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Supplementary Material

Table S1. Literature search strategy

Terms I Terms II

(carbapenem OR carbapenemase OR meropenem OR imipenem OR ertapenem)

A AND (livestock OR pig OR cattle OR cows OR poultry OR chicken OR broiler OR dairy OR milk OR farm OR pork OR beef OR farmer* OR veterinarian*)

B AND (seafood OR fish OR shellfish OR mollusks OR mussel OR oysters OR scallop OR crustacean* OR crabs OR lobster OR shrimp OR crayfish OR squid OR calamari)

C AND (companion animals OR pets OR dogs OR cats OR horses)

D AND (wildlife OR wild animals OR boars OR dear OR seagulls OR birds)

Four independent searches were performed using Terms I in combination with the Terms II versions A-D.

Table S2. Data extraction for studies investigating carbapenem-resistantEnterobacteriaceae in livestock and (sea)food

Study, country, year of sample collection

Source/Samples Technique for analysis of original samples

Phenotypic results Genotypic results

Livestock and related food items

Yaici et al., Algeria, 2015 [18]

34 milk samples and 34 swabs from mammae from 34 healthy cows on 7 farms.

Culture in nutrient broth with ERT (0.5 mg/L), then plated on MacConkey agar with IMI (1 mg/L). Isolation of colonies indicative for E. coli.

4 E. coli isolates from two cows (mamma and milk) from one farm were ERT, MER and IMI resistant.

4 isolates: blaNDM-5

Selma et al., Algeria, 2014-2015 [19]

503 cloacal samples from chickens in eight Algerian regions and 330 cloacal samples from chicken at three French

Genotypic screening for carbapenemase-encoding genes OXA, NDM, KPC, VIM (833 samples pooled in batches of 20).

NA 132/503 (26.2%) samples collected in 5/8 Algerian regions positive for blaOXA58. None of the samples from the French

1

2

3

4

5

6

7




slaughterhouses. slaughterhouses positive.

Mohamed et al., Algeria, NA [20]

Heart, liver, spleen of broiler chickens died from colibacillosis and cloacal swabs or feces from healthy chickens.

Culture on MacConkey agar. Isolation of colonies indicative for E. coli.

3 of 39 tested E. coli were MER resistant NA

Nandi et al., Bangladesh, 2009/2010 [21]

106 cloacal samples from animals at 5 poultry farms.

Culture on MacConkey agar. Isolation of Enterobacter spp. and subsequent AST.

12/18 Enterobacter spp. IMI-resistant. Resistance mechanisms not explored.

Qiao et al., China, 2007-2012 [22]

890 Salmonella isolates from chicken meat.

Phenotypic screening for ESBL and AST. ESBL-positive isolates tested for various carbapenemase-encoding genes.

96 Salmonella isolates phenotypic ESBL-producers. None of these isolates resistant to IMI or MER.

9/96 isolates (10.4%) VIM and 14 (14.6%) KPC encoding genes.

Wang et al., China, 2010 [23]

396 samples from chicken, duck, pig farms and slaughterhouses.

Culture on BHI agar with 8 µg/ml IMI. Isolates tested for carbapenemase-encoding genes.

9 carbapenem-resistant isolates derived from 396 samples: No. CRE detected. Stenotrophomonas maltophilia (n =3), Chryseobacterium indologenes (n= 3), Myroides odoratimimus (n =1), Myroides odoratus (n= 1) (all from pigs) and A. lwoffii (n= 1) (from chicken).

1 A. lwoffii: blaNDM-1. (2 Myroides sp. blaMUS-1)

Yao et al., China, 2014 [24] mcr-1 harboring isolates from chicken meat.

AST of colistin-resistant bacterial isolates. CRE tested for carbapenemase-encoding genes.

1 colistin-, IMI- and MER-resistant E. coli strain.

1 isolate: blaNDM-9

Wang et al., China, 2014/2015 [25]

739 samples from the poultry food chain (hatchery, commercial farms, farmers, slaughterhouse, supermarket).

Culture on CHROMagar KPC plates (CHROMagar Paris, France), then AST. CRE tested for carbapenemase-encoding genes. In addition, direct PCR for mcr-1 gene and carbapenemase-encoding genes from DNA extracted from the samples. For more detailed analysis of carbapenem resistance, focus on E. coli only.

245 CRE recovered from 739 (33.2%) samples. blaNDM identified in 161 E. coli (21.8%), 55 K. pneumoniae (7.4%) and 29 (3.9%) E. cloacae.

Results for direct PCR: blaNDM in 165/330 and 83/330 (50.0 and 25.2%) of samples from commercial farms, 31/50 and 5/50 (62.0 and 10.0%) from a slaughterhouse and 16/48

blaNDM in E. cloacae and K. pneumoniae. In E. coli, blaNDM variants were blaNDM-5 (n = 84), blaNDM-9 (n = 55), blaNDM-1 (n = 21), blaNDM-7 (n = 1). blaKPC not detected, 14 CR-E. coli isolates negative for all tested




and 14/48 (33.3 and 29.2%) from supermarkets.

carbapenemase genes.

Wang et al., China, 2014 [26]

1 Salmonella Indiana isolate from a chicken carcass sample.

AST of 1 Salmonella isolate. CRE tested for carbapenemase-encoding genes.

