUTIs) associated with Escherichia health care facility, including laboratory surveillance of clinical coli or Klebsiella pneumoniae and reported to CDC’s National cultures and targeted patient screening to identify health care Healthcare Safety Network (NHSN) during 2006–2015 from contacts with asymptomatic colonization. This CRE-specific adult medical, surgical, or medical/surgical intensive care units guidance was updated in 2013 and 2015 (https://www.cdc.gov/ at short-stay acute care hospitals. The Centers for Medicare & hai/organisms/cre/cre-toolkit/index.html) and was highlighted Medicaid Services’ (CMS) Hospital Inpatient Quality Reporting by CDC in a 2013 report (7). Program mandated reporting of CLABSI and CAUTI data to In 2017, CDC outlined a new effort to react rapidly to novel NHSN starting in 2011 and 2012, respectively; data from previ- multidrug-resistant organisms (8); this approach includes ous years represent voluntary reporting or reporting to comply encouraging health care facilities and public health authorities with state or local mandates. National pooled mean percentages to respond to single isolates of an emerging antibiotic-resistant for Enterobacteriaceae with CRE phenotype (isolates resistant pathogen. The strategy rests on these five pillars: 1) rapid detec- to imipenem, meropenem, doripenem, or ertapenem), and tion of targeted pathogens and their resistance mechanisms, ESBL phenotype (isolates that tested intermediate or susceptible 2) on-site infection control assessments by trained experts to to carbapenems and intermediate or resistant to ceftazidime, identify gaps in infection prevention, 3) screening of exposed cefepime, ceftriaxone, or cefotaxime) were calculated. Log bino- contacts to identify asymptomatic colonization, 4) coordina- mial regression models were used to estimate the average annual tion of the response among facilities, and 5) continuing these change in the proportion of E. coli and K. pneumoniae that had interventions until transmission is controlled. Detection and a CRE or ESBL phenotype. P-values <0.05 were considered control efforts can extend from the index facility to other statistically significant. Sensitivity analyses were performed to facilities that share patients. account for the change in hospitals reporting to NHSN each To support this approach, CDC established the Antibiotic year. The results of the log binomial regression model were Resistance Laboratory Network (ARLN) (https://www.cdc. confirmed by a robust variance Poisson model. gov/drugresistance/solutions-initiative/ar-lab-networks.html) Enhanced detection and response. CRE and CRPA to improve national capacity to rapidly detect and respond to (P. aeruginosa resistant to imipenem, meropenem, or doripe- antibiotic resistance. ARLN provides carbapenemase testing nem) isolates were submitted to ARLN laboratories for test- for two emerging antibiotic resistant pathogens, CRE and ing for carbapenemases. Among Enterobacteriaceae, E. coli, carbapenem-resistant Pseudomonas aeruginosa (CRPA), at K. oxytoca, K. pneumoniae, and Enterobacter spp. were targeted 56 state and local public health laboratories and screening for for submission. Testing at ARLN laboratories included car- asymptomatic CRE and CRPA carriage at seven regional labo- bapenemase production testing and molecular detection of ratories (9). Carbapenemase-producing strains were targeted genes encoding for the five carbapenemases of primary public for detection and response in part because of their previously health concern: Klebsiella pneumoniae carbapenemase (KPC), demonstrated propensity for spread. CDC also expanded fund- New Delhi metallo-beta-lactamase (NDM), Verona integron ing to state and local health departments to increase capacity encoded metallo-beta-lactamase (VIM), imipenemase (IMP), and build expertise in responding to these and other emerging and oxacillinase-48-like carbapenemase (OXA-48). ARLN antibiotic resistance threats. laboratories were asked to report positive findings to local For this report, data from a national health care–associated public health authorities and CDC within 1 day and to submit infections surveillance system were reviewed to determine if testing summaries to CDC monthly. the more directed approach applied for CRE was associated For each carbapenemase-producing isolate detected, CDC with differences in the percentage of Enterobacteriacae health guidance recommends that state health department staff care–associated infections that were CRE compared with those members contact the health care facility to review infection that had the ESBL phenotype. In addition, findings from the control measures and consider performing on-site infection first 9 months of the enhanced response to emerging resistant control assessments. If indicated, contacts of the index patient organisms are described. are screened to detect transmission; testing capacity for this screening is provided through ARLN. Response activities con- Methods tinue until transmission is controlled. Screening results were stratified by whether the screening took place in a short-stay Percentage of Enterobacteriaceae with CRE or ESBL phe- acute care hospital or a post–acute care facility (i.e., long-term notypes in the National Healthcare Safety Network, 2006– acute care hospital or nursing home). 2015. Included in the analysis were central line–associated US Department of Health and Human Services/Centers for Disease Control and Prevention MMWR / April 6, 2018 / Vol. 67 / No. 13 397 Morbidity and Mortality Weekly Report 13 days. The percentage of carbapenemase-producing isolates Results varied by organism and was highest among Klebsiella species Percentage of Enterobacteriaceae with CRE or ESBL phe- (65%). Among carbapenemase-producing CRE, the most notypes in the National Healthcare Safety Network, 2006– commonly identified carbapenemase was KPC (1,232 of 1,401 2015. Among short-stay acute care hospitals, the percentage of isolates, 88%); VIM was the most common carbapenemase Klebsiella and E. coli isolates with the ESBL phenotype remained identified in CRPA (18 of 25, 72%) (Table 1). relatively stable, ranging from 17.6% (116 of 659 isolates) in To identify asymptomatically colonized health care contacts 2006 to 16.5% (694 of 4,211) in 2015, with a peak of 18.9% of index patients, 1,489 screening tests for carbapenemases in 2009 (Figure 1). The percentage of CRE declined from 8.8% were performed during 70 surveys (defined as all screening (35 of 397 isolates) in 2006 and 10.6% (64 of 604) in 2007 to tests performed at a single facility within a 14-day period) 3.1% (115 of 3,718) in 2015 (Figure 2). During 2006–2015, in 50 facilities. A median of 10.5 contacts (interquartile the annual percentage of isolates with the ESBL phenotype range = 2–25) were screened per survey. Overall, 11% of declined an average of 2% (RR = 0.98, p = 0.009); during the screening tests were positive for at least one of the five carbapen- same period, the proportion that were CRE decreased 15% per emases of primary public health concern (Table 2). A higher year (RR = 