Antimicrobial resistance (AMR) is a global health problem, and emerging semi-intensive farming systems in Southeast Asia are major contributors to the AMR burden. We accessed 12 pig and chicken farms ...at key stages of production in Tien Giang Province, Vietnam, to measure antimicrobial usage and to investigate the prevalence of AMR to five critical antimicrobials (β-lactams, third-generation cephalosporins, quinolones, aminoglycosides, and polymyxins) and their corresponding molecular mechanisms among 180 Escherichia coli isolates. Overall, 94.7 mg (interquartile range IQR, 65.3 to 151.1) and 563.6 mg (IQR, 398.9 to 943.6) of antimicrobials was used to produce 1 kg (live weight) of chicken and pig, respectively. A median of 3 (out of 8) critical antimicrobials were used on pig farms. E. coli isolates exhibited a high prevalence of resistance to ampicillin (97.8% and 94.4% for chickens and pigs, respectively), ciprofloxacin (73.3% and 21.1%), gentamicin (42.2% and 35.6%), and colistin (22.2% and 24.4%). The prevalence of a recently discovered colistin resistance gene, mcr-1, was 19 to 22% and had strong agreement with phenotypic colistin resistance. We conducted plasmid conjugation experiments with 37 mcr-1 gene-positive E. coli isolates and successfully observed transfer of the gene in 54.0% of isolates through a plasmid of approximately 63 kb, consistent with one recently identified in China. We found no significant correlation between total use of antimicrobials at the farm level and AMR. These data provide additional insight into the role of mcr-1 in colistin resistance on farms and outline the dynamics of phenotypic and genotypic AMR in semi-intensive farming systems in Vietnam.
Our study provides accurate baseline information on levels of antimicrobial use, as well as on the dynamics of phenotypic and genotypic resistance for antimicrobials of critical importance among E. coli over the different stages of production in emerging pig and poultry production systems in Vietnam. E. coli isolates showed a high prevalence of resistance (>20%) to critically important antimicrobials, such as colistin, ciprofloxacin, and gentamicin. The underlying genetic mechanisms identified for colistin (the mcr-1 gene) and quinolone (gyrA gene mutations) are likely to play a major role in AMR to those compounds. Conjugation experiments led to the identification of a 63-kb plasmid, similar to one recently identified in China, as the potential carrier of the mcr-1 gene. These results should encourage greater restrictions of such antimicrobials in Southeast Asian farming systems.
The Vietnam Initiative for Zoonotic Infections (VIZIONS) includes community-based 'high-risk sentinel cohort' (HRSC) studies investigating individuals at risk of zoonotic infection due to ...occupational or residential exposure to animals. A total of 852 HRSC members were recruited between March 2013 and August 2014 from three provinces (Ha Noi, Dak Lak, and Dong Thap). The most numerous group (72.8%) corresponded to individuals living on farms, followed by slaughterers (16.3%) and animal health workers (8.5%). Nasal/pharyngeal and rectal swabs were collected from HRSC members at recruitment and after notifying illness. Exposure to exotic animals (including wild pigs, porcupine, monkey, civet, bamboo rat and bat) was highest for the Dak Lak cohort (53.7%), followed by Ha Noi (13.7%) and Dong Thap (4.0%). A total of 26.8% of individuals reported consumption of raw blood over the previous year; 33.6% slaughterers reported no use of protective equipment at work. Over 686 person-years of observation, 213 episodes of suspect infectious disease were notified, equivalent of 0.35 reports per person-year. Responsive samples were collected from animals in the farm cohort. There was noticeable time and space clustering of disease episodes suggesting that the VIZIONS set up is also suitable for the formal epidemiological investigation of disease outbreaks.
Indiscriminate antimicrobial use (AMU) in animal production is a driver of antimicrobial resistance globally. There is a need to define sustainable interventions to reduce AMU in small-scale ...production systems, which currently represent the most widespread farming systems in South East Asia and many low- and middle-income countries. We conducted a before-and-after intervention study on a random sample of small-scale chicken farms in the Mekong Delta of Vietnam from 2016 to 2019. The study included a baseline followed by an intervention phase where farmers were provided with regular veterinary advice on flock health and husbandry, as well as antimicrobial replacement products. Of 102 recruited farms (raising >100 chickens per flock cycle), thirty-five (34.2%) entered the intervention phase, whilst the rest stopped raising chickens, mainly due to suboptimal flock performance. Through the implementation of our intervention, chicken flocks reduced levels of AMU by 66% adjusted hazard ratio (HR) = 0.34;
= 0.002) from a baseline of 343.4 Animal Daily Doses per 1,000 chicken-days and decreased weekly mortality by 40% (adjusted HR = 0.60;
= 0.005) from a baseline mortality of 1.60 per 100 birds. Chicken bodyweight increased by 100 g (
= 0.002) in intervention flocks. Our findings demonstrate that the provision of veterinary advice can achieve substantial reductions in AMU in small-scale production systems without compromising flock health and productivity.
