Highlights
- •Carbapenem-resistant Enterobacterales (CRE) are an important cause of multi drug-resistant infections and are primarily associated with exposure to health care, such as hospitalization or residence in a long-term care facility. CRE that harbor a carbapenemase enzyme have the potential to spread rapidly and are classified as an urgent public health threat by the CDC.
- •The Emerging Infections Programs tracks CRE through laboratory- and population-based surveillance, providing a unique system for identifying CRE in persons without health care exposures.
- •Through this surveillance program we found that 10% of all CRE occurred in persons without known health care risk factors. Some of these community-associated CRE harbored a carbapenemase enzyme and most were identified from urine cultures and occurred in older women and persons of White race.
- •These findings show that a small but notable proportion of CRE occur in persons without health care risk factors. Understanding populations at risk of community-associated CRE infections, as well as tracking the burden of CRE that is community-associated into the future, can inform CRE prevention strategies.
Abstract
Background
Methods
Results
Conclusions
Key Words
Background
Centers for Disease Control and Prevention. Antibiotic resistant threats in the United States, 2019. Accessed January 22, 2021. https://www.cdc.gov/drugresistance/pdf/threats-report/2019-ar-threats-report-508.pdf.
World Health Organization. Prioritization of pathogens to guide discovery, research and development of new antibiotics for drug-resistant bacterial infections, including tuberculosis. Accessed July 29, 2021. https://www.who.int/medicines/areas/rational_use/PPLreport_2017_09_19.pdf.
Centers for Disease Control and Prevention. Interim guidance for a public health response to contain novel or targeted multidrug-resistant organisms (MDROs). Updated 2019. Accessed February 25, 2019. https://www.cdc.gov/hai/pdfs/containment/Health-Response-Contain-MDRO-H.pdf.
- See I
- Ansari U
- Reses H
- et al.
Centers for Disease Control and Prevention. Healtcare-Assocaited Infections, Multidrug-resistant organisms (HAI MDRO) message mapping guide. Accessed April 16, 2021. https://ndc.services.cdc.gov/mmgpage/healthcare-associated-infections-multidrug-resistant-organisms-hai-mdro-message-mapping-guide/.
Methods
Surveillance catchment area
Centers for Disease Control and Prevention. Multi-site gram-negative surveillance initiative. Accessed March 16, 2021. https://www.cdc.gov/hai/eip/mugsi.html.
United States Census Bureau. 2015 population estimates. Accessed June 27, 2016. http://quickfacts.census.gove/qfd/index.html.
United States Census Bureau. 2015 population estimates. Accessed June 27, 2016. http://quickfacts.census.gove/qfd/index.html.
Case definition and epidemiological classification
Centers for Disease Control and Prevention. HAIC Viz Multi-site gram-negative surveillance initiative, carbapenen-resistant enterobacterales. Accessed September 14, 2021. https://www.cdc.gov/hai/eip/haicviz.html.
Case identification and data collection
Centers for Disease Control and Prevention. Urinary tract infectins (catheter-associated urinary tract infections [CAUTI] and non-catheter-associated urinary tract infections [UTI]) events. Accessed November 1, 2018. https://www.cdc.gov/nhsn/pdfs/pscmanual/7psccauticurrent.pdf.
Centers for Disease Control and Prevention. Urinary tract infectins (catheter-associated urinary tract infections [CAUTI] and non-catheter-associated urinary tract infections [UTI]) events. Accessed November 1, 2018. https://www.cdc.gov/nhsn/pdfs/pscmanual/7psccauticurrent.pdf.
Analytic and statistical methods
SAS Institute. Scores for linear rank and one-way ANOVA Tests, Wilcoxon Scores. Accessed January 2, 2019. https://support.sas.com/documentation/cdl/en/statug/63033/HTML/default/viewer.htm#statug_npar1way_a0000000200.htm#statug.npar1way.npar1med.
Isolate collection, submission and evaluation
- Stanton RA
- Vlachos N.
- de Man T.J.B.
- Lawsin A.
- Halpin A.L.