0.85, p<0.001). Results were unchanged when the percentage of post–acute care facility contacts screened positive analysis was limited to facilities that reported in all years. for carbapenemases (14% [147 of 1,074 contacts]) than did Enhanced detection of and response to carbapenemase- contacts from short-stay acute care hospitals (5.8% [21 of 365]) producing organisms. During the first 9 months of 2017, (p<0.01). Screening tests performed increased from 363 in the among 4,442 CRE and 1,334 CRPA isolates that were tested first quarter of 2017, to 732 in the third. for carbapenemases from 32 states, 1,401 (32%) CRE and Illustrative examples. Public health responses using 25 (1.9%) CRPA were carbapenemase producers (Table 1). this new approach have identified single cases without Among the carbapenemase-producing isolates, 221 (15.5%) transmission, transmission within facilities, and spread to expressed carbapenemases other than KPC. Of isolates tested, multiple facilities. Examples from two states are presented to 1,422 (25%) were collected in the first quarter of 2017, illustrate these efforts. 2,141 (37%) in the second quarter, and 2,213 (38%) in In October 2017, the Tennessee Department of Health con- the third quarter. During this period, the median time from tacted CDC regarding identification of an NDM and OXA- specimen collection to CDC notification decreased from 37 to 48–producing Klebsiella pneumoniae isolate through ARLN. FIGURE 1. Percentage of Escherichia coli and Klebsiella pneumoniae isolates from selected health care–associated infections* with the FIGURE 2. Percentage of Escherichia coli and Klebsiella pneumoniae extended-spectrum-β-lactamase (ESBL) phenotype reported as isolates from selected health care–associated infections* reported nonsusceptible to extended-spectrum cephalosporins — National as resistant to a carbapenem — National Healthcare Safety Network, Healthcare Safety Network, United States, 2006–2015 United States, 2006–2015 100 100 12 8 6 4 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 Year Year * Central line–associated bloodstream infections and catheter-associated urinary * Central line–associated bloodstream infections and catheter-associated urinary tract infections. tract infections. Nonsusceptible to at least one extended-spectrum cephalosporin. 398 MMWR / April 6, 2018 / Vol. 67 / No. 13 US Department of Health and Human Services/Centers for Disease Control and Prevention Percentage with ESBL phenotype Percentage resistant to carbapenems Morbidity and Mortality Weekly Report Infection control assessment and screening of hospital contacts of 2017, demonstrating that recent investments in detection was completed and results returned within 48 hours of identifica- and response capacity are facilitating prompt identification tion of carbapenemase presence. No transmission was identified. of and response to emerging resistant organisms. Notably, Because the index patient had a recent health care exposure in 221 isolates with non-KPC carbapenemases were identified; another country, ARLN regional laboratories expanded their these rare forms of resistance have the potential to add to the services to perform CDC-recommended admission screening for U.S. CRE burden and represent an important opportunity patients with a history of overnight health care stays outside the to prevent the spread of novel resistance at its earliest stage. United States during the preceding 6 months (10). Findings from these enhanced prevention efforts are being used In April 2017, the Iowa Department of Public Health contacted to further refine detection and prevention strategies. CDC regarding IMP identified in a Proteus species isolated from Contact screening identified previously undetected transmission a nursing home resident. The state health department assessed and appeared to have the highest yield in post–acute care facilities infection control practices and performed a point prevalence sur- with higher acuity patients. Challenges in these settings that might vey that identified five additional colonized residents among 30 facilitate transmission of resistant organisms include long duration surveyed at the nursing home. The health department conducted of facility stay, less aggressive use of transmission-based precautions additional infection control assessments to ensure adherence to because of concerns about resident quality of life, high staff turnover recommended practices and two follow-up surveys of the nursing rates, and less expertise and training in infection control. Previous home wing, which did not identify any additional cases. work has also identified these settings as potential amplifiers of CRE transmission (11), underscoring the importance of providing Conclusions and Comments ongoing support to these facilities when targeted resistant organisms are identified. This support includes infection control assessments Although the proportion of Klebsiella spp. and E. coli that to improve adherence to recommended interventions and screening had either an ESBL or CRE phenotype both declined during of contacts to identify asymptomatic carriers. 2006–2015, larger decreases and a lower overall percent resis- Although this analysis focused on carbapenemase-producing tant were observed for the CRE phenotype. This difference organisms, the containment strategy can prevent the spread of might be attributable, at least in part, to the more directed other emerging antimicrobial resistant pathogens, including response employed to slow the spread of CRE once it was Candida auris and pan-resistant bacteria. Using existing sur- identified. Although CDC’s containment approach had not veillance systems, including ARLN, further work is under way yet been fully initiated when the decline in CRE began, these to better identify and understand new threats, including those data suggest that an early aggressive response, as outlined in that are emerging outside the United States. CDC continues to CRE-specific infection prevention recommendations released work to develop tests for new resistance mechanisms that can beginning in 2009 (6), can slow emergence and even decrease be made available via ARLN. Resistance is constantly evolving, the occurrence of infections from resistant pathogens. As and the containment strategy and ARLN are designed to be laboratory capacity improved, ARLN testing volume and flexible and nimble to rapidly detect and respond to new threats. public health responses increased over the first three quarters TABLE 1. Carbapenemase testing, by organism — Antibiotic Resistance Laboratory Network laboratories and CDC laboratory, specimens collected January 1–September 30, 2017 Total KPC NDM OXA-48 VIM IMP Positive Positive Positive Positive Positive Positive Tested* no. Tested no. Tested no. Tested no. Tested no. Tested no. Organism no. (%) no. (%) no. (%) no. (%) no. (%) no. (%) Total 5,776 1,426 (25) 5,755 1,234 (21) 5,570 134 (2.4) 5,323 65 (1.2) 4,724 30 (0.6) 4,068 16 (0.4) Enterobacteriaceae 4,442 1,401 (32) 4,430 1,232 (28) 4,247 134 (3.2) 4,050 65 (1.6) 3,448 12 (0.3) 2,827 11 (0.4) Klebsiella spp. 1,439 942 (65) 1,437 862 (60) 1,359 74 (5.4) 1,295 42 (3.2) 1114 4 (0.4) 744 1 (0.1) E. coli 789 144 (18) 783 83 (11) 755 43 (5.7) 719 20 (2.8) 665 0 (0) 585 0 (0) Enterobacter spp. 1,538 201 (13) 1,537 194 (13) 1,468 14 (1.0) 1,387 0 (0) 1,201 0 (0) 1,063 3 (0.3) Other 346 72 (21) 345 53 (15) 336 3 (0.9) 322 2 (0.6) 256 7 (2.7) 238 7 (2.9) Unspecified 330 42 (13) 328 40 (12) 329 0 (0) 327 1 (0.3) 212 1 (0.5) 197 0 (0) Pseudomonas 1,334 25 (1.9) 1,325 2 (0.2) 1,323 0 (0) 1,273 0 (0.0) 1,276 18 (1.4) 1,241 5 (0.4) aeruginosa Abbreviations: IMP  =  imipenemase; KPC  =  Klebsiella pneumoniae carbapenemase; NDM  =  New Delhi metallo-beta-lactamase; OXA-48  =  oxacillinase-48-like carbapenemase; VIM = Verona integron encoded metallo-beta-lactamase. * Number of isolates tested. Positive for at least one of the five carbapenemases tested (IMP, KPC, NDM, OXA-48, or VIM). 