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Carbapenem resistance in critically important human pathogens isolated from companion animals: a systematic literature review

Osong Public Health and Research Perspectives 2022;13(6):407-423.
Published online: December 16, 2022

Molecular Genetics of Pathogens Group, National University of Colombia, Bogotá, Colombia

Corresponding author: Martha Cecilia Suárez-Alfonso Molecular Genetics of Pathogens Group, Universidad Nacional of Colombia, Carrera 30 # 45-03, Facultad de Medicina Veterinaria y de Zootecnia Edificio 503, Laboratorio de Microbiología Veterinaria, 111321 Bogotá, Colombia E-mail: mcsuarezal@unal.edu.co
• Received: January 24, 2022   • Revised: November 1, 2022   • Accepted: November 15, 2022

© 2022 Korea Disease Control and Prevention Agency.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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Carbapenem resistance in critically important human pathogens isolated from companion animals: a systematic literature review
Osong Public Health Res Perspect. 2022;13(6):407-423.   Published online December 16, 2022
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Carbapenem resistance in critically important human pathogens isolated from companion animals: a systematic literature review
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Carbapenem resistance in critically important human pathogens isolated from companion animals: a systematic literature review
Image Image Image Image
Figure 1. Flowchart of the search and selection of articles for this systematic review on carbapenem resistance (CR) in companion animals and related context.
Figure 2. Number of reports and distribution of carbapenem resistance genes from Enterobacteriaceae and non-fermenting bacilli from domestic canines and felines in (A) America and (B) Europe.ST, sequence type; OXA, oxacillin; KPC, Klebsiella pneumoniae carbapenemase; NDM, New Delhi metallo-β-lactamase; VIM, Verona integron-encoded metallo-β-lactamase; NR, not reported.
Figure 3. Number of reports and distribution of carbapenem resistance genes from Enterobacteriaceae and non-fermenting bacilli from domestic canines and felines in Africa, Asia, and Oceania.ST, sequence type; OXA, oxacillin; VIM, Verona integron-encoded metallo-β-lactamase; IMP, active-on-imipenem; NDM, New Delhi metallo-β-lactamase; NR, not reported.
Figure 4. Number of reports and global distribution of carbapenem resistance genes from Enterobacteriaceae and non-fermenting bacilli from veterinary environments, homes, and commercial foods for domestic canines and felines.ST, sequence type; VIM, Verona integron-encoded metallo-β-lactamase; OXA, oxacillin; NDM, New Delhi metallo-β-lactamase.
Carbapenem resistance in critically important human pathogens isolated from companion animals: a systematic literature review
Country First author Microorganism CR mechanisma) Genetic location Study type
Companion animals
 China Li et al. [19] ENB NDM-5 Plasmid Investigation (search)
Wang et al. [21] ENB NDM-5 Plasmid Investigation (search)
Cui et al. [31] ENB NDM-1 Plasmid Surveillance
Liu et al. [39] ENB OXA-48 NR Investigation (search)
Wang et al. [53] GNFB IMP-45 Chromosome Surveillance
 South Korea Hong et al. [22] ENB NDM-5 Plasmid Investigation (report)
Hong et al. [32] ENB NDM-5 Plasmid Surveillance
Hong et al. [45] ENB NDM-5 NR Surveillance
Oh et al. [68] ENB NDM-5 Plasmid Monitoring
Hyun et al. [61] GNFB VIM-2 Integron class I Investigation (search)
 India Pruthvishree et al. [46] ENB NDM-1 NR Investigation (report)
Bandyopadhyay et al. [67] ENB NDM-5 Plasmid Investigation (search)
 Japan Kimura et al. [65] GNFB IMP-1 NR Surveillance
 Pakistan Taj et al. [66] GNFB OXA-23 NR Investigation (report)
 Brazil Sellera et al. [42] ENB KPC-2 Plasmid Surveillance
Fernandes et al. [54] GNFB VIM-2 Chromosome Investigation (report and search)
 United States Liu et al. [36] ENB OXA-48 Plasmid Investigation (search)
Daniels et al. [41] ENB KPC-4 Plasmid Surveillance
Shaheen et al. [47] ENB NDM-1 Plasmid and chromosome Investigation (search)
Tyson et al. [60] ENB NDM-5 Plasmid Surveillance
Cole et al. [69] ENB NDM-5 Plasmid Investigation (search)
 Germany Pulss et al. [25] ENB OXA-48 Plasmid Investigation (search)
Stolle et al. [29] ENB OXA-48 Plasmid Investigation (search)
