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Volume 27, Number 9—September 2021
Dispatch

Gram-Negative Bacteria Harboring Multiple Carbapenemase Genes, United States, 2012–2019

D. Cal HamComments to Author , Garrett Mahon, Sandeep K. Bhaurla, Sam Horwich-Scholefield, Liore Klein, Nychie Dotson, J. Kamile Rasheed, Gillian McAllister, Richard A. Stanton, Maria Karlsson, David Lonsway, Jennifer Y. Huang, Allison C. Brown, and Maroya Spalding Walters
Author affiliations: Centers for Disease Control and Prevention, Atlanta, Georgia, USA (D.C. Ham, G. Mahon, J.K. Rasheed, G. McAllister, R.A. Stanton, M. Karlsson, D. Lonsway, J.Y. Huang, A.C. Brown, M.S. Walters); Los Angeles County Department of Public Health, Los Angeles, California, USA (S.K. Bhaurla); California Department of Public Health, Richmond, California, USA (S. Horwich-Scholefield); Maryland Department of Health, Baltimore, Maryland, USA (L. Klein); Florida Department of Health, Tallahassee, Florida, USA (N. Dotson)

Main Article

Table 2

Characteristics and exposures of incident cases of gram-negative bacilli harboring multiple carbapenemase genes, United States, January 2012–April 2019*

Characteristics and exposures Enterobacterales†
Pseudomonas spp.,‡ KPC + VIM, NDM + VIM, or 
NDM + IMP Acinetobacter baumannii, NDM + 
OXA-23 Total
NDM + 
OXA-48§ KPC + NDM KPC + VIM KPC + OXA-48
Total no. (%) cases
65 (100.0)
23 (100.0)
6 (100.0)
2 (100.0)
7 (100.0)
2 (100.0)
105 (100.0)
Region of specimen collection¶
South 22/65 (33.8) 9/23 (39.1) 2/6 (33.3) 0 3/7 (42.9) 1/2 (50.0) 37/105 (35.2)
West 22/65 (33.8) 3/23 (13.0) 2/6 (33.3) 0 1/7 (14.3) 0 28/105 (26.7)
Northeast 14/65 (21.5) 5/23 (21.7) 0 0 2/7 (28.6) 0 21/105 (20.0)
Midwest
7/65 (10.8)
6/23 (26.1)
2/6 (33.3)
2/2 (100.0)
1/7 (14.3)
1/2 (50.0)
19/105 (18.1)
Location of specimen collection
Acute care hospital 51/57 (89.5) 18/22 (81.8) 3/4 (75.0) 2/2 (100.0) 5/7 (71.4) 0 79/94 (84.0)
Outpatient facility 5/57 (8.8) 1/22 (4.5) 0 0 2/7 (28.6) 1/2 (50.0) 9/94 (9.6)
Long-term acute care 
hospital 0 1/22 (4.5) 1/4 (25.0) 0 0 1/2 (50.0) 3/94 (3.2)
Skilled nursing facility 0 2/22 (9.1) 0 0 0 0 2/94 (2.1)
Joint acute care 
hospital/ inpatient 
rehabilitation facility
1/57 (1.8)
0
0
0
0
0
1/94 (1.1)
Hospitalization in previous 12 mo, United States#
44/56 (78.6)
19/23 (82.6)
4/5 (80.0)
2/2 (100.0)
4/7 (57.1)
2/2 (100.0)
75/95 (78.9)
International travel in previous 12 mo**
Yes 47/59 (79.7)†† 5/19 (26.3)†† 1/4 (25.0) 1/2 (50.0) 7/7 (100.0) 1/2 (50.0) 62/93 (66.7)
International inpatient
healthcare‡‡ 40/43 (93.0) 3/4 (75.0) 0/1 0/1 6/7 (85.7) 1/1 (100.0) 51/57 (89.5)
India 29/39 (74.4) 1/3 (33.3) 1/1 (100.0) 3/6 (50.0) 1/1 (100.0) 35/50 (70.0)
Other§§ 5/39 (12.8) 2/3 (66.7) 0 2/6 (33.3) 0/1 9/50 (18.0)
Pakistan 3/39 (7.7) 0/3 0/1 0/6 1/1 (100.0) 4/50 (8.0)
Egypt 2/39 (5.1) 0/3 0/1 0/6 0/1 2/50 (4.0)
Vietnam 1/39 (2.6) 0/3 0/1 1/6 (16.7) 0/1 2/50 (4.0)
No 12/59 (20.3) 14/19 (73.7) 3/4 (75.0) 1/2 (50.0) 0/7 1/2 (50.0) 31/93 (33.3)
US hospitalization
11/12 (91.7)
12/14 (85.7)
3/3 (100.0)
1/1 (100.0)

