Discussion

In this study using country-level surveillance data from Israel, we reported on 3 indicators of MDRO acquisition and HAI in COVID-19 units. The incidence of acquisition of sentinel MDRO in COVID-19 units in 2020 was higher than in general medical wards but lower than in intensive care units in 2019. MRSA and CRAB infections accounted for approximately 60% of all acquisitions in COVID-19 units. Among the 7 sentinel bacteria monitored, S. aureus was the most common cause of HA-BSI in COVID-19 patients, and MRSA was the most common cause of antimicrobial-resistant HA-BSI.

The incidence of HAI in the context of COVID-19 has been reported on 2 levels: (1) generally, throughout the inpatient population, ^{Reference Polly, de Almeida, Lennon, Cortês, Costa and Guimarães2–Reference Wee, Conceicao and Tan5} and (2) specifically, regarding coinfection of hospitalized patients with SARS-CoV-2 and a healthcare-associated bacterial pathogen. ^{Reference Cona, Tavelli and Renzelli6–Reference Kampmeier, Tönnies, Correa-Martinez, Mellmann and Schwierzeck10} We focused exclusively on COVID-19 patients hospitalized in acute care facilities in Israel during the first 11 months of the pandemic. We considered 3 indicators of acquisition of healthcare-associated bacterial pathogens: incidence of infection or colonization with sentinel bacteria, incidence of bacteremia caused by all sentinel bacteria, and incidence of bacteremia caused specifically by antimicrobial-resistant sentinel bacteria. We focused on incidence among patients with a diagnosis of COVID-19, hospitalized either in designated COVID-19 wards, or in isolation in a general hospital unit during the first year of the pandemic in Israel, which encompassed 3 waves of infection.

We found increased incidence in all 3 acquisition indicators among COVID-19 patients relative to general internal medicine wards in 2019. Among general hospitals of 200 beds and more, the increase in rate was ∼2-fold among the larger hospitals, and less pronounced among the smaller hospitals. The incidence rates among COVID-19 patients remained several-fold lower than those among ICU patients prior to the COVID-19 outbreak. The peak months of absolute incidence for the 3 indicators (ie, October 2020 and January 2021) corresponded as expected, with waves of COVID-19 incidence and resulting high occupancy of acute-care beds with COVID-19 patients.

The peak in May of the incidence rate for all 3 acquisition indicators coincided with the waning of the first wave. This finding can perhaps be explained by a rapid decline in the number of hospitalized COVID-19 patients during the month of May. Those remaining likely had severe illness and prolonged hospitalization, perhaps including immunosuppressive medication used to treat COVID-19. Therefore, they were at high risk for healthcare-associated infection. Differences in illness type and acuity among hospitalized patients with COVID-19, compared with medical and ICU patients prior to the pandemic, may also help explain the difference in distribution of pathogens isolated in cases of antimicrobial-resistant sentinel bacteremia.

During the early months of the pandemic, there were several reports finding a low incidence of HAI and MDRO acquisition among COVID-19 patients. ^{Reference Hughes, Troise, Donaldson, Mughal and Moore11–Reference Cole and Barnard14} The authors of these studies concluded that the heightened emphasis on infection control in response to COVID-19 had a beneficial impact on nosocomial transmission of other pathogens. However, since that early period, a growing body of literature has demonstrated an increase in HA-BSI and MDRO acquisition during the COVID-19 pandemic. Data from the US National Healthcare Safety Network (NHSN) showed a significant increase in the incidence of central line-associated BSI (CLABSI) and MRSA HA-BSI in each of the last three quarters of 2020, compared to the last three quarters of 2019. ^{Reference Weiner-Lastinger, Pattabiraman and Konnor15} Using NHSN data from 148 hospitals, Baker et al reported that for each 0.1 increase in the monthly number of discharges of COVID-19 patients per staffed bed, the incidence of CLABSI rose by 14% and the incidence of MRSA HA-BSI rose by 9%. ^{Reference Baker, Sands and Huang16} In a study from a London hospital group, the HA-BSI rate per 100,000 patient-days was 170.2 among COVID-19 patients, compared with 90.1 among other patients. ^{Reference Zhu, Rawson and Mookerjee17} Proposed explanations for the rise in the incidence of HAI and MDRO acquisition since the earliest months of the pandemic include staffing shortages, higher patient acuity leading to greater and prolonged use of invasive devices, and diversion of infection control staff to COVID-19-related tasks. ^{Reference Gottlieb and Fridkin18}

The care of COVID-19 patients in the hospital setting presents challenges in infection prevention and control above and beyond those of standard inpatient care. Among these challenges are engineering requirements unique to COVID-19 isolation units, cumbersome requirements for use of PPE, the concentration of acutely ill patients with a range of comorbidities, who would normally be cared for in specialized wards, and healthcare workers’ fear of contracting COVID-19.

Interestingly and perhaps counterintuitively, the peak in acquisition rate that we observed early in the study period did not correspond with the proportion of severely ill patients among all COVID-19 patients hospitalized. This proportion peaked at 32% in the first wave, substantially lower than the peak of 55% in the second wave and of 59% in the third wave. A possible explanation for this observation may lie in the fear that accompanied care of COVID-19 patients during the first wave, resulting in inadequate adherence to basic measures of infection prevention, including principles of glove removal and hand hygiene. ^{Reference Gottesman, Fedorowsky, Yerushalmi, Lellouche and Nutman19} Healthcare workers may have been reluctant to enter patient rooms, relying instead on remote care technology but potentially missing early signs of device-associated infection. By the second and third waves, as mechanisms of COVID-19 transmission were better understood, healthcare worker fears subsided and adherence to infection prevention guidance likely improved. Although this proposed explanation is but one of many that are plausible, it is backed by personal observations of the authors on site visits to participating hospitals during the various stages of the pandemic. Focusing, then, on measures to enhance adherence, including alleviation of fears through education, may be key to further improvement in nosocomial infection prevention in future stages of the COVID-19 pandemic.

Among the strengths of this study are the fact that it reports national-level data and includes ongoing surveillance of all common hospital-associated bacterial pathogens. As these are routinely collected data, a limitation of the study is that they do not include factors associated with HAI (eg, staff-patient ratios, ward occupancy, compliance with infection prevention and control measures, and environmental cleaning and disinfection).

In summary, hospitalized COVID-19 patients experienced nosocomial bacterial infection at higher rates than patients on prepandemic general medical wards, adding to the complexity of their care. Our findings confirm those of others worldwide, and they can be explained by a number of factors influencing the inpatient care of COVID-19 patients. Lower rates of nosocomial infection after the first wave suggest that healthcare worker practices, rather than patient-related factors, were perhaps responsible for most of these infections. Addressing these challenges successfully, by infection prevention and control staff and hospital leadership, will be required to improve patient safety in future phases of the pandemic.