Schmiedel et al. [37] ENB OXA-48 NR Investigation (search)
Ewers et al. [55] GNFB OXA-23 Plasmid Investigation (search)
Ewers et al. [57] GNFB OXA-23 Plasmid Investigation (report)
Klotz et al. [63] GNFB OXA-58 Plasmid Investigation (search)
 Spain Gonzalez-Torralba et al. [33] ENB VIM-1 Plasmid Investigation (search)
 Finland Gronthal et al. [34] ENB NDM-5 Plasmid Investigation (report and search)
 France Valat et al. [23] ENB OXA-48 Plasmid Investigation (search)
Melo et al. [48] ENB OXA-48 Plasmid Investigation (search)
Herivaux et al. [56] GNFB OXA-23 NR Investigation (search)
Lupo et al. [64] GNFB OXA-23 Chromosome Surveillance
 Italy Alba et al. [49] ENB NDM-5 Plasmid Investigation (report)
Gentilini et al. [59] GNFB NDM-1, OXA-23, L1b), LP NR Investigation (search)
 Portugal Brilhante et al. [26] ENB OXA-181 Plasmid Investigation (search)
Pomba et al. [58] GNFB OXA-23 Chromosome Investigation (report)
 United Kingdom Reynolds et al. [24] ENB NDM-5 Plasmid Surveillance
 Serbia Misic et al. [62] GNFB OXA-72 Plasmid Investigation (report)
 Switzerland Nigg et al. [20] ENB OXA-181 Plasmid Investigation (search)
Brilhante et al. [38] ENB OXA-48 Plasmid Investigation (report)
Dazio et al. [40] ENB NDM-5, OXA-48, OXA-181 NR Investigation (search)
Peterhans et al. [43] ENB NDM- 5 Plasmid Investigation (NR)
 Algeria Yousfi et al. [27] ENB OXA-48, NDM-5 NR Investigation (search)
Yousfi et al. [28] ENB OXA-48 Plasmid Investigation (search)
Mairi et al. [30] ENB OXA-48 Plasmid Investigation (search)
 Egypt Khalifa et al. [44] ENB VIM-4, OXA-48, OXA-244 Plasmid Investigation (search)
 Australia Abraham et al. [35] ENB IMP-4 Plasmid Investigation (report)
Context associated with companion animalsc)
 Brazil Fernandes et al. [54] GNFB VIM-2 Chromosome Investigation (report and search)
 Egypt Ramadan et al. [51] ENB NDM-5, OXA-181 Plasmid Investigation (search)
 Switzerland Brilhante et al. [38] ENB OXA-48 Plasmid Investigation (report)
Seiffert et al. [50] ENB OXA-48 Plasmid Investigation (search)
Schmidt et al. [52] ENB OXA-48, OXA-181 NR Investigation (search)
Study Sample origin
Antimicrobial use
Carbapenem resistance
Animal n Specimen Carbapenem Others Bacterial species CR origina)
Li et al. [19] Dogs 2 Stool NR NR Escherichia coli NDM-5
Nigg et al. [20] Dogs, cats 21 Rectal swab NO PEN, BET/INHIB, QUIN, NIT, CEP, TET, SUL E. coli OXA-181 (OXA-48-like)
Wang et al. [21] Dogs, cats 6 Stool, urine NR NR E. coli, Enterobacter cloacae, Citrobacter freundii NDM-5
Hong et al. [22] Dogs, cats 2 Rectal swab MERO QUIN, CEP, TET E. coli NDM-5
Valat et al. [23] Dogs 1 NR NR NR E. coli OXA-48
Reynolds et al. [24] Dogs 1 Tissuesb) NO BET/INHIB, CEP, TET, QUIN E. coli NDM-5
Pulss et al. [25] Dogs, cats 130 CVADsc), urine, other fluidsd), tissuesb) NO CEP 2°, 3°, PEN, QUIN, BET/INHB Klebsiella pneumoniae/Klebsiella oxytoca, E. cloacae, E. coli OXA-48
Brilhante et al. [26] Dogs 1 Tissuesb) NR NR E. coli OXA-181 (OXA-48-like)
Yousfi et al. [27] Dogs, cats 5 Rectal swab NR NR E. coli OXA-48, NDM-5
Yousfi et al. [28] Dogs, cats 6 Rectal swab NR NR E. coli, K. pneumoniae, E. cloacae OXA-48
Stolle et al. [29] Dogs 6 CVADsc), tissuesb), stool, urine, other fluidsd) NO PEN, BET/INHIB, QUIN, CEP, 3° TET K. pneumoniae, E. coli OXA-48
Mairi et al. [30] Dogs 1 Rectal swab NR NR K. pneumoniae OXA-48
Cui et al. [31] Dogs 1 Anal swab NR NR E. coli NDM-1
Hong et al. [32] Dogs 4 Rectal swab MERO CEP 1°, QUIN, BET/INHIB, NIT E. coli NDM-5
Gonzalez-Torralba et al.[33] Dogs 1 Rectal swab NO NO K. pneumoniae VIM-1
Gronthal et al. [34] Dogs 2 Ear swab NO QUIN, CEP 1°, BET/INHIB, LIN E. coli NDM-5
Abraham et al. [35] Cats 4 Stool NO TET Salmonella enterica serovar Typhimurium IMP-4
Liu et al. [36] Dogs, cats NR Urine, tissuesb) NR NR E. coli OXA-48
Schmiedel et al. [37] Dogs, cats NR NR NR NR K. pneumoniae, E. cloacae OXA-48
Brilhante et al. [38] Dogs, cats 10 Urine, other fluidsd), tissuesb) NR NR K. pneumoniae OXA-48
Liu et al. [39] Dogs NR Urine, tissuesb) NR NR E. coli OXA-48
Dazio et al. [40] Dogs, cats 25 Rectal swab NO NR E. coli NDM-5, OXA-48, OXA-181 (OXA-48-like)
K. pneumoniae OXA-48
Daniels et al. [41] Dogs 2 Urine, tissuesb) NO TET Enterobacter. hormaechei subsp. xiangfangensis KPC-4
Sellera et al. [42] Dogs 1 Urine NR NR K. pneumoniae KPC-2
Peterhans et al. [43] Dogs 1 Tissuesb) NR NR E. coli NDM-5