Isolate was IMI- and MER-resistant. 1 isolate: blaNDM-1

Liu et al., China, 2015 [27] Unspecified surveillance of E. coli on chicken farms.

Culture for E. coli isolates randomly led to isolation of two isolates of Cronobacter sakazakii. CRE tested for carbapenemase-encoding genes.

Two C. sakazakii isolates from two diseased chickens. Resistance against IMI and MER.


Liu et al., China, 2015 [28] Unspecified surveillance of CRE (total results not shown). 1 E. coli isolate from a chicken.

Culture on CHROMagar KPC (CHROMagar, Paris, France). Study shows only results for 1 isolate.

1 E. coli isolate (cloacal swab of a diseased chicken) ERT-, MER-, IMI-resistant.

blaNDM-17

Kong et al., China, 2015 [29]

105 anal swabs from pigs. Culture on non-selective agar. Isolation of E. coli (1 colony per agar), then AST. CRE tested for carbapenemase-encoding genes.

64/105 E. coli isolates IMI-non-susceptible and subdivided in 16 PFGE clones.

All 16 PFGE clones: blaNDM-5

He et al., China, 2015 [30] 65 samples (raw milk and faecal samples) from cows with clinical mastitis at 3 dairy cow farms.

Culture on CHROMagar KPC (CHROMagar, Paris, France). Isolation of colonies indicative for K. pneumoniae, then AST. CRE tested for carbapenemase-encoding genes.

10 K. pneumoniae isolates from agar plates MER- and IMI-resistant (n=2 from raw milk, 8 from faecal samples) from all 3 farms.


He et al., China, 2015 [31] Milk and faecal samples from 169 cows from three farms (55, 60, 54 of each farm).

Culture on MacConkey agar. Isolation of colonies indicative for E. coli, then tested for blaNDM and AST for blaNDM positive.

3 E. coli isolates from faecal samples of three cows on two farms were MER resistant.


Liu et al., China, 2015 [32] 78 E. coli isolates of diseased chickens from one farm

AST of E. coli isolates 37/78 isolates were MER resistant 34 isolates: blaNDM (incl. blaNDM-1, blaNDM-4, blaNDM-5, blaNDM-9). No carbapenemases in the remaining 3 MER-




resistant isolates

Yassin et al., China, 2004-2012 [33]

862 clinicalE. coli isolates (chickens (n = 644), pigs (n = 113), cows (n = 61) and ducks (n = 44))

AST of E.coli isolates 3 E. coli isolates (from chickens) were non-susceptible to ERT.

NA

Abdallah et al., Egypt, 2013 [34]

Retail chicken meat (112 carcasses collected).

Culture on ESBL selective agar and MacConkey agar, then AST. CRE tested for carbapenemase-encoding genes.

CRE in 12 carcasses: K. pneumoniae (n=11) and K. oxytoca (n=1).

All 12 isolates: blaNDM

Braun et al., Egypt, 2013 [35]

Rectal swabs from healthy cattle (n=210) and environmental samples (n=56).

Culture on ESBL selective agar. Isolation of E. coli indicative for ESBL, then AST. CRE tested for carbapenemase-encoding genes.

6 E. coli isolates resistant to MER and IMI. blaOXA-48 (n=5) and blaOXA-

181 (n=1)

Hamza et al., Egypt, 2014 [36]

100 samples from five poultry farms (internal organs, droppings), as well as faecal samples from humans.

Culture on MacConkey agar. Subculture of K. pneumoniae suspected colonies (based on colony morphology), then AST. CRE tested for carbapenemase-encoding genes.

35/100 samples from broiler farms with K. pneumoniae. 15/35 CR K. pneumoniae isolates from broilers. 4/40 farmers and 1/19 veterinarians carried CR K. pneumoniae.

blaKPC, blaOXA-48, blaNDM in combination (n=11 and all from humans); blaKPC and blaNDM (n = 3); blaOXA-

48 and blaNDM (n = 1).

Poirel et al., France, 2010 [37]

Rectal swabs from 50 cows at a dairy farm.

Culture on Drigalski agar containing 1 µg/ml IMI. Isolates tested for carbapenemase-encoding genes.

No CRE detected. NA

Schwaiger et al., Germany, 2004/2005 [38]

Cloacal samples and eggs from 20 laying hen farms.

Culture on E. coli selective agar (without antibiotic selection), then AST.

Of all 533 E. coli isolates, all susceptible to MER. 16 isolates resistant and 1 intermediate to IMI.

Resistance mechanisms were not explored.

Fischer et al., Germany, 2011 [39]

221 ESBL-producing Enterobacteriaceae isolates from various sources.

Culture on ESBL selective agar, then AST. CRE tested for carbapenemase-encoding genes.

1 E. coli isolate from a pig farm IMI intermediate, MER/ERT susceptible.

blaVIM-1.

Fischer et al., Germany, 221 ESBL-producing Culture on ESBL selective agar, then 3 S. enterica subsp. enterica isolates from blaVIM-1 in all three




2011 [40] Enterobacteriaceae isolates from various sources.

AST. CRE tested for carbapenemase-encoding genes.

two pig farms and a broiler farm with decreased susceptibility to carbapenems (compared to wild type).

isolates in addition to the AmpC- β-lactamase encoding gene blaACC-1

Fischer et al., Germany, 2011/2012 [41]

249 stored cultures from three swine farms (farms known to be VIM-1 positive); n= 83 farm 1, n=102 farm 2, n=64 farm 3.

