In the survey of use of medication containing antibiotics in pigs, beef cattle, and poultry on Guadeloupe, 64.4% (29/45) of all farmers reported use of antimicrobial agents (Table 1). Antimicrobials were usually administered (26/29, 57.7%) as curative treatment (20/29, 69.0%) and under veterinary prescription (22/29, 75.9%). The main causes for which antimicrobials were given were respiratory and digestive diseases in poultry (3/6, 50.0%), respiratory diseases in pigs (5/11, 45.5%) and skin diseases in cattle (5/12, 41.7%) (Table 1).
The most commonly used active substance was tetracycline (20/29, 69.0%); β-lactams and streptomycin were administered by 27.6% (8/29) and 24.1% (7/29) of farmers respectively. The proportion of farmers who used tetracycline was significantly higher in beef cattle production (100.0%) than in pig (54.5%) or poultry husbandry (33.3%), while β-lactams were administrated mainly by pig farmers (54.5%). Trimethoprim-sulfamethoxazole was used predominantly by poultry producers (83.3%, P < 0.001). Antimicrobials were used significantly less frequently in poultry (40.0%) than in pigs (78.6%) or beef cattle (75.0%) farms (P = 0.046). The total annual costs for drugs and veterinary fees was estimated to be 2000 € by half of the pig farmers, and the median cost was estimated to be 500 €/year by beef cattle farmers and 50 €/year by poultry farmers. The median annual cost of veterinary treatment per 100 kg was estimated to be 7.2 € for pigs, 6.5 € for beef cattle, and 1.7 € for poultry.
Table 1 Antimicrobials used in poultry, pig and beef cattle production systems
An additional table file shows this in more detail [see Additional file 1].
A total of 216 samples were collected from food-producing animals living on 28 farms and the slaughterhouse. Fecal samples were collected from 124 pigs (90 collected on farms and 34 at the slaughterhouse), 75 beef cattle (51 on farms and 24 at the slaughterhouse), and 17 hen houses with about 53 000 broilers. ESBL E. coli were isolated mainly from broilers, (35.3% (6/17) sampled in four hen houses but 14.7% (11/75) of beef cattle on four farms, and 7.3% (9/124) of pigs on three farms. Two pigs were carriers of two distinct ESBL-E. coli and three distinct ESBL E. coli were isolated in two hen houses (Table 2).
Table 2
Distribution of ESBL E. coli positive animals and blaCTX−M gene type
| Animals | | E. coli isolates |
| Total | | ESBL E. coli positive | | Total | | bla carrier | | blaCTX−M−15 | | blaCTX−M−1 |
| (n = 216) | | (n = 26) | | (n = 265) | | (n = 32) | | (n = 10) | | (n = 22) |
n, (%) | | | | | | | | | | | | | | | |
Beef cattle | 75 | | 11 | (14.7) | | 85 | | 11 | (12.9) | | 6 | (7.1) | | 5 | (5.9) |
Pig | 124 | | 9 | (7.3) | | 157 | | 11 | (7.0) | | 3 | (1.9) | | 8 | (5.1) |
Broilers | 17 | | 6 | (35.3) | | 23 | | 10 | (43.5) | | 1 | (4.3) | | 9 | (39.1) |
ESBL, extendend spectrum β-lactamase producing |
bla, β-lactamase
The highest resistance levels were observed against ampicillin, cefotaxime, streptomycin, tetracycline, and trimethoprim-sulfamethoxazole. Significant differences in the frequencies of resistant E. coli isolates were found among the three production systems (Tables 1 and 3). The proportion of ampicillin-resistant E. coli was higher in broilers than in beef cattle or pigs (73.9% vs 25.9% and 20.4% respectively). A similar but less marked trend was observed for cefotaxime (43.5% of resistant E. coli in broilers, 12.9% in beef cattle and 7.0% in pigs). The proportion of streptomycin-resistant E. coli was higher in pigs than in beef cattle (47.8% vs 36.5% respectively). The lowest proportion of tetracycline-resistant E. coli was observed in beef cattle (18.8%) with 56.5% in broiler and 59.2% in pig isolates. Trimethoprim-sulfamethoxazole-resistant E. coli were found in a higher proportion in broilers (34.8%) than in pigs (18.5%) or beef cattle (12.9%).
