Social-technical interventions to reduce antimicrobial resistance in agriculture: evidence from poultry Farmer Field Schools in Ghana and Kenya.

OBJECTIVES: To assess the feasibility of the Farmer Field School approach to address the complex problem of antimicrobial resistance in agriculture, specifically within small-to-medium-scale layer poultry systems in Ghana and Kenya. Impact was assessed across three domains relevant to the emergence and selection of antimicrobial resistance, including infection, prevention, and control practices, engagement with animal health professionals, and knowledge, attitudes, and practices on antimicrobial use and antimicrobial resistance. METHODS: Farmer Field Schools were held in Ghana (N = 2) and Kenya (N = 3) across an eight-month period with an average of 18 participants in each school. After completion, a quantitative evaluation survey was administered to participants and a sample of non-participants (Ghana; N = 97) (Kenya; N = 103). Logistic and ordinary least squares regression were used to assess differences between participants and non-participants on the three domains. RESULTS: Participation in a layer poultry Farmer Field School in Ghana and Kenya is associated with self-reported reductions in antibiotic use, particularly for prevention, an increased investment in farm infection, prevention, and control practices, including the use of footbaths and personal protective equipment, and enhanced engagement with animal health professionals. CONCLUSIONS: Antimicrobial resistance is a complex problem driven by a wide range of practices and multiple stakeholders. To holistically address these factors requires the use of complex intervention approaches. The Farmer Field School approach offers a complex intervention methodology that can reduce the emergence and spread of antimicrobial resistance in agricultural systems through targeting the variety of on-farm and off-farm factors that drive resistance.

Narratives of veterinary drug use in northern Tanzania and consequences for drug stewardship strategies in low-income and middle-income countries.

INTRODUCTION: Awareness-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. METHODS: Focus 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. RESULTS: Narratives 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. CONCLUSION: Narratives 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.

A systematic approach toward progressive improvement of national antimicrobial resistance surveillance systems in food and agriculture sectors.

The first Food and Agriculture Organization of the United Nations (FAO) Action Plan on antimicrobial resistance (AMR), published in 2016, identified the need to develop capacity for AMR surveillance and monitoring in food and agriculture sectors. As part of this effort, FAO has developed the "Assessment Tool for Laboratories and AMR Surveillance Systems" (FAO-ATLASS) to assist countries in systematically assessing their AMR surveillance system in food and agriculture. FAO-ATLASS includes two different modules for surveillance and laboratory assessment. Each module includes two questionnaires that collect either qualitative or semi-quantitative data to describe and score the performance of national AMR surveillance system data production network, data collection and analysis, governance, communication and overall sustainability in a standardized manner. Based on information captured in the questionnaire by trained assessors (1) tables and figures describing the outputs of the surveillance system are automatically generated (2) a Progressive Improvement Pathway (PIP) stage, ranging from "1-limited" to "5-sustainable", is assigned to each laboratory assessed in the country, each area of the surveillance system and also to the overarching national AMR surveillance system. FAO-ATLASS allows national authorities to implement a strategic stepwise approach to improving their AMR surveillance systems via the FAO-ATLASS PIP system and provides an evidence base for actions and advocacy. The implementation of FAO-ATLASS at regional and global levels can contribute to harmonize and better coordinate strategies aimed at implementing an integrated AMR surveillance system under the One Health approach.

Knowing Is Not Enough: A Mixed-Methods Study of Antimicrobial Resistance Knowledge, Attitudes, and Practises Among Maasai Pastoralists.

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 (N = 195 households) with extensive qualitative data from focus group discussions (N = 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.

Identification of Escherichia coli and Related Enterobacteriaceae and Examination of Their Phenotypic Antimicrobial Resistance Patterns: A Pilot Study at A Wildlife-Livestock Interface in Lusaka, Zambia.