In the Mekong Delta of Vietnam, poultry farmers use high amounts of antimicrobials, but little is known about the drivers that influence this usage. We aimed to identify these drivers using a novel ...approach that combined participatory epidemiology (PE) and Q-sorting (a methodology that allows the analysis of the subjectivity of individuals facing a common phenomenon). A total of 26 semi-structured collective interviews were conducted with 125 farmers representative of the most common farming systems in the area (chickens, meat ducks, and mobile grazing ducks), as well as with 73 farmers' advisors veterinarians, veterinary drug shop owners, and government veterinarians/commune animal health workers (CAHWs) in five districts of Dong Thap province (Mekong Delta). Through these interviews, 46 statements related to the antimicrobials' perceived reliability, costs, and impact on flock health were created. These statements were then investigated on 54 individuals (28 farmers and 26 farmers' advisors) using Q-sorting interviews. Farmers generally indicated a higher propensity for antimicrobial usage (AMU) should their flocks encounter bacterial infections (75.0-78.6%) compared with viral infections (8.3-66.7%). The most trusted sources of advice to farmers were, in decreasing order: government veterinarian/CAHWs, their own knowledge/experience, veterinary drug shop owners, and sales persons from pharmaceutical and feed companies. The highest peak of AMU took place in the early phase of the production cycle. Farmers and their advisors showed considerable heterogeneity of attitudes with regards to AMU, with, respectively, four and three discourses representing their views on AMU. Overall, farmers regarded the cost of AMU cheaper than other disease management practices implemented on their farms. However, they also believed that even though these measures were more expensive, they would also lead to more effective disease prevention. A key recommendation from this finding would be for the veterinary authorities to implement long-term sustainable training programs aiming at reducing farmers' reliance on antimicrobials.
In the Mekong Delta region of Vietnam, high quantities of products containing antimicrobial are used as prophylactic and curative treatments in small-scale chicken flocks. A large number of these ...contain antimicrobial active ingredients (AAIs) considered of 'critical importance' for human medicine according to the World Health Organization (WHO). However, little is known about the retail prices of these products and variables associated with the expense on antimicrobials at farm level. Therefore, the aims of the study were: (1) to investigate the retail price of antimicrobials with regards to WHO importance criteria; and (2) to quantify the antimicrobial expense incurred in raising chicken flocks. We investigated 102 randomly-selected small-scale farms raising meat chickens (100-2000 per flock cycle) in two districts in Dong Thap (Mekong Delta) over 203 flock production cycles raised in these farms. Farmers were asked to record the retail prices and amounts of antimicrobial used.
A total of 214 different antimicrobial-containing products were identified. These contained 37 different AAIs belonging to 13 classes. Over half (60.3%) products contained 1 highest priority, critically important AAI, and 38.8% 1 high priority, critically important AAI. The average (farm-adjusted) retail price of a daily dose administered to a 1 kg bird across products was 0.40 cents of 1 US$ (₵) (SE ± 0.05). The most expensive products were those that included at least one high priority, critically important AAI, as well as those purchased in one of the two study districts. Farmers spent on average of ₵3.91 (SE ± 0.01) on antimicrobials per bird over the production cycle. The expense on antimicrobials in weeks with disease and low mortality was greater than on weeks with disease and high mortality, suggesting that antimicrobial use had a beneficial impact on disease outcomes (χ
= 3.8; p = 0.052). Farmers generally used more expensive antimicrobials on older flocks.
The retail prices of antimicrobial products used in chicken production in Mekong Delta small-scale chicken farms are very low, and not related to their relevance for human medicine. Farmers, however, demonstrated a degree of sensitivity to prices of antimicrobial products. Therefore, revising pricing policies of antimicrobial products remains a potential option to curb the use of antimicrobials of critical importance in animal production.
