Table 1.
Descriptions of non-antimicrobial factors, tested antimicrobials, bacteria and, animal species in animal population citations (n = 39) that investigated associations between antimicrobial resistance and non-antimicrobial factors
| Antimicrobial class | Antimicrobial (n*) | Bacteria (n*) | Animal species (n*) | Description of factor(s) | Reference |
|---|---|---|---|---|---|
| Aminoglycosides | Apramycin (n = 5) | E. coli (n = 5), Salmonella enterica (n = 1) | Pig (n = 4), cow (n = 1) | Non-conventional management†; Contact with other animals treated with antimicrobials; Treatment with oral competitive exclusion culture made from piglets | [28–32] |
| Gentamicin (n = 12) | E. coli (n = 6), Enterococcus species (n = 1), Campylobacter species (n = 3) | Cow (n = 5), pig (n = 5), chicken (n = 2) | Non-conventional management; Feeding silage or grain; Dietary zinc or copper | [32–43] | |
| Kanamycin (n = 9) | E. coli (n = 4), Campylobacter species (n = 1), Salmonella enteria (n = 3), coliforms (n = 2) | Pig (n = 4), cow (n = 3), chicken (n = 2) | Non-conventional management | [32, 33, 35, 37, 39, 40, 43–45] | |
| Neomycin (n = 4) | E. coli (n = 2), coliforms (n = 2) | Cow (n = 1), pig (n = 3) | Non-conventional management | [44–47] | |
| Spectinomycin (n = 1) | Enterococcus species (n = 1) | Pig (n = 1) | Herd size; Bringing new animals onto the farm | [36] | |
| Streptomycin (n = 14) | E. coli (n = 7), Campylobacter species (n = 2), Salmonella enterica (n = 2) | Cow (n = 5), pig (n = 7), chicken (n = 2) | Non-conventional management; Health status; Treatment with oral competitive exclusion culture made from piglets; Dietary zinc or copper; Pen/group/herd size; Number of suppliers; Education; Bringing new animals onto the farm | [32, 33, 35, 37–39, 44–49] | |
| Vancomycin (n = 2) | Enterococcus species (n = 2) | Cow (n = 2) | Non-conventional management; Dietary zinc and copper | [38, 50] | |
| β-lactams | Ampicillin (n = 18) | E. coli (n = 9), Salmonella enterica (n = 3), Campylobacter species (n = 1), coliforms (n = 4) | Pig (n = 6), cow (n = 8); chicken (n = 2), dog (n = 2) | Non-conventional management; Diet associated with a risk of ruminal acidosis; Bringing new animals onto the farm; Pen/group/herd size; Treatment with oral competitive exclusion culture made from piglets; Education; Oral recombinant β-lactamase administration in dogs treated with parenteral ampicillin. | [28, 32–37, 39, 40, 43–45, 47, 50–54] |
| Amoxicillin-clavulanic acid (n = 7) | E. coli (n = 4), Salmonella enterica (n = 3), Campylobacter species (n = 1) | Pig (n = 2), cow (n = 3); chicken (n = 2) | Non-conventional management; Bringing new animals onto the farm; Pen/group/herd size | [32, 33, 35, 37, 39, 40, 43] | |
| Carbenicillin (n = 1) | Coliforms (n = 1) | Pig (n = 1) | Non-conventional management | [45] | |
| Cefoxitin (n = 5) | E. coli (n = 3), Salmonella enterica (n = 2) | Pig (n = 2), cow (n = 3), chicken (n = 1) | Non-conventional management; Bringing new animals onto the farm; Pen/group/herd size | [32, 33, 39, 43, 50] | |
| Ceftiofur (n = 5) | E. coli (n = 3), Salmonella enterica (n = 2) | Pig (n = 2), cow (n = 2), chicken (n = 1) | Non-conventional management; Pen/group/herd size | [33, 35, 39, 43, 54] | |
| Ceftriaxone (n = 7) | E. coli (n = 3), Salmonella enterica (n = 3), Campylobacter species (n = 1), Enterococcus species (n = 1) | Pig (n = 2), cow (n = 3), chicken (n = 2) | Non-conventional management; Pen/group/herd size | [33, 35, 37, 39, 40, 43, 50] | |
