Table J.2.
Findings and some key limitations of the studies identified
| Study ID | Observational study type | Location | Data analysis | Number of AM evaluated | Study findings | |
|---|---|---|---|---|---|---|
| Account for farm‐level clustering | Confounders/correlated risk factors controlled for | |||||
| 1 | Cross‐sectional | EU [Denmark, France, Italy, Sweden] | Yes | Not stated | Multiple antimicrobials tested | In each of the four countries, resistance to intestinal E. coli (ampicillin, streptomycin, sulfonamides, trimethoprim) was significantly lower in organic than conventional pigs. There were also large differences between countries within each production type |
| 2 | Cross‐sectional | EU [Denmark, France, Italy, Sweden] | No | Country | Multiple antimicrobials tested | There were no extensive differences between the abundance of AMR genes in samples from organic or conventional housed pigs. Samples from southern European countries exhibited significantly higher AMR gene abundance than those from northern Europe |
| 3 | Cross‐sectional (at two points in the production cycle) | EU [Netherlands] | Yes | Not stated | Single antimicrobial (beta‐lactams) | MRSA was not detected in broiler and human samples on organic farms. At 34 days of age, there was no difference by production system in the prevalence of ESBL/AmpC‐producing E. coli. On organic farms, there was an observed fall in the prevalence of ESBL/AmpC‐producing E. coli by day 68 |
| 4 | Cross‐sectional | EU [Portugal] | No | None | Multiple antimicrobials and MDR tested | AMR was common among Campylobacter spp.isolates from both organic and intensive poultry production systems. Isolates from all origins were resistant to fluoroquinolones and tetracyclines. For ciprofloxacin and ofloxacin and for MDR, isolates from extensive indoor chicken were significantly less resistant than that from organic and intensive production |
| 5 | Cross‐sectional | EU [Netherlands] | No | None | MDR tested | The majority of organic chicken meat samples were contaminated with ESBL‐ producing E. coli. Prevalence of ESBL‐producing microorganisms was 100% on conventional and 84% on organic samples (p < 0.001). Median loads of ESBL‐producing microorganisms were 80 (range < 20–1,360) in conventional, and < 20 (range 0–260) CFU/25 g in organic samples (p = 0.001). Co‐resistance rates of ESBL‐positive isolates were: co‐trimoxazole 56%, ciprofloxacin 14%, and tobramycin 2% (no significant differences between organic and conventional isolates). Tetracycline co‐resistance was more prevalent in conventional than in organic samples (73% vs 46%, p < 0.001) |
| 6 | Cross‐sectional | EU [Germany] | No | Type of meat, store and store chain | Single antimicrobial tested | No differences could be observed in the prevalence of ESBL producers between organic and conventional samples |
| 7 | Cross‐sectional | EEA [Norway] | No | parity distributions, proportion dried off quarters, AI vs natural mating, season for first AI | Single antimicrobial tested | There was no significant association between AMR and herd type. There was few S. aureus isolates exhibiting wresistance to penicillin in both management systems: 8.8% and 14% in conventional and organic farming, respectively. Penicillin resistance against coagulase‐negative staphylococci isolated from subclinically infected quarters was 48.5% in conventional herds and 46.5% in organic herds |
| 8 | Cross‐sectional | EU [Spain] | No | Not stated | Multiple antimicrobials tested | In comparison with meat from conventionally raised pigs, E. coli isolates from organic pork meat were significantly less resistant to several antimicrobials (ampicillin, doxycycline, sulfisoxazole) |
| 9 | Cross‐sectional | EU [Spain] | No | Not stated | Multiple antimicrobials and MDR tested | In comparison with meat from conventionally raised chickens, E. coli isolates from organic chicken meat were significantly less resistant to 7 of 10 antimicrobials tested. For S. aureus and Listeria monocytogenes, AMR was significantly higher only for doxycycline |
| 10 | Cross‐sectional | EU [Germany] | No | Not stated | MDR tested | AMR rates and mean inhibitory concentrations of bacteria isolated from organic systems had lower values than from conventional systems |
| 11 | Cross‐sectional | EU [Spain] | No | Not stated | Multiple antimicrobials tested | In comparison with meat from conventionally raised chickens, Enterococcus spp. isolates from organic chicken meat were significantly less resistant to several antimicrobials (ampicillin, chloramphenicol, doxycycline, ciprofloxacin, erythromycin, vancomycin) |
| 12 | Cross‐sectional & longitudinal | EU [Denmark] | Yes | Not stated | Single antimicrobial tested (penicillin) | No statistically significant differences were observed in the prevalence of S. aureus resistant to penicillin between herd groups |