A cross-sectional study was used to identify and assess prevalence and phenotypic antimicrobial resistance (AMR) profiles of Escherichia coli and other enterobacteria isolated from healthy wildlife and livestock cohabiting at a 10,000 acres game ranch near Lusaka, Zambia. Purposive sampling was used to select wildlife and livestock based on similarities in behavior, grazing habits and close interactions with humans. Isolates (n = 66) from fecal samples collected between April and August 2018 (n = 84) were examined following modified protocols for bacteria isolation, biochemical identification, molecular detection, phylogenetic analysis, and antimicrobial susceptibility testing by disc diffusion method. Data were analyzed using R software, Genetyx ver.12 and Mega 6. Using Applied Profile Index 20E kit for biochemical identification, polymerase chain reaction assay and sequencing, sixty-six isolates were identified to species level, of which Escherichia coli (72.7%, 48/66), E. fergusonii (1.5%, 1/66), Shigella sonnei (22.7%, 14/66), Sh. flexinerri (1.5%, 1/66) and Enterobacteriaceae bacterium (1.5%, 1/66), and their relationships were illustrated in a phylogenetic tree. Phenotypic antimicrobial resistance or intermediate sensitivity expression to at least one antimicrobial agent was detected in 89.6% of the E. coli, and 73.3% of the Shigella isolates. The E. coli isolates exhibited the highest resistance rates to ampicillin (27%), ceftazidime (14.3%), cefotaxime (9.5%), and kanamycin (9.5%). Multidrug resistance (MDR) was detected in 18.8% of E. coli isolates while only 13.3% Shigella isolates showed MDR. The MDR was detected among isolates from impala and ostrich (wild animals in which no antimicrobial treatment was used), and in isolates from cattle, pigs, and goats (domesticated animals). This study indicates the possible transmission of drug-resistant microorganisms between animals cohabiting at the wildlife-livestock interface. It emphasizes the need for further investigation of the role of wildlife in the development and transmission of AMR, which is an issue of global concern.

Understanding Antimicrobial Use Contexts in the Poultry Sector: Challenges for Small-Scale Layer Farms in Kenya.

The poultry sector contributes significantly to Kenya's food and economic security. This contribution is expected to rise dramatically with a growing population, urbanization, and preferences for animal-source foods. Antimicrobial resistance is putting the poultry sector in Kenya-and worldwide-at risk of production losses due to the failure of medicines for animal (and human) health. The emergence and spread of antimicrobial resistance has been linked to overuse and misuse of antimicrobials in poultry and other sectors. Previous studies have documented poultry farmer antimicrobial use but without systematic consideration of the contexts (i.e., drivers) as important targets for behavior change, particularly in low- and middle-income countries. To improve understanding of antimicrobial use patterns in poultry systems, we conducted a mixed-methods knowledge, attitudes, and practices study of 76 layer farms in Kiambu County; Kenya. We found that commonly used antibiotics were often labeled for prophylactic, growth promotion, and egg production improvement purposes. Antimicrobial use was also motivated by the presence of diseases/disease symptoms, most of which could instead be managed through infection prevention measures. The results suggest that improving vaccination and biosecurity practices on farms and engaging with drug-makers to ensure proper labeling and marketing of antimicrobial drugs may represent important areas of opportunity for social behavior change communication and/or behavioral science interventions (i.e., nudges) to reduce disease burdens and promote prudent antimicrobial use. We conclude our findings with suggestions for further research into the behavioral insights at play in these scenarios to fuel future intervention development.

"We are doctors": Drivers of animal health practices among Maasai pastoralists and implications for antimicrobial use and antimicrobial resistance.

Animal health service providers can play an important role in limiting drug resistance by promoting responsible and prudent use of veterinary drugs. Recognizing this potential, international agencies and governments have called for these providers to receive drug stewardship training, particularly providers in low- and middle-income countries where top-down regulations (e.g., national regulation of veterinary prescriptions) are largely unfeasible. The success of these stewardship trainings to promote responsible and prudent use will depend on many factors, including understanding how livestock-keeping communities currently interact with animal health service providers. Here, we use a mixed methods approach to identify and understand animal health seeking practices among Maasai pastoralists in Tanzania. Combining qualitative interviews (N = 31) and structured surveys (N = 195), we show the majority of Maasai respondents (≈80 %) do not frequently consult animal health service providers with most relying on advice from family and friends. Logistic regression models of health seeking practices find that increasing age, education, observance of treatment failure, and herd disease burdens are associated with greater odds of seeking out health services. Quantitative results were supported by data from focus group discussions and in-depth interviews that showed Maasai view animal health service providers as measures of last resort, whose input is largely sought after self-treatment with veterinary drugs fail. We argue patterns of animal health seeking among the Maasai are partially the consequence of their high confidence in their own abilities in livestock disease and treatment and generally low confidence in the skills of animal health service providers. We link this high sense of self-efficacy to the culturally engrained process by which Maasai develop mastery in animal health and how the roles and norms in Maasai culture surrounding animal health influence Maasai perceptions of animal health professionals. Our results highlight the need for more research to understand Maasai perceptions of animal health service providers as well as the knowledge, attitudes, and practices of these providers. Finally, our study emphasizes that the success of drug stewardship trainings will require efforts to first understand the cultural and historical contexts driving health seeking practices that impact perceptions of animal health service providers and animal health practices more generally.