Colistin is extensively used in animal production in many low- and middle-income countries. There is a need to develop methods to benchmark and monitor changes in resistance among mixed commensal ...bacterial populations in farms. We aimed to evaluate the performance of a broth microdilution method based on culturing a pooled Escherichia coli suspension (30 to 50 organisms) obtained from each sample. To confirm the biological basis and sensitivity of the method, we cultured 16 combinations of one colistin-susceptible and one mcr-1-carrying colistin-resistant E. coli isolate in the presence of 2 mg/liter colistin. Readings of optical density at 600 nm (OD600) over time were used to generate a growth curve, and these values were adjusted to the values obtained in the absence of colistin (adjusted area under the curve AUCadj). The median limit of detection was 1 resistant in 104 susceptible colonies (1st to 3rd quartile, 102:1 to 105:1). We applied this method to 108 pooled fecal samples from 36 chicken flocks from the Mekong Delta (Vietnam) and determined the correlation between this method and the prevalence of colistin resistance in individual colonies harvested from field samples, determined by the MIC. The overall prevalences of colistin resistance at the sample and isolate levels (estimated from the AUCadj) were 38.9% (95% confidence intervals CI, 29.8 to 48.8%) and 19.4% ± 26.3% (± values are standard deviations SD), respectively. Increased colistin resistance was associated with recent (2 weeks) use of colistin (odds ratio OR = 3.67) and other, noncolistin antimicrobials (OR = 1.84). Our method is a sensitive and affordable approach to monitor changes in colistin resistance in E. coli populations from fecal samples over time. IMPORTANCE Colistin (polymyxin E) is an antimicrobial with poor solubility in agar-based media, and therefore, broth microdilution is the only available method for determining phenotypic resistance. However, estimating colistin resistance in mixed Escherichia coli populations is laborious, since it requires individual colony isolation, identification, and susceptibility testing. We developed a growth-based microdilution method suitable for pooled fecal samples. We validated the method by comparing it with individual MIC determinations for 909 E. coli isolates; we then tested 108 pooled fecal samples from 36 healthy chicken flocks collected over their production cycle. A higher level of resistance was seen in flocks recently treated with colistin in water, although the observed generated resistance was short-lived. Our method is affordable and may potentially be integrated into surveillance systems aiming at estimating the prevalence of resistance at colony level in flocks/herds. Furthermore, it may also be adapted to other complex biological systems, such as farms and abattoirs.
In the Mekong Delta of Vietnam, small-scale poultry farmers use large amounts of antimicrobials to raise their flocks, and veterinary drug shops owners and their staff are a key source of advice to ...farmers on antimicrobial use (AMU). We described the network of veterinary drug shops (
= 93) in two districts within Dong Thap province (Mekong Delta). We also interviewed a randomly selected sample of chicken farmers (
= 96) and described their linkages with veterinary drug shops. Antimicrobials represented 15.0% inter quartile range (IQR) 6.0-25.0 of the shops' income. Fifty-seven percent shop owners had been/were affiliated to the veterinary authority, 57% provided diagnostic services. The median number of drug shops supplying antimicrobials to each farm during one production cycle was 2 IQR 1-2. Visited shops were located within a median distance of 3.96 km IQR 1.98-5.85 to farms. Drug shops owned by persons affiliated to the veterinary authority that did not provide diagnostic services had a higher fraction of their income consisting of antimicrobial sales (
= 1.913;
< 0.001). These results suggest that interventions targeting veterinary drug shop owners and their staff aiming at improving their knowledge base on livestock/poultry diseases and their diagnosis may contribute to reducing overall levels of AMU in the area.
There is a pressing need to establish surveillance systems for antimicrobial use (AMU) intended for animal production particularly in many low- and middle-income countries. This is an extremely ...challenging task, notably due to the wide range of animal species, production types and antimicrobials available in the market. In Vietnam, farmers commonly buy antimicrobials from veterinary drug shops. Therefore, veterinary drug shops are a potential target for data collection on AMU. We collected antimicrobial sales data at veterinary drug shops and estimated the amount of AMU in different animal species by antimicrobial active ingredient (AAI) class using different measurement metrics. We compiled information on all antimicrobials licensed in Vietnam and used this information to develop a mobile application to capture sales of antimicrobials intended for use in poultry, pig, and ruminant. We provided tablets with this application to 60 veterinary drug shops in two provinces of the country (Bac Giang in the north, Dong Thap in the south; three districts and 30 shops per province) for data collection over 3 weeks. Total sales of antimicrobials were extrapolated to 1 year, and these amounts were related to three different denominator estimates in each province including standing animal body weight, animal biomass, and Population Correction Unit (PCU). A total of 3,960 transactions 2,577 (median 75.5 per shop) in Bac Giang; 1,383 (median 28.5 per shop) in Dong Thap of 831 different antimicrobial-containing products were recorded in the 3-week period. Sales of 57 AAIs belonging to 17 classes were recorded. In the three Bac Giang districts, we estimated that 242.0 kg of AAI were hypothetically sold over 1 year. Of those, 202.2 kg (83.6%) were intended for poultry, 19.8 kg (8.1%) for pigs, and 20.0 kg (8.3%) for ruminants. In Dong Thap, an estimated 48.4 kg of antimicrobials were sold, including 28.9 kg (59.7%) for poultry, 16.0 kg (33.1%) for pigs, and 3.5 kg (7.2%) for ruminants. After standardized by different animal population denominators, AMU in Bac Giang amounted to 1129.2 mg/kg standing animal body weight, 480.2 mg/kg biomass, and 636.1 mg/kg PCU. In Dong Thap, AMU figures were 1211.0 mg/kg standing animal body weight, 595.8 mg/kg biomass and 818.5 mg/kg PCU. We discuss the observed differences between species, location and metrics, as well as the potential advantages and limitations (including potential sources of bias) of this methodology and its applicability at country level. Retail level data collection can effectively be integrated into AMU surveillance systems that help identify priority AMU management areas (species, regions, and antimicrobial classes), establish national benchmarks and reduction targets.