53 isolates were positive for more than one mechanism tested (28 KPC and NDM; 24 NDM and OXA-48; one KPC and VIM). US Department of Health and Human Services/Centers for Disease Control and Prevention MMWR / April 6, 2018 / Vol. 67 / No. 13 399 Morbidity and Mortality Weekly Report Despite improvements in capacity to detect carbapenemases The findings in this report are subject to at least four limita- in clinical isolates and asymptomatic carriers through ARLN, tions. First, resistance data in NHSN are collected using the challenges remain. Transmission in one facility in a region final interpretations of resistant, intermediate, or sensitive, and has the potential to affect all of the facilities and patients in a this analysis does not account for differences among laborato- region through patient sharing; therefore, recognition by health ries in the breakpoints used for interpretation or for changes care facilities of the importance of an aggressive, early, and in breakpoints over time. Enterobacteriaceae breakpoints for coordinated response is needed to ensure responses are timely carbapenems and some cephalosporins were lowered during and comprehensive. Mathematic modeling of the containment the analysis period. This might have resulted in an increase in strategy based on a single U.S. state’s patient transfer network isolates reported as resistant in later years of this analysis and suggests that an intervention resulting in a 20% reduction could have resulted in an underestimation of any reductions in in transmission would result in approximately 1,600 fewer CRE or ESBLs described. Second, NHSN data analyzed for this clinical cases, a relative reduction of about 76%, 3 years after report represent only isolates from two infection types (CAUTI introduction (CDC, unpublished data, 2018). In addition, and CLABSI); changes in colonization or other infection types commitment from health care personnel and health care facili- would not be identified. Third, although greater reductions were ties to improve adherence to infection control interventions seen in the percentage of organisms that were CRE compared that can prevent transmission, especially in post–acute care to those with the ESBL phenotype, this analysis is unable to settings, is necessary to prevent amplification of emerging resis- identify the exact cause for this difference. Finally, some states tance. For situations in which a targeted form of antimicrobial and health care facilities with colonization testing capacity chose resistance has emerged more widely in a region, containment to perform screening in-house rather than through the ARLN strategies might be less effective; additional work is required regional laboratory; these tests are not reported to ARLN and for these situations to identify the optimal strategies to reduce therefore are not included in this report, resulting in an under- the prevalence of endemic resistant organisms. Finally, current estimation of the true volume of screening conducted. interventions are challenging to implement and sustain; new Limiting the spread of emerging forms of antibiotic resistance is interventions to reduce transmission are needed to supplement a public health priority, and a timely and coordinated effort among currently available prevention measures. health care facilities, local and state health departments, and CDC Public health departments, because of their expertise and is needed to accomplish this goal. Research is already under way to ability to work across health care facilities, are uniquely posi- expand control strategies through innovative approaches such as tioned to facilitate these responses to emerging antimicrobial patient decolonization and microbiome manipulation, along with resistance. Since 2009, CDC has provided resources to develop a focus on identifying strategies to decrease the time from specimen state and local health care–associated infection programs; cur- collection to public health response. Fortunately, with the parallel rently, CDC supports approximately 500 persons in state and development of an enhanced prevention strategy for emerging local health departments to work on health care-associated antimicrobial resistance and implementation of advanced labora- infections and antimicrobial resistance. Details on funding tory testing in ARLN, the critical tools for controlling the spread provided to each state to combat antimicrobial resistance are of antimicrobial resistance are now available nationwide. In the provided in CDC’s antimicrobial resistance map (https:// first year of ARLN implementation, CDC and state and local wwwn.cdc.gov/arinvestments). public health departments and public health laboratory partners TABLE 2. Screening tests for carbapenem-resistant Enterobacteriaceae colonization, by facility type — Antibiotic Resistance Laboratory Network laboratories and CDC laboratory, specimens collected January 1–September 30, 2017 Total* Post–acute care facility Short-stay acute care hospital Carbapenemase Screened no. Positive no. (%) Screened no. Positive no. (%) Screened no. Positive no. (%) Total 1,489 171 (11) 1,074 147 (14) 365 21 (5.8) KPC 1,480 122 (8.2) 1,065 103 (10) 365 16 (4.4) NDM 1,480 6 (0.4) 1,065 6 (0.6) 365 0 (0) OXA-48 1,311 0 (0) 896 0 (0) 365 0 (0) VIM 1,488 34 (2.3) 1,073 30 (2.8) 365 4 (1.1) IMP 1,311 9 (0.7) 896 8 (0.9) 365 1 (0.3) Abbreviations: IMP  =  imipenemase; KPC  =  Klebsiella pneumoniae carbapenemase; NDM  =  New Delhi metallo-beta-lactamase; OXA-48  =  oxacillinase-48-like carbapenemase; VIM = Verona integron encoded metallo-beta-lactamase. * Includes 50 screening tests without a reported facility type, three of which were positive for KPC. Includes long-term acute care facilities, skilled nursing facilities, and inpatient rehabilitation facilities. Number screened refers to individual screening tests. Not all screening swabs were tested for all five mechanisms. Seven tests were positive for more than one mechanism tested (four KPC and NDM, and three KPC and VIM). 