To quantify associations between antimicrobial use and acquired resistance in indicator Escherichia coli over a period of time which involved sector-wide antimicrobial use reductions in broilers and ...pigs (years 2004-14), veal calves (2007-14) and dairy cattle (2005-14). Prevalence estimates of resistance were predicted for a hypothetical further decrease in antimicrobial use.
Data reported annually for the resistance surveillance programme in the Netherlands were retrieved. Two multivariate random-effects logistic models per animal sector were used to relate total and class-specific antimicrobial use (as defined daily dosages per animal per year, DDDA/Y) with the probability of E. coli resistance to a panel of 10 antimicrobial agents.
Positive dose-response relationships (ORs) were obtained from all models. Specific resistance phenotypes were more often associated with total antimicrobial use than with class-specific use. The most robust associations were found in pigs and veal calves. Resistance to historically widely used antimicrobials (e.g. penicillins, tetracyclines) was, in relative terms, less influenced by drug use changes over time than resistance to newer or less prescribed antimicrobials (e.g. third-/fourth-generation cephalosporins, fluoroquinolones). In pigs and veal calves, prevalence estimates for the most common resistance phenotypes were projected to decline ∼5%-25% during 2014-16 if total antimicrobial use reduction reached 80%; projections for poultry and dairy cows were more modest.
Epidemiological evidence indicated that drug use history and co-selection of resistance are key elements for perpetuation of resistance. Data suggest that recent Dutch policies aimed at reducing total use of antimicrobials have decreased E. coli resistance in the pig and veal calf production sectors while the impact on the dairy cattle and poultry sectors is less clear.
Antimicrobial resistance (AMR) has been clearly identified as a major global health challenge. It is a leading cause of human deaths and also has a toll on animals, plants, and the environment. ...Despite the considerable socio-economic impacts, the level of awareness of the problem remains woefully inadequate, and antimicrobials are not generally recognized as a global common good, one that everyone has a role and responsibility to conserve. It is imperative for antimicrobial stewardship to be more widely implemented to achieve better control of the AMR phenomenon. The Food and Agriculture Organization (FAO) of the United Nations plays an important role in promoting and facilitating antimicrobial stewardship. The specific needs to be addressed and barriers to be overcome, in particular, in low- and middle-income countries in order to implement antimicrobial stewardship practices in agrifood systems are being identified. As a global community, it is essential that we now move beyond discussing the AMR problem and focus on implementing solutions. Thus, FAO provides multi-pronged support for nations to improve antimicrobial stewardship through programs to strengthen governance, increase awareness, develop and enhance AMR surveillance, and implement best practices related to antimicrobial resistance in agrifood systems. For example, FAO is developing a platform to collect data on AMR in animals and antimicrobial use (AMU) in plants (InFARM), working on a campaign to reduce the need to use antimicrobials, studying the use of alternatives to the use of antimicrobials (especially those used for growth promotion) and actively promoting the implementation of the Codex Alimentarius AMR standards. Together, these will contribute to the control of AMR and also bring us closer to the achievement of multiple sustainable development goals.
Comprehensive strategies to improve on-farm antimicrobial use (AMU) are needed to contain antimicrobial resistance (AMR). Little is known about farmers’ motivating and enabling factors, and about ...their influence on AMU. In a cross-sectional online survey, Dutch dairy, veal and pig farmers (n=457) reported their on-farm AMU as “Defined Daily Dose Animal” per year (DDDAF) and completed a detailed questionnaire on their view, knowledge and behavior towards AMU and AMR. Exploratory factor analysis (EFA) on the questionnaire items identified four psychological factors labeled as ‘referent beliefs’, ‘perceived risk’, ‘knowledge’, and ‘undesired attitude to regulations’. Linear regression was done to explore the relationship between the obtained factors and on-farm AMU across the three animal sectors. Dairy farmers showed the highest factor scores for ‘knowledge’ and the lowest for ‘perceived risk’. ‘Knowledge’ scores were significantly and inversely related to AMU (P=0.0004). Borderline significant associations with AMU were found for ‘perceived risk’ and ‘undesired attitude to regulations’ (negative and positive relationships respectively). There were no apparent differences for these relationships between the three livestock sectors. Behavioral interventions in farmers such as educational campaigns or increased support by veterinarians could empower farmers with more prudent and rational practices, eventually reducing AMU in food animals.