Initial culture on MacConkey agar with 1 mg/L cefotaxime; this led to identification of 5 VIM-1 positive isolates in previous studies [39,40]. The complete cultures were stored, then retrospectively tested by enrichment in Luria Bertani broth with imipenem 1 mg/L.

40 VIM-1 positive isolates (n=37 E. coli, n= 3 Salmonella); 1/83 samples from farm 1; 38/102 samples from farm 2, 1/64 samples from farm 3. Overall, an additional 35 VIM-1-producing E. coli isolates were detected, which had remained undetected by screening on cefotaxime-selection agars in previous studies.

blaVIM-1 in all isolates

Roschanski et al., Germany, 2011-2013 [42]

238 anacultures from pooled feaces and environmental samples from 58 pig farms.

Initial culture on MacConkey agar with cefotaxime 1 µg/ml. Colonies harvested and stored. Here, retesting of stored anacultures using MacConkey agar with 0.125 µg/ml MER. Screening for blaVIM, blaKPC, blaNDM, blaOXA-48 and blaGES.

Selective agars grew 4 E. coli, 3 E. cloacae-complex and 1 Proteus isolates in samples from six farms. blaVIM-1 in E. coli from 1/58 (1.7%) farms.

blaVIM-1 in 2 E. coli isolates from 1 farm (same as in [39,40], but no carbapenemase genes in other species.

Singh et al., India, 2008/2009 [43]

27 Salmonella isolates from livestock and meat.

AST of Salmonella isolates. 2/27 Salmonella isolates from animals and meat MER-resistant, but all susceptible to IMI.

Resistance mechanisms not explored.

Ghatak et al., India 2012 [44]

8 E. coli isolates from cows with clinical mastitis

AST of E. coli isolates. 1/8 E. coli isolates was IMI- and MER resistant.

blaNDM-5 (according to [98])

Naik et al., India, 2013/2014 [45]

400 chevon (goat) and chicken meat samples from retail.

AST of Salmonella isolates. 1/32 Salmonella isolates IMI-resistant. Resistance mechanisms not explored.

Pruthvishree et al., India, 2014-2016 [46]

Faecal samples from piglets with (n=172) and without diarrhea (n=501).

Culture on MacConkey agar with IMI 1 mg/L.

112 E. coli isolates identified / initially isolated. Of these, 23 resistant to at least one carbapenem tested (ERT, IMI, MER).

blaNDM in 8/23 isolates (blaNDM-1 n=7, blaNDM-5 n=1); VIM, KPC, IMP, OXA not found.

Bandyopadhyay et al., India, NA [47]

Milk samples from cows with mastitis.

Culture on MacConkey agar, then AST. CRE tested phenotypically for carbapenemase production.

3. E. coli isolates non-susceptible to IMI, MER, ERT.

All isolates negative in phenotypic tests for carbapenemase or




metallo-β-lactamase production.

Pulss et al., Italy (and others), 2015/2016 [48]

7850 potentially pathogenic E. coli isolates (max. 6 per sample) from 2253 porcine faecal samples (2069 from Germany, 19 from Italy, rest: other countries).

E. coli isolates cultured on Mueller–Hinton agar with 0.5 mg/L MER. Strains from this medium tested for the carbapenemase genes blaKPC-like, blaNDM-

like, blaVIM-like and blaOXA-48-like.

11 E. coli isolates from 9 German farms and 2 isolates from one farm in Italy on MER selective medium.

blaOXA-181 in the 2 isolates from Italy. Other isolates negative for carbapenemase genes.

Diab et al., Lebanon, 2015 [49]

154 milk samples from healthy cows on 63 farms

Culture on MacConkey agar with 2 mg/L meropenem

1 K. pneumoniae isolate (from one farm (1.6%))

blaOXA-48

Al-Bayssari et al., Lebanon, 2013 [50]

40 rectal swabs from eight fowl farms

Culture on MacConkey agar with 1 mg/L ERT

1 E. coli isolate on ERT selective medium blaOXA-48

Ceccarelli et al., The Netherlands (and others), 2013-2015 [51]

4,440 faecal samples of broilers, slaughter pigs, veal calves, and dairy cows. 50 batches of imported

live ornamental fish (2 fish and 1 transport water sample per batch)

Molecular detection of blaKPC, blaNDM, blaIMP, blaOXA-48 and blaVIM directly from the samples. Isolation of the bacteria harboring these genes for the positive livestock samples using CRE selective agar, and from 12 randomly selected fish batches

4 of 7 cultured samples positive for blaOXA-48-

like genes grew Shewanella spp. (family Shewanellaceae); CRE not detected.

10 of 12 cultured samples positive for blaOXA-

48-like genes grew Shewanella spp. (family Shewanellaceae); CRE not detected.

blaKPC, blaNDM, blaIMP,

andblaVIM not detected.

blaOXA-48-like genes in 7livestock samples.

blaOXA-48-like genes in 37 fish samples and 39 transport water samples.

Ojo et al., Nigeria, 2009-2014, [52]

289 E. coli isolates from chicken faeces and 116 E. coli isolates from chicken meat.

Culture on MacConkey agar. AST to identify ESBL-producing isolates. ESBL-producing isolates tested.

Of 405 E. coli isolates, 4 ESBL-producers. Of the 4 ESBL-producing isolates, 1 ERT-resistant (MIC 2 mg/L).

