Changes in antibiotic consumption in nursing homes over years

The total antibiotic consumption significantly decreased between 2018 and 2022 in the 220 nursing homes included in this study. This trend is consistent with the steady consumption decline reported in nursing homes without on-site pharmacy since 2015 in France. ¹⁴ The 2022 increase may result from the withdrawal of the stringent measures to prevent infections that had been implemented in 2020 leading to a decrease of respiratory infections. ¹⁵ Indeed, antibiotics are often prescribed even for viral respiratory infection, ^{Reference Fleming-Dutra, Hersh and Shapiro16} particularly to elderly people. ^{Reference Havers, Hicks and Chung17}

During the study period, penicillins represented >60% of nursing-home antibiotic consumption. This proportion is in accordance with a Norwegian study that reported a proportion of 69.6% in 34 nursing homes in 2016. ^{Reference Harbin, Haug, Romøren and Lindbæk18} Penicillins accounted for 30.2% of antibiotic treatments in 2016–2017 during the European prevalence survey in long-term care facilities. ^{Reference Ricchizzi, Latour and Kärki19} This discrepancy between proportion of DDDs and proportion of treatments is likely linked to the values of DDDs for amoxicillin ± clavulanic acid, which are much lower than the actual prescribed doses in many countries. ^{Reference Först, de With and Weber20}

The 2 most used antibiotics were amoxicillin-clavulanic acid and amoxicillin. According to the 2018 French national guidelines for treatment of acute infections in elderly in nursing homes, including urinary tract infections (UTIs) and respiratory tract infections, ²¹ amoxicillin-clavulanic acid is not a first-line option, except in grade 3 of exacerbation of obstructive lung disease or some acute pneumopathy treatment. However, it remains the most consumed antibiotic. In 2019, it was also the most used antibiotic in a sample of 802 Italian nursing homes, where it accounted for almost 40% of their antibiotic consumption, ^{Reference Zito, Poluzzi and Pierantozzi22} compared to 35% in our survey (12.8 of 36.5). In contrast, amoxicillin, which is the most recommended antibiotic depending on the bacteria susceptibility, ²¹ was the second most consumed antibiotic. Interestingly, this first-line antibiotic ranked only 11 among most used antibiotics in Italian nursing homes in 2019. ^{Reference Zito, Poluzzi and Pierantozzi22}

Ceftriaxone was the third most consumed antibiotic and the first among cephalosporins. Indeed, this molecule is recommended in pyelonephritis, prostatitis, bronchitis when the oral route is not possible or in pneumopathy as a second-line treatment. ²¹ Cefixime ranked fifth whereas oral third-generation cephalosporins are not recommended for the treatment of acute infections in elderly. ²¹

Despite a significant decrease during the study period, pristinamycin was still the fourth most used antibiotic. It is often used as an alternative to amoxicillin or amoxicillin-clavulanic acid in case of allergy in France, ²¹ whereas it is hardly used in other countries. ^{Reference Reissier and Cattoir23–Reference Jump, Crnich, Mody, Bradley, Nicolle and Yoshikawa25}

The most used fluoroquinolones were ofloxacin followed by ciprofloxacin and levofloxacin (ranking 10 or 11 depending on the year), the latter being the only fluoroquinolone recommended for the treatment of some UTIs in case of penicillin allergy or in prostatitis. ²¹ Altogether, fluoroquinolones represented almost 7% of total consumption. This is higher than reported in Norway in 2016 (5.2% of total antibiotic consumption in 34 nursing homes) ^{Reference Harbin, Haug, Romøren and Lindbæk18} but much lower than described in Italy ^{Reference Zito, Poluzzi and Pierantozzi22} and the United States. ^{Reference Song, Wilson and Bej26} Although not significantly, fluoroquinolones consumption tended to decrease, in accordance with professional recommendations to restrict the use of these antibiotics. Indeed, fluoroquinolones have a high potential to select resistance, and this is the reason they are classified among the “critical antibiotics with restricted indication” of the 2022 SPILF list ¹² and in the “Watch” list of the 2023 WHO AWaRe index. ²⁷ Moreover, the European Medicines Agency issued safety alerts in 2018, 2019, and again in 2023 calling to restrict their use, namely in the elderly. ^28,29

