key: cord-0890498-9i5k8ruy authors: Rosenthal, Victor D.; Myatra, Sheila Nainan; Divatia, Jigeeshu Vasishtha; Biswas, Sanjay; Shrivastava, Anjana; Ruzzieh, Majeda A. Al-; Ayyad, Omar; Bat-Erdene, Ariungerel; Bat-Erdene, Ider; Narankhuu, Batsaikhan; Gupta, Debkishore; Mandal, Subhranshu; Sengupta, Sankar; Joudi, Hala; Omeis, Ibrahim; Agha, Hala Mounir; Fathallala, Amr; Mohamed, El Hossein; Yesiler, Irem; Oral, Mehmet; Ozcelik, Menekse; Mehta, Yatin; Sarma, Smita; Chatterjee, Souranshu; Belkebir, Souad; Kanaa, Alaa; Jeetawi, Rawan; Mclaughlin, Samantha A.; Shultz, James M.; Bearman, Gonzalo title: The impact of COVID-19 on healthcare-associated infections in intensive care units in low and middle income countries: International Nosocomial Infection Control Consortium (INICC) findings date: 2022-02-24 journal: Int J Infect Dis DOI: 10.1016/j.ijid.2022.02.041 sha: 137c2819876e51ae2536b215c45314b2d19d87f5 doc_id: 890498 cord_uid: 9i5k8ruy Background : This study examines the impact of the COVID-19 pandemic on healthcare-associated infection (HAI) incidence in low-to-middle-income countries (LMICs). Methods : Patients from 7 LMICs were followed during hospital intensive care unit (ICU) stays throughout January 2019 to May 2020. HAI rates were calculated using the INICC Surveillance Online System applying CDC-NHSN criteria. Pre-COVID-19 rates for 2019 were compared to COVID-19 era rates for 2020 for central line associated bloodstream infections (CLABs), catheter associated urinary tract infections (CAUTIs), ventilator associated events (VAEs), mortality and lengths of stay (LOS). Results : 7,775 patients were followed for 49,506 bed-days. 2019 to 2020 rate comparisons: 2.54 and 4.73 CLABSIs per 1,000 central line days (RR=1.85, p = 0.0006), 9.71 and 12.58 VAEs per 1,000 mechanical ventilator days (RR=1.29, p = 0.10), 1.64 and 1.43 CAUTIs per 1,000 urinary catheter days (RR=1.14; p = 0.69). Mortality rates were 15.2% and 23.2% for 2019 and 2020 (RR=1.42; p < 0.0001). Mean LOS were 6.02 and 7.54 days (RR=1.21, p < 0.0001). Discussion : This report documents a rise in HAI rates in 7 LMICs during the first 5 months of the COVID-19 pandemic and highlights the need to reprioritize and return to conventional infection prevention practices. Prior to the appearance and worldwide spread of the coronavirus disease 2019 pandemic, a pervasive decrease in healthcare-associated infection (HAI) incidence had been observed across hospitals in the United States (Weiner-Lastinger et al., 2021b) . Throughout 2020, as COVID-19 swept across the US in multiple waves, regions experienced steep surges in cases and hospitalizations (Ripa et al., 2021) . Some studies specifically noted the occurrence of secondary infections in COVID-19 patients (Ripa et al., 2021) . Single-site studies observed signs of increases in select HAIs in the US as early as the spring of 2020 (Fakih et al., 2021 , LeRose et al., 2021 , McMullen et al., 2020 . During the second quarter of 2020, as US hospitals nationwide responded to the influx of COVID-19 cases, increasing standardized infection ratios (SIRs) were detected (Weiner-Lastinger et al., 2021b) . Initial increases in the SIRs were observed for central-line-associated bloodstream infections (CLABSIs), Methicillinresistant Staphylococcus aureus (MRSA) bacteremia, and ventilator associated events (VAEs) (Weiner-Lastinger et al., 2021b) . Compared with the pre-pandemic rates observed throughout 2019, the third and fourth quarters of 2020 were notable for significant increases in SIRs associated with CLABSIs, VAEs, MRSA bacteremia, and catheter-associated urinary tract infections (CAUTIs) (Weiner-Lastinger et al., 2021b) . When comparing 2020, the first year of COVID-19 hospitalizations throughout the US, to the pre-pandemic experience of 2019, the upward trend in SIRs across all HAI types, was most pronounced for CLABSIs (Weiner-Lastinger et al., 2021b) . According to the National Healthcare