Table 3
Comparison of antimicrobial use and resistant E. coli frequencies in broilers, pigs and beef cattle
| Farmers antimicrobial use | | | Resistant E. coli isolates |
| Broilers (n = 6) | | Pigs (n = 11) | | Beef cattle (n = 16) | | P | | | Broilers (n = 23) | | Pigs (n = 157) | | Beef cattle (n = 85) | | P |
n, (%) | | | | | | | | | | | | n, (%) | | | | | | | | | | |
TET | 2 | (33.3) | | 6 | (54.5) | | 12 | (100.0) | | 0.003 | | TET | 13 | (56.5) | | 93 | (59.2) | | 16 | (18.8) | | < 0.001 |
β-lacta | 0 | (0.0) | | 6 | (54.5) | | 2 | (16.7) | | 0.035 | | AMP | 17 | (73.9) | | 32 | (20.4) | | 22 | (25.9) | | < 0.001 |
SM | 0 | (0.0) | | 5 | (45.5) | | 2 | (16.7) | | NS | | SM | 10 | (43.5) | | 75 | (47.8) | | 31 | (36.5) | | NS |
SXT | 5 | (83.3) | | 0 | (0.0) | | 0 | (0.0) | | < 0.001 | | SXT | 8 | (34.8) | | 29 | (18.5) | | 11 | (12.9) | | 0.054 |
QNR | 0 | (0.0) | | 0 | (0.0) | | 0 | (0.0) | | NS | | NAL | 3 | (13.0) | | 3 | (1.9) | | 2 | (2.4) | | 0.031 |
aPenicillins such as ampicillin and amoxicillin |
TET, tetracyclines; SM, streptomycin; SXT, Trimethoprim-sulfamethoxazole; QNR, quinolones, AMP, ampicillin, NAL, nalidixic acid |
We compared the rates of resistance to tetracycline, ampicillin, streptomycin and trimethoprim-sulfamethoxazole according to the antibiotic or class of antibiotic stated in the survey, according to animal species. As shown in Table 1, tetracyclines were used more often in beef cattle than in broilers (100.0% vs 33.3%, P = 0.003), but more tetracycline-resistant E. coli isolates were found in broilers (56.5%) and pigs (59.2%) than in beef cattle (18.8%, P < 0.001) (Table 3). Use of β-lactams also did not correspond to the level of E. coli β-lactams resistance in broilers (73.9%), as they did not receive these drugs. Congruent findings were observed between the use of sulfonamides in broilers (33.3% and none in pigs or beef cattle, P < 0.001) and the highest proportion of trimethoprim-sulfamethoxazole E. coli-resistant isolates from broilers (34.8%) as compared with 18.5% in pigs and 12.9% in beef cattle, P = 0.054). Congruent results were also observed between the absence of quinolone use and a low frequency of nalidixic acid-resistant E. coli in the three production systems.
The blaCTX−M−1 gene was found predominantly in ESBL isolates (22/32, 68.8%), followed by blaCTX−M−15 (10/32, 31.3%). The blaCTX−M−1 gene was combined with the blaTEM−1C gene in two pigs and with the blaTEM−1B gene in one broiler isolate. The remaining ESBL E. coli carried a blaCTX−M−15 gene, usually with combined cefotaximase-ceftazidimase activity. Comparison of phenotypic and genotypic profiles based on AMR/ARG combined patterns analysis is shown in Fig. 1. The blaCTX−M genes were carried by ESBL E. coli isolates found in the three food producing-animals systems on four farms in distinct geographic areas. Genotypic comparative analysis generated 18 distinct patterns among the 32 ESBL E. coli (Fig. 1). A total of 20 (62.5%) isolates harboring patterns of close genetic relatedness were grouped into seven clusters of similar AMR/ARG patterns comprising two to five isolates, whereas 12 (37.5%) distinct patterns were not clustered. Three clusters included nine ESBL E. coli at the same farm, whereas the other clustered ESBL E. coli were not specific to a production system. Twelve clustered isolates with similar AMR/ARG profiles were found in different food-producing systems (12/32, 37.5%); e.g. one cluster of ESBL E. coli carriers consisted of two pigs and one hen house on three different farms.