| Cephalothin (n = 8) | E. coli (n = 4), Salmonella enterica (n = 3), coliforms (n = 1) | Pig (n = 2), cow (n = 3), chicken (n = 2), dog (n = 1) | Non-conventional management; Bringing new animals onto the farm; Pen/group/herd size; Oral recombinant β-lactamase administration in dogs treated with parenteral ampicillin | [32, 33, 35, 39, 40, 43, 52, 54] | |
| Penicillin (n = 4) | E. coli (n = 1), Enterococcus species (n = 2), coliforms (n = 1) | Pig (n = 1), cow (n = 3) | Non-conventional management; Dietary copper and zinc | [38, 44, 50, 54] | |
| TEM genes (n = 1) | Dog (n = 1) | Oral recombinant β-lactamase administration in dogs treated with parenteral ampicillin | [51] | ||
| Carbadox | Carbadox (n = 2) | E. coli (n = 2) | Pig (n = 2) | Ration supplemented with egg yolk with anti-Salmonella antibody; Bringing new animals onto the farm | [31, 36] |
| Lipopeptide | Daptomycin (n = 1) | Enterococcus species (n = 1) | Cow (n = 1) | Non-conventional management | [50] |
| Macrolides | Azithromycin (n = 2) | Campylobacter species (n = 2) | Pig (n = 1), cow (n = 1) | Non-conventional management | [37, 42] |
| Erythromycin (n = 6) | E. coli (n = 1), Campylobacter species (n = 5), Enterococcus species (n = 1) | Pig (n = 3), cow (n = 3) | Non-conventional management; Ad libitum or restricted feeding; Dietary copper and zinc; Health status | [37, 38, 41, 42, 44, 49, 50] | |
| Macrolides (n = 2) | E. coli (n = 1),Campylobacter species (n = 1) | Pig (n = 1), cow (n = 1) | Steamed flaked corn with or without wet distillers; Dietary copper | [55, 56] | |
| Tilmicosin (n = 1) | E. coli (n = 1) | Cow (n = 1) | Dietary copper and zinc | [38] | |
| Tylosin (n = 2) | E. coli (n = 1), Enterococcus species (n = 1) | Cow (n = 2) | Non-conventional management; Dietary copper and zinc | [38, 50] | |
| ermB gene (n = 1) | Coliforms (n = 1) | Cow (n = 1) | Steamed flaked corn with or without wet distillers | [55] | |
| Nitrofurans | Nitrofurantoin (n = 1) | Enterococcus species (n = 1) | Pig (n = 1) | Pen/group/herd size; Bringing new animals onto a farm | [36] |
| Oxazolidinones | Linezolid (n = 2) | Enterococcus species (n = 2) | Cow (n = 2) | Non-conventional management; Dietary copper and zinc | [38, 50] |
| Phenicols | Chloramphenicol (n = 10) | E. coli (n = 5), Enterococcus species (n = 2), Salmonella enteria (n = 2), Campylobacter species (n = 2) | Cow (n = 6), pig (n = 3), chicken (n = 1) | Non-conventional management; Dietary copper and zinc; Pen/group/herd size; Number of suppliers; Bringing new animals onto the farm | [32, 35, 37–41, 43, 47, 50] |
| Florfenicol (n = 1) | Campylobacter species (n = 1) | Cow (n = 1) | Non-conventional management | [37] | |
| Phosphoglycolipid | Flavomycin (n = 2) | Campylobacter species (n = 1), Enterococcus species (n = 1) | Cow (n = 2) | Non-conventional management; Steamed corn with or without wet distillers | [50, 55] |
| Pleuromutilin | Tiamulin (n = 1) | E. coli (n = 2) | Cow (n = 2) | Dietary copper and zinc | [38] |
| Quinlones/Fluoroquinolones | Ciprofloxacin (n = 8) | E. coli (n = 3), Campylobacter species (n = 4), Enterococcus species (n = 1) | Pig (n = 5), cow (n = 3) | Non-conventional management; All-in/all-out system; Dietary copper and zinc; Ration with or without whey; Ad libitum or restricted feeding Health status; Disinfection; Rodent control | [35, 37–39, 41–43, 49] |
| Nalidixic acid (n = 7) | E. coli (n = 3), Campylobacter species (n = 4) | Pig (n = 4), cow (n = 3) | Non-conventional management; Pen/group/herd size | [35, 37, 39, 41–43, 47] | |
| Streptogamins | Quinpristin/dalfopristin (n = 1) | Campylobacter species (n = 1) | Cow (n = 1) | Steamed flaked corn with or without wet distillers | [55] |