| 13 | Cross‐sectional | EU region [Switzerland] | No | Not stated | Multiple antimicrobials tested | The frequency of AMR on organic farms was not different from conventional farms |
| 14 | Cross‐sectional | EU [Belgium] | No | Health status and farming practices info collected but not stated if they were taken into account in the analysis | Multiple antimicrobials tested | Lower levels of antimicrobial resistance were observed among major mastitis pathogens on organic compared to conventional farms. Marked differences were seen for S. uberis, S. aureus, S. dysgalactaie in favour of organic farming but not for coagulase‐negative staphylococci |
| 15 | Cross‐sectional | EU [Denmark] | No | None | Multiple antimicrobials tested | The prevalence of Campylobacter spp.isolates was higher in organic compared to either conventional or extensive indoor broiler rearing farms. In the present investigation, low numbers of AMR isolates (six of 62 isolates) hampered comparison of resistance patterns of C. jejuni as well as of C. coli isolates between the three rearing systems. Thus, no relation between resistance pattern and origin of the Campylobacter spp. isolates could be established |
| 16 | Cross‐sectional | Non‐EU [USA] | Yes | Not stated | Multiple antimicrobials tested | Evidence of association. On two organic farms compared to three conventional farms, isolates has significantly lower resistance to ciprofloxacin, erthyromycin and tylosin. On a third organic farm (excluded after external validation of results), a relatively high number of AMR Campylobacter spp. were isolated |
| 17 | Cross‐sectional | Non‐EU [South Korea] | No | Not stated | Multiple antimicrobialstested | Isolates of Salmonella Gallinarum from organic and conventional isolates showed similar antimicrobial susceptibilities. Overall resistance was very low for the majority of agents tested |
| 18 | Cross‐sectional | Non‐EU [US] | No | Not stated | Multiple antimicrobials tested | E. coli isolates from conventional systems were significantly more resistant to a range of antimicrobials, compared to conventional systems. Results show that E. coli isolates from conventional systems were significantly more resistant to amoxicillin, ampicillin, chlortetracycline, erythromycin, kanamycin, neomycin, streptomycin, tetracyclines, and tylosin (p < 0.001) |
| 19 | Cross‐sectional | Non‐EU [Korea] | No | Not stated | MDR tested | The prevalence of AMR in Salmonella spp. isolates was significantly higher in pigs from conventional than from organic farms. The prevalence of AMR, MDR phenotype, and resistance to tetracyclines, ampicillin, and gentamicin were significantly higher in swine Salmonella spp. isolates from conventional farms than those from organic farms |
| 20 | Cross‐sectional | Non‐EU [USA] | No | Not stated | Single antimicrobial tested | The prevalence of meticillin‐resistant S. aureus (MRSA) and methicillin‐resistant CNS was low, and no more prevalent in bulk tank milk from either organic (2% resistant coagulase‐negative staphylococci) or conventional (5%) herds |
| 21 | Cross‐sectional | Non‐EU [USA] | No | GROCERY STORE, STORE CHAIN, AND PROCESSING PLANT | Multiple antimicrobials and MDR tested | Similar levels of commensal bacteria harbouring genes conferring resistance were found in organic and ‘antibiotic‐free’ labelled meat compared to meat from conventional farms. Fluoroquinolone‐resistant E. coli recovered using selective media were more common (p < 0.05) in conventional (18.9%) compared to organic (0) and ‘antibiotic‐free’ (2.1%) packages |
| 22 | Cross‐sectional | Non‐EU [USA] | Yes | Not stated | Multiple antimicrobials tested | Among S. Kentucky isolates (n = 41), per cent resistance was statistically significantly lower among isolates recovered from newly organic vs conventional poultry houses for: amoxicillin‐clavulanate (p = 0.049), ampicillin (p = 0.042), cefoxitin (p = 0.042), ceftiofur (p = 0.043) and ceftriaxone (p = 0.042). Per cent MDR (resistance to ≥ 3 antimicrobial classes) was also statistically significantly lower among S. Kentucky isolates recovered from newly organic poultry houses (6%) compared to those recovered from conventional houses (44%) (p = 0.015) |
| 23 | Cross‐sectional | Non‐EU [USA] | Yes | Not stated | Multiple antimicrobials tested | The percentages of AMR Enterococcus faecalis and AMRE. faecium were significantly lower (p < 0.05) among isolates from newly organic vs conventional poultry houses for two (erythromycin and tylosin) and five (ciprofloxacin, gentamicin, nitrofurantoin, penicillin, and tetracyclines) antimicrobials, respectively. Forty‐two per cent of E. faecalis isolates from conventional poultry houses were multidrug resistant (MDR; resistant to three or more antimicrobial classes), compared with 10% of isolates from newly organic poultry houses (p = 0.02); 84% of E. faecium isolates from conventional poultry houses were MDR, compared with 17% of isolates from newly organic poultry houses (p < 0.001) |
