Towards One Health surveillance of antibiotic resistance: characterisation and mapping of existing programmes in humans, animals, food and the environment in France, 2021.

BackgroundInternational organisations are calling for One Health approaches to tackle antimicrobial resistance. In France, getting an overview of the current surveillance system and its level of integration is difficult due to the diversity of surveillance programmes.AimThis study aimed to map and describe all French surveillance programmes for antibiotic resistance (ABR), antibiotic use (ABU) and antibiotic residues, in humans, animals, food and the environment, in 2021. Another objective was to identify integration points, gaps and overlaps in the system.MethodsWe reviewed the literature for surveillance programmes and their descriptions. To further characterise programmes found, semi-directed interviews were conducted with their coordinators.ResultsIn total 48 programmes in the human (n = 35), animal (n = 12), food (n = 3) and/or the environment (n = 1) sectors were identified; 35 programmes focused on ABR, 14 on ABU and two on antibiotic residues. Two programmes were cross-sectoral. Among the 35 ABR programmes, 23 collected bacterial isolates. Bacteria most targeted were Escherichia coli (n = 17 programmes), Klebsiella pneumoniae (n = 13), and Staphylococcus aureus (n = 12). Extended-spectrum beta-lactamase-producing E. coli was monitored by most ABR programmes (15 of 35) in humans, animals and food, and is a good candidate for integrated analyses. ABU indicators were highly variable. Areas poorly covered were the environmental sector, overseas territories, antibiotic-resistant-bacterial colonisation in humans and ABU in companion animals.ConclusionThe French surveillance system appears extensive but has gaps and is highly fragmented. We believe our mapping will interest policymakers and surveillance stakeholders. Our methodology may inspire other countries considering One Health surveillance of ABR.

Time-series modelling for the quantification of seasonality and forecasting antibiotic-resistant episodes: application to carbapenemase-producing Enterobacteriaceae episodes in France over 2010-20.

BACKGROUND: Carbapenemase-producing Enterobacteriaceae (CPE) cause resistant healthcare-associated infections that jeopardize healthcare systems and patient safety worldwide. The number of CPE episodes has been increasing in France since 2009, but the dynamics are still poorly understood. OBJECTIVES: To use time-series modelling to describe the dynamics of CPE episodes from August 2010 to December 2016 and to forecast the evolution of CPE episodes for the 2017-20 period. METHODS: We used time series to analyse CPE episodes from August 2010 to November 2016 reported to the French national surveillance system. The impact of seasonality was quantified using seasonal-to-irregular ratios. Seven time-series models and three ensemble stacking models (average, convex and linear stacking) were assessed and compared with forecast CPE episodes during 2017-20. RESULTS: During 2010-16, 3559 CPE episodes were observed in France. Compared with the average yearly trend, we observed a 30% increase in the number of CPE episodes in the autumn. We noticed a 1 month lagged seasonality of non-imported episodes compared with imported episodes. Average stacking gave the best forecasts and predicted an increase during 2017-20 with a peak up to 345 CPE episodes (95% prediction interval = 124-1158, 80% prediction interval = 171-742) in September 2020. CONCLUSIONS: The observed seasonality of CPE episodes sheds light on potential factors associated with the increased frequency of episodes, which need further investigation. Our model predicts that the number of CPE episodes will continue to rise in the coming years in France, mainly due to local dissemination, associated with bacterial carriage by patients in the community, which is becoming an immediate challenge with regard to outbreak control.

Epidemiology of Clostridioides difficile infections, France, 2010 to 2017.

BackgroundClostridioides difficile is a leading cause of healthcare-associated diarrhoea in middle and high-income countries. Up to 2018, there has been no systematic, annual surveillance for C. difficile infections (CDI) in France.AimsTo provide an updated overview of the epidemiology of CDI in France between 2010 and 2017 based on five different data sources.MethodsThis is a descriptive study of retrospective surveillance and alerts data. Incidence of CDI cases was estimated through the CDI incidence survey (2016) and data from the French National Uniform Hospital Discharge Database (PMSI; 2010-16). Testing frequency for CDI was estimated through the CDI incidence survey and point prevalence studies on healthcare-associated infections (HAI; 2012 and 2017). The national early warning response system for HAI (HAI-EWRS, 2012-17) and National Reference Laboratory data (2012-17) were used to follow the number of severe CDI cases and/or outbreaks.ResultsIn 2016, CDI incidence in acute care was 3.6 cases per 10,000 patient days (PD). There was a statistically significant increase in CDI incidence between 2010 and 2016 (+ 14% annually) and testing frequency was 47.4 per 10,000 PD. The number of CDI HAI-EWRS notifications decreased between 2015 and 2017 with only a few large outbreaks reported.ConclusionThe CDI incidence estimate increased from 2010, but remained below the European average of 7 per 10,000 PD in 2014; there were fewer severe cases or clusters reported in France. The consistency between PMSI and laboratory-based estimated CDI incidence could allow for more routine monitoring of CDI incidence.

