Large increase in bloodstream infections with carbapenem-resistant Acinetobacter species during the first 2 years of the COVID-19 pandemic, EU/EEA, 2020 and 2021

Recent data from the European Antimicrobial Resistance Surveillance Network (EARS-Net) show a large increase of +57% in Acinetobacter species bloodstream infections in the European Union and European Economic Area in the first years of the COVID-19 pandemic (2020–2021) compared with 2018–2019. Most were resistant to carbapenems, from intensive care units, and in countries with ≥ 50% carbapenem resistance in Acinetobacter spp. in 2018–2019. This highlights the requirement for reinforced Acinetobacter preparedness and infection prevention and control in Europe.

Recent data from the European Antimicrobial Resistance Surveillance Network (EARS-Net) show a large increase of +57% in Acinetobacter species bloodstream infections in the European Union and European Economic Area in the first years of the COVID-19 pandemic (2020-2021) compared with 2018-2019. Most were resistant to carbapenems, from intensive care units, and in countries with ≥ 50% carbapenem resistance in Acinetobacter spp. in 2018-2019. This highlights the requirement for reinforced Acinetobact er preparedness and infection prevention and control in Europe.
Bloodstream infections (BSIs) with Acinetobacter species commonly have poor outcomes, especially in intensive care unit (ICU) patients [1]. Acinetobacter spp. is intrinsically resistant to many antimicrobials, and additional acquired resistance further complicates the treatment of serious infections in already vulnerable patient groups. Recent data from the European Antimicrobial Resistance Surveillance Network (EARS-Net) show a large and statistically significant increase in reports of Acinetobacter spp. BSIs in the European Union (EU) and European Economic Area (EEA) during the period from 2017 to 2021 [2]. Most of this increase occurred in 2020 and 2021, the first years of the coronavirus disease (COVID- 19) pandemic. Here we further explore this trend in a subset of data from laboratories that continuously reported data during that period.

Data description
Our data originate from qualitative routine antimicrobial susceptibility testing (AST) results of blood isolates collected by local clinical laboratories in national networks in EU/EEA countries. These results are reported annually by national centres to the European Centre for Disease Prevention and Control (ECDC), according to the EARS-Net reporting protocol [3]. In its analyses, EARS-Net only includes the first isolate per patient each year and for each bacterial species.
All EU countries, Iceland and Norway reported data to EARS-Net every year during the period 2017 to 2021 [2,4]. For this analysis, we restricted the dataset to BSIs with Acinetobacter spp. and to only those laboratories that reported carbapenem (imipenem and/or meropenem) antimicrobial susceptibility testing results for Acinetobacter spp. for every year in 2017 to 2021 (255 of 826 laboratories reporting, on average, per year). We made this restriction to limit bias from year-to-year changes in the number, hospital affiliation and type of reporting laboratories, and because not all countries can discriminate between laboratories that did not report and those that had no cases. The United Kingdom ceased reporting data to ECDC in 2020 when it withdrew from the EU and was hence not included. In addition, France was excluded because, following a major reorganisation of national surveillance in 2020, only a few laboratories were continuously identifiable. The Table presents data for the 28 included countries, with and without restriction to continuously reporting laboratories.

Discussion
The observed trends for Acinetobacter spp. BSI in the EU/EEA are worrying because resistance to carbapenems causes a high burden of disease in vulnerable hospitalised patients [5][6][7]. Our findings suggest that countries where carbapenem-resistant Acinetobacter spp. were already well established before the COVID-19 pandemic (Group 3) had the biggest challenges in controlling further spread in 2020-2021.
Acinetobacter spp. is difficult to eradicate from the hospital environment, colonising hospital patients and staff and causing outbreaks, particularly in ICUs [1]. Several reports have identified Acinetobacter spp. as one of the most frequent causes of infectious complications in hospitalised patients with COVID-19 [8][9][10]. The observed increasing trends at EU/EEA level compared with the pre-pandemic situation [2,11,12] were probably driven by the profound impact of the COVID-19 pandemic on hospital care, which increased the number of patients at risk of Acinetobacter spp. BSI, and also by difficulties in applying infection prevention and control (IPC) measures. In 2020-2021, there were larger numbers of severely ill patients, many with severe pulmonary infection. High occupancy rates necessitated increased provision of ICU beds, often with staff who were overworked or less experienced [13,14]. Inappropriate application of  contact precautions for COVID-19 patients, in particular suboptimal hand hygiene, as well as contamination and insufficient cleaning of the hospital environment, probably contributed to direct or indirect betweenpatient Acinetobacter spp. transmission [15][16][17][18][19][20]. Finally, reduced attention to antimicrobial stewardship, with resulting increased carbapenem use, may have contributed [21].
For context, in 2020-2021 compared with 2018-2019, the laboratories that continuously reported Acinetobacter spp. data to EARS-Net also reported more cases of BSI with Enterococcus faecium (+ 29%), E. faecalis (+ 16%), Pseudomonas aeruginosa (+ 8%), Klebsiella pneumoniae (+ 6%), but these differences were much less pronounced than for BSI with Acinetobacter spp. (+ 57%). Laboratories reported fewer cases of BSI with Streptococcus pneumoniae (− 47%), Escherichia coli (− 5%) and Staphylococcus aureus (− 1%). These differences probably depend on the epidemiological characteristics of the various pathogens. For example, S. pneumoniae and E. coli are more frequently transmitted in the community and in non-ICU hospital settings. During the COVID-19 pandemic, transmission of microorganisms in the community was affected by containment actions such as stay-at-home orders, physical distancing, hygiene measures and the use of face masks. This may have contributed to the sharp decline in typically community-acquired infections such as those caused by S. pneumoniae [22,23].
There were exceptions to the general trends by country group, indicating that the trends were not only explained by the pre-pandemic percentage of carbapenem resistance. For example, Portugal and Spain were outliers in their respective groups by reporting fewer Acinetobacter spp. BSIs in 2020-2021 than in 2018-2019, whereas Slovenia reported a larger increase in Acinetobacter spp. BSIs than other Group 2 countries.
Although reasons for the trends observed during the COVID-19 pandemic remain to be clarified, most factors that potentially favoured the increase in carbapenem-resistant Acinetobacter spp. infections, and in general multidrug-resistant microorganisms, are amenable to public health intervention. Options include rigorous adherence to hand hygiene, environmental cleaning, provision and appropriate use of personal protective equipment, appropriate training of healthcare staff, and promotion of antimicrobial stewardship programmes. While spread of carbapenem-resistant Acinetobacter spp. is difficult to control while established, recent evidence shows that Acinetobacter spp. outbreaks can be controlled through a bundle of measures including thorough environmental cleaning, even without ward closure [16,24]. Finally, any country with an increasing number of infections with carbapenem-resistant Acinetobacter spp. in 2020-2021, particularly those with comparatively moderate resistance percentages (e.g. 10% to < 50%, Group 2), should urgently ensure preparedness for the prevention and control of Acinetobacter spp. infections and outbreaks.

Conclusion
The large increase in carbapenem-resistant Acinetobacter spp. BSI in the EU/EEA during a time of great challenges for healthcare calls for reinforced application of the preparedness and response actions that we present above. Surveillance at local, national and EU/EEA levels will be vital to monitor whether this worrying development is halted or even reversed.   (Table) [2,4].

EARS-Net Study Group participants
For Latvia, the two datapoints for the mean overlap and only the dark symbol is visible.