400 MMWR / April 6, 2018 / Vol. 67 / No. 13 US Department of Health and Human Services/Centers for Disease Control and Prevention Morbidity and Mortality Weekly Report have effectively increased the capacity to identify and respond Key Points to high concern organisms to prevent transmission of resistant pathogens. Although some challenges remain, this national public health strategy represents a critical step in the effort to decrease • The emergence and spread of antibiotic resistance the impact of resistant pathogens. threatens to outpace the development of new antibiotics. Slowing the spread of emerging resistance is a CDC Acknowledgments priority to protect persons and help slow the development Participating state and local health departments and public of antibiotic resistance overall. health laboratories. • Infection data from the National Healthcare Safety Network from 2006-2015 were analyzed to calculate Conflict of Interest changes in the annual proportion of selected No conflicts of interest were reported. pathogens that were nonsusceptible to extended- spectrum cephalosporins (ESBL phenotype) or Division of Healthcare Quality Promotion, National Center for Emerging 2 3 and Zoonotic Diseases, CDC; Tennessee Department of Health; Iowa resistant to carbapenems (carbapenem-resistant Department of Public Health. Enterobacteriaceae [CRE]). Corresponding author: Alexander J. Kallen, MD, akallen@cdc.gov. • The percentage of ESBL phenotype Enterobacteriaceae decreased by 2% per year; by comparison, the CRE References percentage decreased by 15% per year. 1. Weiner L, Webb A, Limbago B, et al. Antimicrobial-resistant pathogens • The proportion of Enterobacteriaceae infections that associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for were CRE remained lower and decreased more over Disease Control and Prevention, 2011–2014. Infect Control Hosp time than the proportion that were ESBL phenotype. Epidemiol 2016;37:1288–1301. This difference might be explained by the more directed 2. Jacoby GA, Medeiros AA, O’Brien TF, Pinto ME, Jiang H. Broad- spectrum, transmissible beta-lactamases. N Engl J Med 1988;319:723–4. control efforts implemented to slow transmission of https://doi.org/10.1056/NEJM198809153191114 CRE than those applied for ESBL-producing strains. 3. Yigit H, Queenan AM, Anderson GJ, et al. Novel carbapenem-hydrolyzing • These data suggest that an early aggressive response, as beta-lactamase, KPC-1, from a carbapenem-resistant strain of Klebsiella pneumoniae. Antimicrob Agents Chemother 2001;45:1151–61. https:// outlined in CRE-specific infection prevention doi.org/10.1128/AAC.45.4.1151-1161.2001 recommendations released beginning in 2009, can slow 4. Schwaber MJ, Carmeli Y. An ongoing national intervention to contain emergence and even decrease the occurrence of the spread of carbapenem-resistant Enterobacteriaceae. Clin Infect Dis infections from resistant pathogens. 2014;58:697–703. https://doi.org/10.1093/cid/cit795 5. Landman D, Bratu S, Kochar S, et al. Evolution of antimicrobial • In 2017, CDC outlined a new effort to react rapidly to resistance among Pseudomonas aeruginosa, Acinetobacter baumannii and novel multidrug-resistant organisms; this approach Klebsiella pneumoniae in Brooklyn, NY. J Antimicrob Chemother includes encouraging health care facilities and public 2007;60:78–82. https://doi.org/10.1093/jac/dkm129 6. CDC. Guidance for control of infections with carbapenem-resistant or health authorities to respond to even single isolates of carbapenemase-producing Enterobacteriaceae in acute care facilities. an emerging antibiotic-resistant pathogen. MMWR Morb Mortal Wkly Rep 2009;58:256–60. • From January to September 2017, carbapenemase 7. CDC. Vital signs: carbapenem-resistant Enterobacteriaceae. MMWR Morb Mortal Wkly Rep 2013;62:165–70. testing was performed by the Antibiotic Resistance 8. CDC. Interim guidance for a public health response to contain novel Lab Network for 4,442 CRE and 1,334 carbapenem- or targeted multidrug-resistant organisms (MDROs). Atlanta, GA: US resistant Pseudomonas aeruginosa (CRPA) isolates; 32% Department of Health and Human Services, CDC; 2017. https://www. and 1.9%, respectively were carbapenemase-producers. cdc.gov/hai/outbreaks/docs/Health-Response-Contain-MDRO.pdf 9. CDC. Antibiotic Resistance Lab Network. Atlanta, GA: US Department Among the carbapenemase-producing isolates, 221 of Health and Human Services, CDC; 2017. https://www.cdc.gov/ (15.5%) expressed carbapenemases other than Klebsiella drugresistance/solutions-initiative/ar-lab-networks.html pneumoniae carbapenemase. Carbapenemases can 10. CDC. New carbapenem-resistant Enterobacteriaceae warrant additional action by healthcare providers; February 14, 2013. Atlanta, GA: US make germs resistant to some of our most powerful Department of Health and Human Services, CDC; 2013. https://stacks. drugs, carbapenems. cdc.gov/view/cdc/25250 • Additional information is available at https://www.cdc. 11. Prabaker K, Lin MY, McNally M, et al.; CDC Prevention Epicenters Program. Transfer from high-acuity long-term care facilities is associated gov/vitalsigns/. with carriage of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae: a multihospital study. Infect Control Hosp Epidemiol 2012;33:1193–9. https://doi.org/10.1086/668435 US Department of Health and Human Services/Centers for Disease Control and Prevention MMWR / April 6, 2018 / Vol. 67 / No. 13 401 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Morbidity and Mortality Weekly Report Pubmed Central

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Pubmed Central
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0149-2195
eISSN
1545-861X
DOI
10.15585/mmwr.mm6713e1
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Abstract

Background: Approaches to controlling emerging antibiotic resistance in health care settings have evolved over time. When resistance to broad-spectrum antimicrobials mediated by extended-spectrum β-lactamases (ESBLs) arose in the 1980s, targeted interventions to slow spread were not widely promoted. However, when Enterobacteriaceae with carbapenemases that confer resistance to carbapenem antibiotics emerged, directed control efforts were recommended. These distinct approaches could have resulted in differences in spread of these two pathogens. CDC evaluated these possible changes along with initial findings of an enhanced antibiotic resistance detection and control strategy that builds on interventions developed to control carbapenem resistance. Methods: Infection data from the National Healthcare Safety Network from 2006–2015 were analyzed to calculate changes in the annual proportion of selected pathogens that were nonsusceptible to extended-spectrum cephalosporins (ESBL phenotype) or resistant to carbapenems (carbapenem-resistant Enterobacteriaceae [CRE]). Testing results for CRE and carbapenem-resistant Pseudomonas aeruginosa (CRPA) are also reported. Results: The percentage of ESBL phenotype Enterobacteriaceae decreased by 2% per year (risk ratio [RR] = 0.98, p<0.001); by comparison, the CRE percentage decreased by 15% per year (RR = 0.85, p<0.01). From January to September 2017, carbapenemase testing was performed for 4,442 CRE and 1,334 CRPA isolates; 32% and 1.9%, respectively, were carbapenemase producers. In