Small-scale farming of meat chicken flocks using local native breeds contributes to the economy of many rural livelihoods in Vietnam and many other low- and middle-income countries (LMICs). These ...systems are also the target of high levels of antimicrobial use (AMU); however, little is known about the profitability and sustainability of such systems. Since small-scale farms are commercial enterprises, this knowledge is essential to develop successful strategies to curb excessive AMU. Using longitudinal data from 203 small-scale (100−2,000 heads) native chicken flocks raised in 102 randomly selected farms in Dong Thap province (Mekong Delta, Vietnam), we investigated the financial and economic parameters of such systems and the main constraints to their sustainability. Feed accounted for the largest financial cost (flock median 49.5 % Inter-quartile range (IQR) 41.5−61.8 %) of total costs, followed by day-old-chicks (DOCs) (median 30.3 % IQR 23.2−38.4 %), non-antimicrobial health-supporting products (median 7.1 % IQR 4.7−10.5 %), vaccines (median 3.1 % IQR 2.2−4.8 %), equipment (median 1.9 % IQR 0.0−4.9 %) and antimicrobials (median 1.9 % IQR 0.7−3.6 %). Excluding labor costs, farmers achieved a positive return on investment (ROI) from 120 (59.1 %) flocks, the remainder generating a loss (median ROI 124 % IQR 36–206 %). Higher ROI was associated with higher flock size and low mortality. There was no statistical association between use of medicated feed and flock mortality or chicken bodyweight. The median daily income per person dedicated to raising chickens was 202,100 VND, lower than alternative rural labor activities in the Mekong Delta. In a large proportion of farms (33.4 %), farmers decided to stop raising chickens after completing one cycle. Farmers who dropped off chicken production purchased more expensive feed (in 1000 VND per kg): 11.1 10.6−11.5 vs. 10.8 10.4−11.3 for farms that continued production (p = 0.039), and experienced higher chicken mortality (28.5 % 12.0−79.0 % vs. 16 7.5−33.0 %; p = 0.004). The rapid turnover of farmers raising chickens in such systems represents a challenge to the uptake of messages on appropriate AMU and chicken health. To ensure sustainability of small-scale commercial systems, advisory services need to be available to farmers as they initiate new flocks, and support them in the early stages to help overcome their limited experience and skills. This targeted approach would support profitability whilst reducing risk of emergence of AMR and infectious disease from these systems.
Chicken is a major reservoir and source of human infections from zoonotic Campylobacter. In southern Thailand, chicken is the most popular meat consumed; however, little is known about the ...antimicrobial resistance (AMR) of Campylobacter spp. in chicken production systems. We aimed to investigate the prevalence and characteristics of AMR in Campylobacter isolates from commercial broiler and native chicken farms in southern Thailand. A total of 286 Campylobacter isolates (adjusted prevalence: 60.3%, SE ± 0.01) were recovered, of which 268 were identified as Campylobacter jejuni and 18 as Campylobacter coli. The adjusted prevalence of resistance was highest for nalidixic acid (98.6%), followed by ciprofloxacin (97.2%), enrofloxacin (96.4%), tetracycline (74.6%), tylosin (38.3%), and erythromycin (10.6%). Commercial broilers had resistance levels 7-11% higher to quinolones and 35-47% lower to macrolides and tetracycline (all P ≤ 0.025) compared to native chickens. Genotypic resistance analyses revealed high prevalence rates (>86%) for gyrA mutant, efflux pump CmeABC, and point mutation A2075G in the 23S rRNA gene. High homogeneity was observed among isolates within study farms. Commercial broilers exhibited higher homogeneity in AMR patterns than native chickens. The best agreement was observed between tetracycline resistance and tet(O) genes (Kappa: k = 0.811, P < 0.001), while the fair agreement was found for quinolone resistance and gyrA mutant genes (k = 0.260-0.271, P < 0.001). No association was detected between macrolide resistance and point mutations in the 23S rRNA gene. These findings fill knowledge gaps on AMR in Campylobacter in Thailand, emphasizing the need for targeted AMR mitigation strategies in both commercial broilers and native chickens.
High Campylobacter prevalence in chickens; C. jejuni more prevalent than C. coli.
Susceptibility to macrolides but resistance to quinolones/tetracyclines in isolates.
Homogeneous resistance patterns within farms; higher in broilers than in native birds.
Partial association between phenotypic and genotypic resistance among isolates.
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