| 24 | Cross‐sectional | Non‐EU [USA] | No | Meat brand | MDR tested | No difference was observed in resistance levels for bacteria isolated from organic chicken and conventional products. The frequency of AMR E. coli tended to be only slightly lower for RWA (raised without antimicrobials), and organic chicken was statistically indistinguishable from conventional products that have no restrictions. Over half of all strains collected exhibited resistance to one or more antimicrobials: 55%, 58%, 60%, and 76% from conventional, RWA, organic, and kosher chicken samples, respectively |
| 25 | Cross‐sectional | Non‐EU [USA] | No | Not stated | MDR tested | During the transition from conventional to organic on two farms, there was a significant decrease in CNS isolates deemed resistant to β ‐lactam antimicrobials, but no significant changes in the sensitivity patterns of antimicrobials to Streptococcus spp. or S. aureus |
| 26 | Cross‐sectional | Non‐EU [USA] | No | Salmonella serovar, chicken type, chicken brand, supermarket chain, store, and sampling date | MDR tested | Salmonella Kentucky isolates from organic chicken samples were susceptible to 11 of the antimicrobials tested, whereas those from conventional chickens were only susceptible to 4 antimicrobials. Three S. Kentucky isolates from conventional chickens possessed multidrug resistance phenotype MDR‐AmpC |
| 27 | Cross‐sectional and Longitudinal | Non‐EU [New Zealand] | No | Not stated | MDR tested | Higher levels of AMR in E. coli and Enterococcus spp. were observed in pigs from conventional compared to organic farms. Isolates of E. coli from conventional pig farms were resistant to gentamicin (0.7%), neomycin (0.7%), ampicillin (2.7%), cotrimoxazole (11%), streptomycin (25%) and tetracyclines (60%). Enterococcus spp. isolates from the same farms were resistant to erythromycin (68%), tetracyclines (66%), streptomycin (54%) and virginiamycin (49%). By contrast, for the organic pig farm < or = 5% of either the E. coli or the Enterococcus spp. isolates were resistant to any of the antimicrobials tested |
| 28 | Cross‐sectional | Non‐EU [USA] | Yes | Not stated | Multiple antimicrobials tested | A larger proportion of isolates from organic rather than conventional farms were susceptible to erythromycin, pirlimycin and tetracyclines. For pirlimycin and tetracycline, different patterns of susceptibility were observed among Staphylococcus categories. This latter result suggests that multiple management practices, including some unrelated to antimicrobial usage, may contribute to the observed difference in susceptibility |
| 29 | Cross‐sectional | Non‐EU [USA] | Yes | Herd size | Multiple antimicrobials tested | Compared with antimicrobial free farms, conventional farms has significantly higher levels of resistance to ampillicin, sulfamethoxazole, tetracyclines and chloramphenicol. Cessation of antimicrobial usage did not appear to result in an immediate reduction in AMR |
| 30 | Cross‐sectional | Non‐EU [USA] | No | Not stated | MDR tested | Resistance to at least one antimicrobial was observed in 18 (62%) isolates from conventional farms and in 11 (48%) isolates from organic farms. The percentage of MDR was 17.2%, 4.3%, and 10% in isolates from conventional farms, organic farms, and exhibition barns at county fairs, respectively. No significant difference in recovery of MDR between isolates from conventional and organic farms was observed |
| 31 | Cross‐sectional | Non‐EU [USA] | No | Not stated | Multiple antimicrobials tested | Variable results were obtained. This study demonstrated a dose–response effect for several antimicrobial drug exposures and the MIC of the studied pathogens (S. aureus & pirlimycin p = 0.04; CNS & erythromycin p = 0.038, penicillin p = 0.007 pirlimycin p < 0.001, tetracyclines p = 0.004 Streptococci: pirlimycin p < 0.001 and tetracycline p = 0.001) |
| 32 | Cross‐sectional | Non‐EU [USA] | No | Not stated | MDR tested | Salmonella prevalence was not different between conventional and organic farms. A higher frequency of resistance was observed on conventional farms. MDR (resistance to three or more classes of antimicrobials) was found in 69% of the isolates from conventional farms and 11% on pasture farms (p < 0.0001), with the predominant resistance type of AmCSSuTeAx (ampicillin, chloramphenicol, streptomycin, sulfasoxazole, tetracyclines, amoxicillin/clavulanic acid; 62%). About 5% of the pasture isolates showed the AmAxCFCRO (ampicillin, amoxicillin/clavulanic acid, cephalothin, ceftriaxone) MDR pattern |