Phenotypic carbapenemase test and microarray negative.

Morar et al., Romania, NA [53]

108 samples from a pig slaughterhouse (meat, environment).

AST of Salmonella isolates. 1/26 Salmonella isolates IMI-resistant. Resistance mechanisms not explored.

Hernandez et al., Spain, 1999/2000 [54]

110 Salmonella isolates from from 691 frozen and fresh chicken meat from

AST of Salmonella isolates. 7/54 S. Enteritidis and 2/32 S. Typhimuriumisolates IMI-resistant





different retail markets.

Stephan et al., Switzerland, 2012 [55]

Faecal samples from

200 pigs, 150 cattle and 110 sheep, 99 herd-level pooled samples from chickens.

Culture on Brilliance CRE agar (Oxoid, UK). Isolation, AST and testing carbapenemase phenotype and for carbapenemase-encoding genes of all oxidase-negative isolates (however, article only shows results for enterobacteria).

S. maltophilia (n=3), A. baumannii (n=4), E. coli (n=4), C. freundii (n=5). IMI MICs ranged between 0.19 and 1.5 μg/ml for Citrobacter and E. coli. Phenotypic tests for carbapenemases were negative for all enterobacterial isolates.

PCRs for blaVIM, blaGIM, blaSPM, blaSIM, blaNDM-1, blaIMI, blaKPC, blaOXA-48, blaOXA-23-like, blaOXA-40-like, blaOXA-51-like, blaOXA-58-like negative for the nine CRE.

Zurfluh et al., Switzerland, 2014/2015 [56]

Faecal samples from 83 pigs and 160 cattle at slaughterhouses

Culture on SUPERCARBA II medium (after enrichment), AST and testing carbapenemase phenotype of all isolates growing on the agar.

Aeromonas spp. (n=5), P. alcaligenes (n=1), Stenotrophomonas maltophilia (n=1). No detection of CRE.

NA

Ibrahim et al., United Kingdom, 2012/2014[57]

Slurry samples from one dairy cow farm.

Culture on non-selection agars (partly) and ESBL selective media. Isolation of E. coli (5 colonies per agar).

126 E. coli isolates tested. 6/126 isolates IMI-resistant or intermediate.


Randall et al., United Kingdom, 2013/2014 [58]

397 meat samples from retail (beef, chicken, pork).

Culture on CHROMagar KPC (CHROMagar, Paris, France) (direct and after non-selective enrichment). Isolation of colonies indicative for E. coli (red), then AST.

After enrichment, 37 samples (9.3%; 16 beef, 18 chicken, and 3 pork) with colonies indicative for CR-E. coli. None of the isolates confirmed as E. coli (Aeromonas spp. (n = 30), Hafnia alvei (n = 4), Proteus vulgaris (n = 1), Pseudomonas mosselii (n = 1) and Stenotrophomonas maltophilia (n = 1)).


Webb et al., USA, 2014 [59] 159 faecal samples from two dairy farms.

Enrichment in MacConkey broth with ERT (0.5 mg/L). Then culture on MacConkey agar with ERT (1 mg/L) (ME) and modified-SUPERCARB (SC) agar (1 colony from each agar). Analysis of isolates with positive results in carbapenemase test (all bacteria) or ERT-resistant enterobacteria in AST.

151 and 172 isolates initially obtained from SC and ME agars. Of these, 28 selected for whole genome sequencing: Aeromonas spp. (n = 18), A. baumannii (n = 1), Pseudomonas spp. (n = 6), and E. coli (n = 3). No CRE detected.

NA

Mollenkopf et al., USA, 2015 [60]

Environmental and faecal samples from four consecutive visits (a-d) at

Culture on ESBL selective medium (2 µg/ml cefotaxime), then on MacConkey agar with 1 µg/ml MER (initial visit) or

Visit a.) 2 E. coli and 1 P. mirabilis with carbapenem-resistance. Visits b.-d.) Another 15 isolates (Morganella spp.,

All carbapenem-resistant isolates with blaIMP-27 on




a pig farm (a: 30, b: 73, c: 74 samples, d: 108 samples).

0.5 µg/ml MER/70 µg/ml zinc sulfate heptahydrate (visits b-d).

Providencia spp., Proteus spp., Enterobacter spp., Citrobacter spp., Klebsiella spp., E. coli).

an IncQ1 plasmid.

Seafood

Vieira et al., Brazil, NA[61] Shrimp pond water and shrimp tissue from three shrimp farms

AST of E. coli isolates. 15/21 E. coli (70%) isolates tested were IMI-resistant


Janecko et al., Canada, 2011-2015[62]

1328 retail seafood samples incl. 928 imported fresh and frozen raw shrimp, 400 imported niche-market fresh and frozen raw seafood

Culture on chromID CARBA agar. CRE in 8/1328 (0.6%) of all samples; all imported from South East Asia: 3/928 shrimp samples (0.3%) contained carbapenem-resistant E. cloacae and E. aerogenes; 5/101 (5%) bivalve mollusk samples contained CR-E. cloacae.

E. cloacae (blaIMP-1), E. aerogenes (blaIMP-2) from shrimp, E. cloacae (blaIMP-1, blaNDM-1) from mollusks.

Morrison et al., Canada, NA[63]

121 samples (incl. products from cephalopod, tunicate, bivalve and gastropod mollusk,crustacean cnidarian, anuran, chelonian, finned

fish species, seafood medley products).