Khalifa et al. [44] Dogs, cats 7 Nasal swab, eye swab NR NR E. hormaechei subsp. xiangfangensis VIM-4
K. pneumoniae OXA-48
E. coli OXA-244 (OXA-48-like)
Hong et al. [45] Dogs 4 Rectal swab NR NR E. coli NDM-5
Pruthvishree et al. [46] Dogs 1 Other fluidsd) NR NR E. coli NDM-1
Shaheen et al. [47] Dogs, cats 6 Urine, tissuesb) NR NR E. coli NDM-1
Melo et al. [48] Dogs 1 Rectal swab NO BET/INHIB E. coli OXA-48
Alba et al. [49] Dogs 1 Urine NR NR E. coli NDM-5
Wang et al. [53] Dogs 1 Anal swab NR NR Pseudomonas aeruginosa IMP-45
Fernandes et al. [54] Dogs 1 Oral swab, rectal swab, other fluidsd) NR NR P. aeruginosa VIM-2
Ewers et al. [55] Dogs, cats 3 Vaginal swab, urine, other fluidsd) NR NR Acinetobacter baumannii OXA-23
Herivaux et al. [56] Dogs 2 Oral swab, rectal swab NO NO A. baumannii OXA-23
Ewers et al. [57] Cats 1 Urine NR NR A. baumannii OXA-23
Pomba et al. [58] Cats 1 Urine NO BET/INHB A. baumannii OXA-23
Gentilini et al. [59] Dogs, cats 11 Rectal swab NO BET/INHIB, TET, QUIN, NIT A. radioresistens NDM-1
A. baumannii OXA-23
P. aeruginosa Loss of porine)
Stenotrophomonas maltophilia L1f)
Tyson et al. [60] Dogs 1 Other fluidsd) NR NR E. coli NDM-5
Hyun et al. [61] Dogs 10 Other fluidsd), tissuesb) NR NR P. aeruginosa VIM- 2
Misic et al. [62] Dogs 1 Urine NR NR A. baumannii OXA-72 (OXA-40-like)
Klotz et al. [63] Dogs, cats 4 Nasal swab, other fluidsd), tissuesb) NR NR Acinetobacter pittii OXA-58 (OXA-58-like)
Lupo et al. [64] Dogs, cats 7 NR NR NR A. baumannii OXA-23
Kimura et al. [65] Dogs, cats 2 Urine, other fluidsd) NO PHOS A. radioresistens IMP-1
Taj et al. [66] Cats 1 Urine NO BET/ INHIB, QUIN A. baumannii OXA-23
Bandyopadhyay et al. [67] Dogs 16 Rectal swab, vaginal swab, tissuesb) NR NR E. coli NDM-5
Oh et al. [68] Dogs 4 Stool, nasal swab, urine MERO BET/ INHIB, TET E. coli NDM-5
Cole et al. [69] Dogs, cats 6 Urine, other fluidsd), tissuesb) NO PEN, CEP, AMN, NIT, BET/ INHIB E. coli NDM-5
Brilhante et al. [38] Veterinary surfaces NA Environmental swabs NA K. pneumoniae OXA-48
Seiffert et al. [50] Pet foodg) NA Pet food packages NA Enterobacterales (undetermined species) OXA-48
Ramadan et al. [51] Veterinary surfaces NA Environmental swabs NA E. coli NDM-5, OXA-181 (OXA-48-like)
Schmidt et al. [52] Veterinary surfaces NA Environmental swabs NA E. coli OXA-48, OXA-181 (OXA-48-like)
K. pneumoniae OXA-48
E. cloacae OXA-48
Fernandes et al. [54] Household surfacesh) NA Environmental swabs NA P. aeruginosa VIM-2
First author Country Isolation place Sampled animals (n)
Animals with CR microorganisms (n)
Frequency of animals with CR (%)
Dogs Cats Total Dogs Cats Total Dogs Cats Total
Li et al. [19] China Households with backyard pig farms 92 19 111 2 0 2 2.17 0.00 1.80
Nigg et al. [20] Switzerland University veterinary hospital 76 21 97 17 4 21 22.37 19.05 21.65
Reynolds et al. [24] United Kingdom Veterinary clinics 158 27 185 1 0 1 0.63 0.00 0.54
Pulss et al. [25] Germany Veterinary microbiology laboratory 3,375 932 4,307 117 13 130 3.47 1.39 3.02
Brilhante et al. [26] Portugal Homes and university veterinary hospital 71 27 98 1 0 1 1.41 0.00 1.02
Yousfi et al. [27] Algeria Local veterinary office 116 84 200 3 2 5 2.59 2.38 2.50
Yousfi et al. [28] Algeria Local veterinary office and homes 265 49 314 4 2 6 1.51 4.08 1.91
Mairi et al. [30] Algeria NR 75 37 112 1 0 1 1.33 0.00 0.89
Cui et al. [31] China University veterinary hospital NR NR 226 1 0 1 NA NA 0.44
Hong et al. [32] South Korea Veterinary clinics 353 0 353 4 0 4 1.13 0.00 1.13
Gonzalez-Torralba et al. [33] Spain Companion animal shelter 160 0 160 1 0 1 0.63 0.00 0.63
Khalifa et al. [44] Egypt NR NR NR 1,348 3 4 7 NA NA 0.52
Hong et al. [45] South Korea Veterinary hospitals 315 74 389 4 0 4 1.27 0.00 1.03
Melo et al. [48] France University veterinary hospital 166 227 393 1 0 1 0.60 0.00 0.25
Bandyopadhyay et al. [67] India Veterinary clinics and university veterinary hospital 237 0 237 16 0 16 6.75 0.00 6.75
Herivaux et al. [56] France University veterinary hospital 104 46 150 2 0 2 1.92 0.00 1.33
Gentilini et al. [59] Italy Veterinary hospitals and homes 134 72 206 8 3 11 5.97 4.17 5.34
Hyun et al. [61] South Korea Veterinary medical teaching hospital 80 0 80 10 0 10 12.5 0.00 12.50
Klotz et al. [63] Germany Veterinary clinics 110 48 158 2 2 4 1.82 4.17 2.53
Table 1. Geographical distribution of CR isolates obtained from canines and felines, their settings, and the study type