Moving towards One Health surveillance of antibiotic resistance in France: a semi-quantitative evaluation of the level of collaboration within the national surveillance system.

Objectives: Collaboration between surveillance programmes is the keystone of One Health surveillance and international organizations call for integrated surveillance systems to manage antibiotic resistance (ABR). In France, the ABR surveillance system covers human, animal, food and the environment sectors, but appears to be fragmented, questioning its level of integration. This study aimed to evaluate collaboration within this system and to formulate recommendations towards more integration. Methods: ECoSur, a semi-quantitative tool, was used to evaluate collaboration between surveillance programmes. A total of 31 attributes were evaluated using information from the literature and 52 interviews with surveillance actors from all four sectors. Evaluation results were visualized via three output figures displaying aspects related to governance and functionality of collaboration. Results were validated by an expert committee. Results: Overall, the French collaborative strategy for ABR surveillance was well formalized and relevant to its objectives. However, a cross-sectoral coordination body was lacking to help with its practical implementation. The environmental sector was largely uncovered, but its integration appeared necessary to meet the strategy objectives. Data sharing and joint data analyses between programmes were insufficient, mainly due to limited resources and data interoperability issues. Collaboration was operational for internal and external communication of the results. Twelve recommendations were suggested to decision makers to foster collaboration within the French surveillance system and feed future strategies against ABR. Conclusions: This first evaluation of collaboration within the French ABR surveillance system produced concrete recommendations to move towards One Health integrated surveillance. Both the approach and the findings could be of interest to other countries.

How to move towards One Health surveillance? A qualitative study exploring the factors influencing collaborations between antimicrobial resistance surveillance programmes in France.

Introduction: Antimicrobial resistance (AMR) is a major public health issue, against which international organisations and governmental bodies call for integration between surveillance programmes involved in human, animal, and environmental sectors. Collaborations are the primary feature of integration and deserve to be supported. However, little is known about the factors that can foster collaborations between surveillance programmes. This study aimed to provide a better understanding of the factors for setting-up collaborations between AMR surveillance programmes in France. Methods: We performed a qualitative study based on 36 semi-structured interviews with programmes' coordinators and 15 with key-informant experts involved in AMR surveillance. Results: The implementation of collaboration between sectors was multifactorial: we identified 42 factors grouped into six categories (i.e., characteristics of the overall AMR surveillance system, features of the collaborating programme, profile of the actors involved, characteristics of the collaboration itself, broader context, and AMR research activities). Collaborations were mainly fostered by good interpersonal relationship between actors, their interest in transdisciplinary approaches and the benefits of collaboration on the programmes involved. Limited resources and the complexity of the AMR surveillance system hindered collaboration. Paradoxically, coordinators generally did not perceive collaborations as a resource-pooling tool since they generally set them up only after consolidating their own programme. Discussion: Since most factors identified were not specific to AMR, these results can be useful for other collaborative surveillance system. Ultimately, they provide a better understanding of stakeholders' motivations and influences driving collaboration, and can help researchers and risk managers promoting a One Health approach against public health threats.

Users' perception of the OH-EpiCap evaluation tool based on its application to nine national antimicrobial resistance surveillance systems.

Introduction: Antimicrobial resistance (AMR) is a One Health (OH) challenge. To achieve or maintain an effective and efficient AMR surveillance system, it is crucial to evaluate its performance in meeting the proposed objectives, while complying with resource restrictions. The OH-EpiCap tool was created to evaluate the degree of compliance of hazard surveillance activities with essential OH concepts across the following dimensions: organization, operational activities, and impact of the surveillance system. We present feedback on the application of the OH-EpiCap tool from a user's perspective, based on the use of the tool to evaluate nine national AMR surveillance systems, each with different contexts and objectives. Methods: The OH-EpiCap was assessed using the updated CoEvalAMR methodology. This methodology allows the evaluation of the content themes and functional aspects of the tool and captures the user's subjective experiences via a strengths, weaknesses, opportunities, and threats (SWOT) approach. Results and Discussion: The results of the evaluation of the OH-EpiCap are presented and discussed. The OH-EpiCap is an easy-to-use tool, which can facilitate a fast macro-overview of the application of the OH concept to AMR surveillance. When used by specialists in the matter, an evaluation using OH-EpiCap can serve as a basis for the discussion of possible adaptations of AMR surveillance activities or targeting areas that may be further investigated using other evaluation tools.

Evolution of antibiotic treatments for healthcare-associated infections caused by extended-spectrum beta-lactamase-producing Enterobacteriaceae in France.