response, 1,489 screening tests were performed to identify asymptomatic carriers; 171 (11%) were positive. Conclusions: The proportion of Enterobacteriaceae infections that were CRE remained lower and decreased more over time than the proportion that were ESBL phenotype. This difference might be explained by the more directed control efforts implemented to slow transmission of CRE than those applied for ESBL-producing strains. Increased detection and aggressive early response to emerging antibiotic resistance threats have the potential to slow further spread. Introduction remained susceptible to some first-line therapies, including The emergence and spread of antibiotic resistance threat- carbapenems. In general, facilities independently selected ens to outpace the development of new antimicrobials, and approaches to control spread, which often included core slowing the spread of these organisms has become a priority. infection control practices, such as hand hygiene, and placing Among Enterobacteriaceae, the family of pathogens most patients with ESBL-producing strains in single rooms under frequently associated with health care–associated infec- Contact Precautions. tions (1), resistance to the broad-spectrum antimicrobials Enterobacteriaceae resistance to even broader spectrum extended-spectrum cephalosporins and carbapenems has been antimicrobials, including carbapenems, was reported with driven largely by the spread of plasmid-mediated resistance increasing frequency beginning in 2001 (3). Rapid spread of genes encoding extended-spectrum β-lactamases (ESBLs) these carbapenem-resistant Enterobacteriaceae (CRE) in parts and carbapenemases, respectively. In the United States, of the United States and other countries (4,5) highlighted a ESBL-producing Enterobacteriaceae were first reported in need to more aggressively control CRE transmission. In 2009, 1988 (2). The emergence of these ESBL-producing isolates CDC created CRE-specific guidance, which was endorsed limited the options available for treatment, but these organisms by the Healthcare Infection Control Practices Advisory 396 MMWR / April 6, 2018 / Vol. 67 / No. 13 US Department of Health and Human Services/Centers for Disease Control and Prevention Morbidity and Mortality Weekly Report Committee (6). This guidance included recommendations bloodstream infections (CLABSIs) and catheter-associated for additional interventions when CRE was identified at a urinary tract infections (CAUTIs) associated with Escherichia health care facility, including laboratory surveillance of clinical coli or Klebsiella pneumoniae and reported to CDC’s National cultures and targeted patient screening to identify health care Healthcare Safety Network (NHSN) during 2006–2015 from contacts with asymptomatic colonization. This CRE-specific adult medical, surgical, or medical/surgical intensive care units guidance was updated in 2013 and 2015 (https://www.cdc.gov/ at short-stay acute care hospitals. The Centers for Medicare & hai/organisms/cre/cre-toolkit/index.html) and was highlighted Medicaid Services’ (CMS) Hospital Inpatient Quality Reporting by CDC in a 2013 report (7). Program mandated reporting of CLABSI and CAUTI data to In 2017, CDC outlined a new effort to react rapidly to novel NHSN starting in 2011 and 2012, respectively; data from previ- multidrug-resistant organisms (8); this approach includes ous years represent voluntary reporting or reporting to comply encouraging health care facilities and public health authorities with state or local mandates. National pooled mean percentages to respond to single isolates of an emerging antibiotic-resistant for Enterobacteriaceae with CRE phenotype (isolates resistant pathogen. The strategy rests on these five pillars: 1) rapid detec- to imipenem, meropenem, doripenem, or ertapenem), and tion of targeted pathogens and their resistance mechanisms, ESBL phenotype (isolates that tested intermediate or susceptible 2) on-site infection control assessments by trained experts to to carbapenems and intermediate or resistant to ceftazidime, identify gaps in infection prevention, 3) screening of exposed cefepime, ceftriaxone, or cefotaxime) were calculated. Log bino- contacts to identify asymptomatic colonization, 4) coordina- mial regression models were used to estimate the average annual tion of the response among facilities, and 5) continuing these change in the proportion of E. coli and K. pneumoniae that had interventions until transmission is controlled. Detection and a CRE or ESBL phenotype. P-values <0.05 were considered control efforts can extend from the index facility to other statistically significant. Sensitivity analyses were performed to facilities that share patients. account for the change in hospitals reporting to NHSN each To support this approach, CDC established the Antibiotic year. The results of the log binomial regression model were Resistance Laboratory Network (ARLN) (https://www.cdc. confirmed by a robust variance Poisson model. gov/drugresistance/solutions-initiative/ar-lab-networks.html) Enhanced detection and response. CRE and CRPA to improve national capacity to rapidly detect and respond to (P. aeruginosa resistant to imipenem, meropenem, or doripe- antibiotic resistance. ARLN provides carbapenemase testing nem) isolates were submitted to ARLN laboratories for test- for two emerging antibiotic resistant pathogens, CRE and ing for carbapenemases. Among Enterobacteriaceae, E. coli, carbapenem-resistant Pseudomonas aeruginosa (CRPA), at K. oxytoca, K. pneumoniae, and Enterobacter spp. were targeted 56 state and local public health laboratories and screening for for submission. Testing at ARLN laboratories included car- asymptomatic CRE and CRPA carriage at seven regional labo- bapenemase production testing and molecular detection of ratories (9). Carbapenemase-producing strains were targeted genes encoding for the five carbapenemases of primary public for detection and response in part because of their previously health concern: Klebsiella pneumoniae carbapenemase (KPC), demonstrated propensity for spread. CDC also expanded fund- New Delhi metallo-beta-lactamase (NDM), Verona integron ing to state and local health departments to increase capacity encoded metallo-beta-lactamase (VIM), imipenemase (IMP), and build expertise in responding to these and other emerging and oxacillinase-48-like carbapenemase (OXA-48). ARLN antibiotic resistance threats. laboratories were asked to report positive findings to local For this report, data from a national health care–associated public health authorities and CDC within 1 day and to submit infections surveillance system were reviewed to determine if testing summaries to CDC monthly. the more directed approach applied for CRE was associated For each carbapenemase-producing isolate detected, CDC with differences in the percentage of Enterobacteriacae health guidance recommends that state health department staff care–associated infections that were CRE compared with those members contact the health care facility to review infection that had the ESBL phenotype. In addition, findings from the control measures and consider performing on-site infection first 9 months of the enhanced response to emerging resistant control assessments. If indicated, contacts of the index patient organisms are described. are screened to detect transmission; testing capacity for this screening is provided through ARLN. Response activities con- Methods tinue until transmission is controlled. Screening results were stratified by whether the screening took place in a short-stay Percentage of Enterobacteriaceae with CRE or ESBL phe- acute care hospital or a post–acute care facility (i.e., long-term notypes in the National Healthcare Safety Network, 2006– acute care hospital or nursing home). 