Safety Network (NHSN), increasing rates for CLABSIs were noted in the earliest months of the pandemic (Patel et al., 2021) . Elevated CLABSI incidence during the COVID-19 pandemic, in the context of the likely impacts of hospital COVID-19 prevention activities on central line insertion and maintenance practices, have been repeatedly documented (Fakih et al., 2021 , LeRose et al., 2021 , McMullen et al., 2020 . Potential contributors to increased risks for device-associated infection during the COVID-19 pandemic in 2020 included: longer patient lengths of stay, increased numbers of comorbidities, elevated patient acuity levels, and longer durations of device use (Weiner-Lastinger et al., 2021b) . Increased reliance on acute-care hospitals (ACHs) during the pandemic may also have increased HAI risks in several ways including altered staffing patterns and practices, increased critical care capacity, and modified use of personal protective equipment (PPE) (Rebmann et al., 2021 , Weiner-Lastinger et al., 2021a . The International Nosocomial Infection Control Consortium (INICC) is the largest international HAI surveillance system. INICC surveillance is used by hospitals in multiple Low-to-Middle-Income Countries (LMICs) (Rosenthal, 2016 , Rosenthal et al., 2008 . INICC data are used to both update HAI rates and measure the impact of infection prevention interventions (Rosenthal et al., 2021 , Rosenthal et al., 2013b . For almost two decades, from 2002 through 2019, the INICC's LMIC members have seen significant reductions in the rates of CLABSI, VAE, and CAUTI, related to their adoption and application of INICC online platforms and prevention methods (Rosenthal et al., 2013a , Rosenthal et al., 2010 , Rosenthal et al., 2014 , Rosenthal et al., 2012a , Rosenthal et al., 2012b , Rosenthal et al., 2012c , Rosenthal et al., 2012d . Given the likelihood for COVID-19 response activities to impact HAI risks and practices, the INICC team analyzed HAI incidence, comparing pre-pandemic rates from 2019 to pandemic-era rates in 2020 to explore potential changes. Data were collected using the INICC Surveillance Online System (ISOS) platform (Rosenthal, 2016 , Rosenthal et al., 2008 . ISOS applies National Healthcare Safety Network (NHSN) criteria, developed by the Centers for Disease Control and Prevention (CDC), for the calculation of HAI rates and device utilization ratios (DURs) (CDC/NHSN, 2019 , Emori et al., 1991 . HAI definitions include both laboratory and clinical criteria (CDC/NHSN, 2019 , Emori et al., 1991 . Acute care hospital patients from 7 LMICs that report to the INICC (India, Mongolia, Jordan, Lebanon, Palestine, Egypt, and Turkey) were followed from intensive care unit (ICU) admission to discharge. Infection preventionists (IPs) collected data on HAIs occurring in all patients admitted to the ICU. The corresponding denominator data, consisting of specific device days, were collected and validated. Rates of CLABSIs, VAEs, CAUTIs, and mortality, along with lengths of stay, were computed from analyses of compiled individual patient data. INICC methods include includes daily data collection for all patients, the use of invasive devices, confirmation that CDC-NHSN criteria for diagnosed HAIs are met in each case, along with a check of numerators and denominators (Rosenthal, 2016 , Rosenthal et al., 2008 . Using INICC data, HAI incidence rates were calculated and compared for 2019 (prepandemic year) and first five months of 2020 (pandemic year). Data analyses were conducted using SPSS 16.0 (SPSS Inc., an IBM company, Chicago, IL); ISOS (Buenos Aires, Argentina) (Rosenthal, 2016 , Rosenthal et al., 2008 ; and EpiInfo version 6.04b (CDC, Atlanta, GA). In order to compare hospitalization type and gender among both periods, we applied a test of homogeneity, Pearson's Chi-squared test, with Yates' continuity correction; to compare age among both periods, we applied two Sample t-test, for 2 independent