Culture on Mueller-Hinton agar with MER 2 mg/L.

CRE were not detected. 4/121 samples (imported from Korea and China) contained MER-resistant Stenotrophomonas, Myroides and Pseudomonas.

All 4 isolates contained blaOXA-48.

Sanjit Singh et al., India; 2013-2014[64]

19 samples from retail markets: fish (14), shrimps (3), clam (1), and squid (1).

Culture on MacConkey agar, isolation of Oxidase-negative colonies, then culture on ESBL-selective agar and subculture/further testing of isolates from this agar.

169 isolates growing on ESBL-selective agar. 18/169 (11%), 53 (31%) and 69 (41%) were IMI-, MER- and ERT-resistant.

blaNDM-1 deteted in two isolates (E. coli and Citrobacter diversus). Reason for carbapenem resistance in other CRE unknown (only blaNDM

was tested).

Roschanski et al., Germany, 2015-2016[65]

160 seafood samples from retail (80 shrimp, 49 blue mussels, 15 Venus clams,

Culture on unspecified agar selective for ESBL/AmpC producing bacteria. Isolates indicative for ESBL/AmpC

1/45 isolates (E. coli) was blaVIM-1 positive. This isolate was from a Venus clam and showed varying phenotypic test results

blaVIM-1 in 1 E. coli isolate




11 razor shells and five cockles)

production were tested for carbapenemase-encoding genes.

(initially IMI, MER-susceptible, then resistant)

Capkin et al. [66] Turkey Culture on eosin methylene blue agar (EMB) agar.

57/170 enterobacterial isolates were IMI-resistant (Escherichia, Citrobacter, Enterobacter, Serratia, Klebsiella, Erwinia, Yersinia)


The table is ordered according to countries in which the investigations were performed. AST = antimicrobial susceptibility testing; ERT = ertapenem; IMI = imipenem; MER = meropenem; CRE = carbapenem-resistant Enterobacteriaceae; NA = not available for Enterobacteriaceae.

89

10

11

Table S3. Data extraction for studies investigating carbapenem-resistant Enterobacteriaceae in companion animals and wildlife




Companion animals

Wang et al., China, 2014/2015 [25]

17 faecal samples from dogs at poultry farms

Culture on CHROMagar KPC plates (CHROMagar Paris, France), then AST. CRE tested for carbapenemase-encoding genes. In addition, direct PCR for mcr-1 gene and carbapenemase-encoding genes from DNA extracted from the samples. For more detailed analysis of carbapenem resistance, focus on E. coli only.

14 CRE recovered from 17 (82.4%) samples. blaNDM identified in 14E. coliisolates(100%).

Results for direct PCR: blaNDM in 17/17(100%) of samples from dogs.

E. coliblaNDM-5 (n = 12), blaNDM-9 (n = 1), blaNDM-1 (n = 1)

Yousfi et al., Algeria, 2014-2015[67]

200 rectal swab from healthy and diseased pets (116 dogs, 84 cats) at a veterinary office

After enrichment in broth (with ½ disc of 10 mg ERT) culture on MacConkey agar with 0.5 mg/L IMI and 16 mg/L vancomycin. Isolation of E. coli, then AST and test for carbapenemase-encoding genes, blaKPC, blaVIM, blaIMP, blaNDM-1, blaOXA-23-like, blaOXA-58-like, and blaOXA-48-like

5 ERT-resistant E. coli isolates (3 from dog, 2 from cats).

blaOXA-48 in 4 isolates, blaNDM-5 in 1 isolate (from a dog)

Yousfi et al., Algeria, 2015-2016 [68]

533 rectal swabs from healthy and diseased pets (265 dogs, 49 cats, 100 horses,119 pet birds) at a veterinary office, farms, pet shops

After enrichment in broth (with ½ disc of 10 mg ERT) culture on MacConkey agar with 0.5 mg/L ERT. Isolation of Enterobacteriaceae, then AST and test for carbapenemase-encoding genes, blaKPC, blaVIM, blaIMP, blaNDM-1, blaOXA-23-like,

12 IMI-susceptible isolates grew on the agar: 2E. coli from 2 dogs, 2 K. pneumoniae from 2 cats and 8 E. cloacae from 2 birds, 4 horses and 2 dogs.

E. coli, K. pneumoniae, E. cloacae (all blaOXA-48)

12




blaOXA-58-like, and blaOXA-48-like

Abraham et al., Australia, NA [69]

rectal samples of a diseased index cat and 8 other cats from 1 cat shelter

Culture on Salmonella selective agar, then AST, CarbaNP test and blaIMP PCR

4 MER-resistantSalmonella enterica Typhimuriumisolates from the index cat and 3 others.

Salmonella enterica Typhimurium (blaIMP-4)

Melo et al., France 2015 [70]

rectal swabs of 227 cats 166 dogs (unrelated, healthy) at 1 veterinary office

Culture on ESBL- and carbapenem-selective agars (ChromID and CarbaSMART, Marcy l’Etoile, France), then AST

1 ERT-non-susceptible E. coli isolate from 1 dog (previously hospitalized)

E. coli (blaOXA-48)

Schmiedel et al., Germany, 2009-2011 [71]

178 ESBL-producing isolates from clinical specimens from 100 horses, 67 dogs, 11 cats

AST of enterobacterial isolates growing on MacConkey agar with 2 mg/L cefotaxime and positive in an ESBL double disc synergy test. Then MAST carbapenemase detection test and blaOXA-48 PCR for ERT-resistant isolates.