1/1 (100.0)
28/31 (90.3)
Transplant recipient¶¶ 11/48 (22.9) 4/17 (23.5) 0/5 1/2 (50.0) 1/6 (16.7) 0/2 17/80 (21.3)
Before incident case 8/11 (72.7) 4/4 (100.0) 1/1 (100) 1/1 (100.0) 14/17 (82.4)
Transplant to incident 
case, d, median (IQR) 44 (15–446)
After incident case 3/11 (27.3) 0/4 0/1 0/1 3/17 (17.6)
Incident case to 
transplant, d, median 
(IQR)






96 (28–188)
Type of transplant##
Solid organ 11/11 (100.0) 2/4 (50.0) 0/1 0/1 13/17 (76.5)
Kidney 7/11 (63.6) 0/2 7/13 (53.8)
Liver 3/11 (27.3) 1/2 (50.0) 4/13 (30.8)
Lung 1/11 (9.1) 1/2 (50.0) 2/13 (15.4)
Bone marrow 0/11 2/4 (50.0) 1/1 (100.0) 1/1 (100.0) 4/17 (23.5)

*Values are no. cases/total no. in category (%) except as indicated. Three incident cases occurred in 3 patients who reported no international travel or hospitalization in the United States during the previous 12 mo (1 case of E. coli harboring blaNDM and blaKPC, 1 case of K. pneumoniae harboring blaNDM and blaKPC, and 1 case of E. coli harboring blaNDM and blaOXA-48-like). Among these patients, 1 was a nursing home resident, 1 did not have additional information provided, and 1 had a spouse who had traveled to India and returned ≈1 mo before their incident case. Exposures are described for the 12 mo before identification of incident case. IMP, active-on-imipenem metallo-β-lactamase; KPC, Klebsiella pneumoniae carbapenemase; NDM, New Delhi metallo-β-lactamase; OXA, oxacillinase; VIM, Verona integron-encoded metallo-β-lactamase. †Citrobacter freundii, Enterobacter cloacae, Escherichia coli, Klebsiella aerogenes, K. oxytoca, K. pneumoniae, and Providencia rettgeri isolates. ‡Pseudomonas aeruginosa and Pseudomonas fluorescens isolates. §Includes 1 K. pneumoniae isolate harboring blaNDM, blaOXA-48-like, and blaVIM. ¶Based on census regions of residence (US Census Bureau, https://www2.census.gov/geo/pdfs/maps-data/maps/reference/us_regdiv.pdf). #Of 90 unique patients who contributed 95 incident cases with complete data. **Of 88 unique patients who contributed 93 incident cases with complete data. ††Significant difference; p<0.01. Exclusion of incident cases associated with an outbreak or cluster did not change this association: 47/56 (83.9%) incident cases harboring blaNDM and blaOXA-48-like occurred in patients who reported international travel, compared with 4/14 (28.6%; p<0.01) with blaKPC and blaNDM. ‡‡Two patients reported international inpatient healthcare in 2 countries. §§One hospitalization in Bangladesh, 1 in Columbia, 1 in Iraq, 1 in Mexico, 1 in Nigeria, 1 in Tajikistan, 1 in Thailand, 1 in Turkey, and 1 in Yemen. ¶¶Solid organ or bone marrow transplants; of 75 unique patients who contributed 80 incident cases with complete data. ##Of includes 17 unique patients who contributed 17 incident cases with complete data.

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Page created: August 11, 2021
Page updated: August 19, 2021
Page reviewed: August 19, 2021
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