2015. Included in the analysis were central line–associated US Department of Health and Human Services/Centers for Disease Control and Prevention MMWR / April 6, 2018 / Vol. 67 / No. 13 397 Morbidity and Mortality Weekly Report 13 days. The percentage of carbapenemase-producing isolates Results varied by organism and was highest among Klebsiella species Percentage of Enterobacteriaceae with CRE or ESBL phe- (65%). Among carbapenemase-producing CRE, the most notypes in the National Healthcare Safety Network, 2006– commonly identified carbapenemase was KPC (1,232 of 1,401 2015. Among short-stay acute care hospitals, the percentage of isolates, 88%); VIM was the most common carbapenemase Klebsiella and E. coli isolates with the ESBL phenotype remained identified in CRPA (18 of 25, 72%) (Table 1). relatively stable, ranging from 17.6% (116 of 659 isolates) in To identify asymptomatically colonized health care contacts 2006 to 16.5% (694 of 4,211) in 2015, with a peak of 18.9% of index patients, 1,489 screening tests for carbapenemases in 2009 (Figure 1). The percentage of CRE declined from 8.8% were performed during 70 surveys (defined as all screening (35 of 397 isolates) in 2006 and 10.6% (64 of 604) in 2007 to tests performed at a single facility within a 14-day period) 3.1% (115 of 3,718) in 2015 (Figure 2). During 2006–2015, in 50 facilities. A median of 10.5 contacts (interquartile the annual percentage of isolates with the ESBL phenotype range = 2–25) were screened per survey. Overall, 11% of declined an average of 2% (RR = 0.98, p = 0.009); during the screening tests were positive for at least one of the five carbapen- same period, the proportion that were CRE decreased 15% per emases of primary public health concern (Table 2). A higher year (RR = 0.85, p<0.001). Results were unchanged when the percentage of post–acute care facility contacts screened positive analysis was limited to facilities that reported in all years. for carbapenemases (14% [147 of 1,074 contacts]) than did Enhanced detection of and response to carbapenemase- contacts from short-stay acute care hospitals (5.8% [21 of 365]) producing organisms. During the first 9 months of 2017, (p<0.01). Screening tests performed increased from 363 in the among 4,442 CRE and 1,334 CRPA isolates that were tested first quarter of 2017, to 732 in the third. for carbapenemases from 32 states, 1,401 (32%) CRE and Illustrative examples. Public health responses using 25 (1.9%) CRPA were carbapenemase producers (Table 1). this new approach have identified single cases without Among the carbapenemase-producing isolates, 221 (15.5%) transmission, transmission within facilities, and spread to expressed carbapenemases other than KPC. Of isolates tested, multiple facilities. Examples from two states are presented to 1,422 (25%) were collected in the first quarter of 2017, illustrate these efforts. 2,141 (37%) in the second quarter, and 2,213 (38%) in In October 2017, the Tennessee Department of Health con- the third quarter. During this period, the median time from tacted CDC regarding identification of an NDM and OXA- specimen collection to CDC notification decreased from 37 to 48–producing Klebsiella pneumoniae isolate through ARLN. FIGURE 1. Percentage of Escherichia coli and Klebsiella pneumoniae isolates from selected health care–associated infections* with the FIGURE 2. Percentage of Escherichia coli and Klebsiella pneumoniae extended-spectrum-β-lactamase (ESBL) phenotype reported as isolates from selected health care–associated infections* reported nonsusceptible to extended-spectrum cephalosporins — National as resistant to a carbapenem — National Healthcare Safety Network, Healthcare Safety Network, United States, 2006–2015 United States, 2006–2015 100 100 12 8 6 4 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 Year Year * Central line–associated bloodstream infections and catheter-associated urinary * Central line–associated bloodstream infections and catheter-associated urinary tract infections. tract infections. Nonsusceptible to at least one extended-spectrum cephalosporin. 398 MMWR / April 6, 2018 / Vol. 67 / No. 13 US Department of Health and Human Services/Centers for Disease Control and Prevention Percentage with ESBL phenotype Percentage resistant to carbapenems Morbidity and Mortality Weekly Report Infection control assessment and screening of hospital contacts of 2017, demonstrating that recent investments in detection was completed and results returned within 48 hours of identifica- and response capacity are facilitating prompt identification tion of carbapenemase presence. No transmission was identified. of and response to emerging resistant organisms. Notably, Because the index patient had a recent health care exposure in 221 isolates with non-KPC carbapenemases were identified; another country, ARLN regional laboratories expanded their these rare forms of resistance have the potential to add to the services to perform CDC-recommended admission screening for U.S. CRE burden and represent an important opportunity patients with a history of overnight health care stays outside the to prevent the spread of novel resistance at its earliest stage. United States during the preceding 6 months (10). Findings from these enhanced prevention efforts are being used In April 2017, the Iowa Department of Public Health contacted to further refine detection and prevention strategies. CDC regarding IMP identified in a Proteus species isolated from Contact screening identified previously undetected transmission a nursing home resident. The state health department assessed and appeared to have the highest yield in post–acute care facilities infection control practices and performed a point prevalence sur- with higher acuity patients. Challenges in these settings that might vey that identified five additional colonized residents among 30 facilitate transmission of resistant organisms include long duration surveyed at the nursing home. The health department conducted of facility stay, less aggressive use of transmission-based precautions additional infection control assessments to ensure adherence to because of concerns about resident quality of life, high staff turnover recommended practices and two follow-up surveys of the nursing rates, and less expertise and training in infection control. Previous home wing, which did not identify any additional cases. work has also identified these settings as potential amplifiers of CRE transmission (11), underscoring the importance of providing Conclusions and Comments ongoing support to these facilities when targeted resistant organisms are identified. This support includes infection control assessments Although the proportion of Klebsiella spp. and E. coli that to improve adherence to recommended interventions and screening had either an ESBL or CRE phenotype both declined during of contacts to identify asymptomatic carriers. 