Results
Cases and crude incidence rates
EIP Site | Crude incidence rates per 100,000 population (95% confidence cnterval) | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
2012 | 2013 | 2014 | 2015 | Overall | ||||||
CA | HCA | CA | HCA | CA | HCA | CA | HCA | CA | HCA | |
CO | 0.12 (0.02, 0.34) | 0.93 (0.60, 1.38) | 0.04 (0.00, 0.21) | 0.61 (0.35, 0.99) | 0.33 (0.15, 0.63) | 0.93 (0.60, 1.37) | 0.16 (0.09, 0.28) | 0.82 (0.63, 1.05) | ||
GA | 0.21 (0.09, 0.41) | 4.16 (3.54, 4.86) | 0.13 (0.04, 0.30) | 4.11 (3.50, 4.81) | 0.20 (0.09, 0.40) | 3.90 (3.30, 4.57) | 0.13 (0.04, 0.29) | 3.43 (2.88, 4.06) | 0.17 (0.11, 0.24) | 3.90 (3.59, 4.22) |
MD | 0.05 (0.00, 0.29) | 4.43 (3.54, 5.48) | 0.52 (0.25, 0.95) | 7.68 (6.49, 9.02) | 0.31 (0.11, 0.68) | 6.67 (5.57, 7.93) | 0.29 (0.17, 0.47) | 6.27 (5.64, 6.94) | ||
MN | 0.29 (0.10, 0.68) | 1.53 (1.00, 2.23) | 0.35 (0.13, 0.76) | 1.85 (1.27, 2.62) | 0.23 (0.06, 0.59) | 2.18 (1.54, 2.99) | 0.40 (0.16, 0.82) | 2.55 (1.86, 2.42) | 0.32 (0.20, 0.48) | 2.03 (1.71, 2.40) |
NM | 0.00 (0.00, 0.44) | 1.33 (0.61, 2.53) | 2.66 (1.58, 4.21) | 4.29 (2.87, 6.17) | 1.48 (0.71, 2.72) | 3.10 (1.92, 4.74) | 1.38 (0.92, 2.00) | 2.91 (2.22, 3.76) | ||
NY | 0.93 (0.38, 1.92) | 2.53 (1.53, 3.96) | 1.33 (0.64, 2.45) | 4.80 (3.36, 6.65) | 0.80 (0.29, 1.74) | 1.73 (0.92, 2.97) | 1.02 (0.65, 1.53) | 3.02 (2.35, 3.83) | ||
OR | 0.12 (0.01, 0.43) | 0.24 (0.06, 0.61) | 0.23 (0.06, 0.60) | 0.47 (0.20, 0.92) | 0.00 (0.00, 0.17) | 0.52 (0.24, 0.98) | 0.28 (0.09, 0.66) | 0.17 (0.04, 0.50) | 0.16 (0.08, 0.29) | 0.35 (0.22, 0.52) |
TN | 0.31 (0.10, 0.72) | 0.68 (0.34, 1.22) | 0.24 (0.07, 0.62) | 0.73 (0.37, 1.27) | 0.27 (0.13, 0.52) | 0.70 (0.45, 1.05) | ||||
Overall | 0.21 (0.12, 0.34) | 2.62 (2.26, 3.02) | 0.20 (0.13, 0.29) | 2.54 (2.28, 2.83) | 0.37 (0.28, 0.48) | 2.93 (2.66, 3.22) | 0.34 (0.26, 0.45) | 2.53 (2.28, 2.79) | 0.29 (0.25, 0.35) | 2.66 (2.52, 2.81) |
Organism, culture source and infection syndrome
Number of cases (%) | P value | |||
---|---|---|---|---|
All, n = 1499 | CA, n = 149 | HCA, n = 1350 | ||
Organism type | ||||
Klebsiella pneumoniae Escherichia coli Enterobacter cloacae Klebsiella aerogenes Klebsiella oxytoca | 800 (53.4) 275 (18.3) 208 (13.9) 191 (12.7) 25 (1.7) | 28 (18.8) 61 (40.9) 27 (18.1) 32 (21.5) 1 (0.7) | 772 (57.2) 214 (15.9) 181 (13.4) 159 (11.8) 21 (1.8) | .0008 .1142 <.0001 .5039 <.0001 |
Culture Source | ||||
Urine Blood Other normally sterile site | 1305 (87.1) 162 (10.8) 32 (2.1) | 146 (97.9) 3 (2.0) 0 (0.0) | 1159 (85.9) 159 (11.8) 32 (2.4) | <.0001 |
Selected Infection Syndromes | ||||
Urinary Tract Infection Bacteremia/Sepsis Septic Shock Pneumonia Pyelonephritis Vascular Graft Infection No infection syndrome documented | 1024 (63.7) 197 (13.1) 64 (4.3) 34 (2.3) 23 (1.5) 1 (0.1) 218 (14.5) | 123 (82.6) 4 (2.7) 0 (0.0) 0 (0.0) 4 (2.7) 1 (0.7) 19 (12.8) | 901 (66.7) 193 (14.3) 64 (4.7) 34 (2.5) 19 (1.4) 0 (0.0) 199 (14.7) | <.0001 <.0001 .0020 .0425 .2769 .0994 .5134 |