35 or 40 of 178 isolates were ERT-resistant (unclear). Of these, 19 (16 from dogs, 2 from cats, 1 from a horse) harboured blaOXA-48. For the remaining isolates, the presence of other carbapenemase-encoding genes was not tested.

K. pneumoniae, E. cloacae (both blaOXA-48)

Stolle et al., Germany, 2012 [72]

clinical E. coli (n=1175)

and Klebsiella spp. (n=109 K. pneumoniae; n=27 K. oxytoca) isolates from dogs

AST of E. coli and Klebsiella isolates. Test for carbapenemase-encoding genes for carbapenem-non-susceptible isolates (blaOXA-48, blaVIM, blaNDM-1, blaIMP, blaKPC)

5 K. pneumoniae, 3 E. coliCarbapenem-non-susceptible isolates fromsix dogs admitted to one veterinary clinic

K. pneumoniae, E. coli (all isolates blaOXA-48)

González-Torralba et al., Spain, 2014-2015 [73]

160 rectal swabs from dogs at one veterinary hospital

Culture on selective chromogenic medium (chromID Carba Smart, bioMérieux), then AST and test for carbapenemase-encoding genes (blaOXA-48,

2 K. pneumoniae and 1 E. cloacae isolates from three dogs grew on the agar plates.

1 K. pneumoniae (blaVIM-1) isolate, the other two isolates harbored no carbapenemases




blaKPC, blaVIM, blaIMP, and blaNDM)

Shaheen et al., USA, 2008-2009 [74]

944 clinical E. coli isolates from dogs and cats; 100 isolates subjected to carbapenemase tests.

AST of E. coli isolates, the test for carbapenemase-encoding genes (blaKPC, blaNDM, blaAIM, blaGIM, blaSIM, blaDIM, blaIMP, blaVIM, blaSPM, and blaOXA-48) in isolates with reduced susceptibility for cefotaxime, ceftazidime, meropenem

100 isolates with reduced susceptibility to the antibiotics mentioned; of these, 6E. coli isolates (5 from dogs, 1 from a cat) carbapenemase-positive.

E. coli (all 6 isolates blaNDM-1)

Liu et al., USA 2009-2013 [75]

2443 clinical E. coli isolates from dogs and cats; 68 subjected to carbapenemase tests.

AST of E. coli isolates and ESBL-test (Trek Sensititre). Test for β-lactam-resistance-encoding genes that were multidrug-resistant ESBL-producers (blaCTX−Ms, blaTEM, blaSHV, blaCMY−2, blaKPC, blaNDM−1,blaOXA−48)

68 E. coli isolates were multidrug-resistant ESBL-producers, 17.6% of which were MER-resistant. 13 isolates harbored carbapenemase-encoding genes (unspecified whether from cats or dogs).

E. coli (all 13 isolates blaOXA-48)

Thungrat et al. USA 2008-2013 [76]

3172 clinical E. coli isolates from dogs and cats

AST of E. coli isolates 1.3% of 2390 isolates from dogs and 1.8% of 780 isolates from cats were MER-resistant.

E. coli (NA)

Wildlife

Wang et al., China, 2014/2015 [25]

10 faecal samples from nests of swallows at poultry farms

Culture on CHROMagar KPC plates (CHROMagar Paris, France), then AST. CRE tested for carbapenemase-encoding genes. In addition, direct PCR for mcr-1 gene and carbapenemase-encoding genes from DNA extracted from the samples. For more detailed analysis of

4 CR-E.coli recovered from 10 (40.0%) samples. blaNDM identified in 3E. coli.

Results for direct PCR: blaNDM in 6/10 (60.0%) of samples from swallows.

E. coliblaNDM-1 (n=1),blaNDM-5 (n = 2)




carbapenem resistance, focus on E. coli only.

Bachiri et al., Algeria, 2014-2016 [77]

13 individual

rectal swabs from wild boars; stool samples found along forest roads and foot paths (155 from wild boars, 212 from Barbary macaques)

After enrichment, culture on MacConkey agar with ERT (0.5 mg/L). Isolation of up to three colonies (per fecal

sample). Then AST and test for carbapenemase-encoding genes blaKPC, blaOXA-48,blaNDM

CRE in 3/168 samples (2/13 swabs and 1/155 stool samples) from wild boars and 0/212 samples from macaques (2 E. coli, 1 K. pneumoniae).