A descriptive survey of porcine epidemic diarrhea in pig populations in northern Vietnam.

Porcine epidemic diarrhea (PED) virus (PEDV) is a globally emerging and re-emerging epizootic swine virus that causes massive economic losses in the swine industry, with high mortality in piglets. In Vietnam, PED first emerged in 2009 and has now developed to an endemic stage. This is the first cross-sectional survey performed to evaluate the proportion of PEDV-positive swine farms in Vietnam from January 2018 to February 2019. Fecal samples from 327 pig farms in northern Vietnam were collected and tested for PEDV infection by reverse transcription-loop-mediated isothermal amplification (RT-LAMP) method. The proportion of PEDV-positive farms was 30.9% and PEDV-positive farms were distributed throughout the study area. The highest proportion of PEDV-positive farms was 70% (7/10) among nucleus production type farms (P < 0.05). Higher proportions of PEDV-positive farms were found in the Northeast and Red River Delta areas, which are the major areas of pig production (P < 0.05). The proportion of PEDV-positive farms was higher among larger farms (P < 0.05). Our findings illustrate the high proportion of PEDV-positive farms in the Vietnamese pig population and will help to better understand the epidemiological dynamics of PED infection, to estimate impact, and establish and improve prevention and control measures.

The Impacts of Animal Health Service Providers on Antimicrobial Use Attitudes and Practices: An Examination of Poultry Layer Farmers in Ghana and Kenya.

International organizations and governments have argued that animal health service providers can play a vital role in limiting antimicrobial resistance by promoting the prudent use of antimicrobials. However, there is little research on the impact of these service providers on prudent use at the farm level, especially in low- and middle-income countries where enforcement of prudent-use regulations is limited. Here, we use a mixed-methods approach to assess how animal health-seeking practices on layer farms in Ghana (n = 110) and Kenya (n = 76) impact self-reported antimicrobial usage, engagement in prudent administration and withdrawal practices and perceptions of antimicrobial resistance. In general, our results show that the frequency of health-seeking across a range of service providers (veterinarians, agrovets, and feed distributors) does not significantly correlate with prudent or non-prudent use practices or the levels of antimicrobials used. Instead, we find that patterns of antimicrobial use are linked to how much farmers invest in biosecurity (e.g., footbaths) and the following vaccination protocols. Our results emphasize that more research is required to understand the interactions between animal health service providers and farmers regarding antimicrobial use and antimicrobial resistance. Addressing these gaps will be crucial to inform antimicrobial stewardship training, curriculums and, guidelines whose ultimate purpose is to limit the selection and transmission of antimicrobial resistance.

Towards a bottom-up understanding of antimicrobial use and resistance on the farm: A knowledge, attitudes, and practices survey across livestock systems in five African countries.

The nutritional and economic potentials of livestock systems are compromised by the emergence and spread of antimicrobial resistance. A major driver of resistance is the misuse and abuse of antimicrobial drugs. The likelihood of misuse may be elevated in low- and middle-income countries where limited professional veterinary services and inadequately controlled access to drugs are assumed to promote non-prudent practices (e.g., self-administration of drugs). The extent of these practices, as well as the knowledge and attitudes motivating them, are largely unknown within most agricultural communities in low- and middle-income countries. The main objective of this study was to document dimensions of knowledge, attitudes and practices related to antimicrobial use and antimicrobial resistance in livestock systems and identify the livelihood factors associated with these dimensions. A mixed-methods ethnographic approach was used to survey households keeping layers in Ghana (N = 110) and Kenya (N = 76), pastoralists keeping cattle, sheep, and goats in Tanzania (N = 195), and broiler farmers in Zambia (N = 198), and Zimbabwe (N = 298). Across countries, we find that it is individuals who live or work at the farm who draw upon their knowledge and experiences to make decisions regarding antimicrobial use and related practices. Input from animal health professionals is rare and antimicrobials are sourced at local, privately owned agrovet drug shops. We also find that knowledge, attitudes, and particularly practices significantly varied across countries, with poultry farmers holding more knowledge, desirable attitudes, and prudent practices compared to pastoralist households. Multivariate models showed that variation in knowledge, attitudes and practices is related to several factors, including gender, disease dynamics on the farm, and source of animal health information. Study results emphasize that interventions to limit antimicrobial resistance should be founded upon a bottom-up understanding of antimicrobial use at the farm-level given limited input from animal health professionals and under-resourced regulatory capacities within most low- and middle-income countries. Establishing this bottom-up understanding across cultures and production systems will inform the development and implementation of the behavioral change interventions to combat antimicrobial resistance globally.