Global, national, and local efforts to limit antimicrobial resistance (AMR) often stress the importance of raising awareness among users, sellers, and prescribers of antimicrobial drugs. This ...emphasis is founded upon two assumptions. First, awareness is limited, particularly concerning the links between antimicrobial use (AMU) and AMR. Second, "filling the awareness gaps" will motivate practises that will limit AMR. The first assumption is supported by knowledge, attitudes, and practises (KAP) surveys but these same studies provide mixed support for the second, with several studies finding that knowledge and attitudes are not correlated with related practises. This disconnect may arise as these surveys typically do not collect data on the cultural or historical contexts that pattern AMU. To explore how these contexts impact KAP related to AMU and AMR, we use a mixed-methods approach to examine veterinary practises among Maasai pastoralists in Tanzania. We combine a quantitative KAP survey (
= 195 households) with extensive qualitative data from focus group discussions (
= 55 participants). Results document limited awareness of AMR but also find that knowledge and attitudes are not correlated with practise. Thematic analysis of qualitative data pointed to three reasons behind this disconnect, including (1) Maasai self-perceptions as veterinary experts, (2) the central role of livestock in Maasai culture, and (3) the use of ethnoveterinary knowledge in animal health treatment. We argue that mixed-method approaches will be critical to developing the targeted awareness campaigns needed to limit the emergence and transmission of AMR.
IntroductionAwareness-raising campaigns play a central role in efforts to combat drug resistance. These campaigns assume that knowledge deficits drive poor practices that increase resistance. ...Therefore, increasing awareness will promote prudent practices and reduce resistance. However, most awareness campaigns have been developed and evaluated in high-income and public health settings. Consequently, it is not clear whether these campaigns are effective in low-income and middle-income countries and/or within animal health settings.MethodsFocus group discussions and in-depth interviews were used to collect narratives of veterinary drug use among Maasai pastoralists (n=70), animal health professionals (n=10) and veterinary drug sellers (n=5). Thematic analysis was used to identify recurring themes across narratives and groups.ResultsNarratives of Maasai and animal health professionals indicated that Maasai treated their livestock with limited input from the professional sector and that non-prudent treatment practices were observed (eg, using antimicrobials as ‘energizers’). Professionals linked these practices to knowledge and attitudinal deficits among the Maasai, while Maasai narratives highlighted the importance of climatic uncertainties and cultural beliefs surrounding veterinary care.ConclusionNarratives of veterinary drug use from animal health professionals are consistent with the knowledge deficit assumption guiding awareness-raising efforts. In contrast, Maasai narratives highlight how animal health practices are patterned by cultural norms interacting with factors largely outside of Maasai control, including a constrained professional veterinary sector. If these cultural and structural contexts remain unconsidered in awareness-raising strategies, current campaigns are unlikely to motivate practices necessary to limit drug resistance, especially within low-income and middle-income settings.
Extended-spectrum β-lactamase-producing Escherichia coli (ESBL-EC), plasmid-mediated AmpC-producing E coli (pAmpC-EC), and other bacteria are resistant to important β-lactam antibiotics. ESBL-EC and ...pAmpC-EC are increasingly reported in animals, food, the environment, and community-acquired and health-care-associated human infections. These infections are usually preceded by asymptomatic carriage, for which attributions to animal, food, environmental, and human sources remain unquantified.
In this population-based modelling study, we collected ESBL and pAmpC gene data on the Netherlands population for 2005–17 from published datasets of gene occurrences in E coli isolates from different sources, and from partners of the ESBL Attribution Consortium and the Dutch National Antimicrobial Surveillance System. Using these data, we applied an established source attribution model based on ESBL-EC and pAmpC-EC prevalence and gene data for humans, including high-risk populations (ie, returning travellers, clinical patients, farmers), farm and companion animals, food, surface freshwater, and wild birds, and human exposure data, to quantify the overall and gene-specific attributable sources of community-acquired ESBL-EC and pAmpC-EC intestinal carriage. We also used a simple transmission model to determine the basic reproduction number (R0) in the open community.