E. coli and K. pneumoniae (both blaOXA-48)

Bouaziz et al., Algeria, 2015 [78]

32 fecal samples of white stork

After pooling in batches of 1-3 samples and pre-enrichment in unselective broth, selective culture in BHI broth with ERT (1 mg/ml) and vancomycin (64 mg/ml). Then culture on MacConkey Agarwith ERT (1 mg/ml) and vancomycin

(64 mg/ml). Then AST of and test of carbapenemase-encoding genes (blaOXA-48, blaKPC, blaNDM,blaVIM,blaIMP)

3 E coli isolates were ERT-resistant and IMI-susceptible.

E. coli (blaOXA-48)

Dolejska et al., Australia 2012 [79]

504 cloacal samples from silver gull chicks (Chroicocephalus novaehollandiae) within

three nesting colonies

After enrichment in peptone water, culture on CHROMagarTM KPC (CHROMagar, Paris, France), MacConkey with MER (0.125 mg/L) and ZnSO4

(100 mg/L) (MCAmer)and Salmonella-selective agar. Test of isolates for

167 Enterobacteriaceae isolates; 150 and 17 from MCAmer and CHROMagar

KPC, respectively.

blaIMP in 120/167 isolates (72%; other genes not found). Escherichiaspp. (blaIMP-4), Klebsiella spp. (blaIMP-4, blaIMP-26), Enterobacter(blaIMP-4), Proteus spp.(blaIMP-4), Kluyvera spp.(blaIMP-4), Citrobacter spp.(blaIMP-4,




carabpenemase-encoding genes (blaIMP,blaNDM, blaKPC, blaVIM and blaOXA-48-type)

blaIMP-38)

Du et al., China, 2012 [80]

10 clinical samples from Chinese hares (Lepus sinesis) affected by pneumonia

Unspecified culture technique. AST of K. pneumoniae isolates.

K. pneumoniae in 8/10 hares. 8/8 isolates were IMI- and MER-resistant.

K. pneumoniae (NA)

Morakchi et al., France, Algeria, 2013[81]

73 stool samples from free-living feral pigeons in two Mediterranean

Cities (Annaba (n = 33) and Marseille (n = 40))

Screening for carbapenemase-encoding genes by real-time

PCR (blaOXA-23-like, blaOXA-24, blaOXA-48, blaOXA-51-like, blaOXA-58, blaNDM-1, blaVIM and blaKPC. Then testing positive samples for presence of genes typical for Acinetobacter

None. The study did not aim at identifying CRE, but carbapenemase-producing Acinetobacter. However, samples were screened for carbapenemase-encoding genes typically found in CRE as well.

No samples positive for blaNDM-

1, blaOXA-24, blaOXA-48, blaVIM or blaKPC.(genes blaOXA-23, blaOXA-51-

like, blaOXA-58and presence of Acinetobacter spp. in these samples; it was not tested whether these genes were (also) positive for CRE):

Vittecoq et al., France, 2012[82]

158 cloacal swabs samples fromgulls (yellow-leggedLarus michahellis, and slender-billed, Chroicocephalus genei) in two colonies

After enrichment in tryptone soya broth, culture on CRE selective agar (Oxoid Brilliance CRE). Then AST and test for carbapenemase-encoding genes.

22 CR-E. coliisolates from 18/93 yellow-legged gulls tested (2 gulls carried 2 and 1 gull 3 isolates). Slender-billed gulls carried no CRE.

All blaVIM-1

Fischer et al., Germany, NA[83]

Salmonella isolates from animals at a reference center

AST of Salmonella isolates. Test for carbapenemase-encoding genes for isolates with reduced susceptibility in disk diffusion test.

1 Salmonella enterica subsp. entericaserovar Corvallis isolate from a black kite with reduced susceptibility to carbapenems in disk diffusion test

blaNDM-1

Glover et al., South Africa,

300 faecal samples from baboons and

Culture on MacConkey agar then screening for E. coli-like

Of 23 Escherichia fergusonii isolates, 53%, 46% and 40% were ERT-, MER-,

Resistance mechanisms not




NA[84] vervets at two wildlife rehabilitation centers

bacteria and AST and IMI-non-susceptible. explored.

Vergara et al., Spain, 2014 [85]

132 Faecal samples from yellow-legged gulls

Culture on ESBL-selective agar then AST of E. coli isolates and test for carbapenemase-encoding genes

132 fecal samples positive for E. coli producing ESBL (68/132, 51.5%), carbapenemase (2/132, 1.5%), carbapenemase-producing isolates were MER-resistant

E. coli (positive for both blaKPC-

2, blaVIM-1) in 2/132 samples (1.5%)

13

14

Table S4.Sequence types (ST) of Enterobacteriaceae associated with carbapenemase-encoding genes

Carbapenemase Species MLST sequence types (ST)

IMP E. coli ST218 and ST101 [60]. ST541, ST1178, ST189, ST354, ST216, ST1139, ST58, ST167, ST746, ST48, ST1421, ST4657, ST4658, ST744, ST542,

ST224, ST345, ST2178, ST1114 [79]. IMP E. cloacae ST373, ST411, ST412, ST477, ST478 [62].

IMP Salmonella serovar Typhimurium ST19 [69]

KPC & VIM E. coli ST1011, ST354 [85].

NDM E. coli ST2 [31], ST446 [31], ST1284 [18], ST167 [24], ST48 [28], as well as 36 different STs in 161 isolates among which ST156 (n=31), ST101 (n=19) and ST746 (n=13) were predominant[25].

64 isolates belonged to 16 different STs (predominant ST48 (n=12), ST4463 (n=8)) [29]. NDM K. pneumoniae ST17, ST530, ST1661, ST2108 and ST2293 [30].

NDM E. cloacae ST479 [62].

NDM Salmonella serovar Corvallis ST1541 [83].

OXA E. coli ST38, ST359 and ST641 [48,50]. ST38 [78] ST635 [77]. ST12, ST131, ST405, ST648, ST1800, ST1088 [75]. ST372 [70]. ST1196, ST1431 [72].

OXA K. pneumoniae ST530 [49]. ST13 [77]. ST15 [72].