BACKGROUND: Infections caused by extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBLE) remain a public health challenge. AIM: We traced the evolution of antibiotics prescribed for patients with ESBLE-healthcare associated infections (ESBLE-HAI) between 2012 and 2017, with a specific focus on treatments for lower urinary tract infections (LUTI). METHODS: We used the 2012 and 2017 French point prevalence survey data. Patients with ESBLE-HAI were defined as those diagnosed with at least one Enterobacteriaceae with ESBL production. Patients with LUTI caused by ESBLE (ESBLE-LUTI) were defined as those with LUTI as the reported infection site and diagnosed with ESBLE. We only analysed treatments intended for HAI. RESULTS: In 2017, more than half of treatments for ESBLE-HAIs were ß-lactams. While from 2012 to 2017 the proportion of carbapenem treatments decreased from 30% to 25%, penicillin treatments doubled. Among patients treated for ESBLE-LUTI, a larger proportion received a single antibiotic in 2017. The most frequently prescribed antibiotics for these infections were amoxicillin/clavulanic acid, nitrofurantoin and ofloxacin. More than one out of six treatments lasted for more than 7 days. Carbapenem use was halved between 2012 and 2017, and decreases were likewise observed for aminoglycosides. CONCLUSION: In accordance with French recommendations, comparison of the two most recent French point prevalence surveys showed an evolution in ESBLE-HAI treatment, especially for ESBLE-LUTI. However, treatment durations remained longer than recommended. Data from the 2022 survey should provide insights on the future evolution of prescription trends.

Decreasing proportion of extended-spectrum beta-lactamase among E. coli infections during the COVID-19 pandemic in France.

OBJECTIVES: We investigated the impact of the COVID-19 and national pandemic response on the epidemiology of Extended Spectrum Beta-Lactamase producing E. coli (ESBL-E.coli) in France. METHODS: Individual microbiology records from clinical laboratories were analyzed between 1 January 2019 to 31 December 2020. The ESBL-E.coli rates from clinical samples of patients in primary care and nursing home residents were compared before and after the general lockdown in March 2020, according to demographic and geographical characteristics. Interrupted time series analyses were performed to detect measurable changes in the trend of ESBL-E.coli rates. RESULTS: Records covering 793,954 E. coli isolates from 1022 clinical laboratories were analyzed. In primary care, 3.1% of E. coli isolates from clinical samples were producing ESBL before March 2020 and 2.9% since May 2020 (p < 0.001). The proportion of ESBL-E.coli decreased significantly among urine cultures, females, age categories 5-19, 40-64, > 65 year-old, and in the North, West, East and South-East regions. In nursing home, the ESBL-E.coli rate was 9.3% (monthly rate min-max: 6.5-10.5%) before March 2020 and 8.3% (7.2-9.1%) since May 2020 (p < 0.001). The reduction rate accelerated from -0.04%/month to -0.22%/month from May 2020 (p < 0.001). CONCLUSION: Investigation of factors that led to the decreased proportion of ESBL-E.coli during the COVID-19 pandemic is urgently needed.

Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis.

BACKGROUND: Infections due to antibiotic-resistant bacteria are threatening modern health care. However, estimating their incidence, complications, and attributable mortality is challenging. We aimed to estimate the burden of infections caused by antibiotic-resistant bacteria of public health concern in countries of the EU and European Economic Area (EEA) in 2015, measured in number of cases, attributable deaths, and disability-adjusted life-years (DALYs). METHODS: We estimated the incidence of infections with 16 antibiotic resistance-bacterium combinations from European Antimicrobial Resistance Surveillance Network (EARS-Net) 2015 data that was country-corrected for population coverage. We multiplied the number of bloodstream infections (BSIs) by a conversion factor derived from the European Centre for Disease Prevention and Control point prevalence survey of health-care-associated infections in European acute care hospitals in 2011-12 to estimate the number of non-BSIs. We developed disease outcome models for five types of infection on the basis of systematic reviews of the literature. FINDINGS: From EARS-Net data collected between Jan 1, 2015, and Dec 31, 2015, we estimated 671 689 (95% uncertainty interval [UI] 583 148-763 966) infections with antibiotic-resistant bacteria, of which 63·5% (426 277 of 671 689) were associated with health care. These infections accounted for an estimated 33 110 (28 480-38 430) attributable deaths and 874 541 (768 837-989 068) DALYs. The burden for the EU and EEA was highest in infants (aged <1 year) and people aged 65 years or older, had increased since 2007, and was highest in Italy and Greece. INTERPRETATION: Our results present the health burden of five types of infection with antibiotic-resistant bacteria expressed, for the first time, in DALYs. The estimated burden of infections with antibiotic-resistant bacteria in the EU and EEA is substantial compared with that of other infectious diseases, and has increased since 2007. Our burden estimates provide useful information for public health decision-makers prioritising interventions for infectious diseases. FUNDING: European Centre for Disease Prevention and Control.