We identified 1220 occurrences of ESBL-EC and pAmpC-EC genes in humans, of which 478 were in clinical patients, 454 were from asymptomatic carriers in the open community, 103 were in poultry and pig farmers, and 185 were in people who had travelled out of the region. We also identified 6275 occurrences in non-human sources, including 479 in companion animals, 4026 in farm animals, 66 in wild birds, 1430 from food products, and 274 from surface freshwater. Most community-acquired ESBL-EC and pAmpC-EC carriage was attributed to human-to-human transmission within or between households in the open community (60·1%, 95% credible interval 40·0–73·5), and to secondary transmission from high-risk groups (6·9%, 4·1–9·2). Food accounted for 18·9% (7·0–38·3) of carriage, companion animals for 7·9% (1·4–19·9), farm animals (non-occupational contact) for 3·6% (0·6–9·9), and swimming in freshwater and wild birds (ie, environmental contact) for 2·6% (0·2–8·7). We derived an R0 of 0·63 (95% CI 0·42–0·77) for intracommunity transmission.
Although humans are the main source of community-acquired ESBL-EC and pAmpC-EC carriage, the attributable non-human sources underpin the need for longitudinal studies and continuous monitoring, because intracommunity ESBL-EC and pAmpC-EC spread alone is unlikely to be self-maintaining without transmission to and from non-human sources.
1Health4Food, Dutch Ministry of Economic Affairs, and the EU's Horizon-2020 through One-Health European Joint Programme.
In recent years, ESBL/AmpC-producing Escherichia coli (ESBL/AmpC-EC) have been isolated with increasing frequency from animals, food, environmental sources and humans. With incomplete and scattered ...evidence, the contribution to the human carriage burden from these reservoirs remains unclear.
To quantify molecular similarities between different reservoirs as a first step towards risk attribution.
Pooled data on ESBL/AmpC-EC isolates were recovered from 35 studies in the Netherlands comprising >27 000 samples, mostly obtained between 2005 and 2015. Frequency distributions of ESBL/AmpC genes from 5808 isolates and replicons of ESBL/AmpC-carrying plasmids from 812 isolates were compared across 22 reservoirs through proportional similarity indices (PSIs) and principal component analyses (PCAs).
Predominant ESBL/AmpC genes were identified in each reservoir. PCAs and PSIs revealed close human-animal ESBL/AmpC gene similarity between human farming communities and their animals (broilers and pigs) (PSIs from 0.8 to 0.9). Isolates from people in the general population had higher similarities to those from human clinical settings, surface and sewage water and wild birds (0.7-0.8), while similarities to livestock or food reservoirs were lower (0.3-0.6). Based on rarefaction curves, people in the general population had more diversity in ESBL/AmpC genes and plasmid replicon types than those in other reservoirs.
Our 'One Health' approach provides an integrated evaluation of the molecular relatedness of ESBL/AmpC-EC from numerous sources. The analysis showed distinguishable ESBL/AmpC-EC transmission cycles in different hosts and failed to demonstrate a close epidemiological linkage of ESBL/AmpC genes and plasmid replicon types between livestock farms and people in the general population.
The farming community can be a vehicle for introduction of livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) in hospitals. During 2011-2013, an 18-month longitudinal study ...aimed at reducing the prevalence of LA-MRSA was conducted on 36 pig farms in the Netherlands. Evaluations every 6 months showed a slight decrease in MRSA prevalence in animals and a stable prevalence in farmers and family members. Antimicrobial use, expressed as defined daily dosages per animal per year, decreased 44% during the study period and was associated with declining MRSA prevalence in pigs. MRSA carriage in animals was substantially higher at farms using cephalosporins. Antimicrobial use remained strongly associated with LA-MRSA in humans regardless of the level of animal contact. A risk factor analysis outlined potential future interventions for LA-MRSA control. These results should encourage animal and public health authorities to maintain their efforts in reducing antimicrobial use in livestock and ask for future controlled intervention studies.