CR, carbapenem resistant; ENB, enterobacteria; NDM, New Delhi metallo-β-lactamase; OXA, oxacillin; NR, not reported; GNFB, glucose non-fermenting bacilli; IMP, active-on-imipenem; VIM, Verona integron-encoded metallo-β-lactamase; KPC, Klebsiella pneumoniae carbapenemase; LP, loss of porine.

Carbapenemase production or loss of porins.

Intrinsic metallo-β-lactamase L1 of the species Stenotrophomonas maltophilia encoded by chromosomes.

Veterinary medical care surfaces, household surfaces, and companion animal food.

Table 2. CR in microorganisms isolated from canine and feline samples and their history of antimicrobial use

CR, carbapenem resistant; NR, not reported; NDM, New Delhi metallo-β-lactamase; NO, non-use; PEN, penicillins; BET/INHIB, beta-lactams/beta-lactam inhibitors; QUIN, quinolones; NIT, nitroimidazoles; CEP, cephalosporins; TET, tetracyclines; SUL, sulfonamides; OXA, oxacillin; MERO, meropenem; CVADs, central venous access devices; VIM, Verona integron-encoded metallo-β-lactamase; LIN, lincosamides; IMP, active-on-imipenem; KPC, Klebsiella pneumoniae carbapenemase; PHOS, phosphonic acids; NA, not applicable; AMN, aminoglycosides.

Referred to the mechanism that confers resistance to the microorganism: production of carbapenemases or loss of the bacterial target.

Included wound tissues, nasal structure, skin, abdominal cavity, anal sacs, intestine, and lung.

Included central venous catheters.

Included bronchoalveolar and tracheobronchial lavage, scrotal fluid, pus, bile, ear discharge, and eye discharge.

The authors determined that the loss of the oprD porin was caused by different mutations within the gene that caused a premature stop codon because of a large insertion, a frameshift, or a nonsense mutation.

Chromosome-encoded intrinsic metallo-β-lactamase L1 of S. maltophilia species.

Mixed wet pet food with different flavors.

Home surfaces (sofa, balcony, water cooler).

Table 3. Frequency of animals with CR isolates

CR, carbapenem resistant; NA, not applicable; NR, not reported.