| 33 | Cross‐sectional | Non‐EU [USA] | Yes | age of cattle | Multiple antimicrobials tested | Study discovered a significant association between low MDR, organic farms, and strains of the numerically dominant phylogroup B1. The results suggest that organic farming practices changes the frequency of AMR isolates, and also impacts the genetic composition of the resident E. coli flora in the overall population |
| 34 | Cross‐sectional | Non‐EU [USA] | No | Not stated | Multiple antimicrobials and MDR tested | Salmonella prevalence was significantly higher among antimicrobial free compared to conventional farms. In general, antimicrobial resistance is more common in conventional farms. Frequency of resistance to most classes of antimicrobials (except tetracyclines) was significantly higher among conventional farms than antimicrobial‐free farms, with ORs ranging from 2.84 for chloramphenicol to 23.22 for kanamycin at the on‐farm level. A pentaresistance pattern with ampicillin, chloramphenicol, streptomycin, sulfamethoxazole, and tetracyclines was strongly associated with antimicrobial‐free groups (OR = 5.4; p = 0.01). Distinct MDR isolates of Salmonella spp. were common in antimicrobial‐free herds |
| 35 | Cross‐sectional | Non‐EU [USA] | No | Not stated | Multiple antimicrobials tested | Similar levels of AMR were found in organic and conventional farms. The proportion of AMR isolates was higher for conventional than for organic farms. |
| 36 | Cross‐sectional | Non‐EU [USA] | No | Not stated | Multiple antimicrobials tested | The AMR rates were significantly different between the organic and conventional farms. Less than 2% of Campylobacter spp. isolates from organically raised poultry were resistant to fluoroquinolones, while 46% and 67% of Campylobacter spp.isolates from conventionally raised broilers and conventionally raised turkeys, respectively, were resistant to these antimicrobials. In addition, a high frequency of resistance to erythromycin (80%), clindamycin (64%), kanamycin (76%), and ampicillin (31%) was observed among Campylobacter spp. isolates from conventionally raised turkeys. None of the Campylobacter spp. isolates obtained in this study was resistant to gentamicin, while a large number of the isolates from both conventional and organic poultry operations were resistant to tetracyclines. MDR was observed mainly among Campylobacter spp. isolates from the conventional turkey operation (81%). Findings from this study clearly indicate the influence of conventional and organic poultry production practices on AMR of Campylobacter spp. isolates on poultry farms |
| 37 | Cross‐sectional | Non‐EU [USA] | Yes | Herd size and state | Multiple antimicrobials tested | Although not statistically significant, conventional farms tended to be more likely than organic farms to have at least one Salmonella isolate resistant to five or more antimicrobial drugs |
| 38 | Cross‐sectional | Non‐EU [USA] | No | Not stated | Multiple antimicrobials tested | The prevalence and antimicrobial susceptibility of campylobacters and salmonellae varied by farming system. Organic chickens were more frequently contaminated with campylobacters and salmonellae; the pathogens from organic animal production were more susceptible to certain antimicrobials |
| 39 | Cross‐sectional | Non‐EU [USA] | No | Not stated | Single antimicrobials tested | Conventional products has significantly higher odds of carrying resistant strains of Campylobacter spp.isolates compared with antimicrobial‐free products |
| 40 | Cross‐sectional | Non‐EU [USA] | No | Animal age (cow vs calf) and season(September vs March) | Multiple antimicrobials tested | There was a significant association with herd type for 7 of 17 antimicrobials. After controlling for age, logistic regression analyses indicated that isolates from conventional dairy farms had significantly higher rates of resistance to ampicillin, streptomycin, kanamycin, gentamicin, chloramphenicol, tetracyclines, and sulfamethoxazole than did isolates from organic dairy farms. No significant differences were detected for the 10 other antimicrobials that were tested |
| 41 | Cross‐sectional | Non‐EU [USA] | Yes |
Animal age (cow vs calf) and season (September vs March) |
Multiple antimicrobials tested | Farm type (organic or conventional) was not a significant predictor of resistance to any of the four tested antimicrobials: ciprofloxacine, gentamicin, erythromycin or tetracyclines |
| 42 | Cross‐sectional | Non‐EU [USA] | Yes | Herd | Multiple antimicrobials tested | Significant difference observed with 7 of 9 antimicrobials. S. aureus isolates from both organic and conventional herds showed good susceptibility to most commonly used bovine mastitis antimicrobials isolates from organic herds were significantly more susceptible |
AMR: antimicrobial resistance; CIA: critically important antimicrobials; ESBL: extended‐spectrum beta‐lactamase; MDR: multidrug resistance; MIC: minimum inhibitory concentration; MRSA: meticillin‐resistant S. aureus; OR: odds ratio; RWA: raised without antimicrobials.