The presence of extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-E. coli) in food animals is a public health concern. This study aimed to determine prevalence of ESBL-E. coli on pig ...farms and to assess the effect of reducing veterinary antimicrobial use (AMU) and farm management practices on ESBL-E. coli occurrence on pig farms. During 2011-2013, 36 Dutch conventional pig farms participated in a longitudinal study (4 sampling times in 18 months). Rectal swabs were taken from 60 pigs per farm and pooled per 6 pigs within the same age category. Presence of ESBL-E. coli was determined by selective plating and ESBL genes were characterized by microarray, PCR and gene sequencing. An extensive questionnaire on farm characteristics and AMU as Defined Daily Dosages per Animal Year (DDDA/Y) was available for the 6-month periods before each sampling moment. Associations between the presence of ESBL-E. coli-positive pigs and farm management practices were modelled with logistic regression. The number of farms with ESBL-E. coli carrying pigs decreased from 16 to 10 and the prevalence of ESBL-E. coli-positive pooled pig samples halved from 27% to 13%. Overall, the most detected ESBL genes were blaCTX-M-1, blaTEM-52 and blaCTX-M-14. The presence of ESBL-E. coli carrying pigs was not related to total AMU, but it was strongly determined by the presence or absence of cephalosporin use at the farm (OR = 46.4, p = 0.006). Other farm management factors, related with improved biosecurity, were also plausibly related to lower probabilities for ESBL-E. coli-positive farms (e.g. presence of a hygiene lock, pest control delivered by a professional). In conclusion, ESBL-E. coli prevalence decreased in pigs during 2011 and 2013 in the Netherlands. On pig farms, the use of cephalosporins was associated with the presence of ESBL-E. coli carrying pigs.
•Food chain workers are exposed to antimicrobial resistant (AMR) bacteria in livestock.•We describe faecal resistomes and microbiomes of farmers and slaughterhouse workers.•Faecal AMR gene loads in ...pork exposed workers exceed those in broiler farmers/controls.•Resistome and microbiome differences are shown between and within occupational groups.•On-farm working hours and working/living on a pig farm determinethe faecal resistome.•Contact with livestock may be a determinant for human AMR gene carriage.
By studying the entire human faecal resistome and associated microbiome, the diversity and abundance of faecal antimicrobial resistance genes (ARGs) can be comprehensively characterized. Prior culture-based studies have shown associations between occupational exposure to livestock and carriage of specific antimicrobial resistant bacteria. Using shotgun metagenomics, the present study investigated 194 faecal resistomes and bacteriomes from humans occupationally exposed to ARGs in livestock (i.e. pig and poultry farmers, employees and family members and pig slaughterhouse workers) and a control population (Lifelines cohort) in the Netherlands. In addition, we sought to identify determinants for the human resistome and bacteriome composition by applying a combination of multivariate (NMDS, PERMANOVA, SIMPER and DESeq2 analysis) and multivariable regression analysis techniques.
Pig slaughterhouse workers and pig farmers carried higher total ARG abundances in their stools compared to broiler farmers and control subjects. Tetracycline, β-lactam and macrolide resistance gene clusters dominated the resistome of all studied groups. No significant resistome alpha diversity differences were found among the four populations. However, the resistome beta diversity showed a separation of the mean resistome composition of pig and pork exposed workers from broiler farmers and controls, independent of their antimicrobial use. We demonstrated differences in resistome composition between slaughter line positions, pig versus poultry exposed workers, as well as differences between farmers and employees versus family members. In addition, we found a significant correlation between the bacteriome and resistome, and significant differences in the bacteriome composition between and within the studied subpopulations. Finally, an in-depth analysis of pig and poultry farms – of which also farm livestock resistomes were analysed – showed positive associations between the number of on-farm working hours and human faecal AMR loads.
We found that the total normalized faecal ARG carriage was larger in persons working in the Dutch pork production chain compared to poultry farmers and controls. Additionally, we showed significant differences in resistome and bacteriome composition of pig and pork exposed workers compared to a control group, as well as within-population (farms, slaughterhouse) compositional differences. The number of on-farm working hours and the farm type (pig or broiler) that persons live or work on are determinants for the human faecal resistome. Overall, our results may suggest direct or indirect livestock contact as a determinant for human ARG carriage. Future studies should further focus on the connection between the human and livestock resistome (i.e. transmission routes) to substantiate the evidence for livestock-associated resistome acquisition.
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