OXA E. cloacae ST527 [68].

VIM E. coli ST88 and ST10 [39,65].

VIM Salmonella serovar Infantis ST32 [40].

VIM K. pneumoniae ST2090 [73].

MLST = Multilocus Sequence Typing

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16

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Table S5. Prevalence of Carbapenem-resistant Enterobacteriaceae(CRE) in studies using selective screening approaches

Country No. of samples positive for CRE or carbapenemases/ no. of all samples tested

Prevalence Type of specimens, comments

Algeria [18] 2/34 6% Milk and mammal swabs from cows. Positive cows were from 1/7 farms tested; farm prevalence 14%.

Algeria [19] 132/503(blaOXA-58) 26.2% Faecal samples from chickens.

Algeria [67] 3/116 (dogs), 2/84 (cats) 2.6% (dogs, 2.4% (cats) Rectal swabs from healthy and diseased dogs and cats.

Algeria [68] 2/49 (cats), 4/100 (horses), 2/119 (pet birds), 4/265 (dogs)

4% (cats), 4% (horses), 1.7% (pet birds), 1.5% (dogs)

Rectal swabs from healthy and diseased dogs, cats, horses, pet birds.

Algeria [77] 2/13 (rectal swabs), 1/155 (boar stool samples), 0/212 (macaque stool samples)

15.4% (rectal swabs), 0.6% (stool boars), 0% (stool macaques)

Rectal swabs from wild boars, stool samples from wild boars, stool samples from macaques. For stool samples unspecified from how many animals the samples were obtained (collected along the way).

Algeria [78] Not available Not available Selective approach used, but data cannot be interpreted regarding prevalence, as samples were pooled and it is unspecified from how many pools the isolates were obtained.

Australia [79] 80/504 15.9% Cloacal samples from gulls. Positive samples were from 1/3 nests tested; nest prevalence 33.3%

Canada [62] 8/1328 0.6% Imported retail seafood samples.

Canada [63] 4/121 0.3% Seafood samples.

China [23] 0/396 0% Samples from chicken, duck, pig farms and slaughterhouses.

China[25] 0/120& 0/120 (a), 165/330 & 83/330 (b), 31/50 & 5/50 (c), 16/48 & 14/48 (d), 6/10& 4/10 (e), 3/6& 3/6 (f), 17/17 & 14/17 (g), 62/120& 31/120 (h)

0/0% (a), 50/25% (b), 62/10% (c), 33/29% (d), 60/40% (e), 50/50% (f), 100/82% (g), 52/26% (h)

a.) Cloacal swabs from 2 hatchery farms; b.) cloacal swabs from batches of chickens at four commercial farms; c.) caecafrom slaughterhouses; d.) meat from supermarkets;e.) faecal swabs from swallow nests; f.)faecal swabs from farmers; g.)faecal swabs from dogs; h.) flies.

Prevalence data shown for PCR directly from the specimen / culture (%).

China [28] Not available Not available Selective approach used, but prevalence-related data not shown

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Country No. of samples positive for CRE or carbapenemases/ no. of all samples tested

Prevalence Type of specimens, comments

China [30] 10/65 15.4% Milk and faecal samples from three farms

France[70] 0/227 (cats), 1/166 (dogs) 0%(cats), 0.6% (dogs) Rectal swabs of unrelated healthy cats and dogs

France, Algeria [81] 0/73 0% Stool samples from pigeons. Describes the prevalence for the genesblaNDM-1, blaOXA-24, blaOXA-48, blaVIM or blaKPC. For blaOXA genes it was not tested by culture-based methods whether they occurred in CRE or in Acinetobacter.

France [82] 18/93 (YL), 0/65 (SB) 19.4% (YL), 0% (SB) Cloacal samples from yellow-legged (YL) gulls (from1 colony) and slender-billed (SB) gulls from 1 colony)

India [46] 23/673 (culture), 8/673 (PCR) 3.4% (culture), 1.2% (PCR) Piglets

Lebanon [49] 1/154 (cows), 0.7% (cows) Milk samples from healthy cows. Positive samples were from 1/63 farms tested; farm prevalence 1.6%.

Lebanon [50] 1/40 2.5% Rectal swabs from fowl. Positive samples were from 1/8 farms tested; farm prevalence 12.5%.

Netherlands [51] 0/4440 (culture) 0% Faecal samples from broilers, slaughter pigs, veal calves, and dairy cows. blaOXA-like

genes in 0.16% of these samples, but chromosomally encoded and associated with Shewanella spp. rather than with Enterobacteriaceae.

Spain[73] 1/160 0.6% Rectal swabs from dogs at one veterinary hospital.

Switzerland [55] 0/200 (pigs), 0/150 (cattle), 0/110 (sheep), 0/99 (chicken herds)

0% Faecal samples from pigs, cattle, sheep, chickens.

Switzerland [56] 0/83 (pigs), 0/160 (cattle) 0% Faecal samples from pigs and cattle at slaughterhouses.

UK [58] 0/397 0% Meat samples from retail (beef, chicken, pork).

USA [59] 0/159 0% Faecal samples from two dairy farms.

USA [60] 3/30 (a), 0/73 (b), 15/74 (c), 10/108 (d)

6.7% (a), 20.3% (c) Environmental and faecal samples from four consecutive visits (a-d) at one pig farm. The prevalence is not comparable, as sampling techniques changed over time.

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