Changes in quality indicators

As information on prescribing appropriateness is not easily available, monitoring antibiotic indicators calculated from quantitative data is promoted by health authorities to evaluate quality of use in nursing homes. ^{Reference Renggli, Plüss-Suard, Gasser, Sonderegger and Kronenberg30} They provide more qualitative information than quantitative data and are less time and resource consuming than practice audits. The consumption of critical antibiotics with restricted indications ¹² has increased, making it very difficult to achieve the expected goal of a 20% reduction by 2025, according to the national action plan to prevent infections and antimicrobial resistance. ⁶ As for the proportion of oral cephalosporins among total cephalosporin consumption, despite a significant decrease during the study period, it remains far above the optimal value of 10% and still slightly higher than the “acceptable” 30% threshold in 2022. The third indicator, the proportion of parenteral antibiotics, did not show the decrease expected during the study period; their use must be limited to the situation that required it. ^{Reference Asquier-Khati, Deschanvres, Chaslerie, Pereira, Boutoille and Birgand13} Indeed, using these indicators in addition to the quantitative data on consumption add useful information to steer antimicrobial stewardship activities in nursing homes.

Changes during COVID-19 pandemic

The decrease in total antibiotic consumption had already started in 2019, but this trend seemed to accelerate during COVID-19 pandemic, from 2020 to 2021. Indeed, the infection prevention and control (IPC) measures implemented during this period limited the number of bacterial infections, especially those transmitted by the respiratory route. ^{Reference Shaw, Abad and Amin-Chowdhury31} Similar trends in antibiotic use have been reported in 1,944 US nursing homes, in 2020 compared to 2019, ^{Reference Gouin, Creasy and Beckerson32} and in Alberta, Canada, but not in Ontario. ^{Reference Haverkate, Macfadden and Daneman33}

Beyond this decrease in total antibiotic consumption, the use of some antibiotics increased during the pandemic in the nursing homes included in our survey. Azithromycin consumption increased sharply as its potential efficacy in COVID-19 treatment was studied at that time. ^{Reference Vaz, Vassiliades, Giarolla, Polli and Parise-Filho34} There was also a slight increase in ceftriaxone use in 2020, probably linked with prescriptions to cover the risk of infection by S. pneumoniae and S. aureus. ^{Reference Huttner, Catho, Pano-Pardo, Pulcini and Schouten35} Indeed, other researchers reported that despite a low proportion (6.9%) of bacterial coinfection in patients hospitalized for COVID-19, 71.9% received antibiotics, often broad-spectrum agents such as third-generation cephalosporins. ^{Reference Langford, So and Raybardhan36}

These results highlight the need to reinforce antibiotic stewardship actions in nursing homes during pandemic periods to ensure appropriate use of antibiotics. Despite disproval of azithromycin efficacy in the treatment of patients suffering from COVID-19, its consumption remained higher in 2021 and in 2022 than before 2020.

This study had several limitations. We explored antibiotic consumption in nursing homes with on-site pharmacies, which account for 20% of all French nursing homes. These facilities have their own pharmacist and are often hospital-based. For these reasons, they might have easier access to infectious diseases or geriatric experts and might be more likely to benefit from antimicrobial stewardship activities performed by the pharmacist than nursing homes without an on-site pharmacy. ^{Reference Takito, Kusama, Fukuda and Kutsuna37} Moreover, as they voluntarily participated in the survey, professionals in the included nursing homes may be more aware of the need for rational antibiotic use. For these reasons, consumption data may not be representative of the entire nursing-home sector in France. Nevertheless, characteristics of antibiotic use described in this survey suggest unwise use, even in nursing homes with on-site pharmacies.

Because prescribing data were not available, no information could be collected on indication or treatment duration. This is why we calculated quality indicators to approximate rational use of antibiotics.

In conclusion, this survey of antibiotic use in nursing homes with on-site pharmacies brought useful information on the pattern of use over years to inform antimicrobial stewardship activities at the national and at the local level. Contrasting results and changes during pandemic periods advocate support for nursing homes professionals to implement antimicrobial stewardship activities tailored to their need and resources. ⁸ Implementation of antibiotic multidisciplinary teams is underway in France. They should support professionals in hospitals and in nursing homes to develop actions to improve rational use of antibiotics in close relation with mobile infection control teams. Preventing respiratory tract infections and appropriate treatment of these infections could be a priority. In addition, feedback of surveillance data to nursing home professionals each year may foster awareness and will lead to the implementation of prevention measures and antimicrobial stewardship to increase patient safety. ^{Reference Kabbani, Palms and Bartoces38,Reference Daneman, Campitelli and Giannakeas39} We intend to further promote surveillance of antibiotic use in nursing homes and to help professionals to use their data, including indicators to approach prescribing quality. ^{6,Reference Renggli, Plüss-Suard, Gasser, Sonderegger and Kronenberg30}