Volume 27, Number 9—September 2021
    
    Dispatch
Gram-Negative Bacteria Harboring Multiple Carbapenemase Genes, United States, 2012–2019
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.