Outcomes | ||||
Hospitalized at the time of, or within 30 days after, the date of incident culture Admission to an intensive care unit on the day of, or within 7 days after, initial culture | 908/1490 (61.0) 316/908 (34.8) | 29/149 (19.5) 2/29 (6.9) | 879/1341 (65.6) 314/879 (35.7) | <.0001 .0006 |
Died within 30 days of date of incident culture | 167/1499 (11.1) | 4/149 (2.7) | 163/1350 (12.1) | .0002 |
Among cases with a sterile site culture Among cases with a urine culture | 58/167 (34.7) 109/167 (65.3) | 0/4 (0.0) 4/4 (100.0) | 58/163 (35.6) 105/163 (64.4) | .2992 |
Demographics and clinical characteristics of case-patients
Risk factors for infection and outcomes of cases
Antimicrobial susceptibility testing of incident case isolates at local clinical laboratories
Antimicrobial agent | Number susceptible/ Total number tested (%) | P-value | ||
---|---|---|---|---|
All, n = 1499 | CA, n = 149 | HCA, n = 1350 | ||
Aminoglycosides | ||||
Any tested | 1253/1473 (85.1) | 141/146 (96.6) | 1112/1327 (83.8) | <.0001 |
Amikacin Gentamicin Tobramycin | 875/1286 (68.0) 973/1462 (66.6) 534/1325 (39.9) | 112/118 (94.9) 129/145 (89.0) 88/113 (77.9) | 763/1168 (65.3) 844/1317 (64.1) 436/1212 (36.0) | <.0001 <.0001 <.0001 |
Fluoroquinolones | ||||
Any tested | 454/1465 (31.0) | 102/145 (70.3) | 352/1320 (26.7) | <.0001 |
Ciprofloxacin Levofloxacin | 391/1314 (29.8) 328/1133 (29.0) | 98/142 (69.0) 63/98 (64.3) | 293/1172 (25.0) 265/1035 (25.4) | <.0001 <.0001 |
Other antimicrobials | ||||
Ampicillin Aztreonam Colistin Piperacillin-tazobactam Nitrofurantoin Tigecycline Trimethoprim-sulfamethoxazole | 34/1295 (2.6) 87/1161 (7.5) 194/222 (87.4) 208/1397 (14.9) 90/377 (23.9) 188/657 (28.6) 463/1456 (31.8) | 22/121 (18.2) 35/105 (33.3) 2/2 (100.0) 57/138 (41.3) 23/39 (59.0) 11/28 (39.3) 80/144 (55.6) | 12/1174 (1.0) 52/1056 (4.9) 192/220 (87.3) 151/1259 (12.0) 67/338 (19.8) 177/629 (28.1) 383/1312 (29.2) | <.0001 <.0001 .5894 <.0001 <.0001 .2017 <.0001 |
Characterization of isolates from community-associated CRE cases
Organism type | Carbapenemase gene variants | MLST | Non-carbapenemase beta-lactamase gene variants | Antimicrobial resistance profile ‡ Antimicrobials reported if the isolate tested resistant based on reference broth microdilution testing performed at CDC. Isolates were tested against the following unless noted: AMK, amikacin; AMC, amoxicillin-clavulanic acid; AMP, ampicillin; ATM, aztreonam; CFZ, cefazolin; FEP, cefepime; CTX, cefotaxime; CAZ, ceftazidime; FOX, cefoxitin; CRO, ceftriaxone; CIP, ciprofloxacin; CST, colistin; DOR, doripenem; ETP, ertapenem; GEN, gentamicin; IPM, imipenem; LVX, levofloxacin; MEM, meropenem; TZP, piperacillin-tazobactam; PMB, polymyxin B; TET, tetracycline; TGC, tigecycline; SXT, trimethoprim-sulfamethoxazole; TOB, tobramycin. Interpretations are based on the 2019 Clinical and Laboratory Standards Institute; CLSI, interpretative criteria. Performance standards for antimicrobial susceptibility testing: twenty-ninth informational supplement, M100-S29. Wayne [PA]: The Institute; 2019). |
