Impact of the COVID-19 pandemic on extended-spectrum β-lactamase producing Escherichia coli in urinary tract and blood stream infections: results from a nationwide surveillance network, Finland, 2018 to 2022

Our study based on the national surveillance data indicates that the annual proportions of ESBL-producing isolates among E. coli from urine and blood cultures significantly decreased after the onset of the COVID-19 pandemic during 2019–2022. Concurrently, the incidence of ESBL-producing E. coli significantly decreased in urine cultures in both sexes in all age groups, and also in blood cultures of both males and females ≥ 60 years of age. In addition, we observed a clear decrease in the annual number of urine isolates reported to the surveillance database during the pandemic. However, for blood isolates, there was a slight increase during this timeframe. Furthermore, for ESBL-producing E. coli isolates, coincident resistance to fluoroquinolones remained high during the study period.

Our study shows that, the observed decreasing trends in the proportion of ESBL-producing E. coli were more than a mirror image of the trends observed in our previous study in Finland covering the pre-pandemic years 2008–2019 (AAD during 2019–2022: 11.3% in urine and 11.4% in blood (Supplementary table S2) vs. AAI during 2008–2019: 8.9% in urine and 8.7% in blood) [19]. The lowest proportions observed in this study in 2022 were roughly at the same level as observed in 2015, 5 years before the onset of the pandemic. Notably, the previously observed differences between sexes and sample types in the levels of the proportions remained the same, with the proportion of ESBL-producing isolates being higher among males than females and higher in blood isolates than in urine isolates. Our results are also partly paralleled by three previous studies [23,24,25]. In France, an overall significant decrease in ESBL production among E. coli isolates from clinical samples of primary care patients and nursing home residents was reported after the national lockdown on the 11th of May 2020 [23]. The decrease was statistically significant for urine cultures, females, and the age groups of 5–19, 40–64, and > 60 years. In Ontario, Canada, a decreasing trend for ESBL-producing E. coli in urine cultures from community patients and patients in long-term care facilities (LTCF) during the COVID-19 pandemic was also observed [24]. However, the study periods in these two studies were shorter than ours. In the Netherlands, in hospitalised patients, a significantly lower prevalence of ESBL-producing E. coli and Klebsiella pneumoniae was observed from June to August 2022 compared to the pre-COVID-19 period [25]. In addition to these studies, a review including 30 studies demonstrated differences in trends of different MDR bacteria during the pandemic [26]: the proportions of ESBL-producing E. coli and K. pneumoniae and carbapenem-resistant Pseudomonas aeruginosa (CRPA) decreased in most studies, whereas the proportions of other MDR bacteria including carbapenem-resistant Enterobacteriaceae (CRE), carbapenem-resistant Acinetobacter baumannii (CRAB), methicillin-resistant Staphylococcus aureus (MRSA), and vancomycin-resistant Enterococci (VRE) increased.

The decreasing trends in the proportions of ESBL-producing E. coli in blood E. coli isolates observed in this study are in line with the latest EARS-Net report for years 2018–2022, although EARS-Net reports 3GC-resistance proportion instead of ESBL proportion [18, 22]. The population-weighted mean proportion of 3GC resistance among invasive E. coli isolates decreased by 22.8%: from 7.9% in 2019 to 6.1% in 2022 in Finland [22]. This was nearly triple compared to the mean decrease in European Union (EU) and European Economic Area (EEA) countries (8.3%, from 15.6 to 14.3%), as well as greater than in some other European countries with traditionally low rates of AMR: Norway, 6.5%, from 6.2% in 2019 to 5.8% in 2022; Sweden, 3.8%, from 7.8 to 7.5%; and Denmark, 12,0%, from 7.5 to 6.6%. Moreover, in contrast to what we observed in Finland, the lowest 3CG resistance proportions were encountered already in 2021 in these countries, after which the trend may have reversed. Interestingly, in the Netherlands, the proportion of 3GC resistance remained stable during the COVID-19 pandemic (7.5% in 2019 and 7.7% in 2022). A similar phenomenon has also been reported in the UK, which was not included in the latest EARS-Net reports, where 3GC E. coli resistance in BSIs remained relatively stable at 14.5% between 2018 and 2022 [27]. Notably, in one Nordic country, Iceland, the proportion of 3GC resistance actually increased by 40%, from 7.0% in 2019 to 9.8% in 2022 [22].