2006–2015, larger decreases and a lower overall percent resis- Although this analysis focused on carbapenemase-producing tant were observed for the CRE phenotype. This difference organisms, the containment strategy can prevent the spread of might be attributable, at least in part, to the more directed other emerging antimicrobial resistant pathogens, including response employed to slow the spread of CRE once it was Candida auris and pan-resistant bacteria. Using existing sur- identified. Although CDC’s containment approach had not veillance systems, including ARLN, further work is under way yet been fully initiated when the decline in CRE began, these to better identify and understand new threats, including those data suggest that an early aggressive response, as outlined in that are emerging outside the United States. CDC continues to CRE-specific infection prevention recommendations released work to develop tests for new resistance mechanisms that can beginning in 2009 (6), can slow emergence and even decrease be made available via ARLN. Resistance is constantly evolving, the occurrence of infections from resistant pathogens. As and the containment strategy and ARLN are designed to be laboratory capacity improved, ARLN testing volume and flexible and nimble to rapidly detect and respond to new threats. public health responses increased over the first three quarters TABLE 1. Carbapenemase testing, by organism — Antibiotic Resistance Laboratory Network laboratories and CDC laboratory, specimens collected January 1–September 30, 2017 Total KPC NDM OXA-48 VIM IMP Positive Positive Positive Positive Positive Positive Tested* no. Tested no. Tested no. Tested no. Tested no. Tested no. Organism no. (%) no. (%) no. (%) no. (%) no. (%) no. (%) Total 5,776 1,426 (25) 5,755 1,234 (21) 5,570 134 (2.4) 5,323 65 (1.2) 4,724 30 (0.6) 4,068 16 (0.4) Enterobacteriaceae 4,442 1,401 (32) 4,430 1,232 (28) 4,247 134 (3.2) 4,050 65 (1.6) 3,448 12 (0.3) 2,827 11 (0.4) Klebsiella spp. 1,439 942 (65) 1,437 862 (60) 1,359 74 (5.4) 1,295 42 (3.2) 1114 4 (0.4) 744 1 (0.1) E. coli 789 144 (18) 783 83 (11) 755 43 (5.7) 719 20 (2.8) 665 0 (0) 585 0 (0) Enterobacter spp. 1,538 201 (13) 1,537 194 (13) 1,468 14 (1.0) 1,387 0 (0) 1,201 0 (0) 1,063 3 (0.3) Other 346 72 (21) 345 53 (15) 336 3 (0.9) 322 2 (0.6) 256 7 (2.7) 238 7 (2.9) Unspecified 330 42 (13) 328 40 (12) 329 0 (0) 327 1 (0.3) 212 1 (0.5) 197 0 (0) Pseudomonas 1,334 25 (1.9) 1,325 2 (0.2) 1,323 0 (0) 1,273 0 (0.0) 1,276 18 (1.4) 1,241 5 (0.4) aeruginosa Abbreviations: IMP  =  imipenemase; KPC  =  Klebsiella pneumoniae carbapenemase; NDM  =  New Delhi metallo-beta-lactamase; OXA-48  =  oxacillinase-48-like carbapenemase; VIM = Verona integron encoded metallo-beta-lactamase. * Number of isolates tested. Positive for at least one of the five carbapenemases tested (IMP, KPC, NDM, OXA-48, or VIM). 53 isolates were positive for more than one mechanism tested (28 KPC and NDM; 24 NDM and OXA-48; one KPC and VIM). US Department of Health and Human Services/Centers for Disease Control and Prevention MMWR / April 6, 2018 / Vol. 67 / No. 13 399 Morbidity and Mortality Weekly Report Despite improvements in capacity to detect carbapenemases The findings in this report are subject to at least four limita- in clinical isolates and asymptomatic carriers through ARLN, tions. First, resistance data in NHSN are collected using the challenges remain. Transmission in one facility in a region final interpretations of resistant, intermediate, or sensitive, and has the potential to affect all of the facilities and patients in a this analysis does not account for differences among laborato- region through patient sharing; therefore, recognition by health ries in the breakpoints used for interpretation or for changes care facilities of the importance of an aggressive, early, and in breakpoints over time. Enterobacteriaceae breakpoints for coordinated response is needed to ensure responses are timely carbapenems and some cephalosporins were lowered during and comprehensive. Mathematic modeling of the containment the analysis period. This might have resulted in an increase in strategy based on a single U.S. state’s patient transfer network isolates reported as resistant in later years of this analysis and suggests that an intervention resulting in a 20% reduction could have resulted in an underestimation of any reductions in in transmission would result in approximately 1,600 fewer CRE or ESBLs described. Second, NHSN data analyzed for this clinical cases, a relative reduction of about 76%, 3 years after report represent only isolates from two infection types (CAUTI introduction (CDC, unpublished data, 2018). In addition, and CLABSI); changes in colonization or other infection types commitment from health care personnel and health care facili- would not be identified. Third, although greater reductions were ties to improve adherence to infection control interventions seen in the percentage of organisms that were CRE compared that can prevent transmission, especially in post–acute care to those with the ESBL phenotype, this analysis is unable to settings, is necessary to prevent amplification of emerging resis- identify the exact cause for this difference. Finally, some states tance. For situations in which a targeted form of antimicrobial and health care facilities with colonization testing capacity chose resistance has emerged more widely in a region, containment to perform screening in-house rather than through the ARLN strategies might be less effective; additional work is required regional laboratory; these tests are not reported to ARLN and for these situations to identify the optimal strategies to reduce therefore are not included in this report, resulting in an under- the prevalence of endemic resistant organisms. Finally, current estimation of the true volume of screening conducted. interventions are challenging to implement and sustain; new Limiting the spread of emerging forms of antibiotic resistance is interventions to reduce transmission are needed to supplement a public health priority, and a timely and coordinated effort among currently available prevention measures. health care facilities, local and state health departments, and CDC Public health departments, because of their expertise and is needed to accomplish this goal. Research is already under way to ability to work across health care facilities, are uniquely posi- expand control strategies through innovative approaches such as tioned to facilitate these responses to emerging antimicrobial patient decolonization and microbiome manipulation, along with