| Sulphonamides/Pyrimidines | Sulfadimethoxine (n = 2) | E. coli (n = 2) | Cow (n = 2) | Non-conventional management; Steamed flaked corn with or without wet distillers | [54, 55] |
| Sulfamethizole (n = 1) | Coliforms (n = 1) | Pig (n = 1) | Non-conventional management | [44] | |
| Sulfamethoxazole (n = 6) | E. coli (n = 5), Campylobacter species (n = 1) | Pig (n = 2), cow (n = 4) | Non-conventional management; Pen/group/herd size; Number of supplies; Bringing new animals onto the farm; Education | [32, 35, 37, 39, 43, 47] | |
| Sulfasoxazole (n = 3) | E. coli (n = 2), Salmonella enterica (n = 1), coliforms (n = 1) | Pig (n = 2), chicken (n = 1) | Non-conventional management; Pen/group/herd size; Bringing new animals onto the farm | [40] | |
| Sulfathiazole (n = 1) | E. coli (n = 1) | Cow (n = 1) | Steamed flaked corn with or without wet distillers | [55] | |
| Sulfachloropyridazine (n = 1) | E. coli (n = 1) | Cow (n = 1) | Steamed flaked corn with or without wet distillers | [55] | |
| Trimethoprim- sulfamethoxazole (n = 6) | E. coli (n = 5), Salmonella enterica (n = 1), coliforms (n = 1) | Pig (n = 2), cow (n = 2), dog (n = 1) | Non-conventional management; Pen/group/herd size; Number of suppliers; Education; Bringing new animals onto the farm; Oral recombinant β-lactamase administration in dogs treated with parenteral ampicillin | [32, 35, 39, 43, 47, 52] | |
| Tetracyclines | Tetracycline (n = 21) | E. coli (n = 11), Salmonella enterica (n = 3), Campylobacter species (n = 6), Enterococcus species (n = 1), coliforms (n = 1) | Pig (n = 12), cow (n = 6), chicken (n = 2), dog (n = 1) | Non-conventional management; All-in/all-out; Ventilation system; Contact with animals treated with antimicrobials; Disinfection and sanitation; Ration supplemented with egg yolk with anti-Salmonella antibody; Flooring; Pen/group/herd size; Diet associated with a risk of ruminal acidosis; Education; Bringing new animals onto the farm; Number of suppliers; Treatment with oral competitive exclusion culture made from piglets; Oral recombinant β-lactamase administration in dogs treated with parenteral ampicillin; Health status; Silage vs. a grain based ration. | [28, 30–37, 39–45, 47, 49, 50, 52–54, 57, 58] |
| tetM gene (n = 1) | Cow (n = 1) | Steamed flaked corn with or without wet distillers | [55] | ||
| Other | Any resistance (n = 5) | E. coli (n = 3), Salmonella enterica (n = 1), coliforms (n = 1) | Cow (n = 3), pig (n = 2) | Non-conventional management; All-in/all-out; Pen/group/herd size; Health status | [45, 59–62] |
| Multiple resistance‡ (n = 15) | E. coli, Salmonella enterica, Campylobacter species, coliforms | Cow (n = 6), pig (n = 6), chicken (n = 2), dog (n = 1) | Non-conventional management; Health status; All-in/all-out; Ad libitum or restricted feeding; Disinfection and sanitation; Bringing new animals onto the farm; Mixing of animals from different sources; Pen/group/herd size; Oral recombinant β-lactamase administration in dogs treated with parenteral ampicillin; Addition of live S. cerevisisae boulardii to milk replacer | [32, 33, 35, 40–42, 44, 45, 49, 52, 61, 63–66] |
*
Number of citations.
†
The following management systems as defined in the studies were aggregated under non-conventional management systems: organic, antimicrobial-free, extensive (e.g. pasture raised pigs), natural production, animal friendly or ecological.
‡
Multiple drug resistance was captured from studies where multiple drug resistance was defined and investigated, as well as any study where susceptibility two or more antimicrobials in combination were reported (excluding trimethoprim-sulfamethoxazole and quinpristin-dalfopristin).