---|---|---|---|---|
Enterobacter cloacae | None | Novel | ACT-70 | AMC, AMP, ATM, CFZ, FOX, TZP |
complex (n = 6) | None | 108 | ACT-55 | AMP, ATM, CFZ, FOX, TZP |
KPC-3 | 171 | ACT-45, OXA-9, SHV-12, TEM-1A | AMC, AMP, ATM, CFZ, FEP, FOX, CIP, LVX, TZP, SXT, TOB | |
None | 45 | TEM-1B | AMC, AMP, ATM, CFZ, FOX, CST, TZP, PMB, SXT | |
None | 365 | None | AMC, AMP, ATM, CFZ, FOX, CST, TZP, PMB | |
None | 125 | ACT-28 | AMC, AMP, ATM, CFZ, FOX, CST, TZP, PMB | |
Escherichia coli (n = 3) | NDM-1 | 5498 | TEM-1A | AMP, CFZ, FEP, FOX, CIP, GEN, LVX, TZP, TET, SXT, TOB |
None | 167 | CTX-M-15, OXA-1 | AMP, ATM, CFZ, FEP, FOX, CIP, GEN, LVX, TET, SXT | |
None | 131 | CTX-M-15, OXA-1, TEM-1B | AMC, AMP, ATM, CFZ, FEP, FOX, CIP, LVX, TZP, SXT, TOB | |
Klebsiella pneumoniae (n = 3) | KPC-3 | 258 | SHV-11 | AMC, AMP, ATM, CFZ, CIP, LVX, TZP, SXT, TOB |
KPC-3 | 1737 | LEN-17 | AMC, AMP, ATM, CFZ, FEP, CIP, LVX, TZP, SXT, TOB | |
KPC-3 | 485 | SHV-27 | AMC, AMP, ATM, CFZ, FEP, CIP, LVX, TZP, SXT |
Epidemiology of carbapenemase-producing CA-CRE cases
Discussion
- Thaden JT
- Lewis SS
- Hazen KC
- et al.
- Gupta K
- Hooton TM
- Naber KG
- et al.
World Health Organization. Prioritization of pathogens to guide discovery, research and development of new antibiotics for drug-resistant bacterial infections, including tuberculosis. Accessed July 29, 2021. https://www.who.int/medicines/areas/rational_use/PPLreport_2017_09_19.pdf.
- Sarah J
Centers for Disease Control and Prevention. Antibiotic resistance and patient safety portal: carbapenem-resistant enterobacterales. Accessed January 7, 2022. https://arpsp.cdc.gov/profile/arln/cre.
Centers for Disease Control and Prevention. Antibiotic resistance and patient safety portal: carbapenem-resistant enterobacterales. Accessed January 7, 2022. https://arpsp.cdc.gov/profile/arln/cre.
- Sarah J
- See I
- Ansari U
- Reses H
- et al.
World Health Organization. Prioritization of pathogens to guide discovery, research and development of new antibiotics for drug-resistant bacterial infections, including tuberculosis. Accessed July 29, 2021. https://www.who.int/medicines/areas/rational_use/PPLreport_2017_09_19.pdf.
Acknowledgments
Appendix. SUPPLEMENTARY MATERIALS
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Funding/support: The Health Care-Associated Infections Community Interface's Multi-Site Gram-negative Surveillance Initiative of the Emerging Infections Program is supported through the CDC's cooperative agreement, CDC-RFA-CK17-1701.
Conflict of Interest: The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention. Included authors have nothing to disclose.
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