For urine E. coli isolates, during 2019–2022, decreasing trends for cefadroxil-resistant isolates (representing ESBL-producing isolates) and 3GC-resistant isolates have been reported in the national surveillance reports of Sweden and Denmark, respectively [15, 17]. However, the relative changes in these proportions were again smaller than observed in our study in Finland. Moreover, the lowest proportions of these isolates were reported already in 2021, after which the trend may have reversed, contrasting the data from Finland (Sweden: from 6.2% in 2019 to 5.9% in 2021 and 6.2% in 2022; Denmark: at hospital level from 6.9 to 5.8% in 2021 and 6.2% in 2022 and at primary health care from 5.2 to 4.4% in 2021 and 4.8% in 2022). Of note, in Norway, the proportion of ESBL-producing isolates was not reported to decrease among urine E. coli isolates during 2019–2022 [16]. However, the proportion there remained very low (3.0% in 2019 and 3.8% in 2022).

In contrast to most previous studies and reports, we showed that, although the decreases in the proportions of ESBL-producing E. coli were similar in most demographic groups and between sample types, the decreases in the incidence differed, reflecting the changes in tested isolates during the study period. The observed decrease in the total annual number of urine isolates tested and the resulting decrease in the number of E. coli isolates might reflect changes in diagnostic activity of UTIs or healthcare service access after the onset of the pandemic. Hence, particularly uncomplicated and/or non-severe UTIs may have been underdiagnosed during the pandemic years. Due to this selection bias, the proportion of ESBL-producing E. coli among urine E. coli isolates may be slightly overestimated, and the actual annual decrease may have been even larger. In addition, the reduction in elective care in hospitals may have decreased routinely sampled urine cultures, further affecting the numbers and proportions. For blood isolates, the previously observed continuous increase in the annual numbers [19] nearly stopped. This raises a question whether BSIs were also underdiagnosed during the pandemic. Importantly, in both sample types, the annual testing patterns did not clearly change, and the proportion of E. coli as a causative agent of UTIs and BSIs remained similar to pre-pandemic period, 69.3% and 44.0% during 2008–2019 [19] and 71.0% and 46.1% during 2020–2022, respectively.

In the context of COVID-19 pandemic, several factors may have influenced the decreasing trends observed in this study [28, 29]. First, restrictions in travel, in particular international travel, may have significantly decreased the acquisition and cross-border import of ESBL-producing E. coli in Finland [30, 31]. The number of travellers in Finnish airports decreased dramatically from 1.9 million in February 2020 to less than half in March 2020 and to only 1% in April 2020 [32]. Thereafter, the annual number of travellers increased but was over 10 million less in 2022 (15.6 million) compared to the pre-pandemic year 2019 (26.3 million) [33]. Similar trends were seen in at Swedish, Danish, Norwegian, and Dutch airports [34,35,36,37]. The decreased import of ESBL-producing E. coli via travel likely leads also in reduced onward transmission within household members, which is known to occur in up to 12% of the cases [38]. Second, the selective pressure of antibacterials reduced during the study period. The total consumption of antibacterials for systemic use in Finland decreased by 14.9% from 2019 to 2022, which was the greatest decrease among EU countries during the pandemic (EU mean: -2,5%) [39]. In 2022, Finland was among the EU/EAA countries with the lowest antibacterial consumption. The decrease in antibacterial consumption has been related to more stringent hygiene measures in prevention of COVID-19, which also decreased the spread of other respiratory pathogens [40, 41] and resulted in the decreased usage of antibacterials. Third, the IPC measures in the hospitals and LTCFs in response to the pandemic may have decreased the spread of ESBL-producing E. coli in the health care setting [42].

Our study is not without limitations. First, the results of one major Finnish laboratory were not reported to the Finres database for year 2022. However, similar trends in the proportions of ESBL-producing isolates among blood E. coli isolates were observed according to local statistics (personal communication, KRJ, 13th of February 2024). Second, we do not know to what extent different factors (international travel, antimicrobial use, and IPC measures) contributed to the decrease in the proportions of ESBL-producing isolates. Third, the Finres database did not include information about community- or healthcare origin of the isolates. However, decreases in the proportions of ESBL-producing isolates in E. coli UTIs and BSIs in all age groups and both sexes suggest that the decrease likely happened in all settings, the community, acute care hospitals, and LTCFs. Last, we do not know whether the clinical outcome of these infections has changed during the study period.

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