resistance. Since 2009, CDC has provided resources to develop a focus on identifying strategies to decrease the time from specimen state and local health care–associated infection programs; cur- collection to public health response. Fortunately, with the parallel rently, CDC supports approximately 500 persons in state and development of an enhanced prevention strategy for emerging local health departments to work on health care-associated antimicrobial resistance and implementation of advanced labora- infections and antimicrobial resistance. Details on funding tory testing in ARLN, the critical tools for controlling the spread provided to each state to combat antimicrobial resistance are of antimicrobial resistance are now available nationwide. In the provided in CDC’s antimicrobial resistance map (https:// first year of ARLN implementation, CDC and state and local wwwn.cdc.gov/arinvestments). public health departments and public health laboratory partners TABLE 2. Screening tests for carbapenem-resistant Enterobacteriaceae colonization, by facility type — Antibiotic Resistance Laboratory Network laboratories and CDC laboratory, specimens collected January 1–September 30, 2017 Total* Post–acute care facility Short-stay acute care hospital Carbapenemase Screened no. Positive no. (%) Screened no. Positive no. (%) Screened no. Positive no. (%) Total 1,489 171 (11) 1,074 147 (14) 365 21 (5.8) KPC 1,480 122 (8.2) 1,065 103 (10) 365 16 (4.4) NDM 1,480 6 (0.4) 1,065 6 (0.6) 365 0 (0) OXA-48 1,311 0 (0) 896 0 (0) 365 0 (0) VIM 1,488 34 (2.3) 1,073 30 (2.8) 365 4 (1.1) IMP 1,311 9 (0.7) 896 8 (0.9) 365 1 (0.3) Abbreviations: IMP  =  imipenemase; KPC  =  Klebsiella pneumoniae carbapenemase; NDM  =  New Delhi metallo-beta-lactamase; OXA-48  =  oxacillinase-48-like carbapenemase; VIM = Verona integron encoded metallo-beta-lactamase. * Includes 50 screening tests without a reported facility type, three of which were positive for KPC. Includes long-term acute care facilities, skilled nursing facilities, and inpatient rehabilitation facilities. Number screened refers to individual screening tests. Not all screening swabs were tested for all five mechanisms. Seven tests were positive for more than one mechanism tested (four KPC and NDM, and three KPC and VIM). 400 MMWR / April 6, 2018 / Vol. 67 / No. 13 US Department of Health and Human Services/Centers for Disease Control and Prevention Morbidity and Mortality Weekly Report have effectively increased the capacity to identify and respond Key Points to high concern organisms to prevent transmission of resistant pathogens. Although some challenges remain, this national public health strategy represents a critical step in the effort to decrease • The emergence and spread of antibiotic resistance the impact of resistant pathogens. threatens to outpace the development of new antibiotics. Slowing the spread of emerging resistance is a CDC Acknowledgments priority to protect persons and help slow the development Participating state and local health departments and public of antibiotic resistance overall. health laboratories. • Infection data from the National Healthcare Safety Network from 2006-2015 were analyzed to calculate Conflict of Interest changes in the annual proportion of selected No conflicts of interest were reported. pathogens that were nonsusceptible to extended- spectrum cephalosporins (ESBL phenotype) or Division of Healthcare Quality Promotion, National Center for Emerging 2 3 and Zoonotic Diseases, CDC; Tennessee Department of Health; Iowa resistant to carbapenems (carbapenem-resistant Department of Public Health. Enterobacteriaceae [CRE]). Corresponding author: Alexander J. Kallen, MD, akallen@cdc.gov. • The percentage of ESBL phenotype Enterobacteriaceae decreased by 2% per year; by comparison, the CRE References percentage decreased by 15% per year. 1. Weiner L, Webb A, Limbago B, et al. Antimicrobial-resistant pathogens • The proportion of Enterobacteriaceae infections that associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for were CRE remained lower and decreased more over Disease Control and Prevention, 2011–2014. Infect Control Hosp time than the proportion that were ESBL phenotype. Epidemiol 2016;37:1288–1301. This difference might be explained by the more directed 2. Jacoby GA, Medeiros AA, O’Brien TF, Pinto ME, Jiang H. Broad- spectrum, transmissible beta-lactamases. N Engl J Med 1988;319:723–4. control efforts implemented to slow transmission of https://doi.org/10.1056/NEJM198809153191114 CRE than those applied for ESBL-producing strains. 3. Yigit H, Queenan AM, Anderson GJ, et al. Novel carbapenem-hydrolyzing • These data suggest that an early aggressive response, as beta-lactamase, KPC-1, from a carbapenem-resistant strain of Klebsiella pneumoniae. Antimicrob Agents Chemother 2001;45:1151–61. https:// outlined in CRE-specific infection prevention doi.org/10.1128/AAC.45.4.1151-1161.2001 recommendations released beginning in 2009, can slow 4. Schwaber MJ, Carmeli Y. An ongoing national intervention to contain emergence and even decrease the occurrence of the spread of carbapenem-resistant Enterobacteriaceae. Clin Infect Dis infections from resistant pathogens. 2014;58:697–703. https://doi.org/10.1093/cid/cit795 5. Landman D, Bratu S, Kochar S, et al. Evolution of antimicrobial • In 2017, CDC outlined a new effort to react rapidly to resistance among Pseudomonas aeruginosa, Acinetobacter baumannii and novel multidrug-resistant organisms; this approach Klebsiella pneumoniae in Brooklyn, NY. 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Atlanta, GA: US resistant Pseudomonas aeruginosa (CRPA) isolates; 32% Department of Health and Human Services, CDC; 2017. https://www. and 1.9%, respectively were carbapenemase-producers. cdc.gov/hai/outbreaks/docs/Health-Response-Contain-MDRO.pdf 9. CDC. Antibiotic Resistance Lab Network. Atlanta, GA: US Department Among the carbapenemase-producing isolates, 221 of Health and Human Services, CDC; 2017. https://www.cdc.gov/ (15.5%) expressed carbapenemases other than Klebsiella drugresistance/solutions-initiative/ar-lab-networks.html pneumoniae carbapenemase. Carbapenemases can 10. CDC. New carbapenem-resistant Enterobacteriaceae warrant additional action by healthcare providers; February 14, 2013. Atlanta, GA: US make germs resistant to some of our most powerful Department of Health and Human Services, CDC; 2013. https://stacks. drugs, carbapenems. cdc.gov/view/cdc/25250 • Additional information is available at https://www.cdc. 11. Prabaker K, Lin MY, McNally M, et al.; CDC Prevention Epicenters Program. Transfer from high-acuity long-term care facilities is associated gov/vitalsigns/. with carriage of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae: a multihospital study. Infect Control Hosp Epidemiol 2012;33:1193–9. https://doi.org/10.1086/668435 US Department of Health and Human Services/Centers for Disease Control and Prevention MMWR / April 6, 2018 / Vol. 67 / No. 13 401

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Published: Apr 6, 2018

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