Meteorological factors affecting the risk of transmission of HPAI in Miyazaki, Japan.

Highly pathogenic avian influenza (HPAI) outbreaks engender a severe economic impact on the poultry industry and public health. Migratory waterfowl are considered the natural hosts of HPAI virus, and HPAI viruses are known to be transmitted over long distances during seasonal bird migration. Bird migration is greatly affected by the weather. Many studies have shown the relationship between either autumn or spring bird migration and climate. However, few studies have shown the relationship between annual bird migration and annual weather. This study aimed to establish a model for the number of migratory waterfowl involved in HPAI virus transmission based on meteorological data. From 136 species of waterfowl that were observed at Futatsudate in Miyazaki, Japan, from 2008 to 2016, we selected potential high-risk species that could introduce the HPAI virus into Miyazaki and defined them as 'risky birds'. We also performed cluster analysis to select meteorological factors. We then analysed the meteorological data and the total number of risky birds using a generalised linear mixed model. We selected 10 species as risky birds: Mallard (Anas platyrhynchos), Northern pintail (Anas acuta), Eurasian wigeon (Anas penelope), Eurasian teal (Anas crecca), Common pochard (Aythya ferina), Eurasian coot (Fulica atra), Northern shoveler (Anas clypeata), Common shelduck (Tadorna tadorna), Tufted duck (Aythya fuligula) and Herring gull (Larus argentatus). We succeeded in clustering 35 meteorological factors into four clusters and identified three meteorological factors associated with their migration: (1) the average daily maximum temperature; (2) the mean value of global solar radiation and (3) the maximum daily precipitation. We thus demonstrated the relationship between the number of risky birds and meteorological data. The dynamics of migratory waterfowl was relevant to the risk of an HPAI outbreak, and our data could contribute to cost and time savings in strengthening preventive measures against epidemics.

Detection of neutralizing antibody against porcine epidemic diarrhea virus in subclinically infected finishing pigs.

The purpose of this study was to detect porcine epidemic diarrhea virus (PEDV) subclinically infected pigs shipped from non-case farms to slaughterhouses. Systematic sampling was conducted at two slaughterhouses. A total of 1,556 blood samples were collected from 80 case and non-case farms from pigs over 6 months old. Blood samples were centrifuged to obtain sera. Serial serum dilutions were subjected to serological examination for PEDV presence using Neutralization test (NT). The cut-off titer was set at titer of 1:2 dilution and farms with at least one positive sample in duplicate were classified as PED-positive farms. Several non-case farms (9.4%, 6/64) and 100% (16/16) of the case farms were indeed positive for PEDV. The proportion of seropositive animals from case farms was 63.7%, significantly different from that of non-case farms (4.3%, P<0.05). In both case and non-case farms, the proportion of seropositive animals in farrow-to-finish farms was significantly higher than in wean-to-finish farms (P<0.05). Seropositive animals in non-case farms were detected by NT in a sero-survey by sampling at slaughterhouses. Therefore, subclinically infected pigs should be considered prior to shipment.

In situ hybridization and immunohistochemistry for the detection of porcine cytomegalovirus.

To establish in situ hybridization and immunohistochemistry based-assays for the detection of porcine cytomegalovirus, routinely processed renal tissue sections from 34 diseased piglets suspected of having the infection were obtained and examined. Using hematoxylin and eosin, porcine cytomegalovirus inclusion bodies were found in the nucleus of renal epithelial cells and capillary endothelial cells in the renal medulla in 30 cases. Inclusion bodies corresponding to porcine cytomegalovirus mRNA after in situ hybridization or porcine cytomegalovirus antigens after immunohistochemistry were easily determined. The cells were characterized by cytomegaly and basophilic intranuclear inclusion bodies. Using in situ hybridization, porcine cytomegalovirus mRNA were clearly detected in the nucleus and cytoplasm of the cells in 28 of the 30 (93.3%) cases. Using immunohistochemistry, porcine cytomegalovirus antigens were clearly detected in the cytoplasm of the cells in 21 of the 30 (70.0%) cases. Higher specificities and increased intensity of staining was observed with minimal background using in situ hybridization and immunohistochemistry compared with hematoxylin and eosin. Thus, the two established methods are useful and helpful tools for detecting the presence of a porcine cytomegalovirus infection.