groups; and to compare mechanical ventilator-days, central line-days, urinary catheter-days, and peripheral catheter-days among both periods, we applied two Sample t-test for 2 independent groups. Data for ICUs were not stratified by type or size of hospital. A total of 7,775 patients admitted to ICUs in hospitals in 7 LMICs were followed from admission to discharge from the ICU, totaling 49,506 bed days of observation. In pre-pandemic period, from January 1 st to December 31 st 2019, 5,997 patients were hospitalized in ICUs for a total of 36,106 bed days. In pandemic period, from January 1 st 2020 to May 31 st 2020, 1,778 admitted patients were hospitalized for 13,400 bed days. The average length of stay was 6.02 days in 2019 and 7.54 This is the first international report comparing HAI, mortality rates, and LOS among patients hospitalized in ICUs in multiple LMICs in 2019, prior to the COVID-19 pandemic, and in 2020, during the first 5 months of the pandemic. Data reported here provide an international picture of how patient safety generally, and incidence rates of HAIs specifically may have been affected by the COVID-19 pandemic. Prior to the arrival of COVID-19, decreasing HAI incidence rates had been observed in LMICs (Rosenthal et al., 2013a , Rosenthal et al., 2010 , Rosenthal et al., 2014 , Rosenthal et al., 2012a , Rosenthal et al., 2012b , Rosenthal et al., 2012c , Rosenthal et al., 2012d , as well as in US hospitals. showing sharp rises in CLABSI rates (highest among all HAI types) during the pandemic. These complementary findings suggest that COVID-19 prevention activities may have impacted central line insertion and maintenance practices, as previously documented in multiple studies (Fakih et al., 2021 , LeRose et al., 2021 , McMullen et al., 2020 , Patel et al., 2021 . It is likely that 2020 COVID cases that were populating the hospital ICUs were associated with longer mean LOS, multiple comorbidities, elevated patient acuity levels, and longer durations of device use, all factors that could have increased risks for HAIs during the pandemic (Fakih et al., 2021 , LeRose et al., 2021 , McMullen et al., 2020 . Moreover, several studies identified an increased risk of ventilator-associated conditions in critically ill COVID-19 patients (Fakih et al., 2021 , LeRose et al., 2021 , Maes et al., 2021 , McMullen et al., 2020 . The characteristic worsening of respiratory status in some patients with COVID-19 resulted in an increase in the number of hospitalized patients in 2020 that required ventilation, and an increase in patients' average duration of ventilation, both of which could have contributed to an increased risk of VAEs. Further support for this reasoning comes from CDC analyses, spanning many states that experienced high rates of COVID-19 hospital admissions, showing significant increases in rates of both CLABSI and VAE during 2020 compared to 2019 pre-pandemic rates of these HAIs (Sapiano et al., 2021) . Increment on CLABSI rate during period of 2020 was not influenced by hospitalization type, by age, or by gender, because hospitalization type and gender were similar comparing both periods, and the patients were younger during period of 2020. Also increment of CLABSI rates was not associated to heavier device utilization of vascular catheters, because device utilization of central line and peripheral catheter were similar comparing both periods. Usage of urinary catheter was similar and CAUTI rates were also similar comparing both periods, meaning that usage of urinary catheter didn't have any influence on rates. Utilization of mechanical ventilator was significantly higher during 2020 period, but VAE rates were not significantly higher. The current study has several limitations. Analyses were was limited to hospitals that reported data for both 2019 and 2020. New hospitals and units that opened in 2020 in response to COVID-19 were not included. Many LMIC hospitals and healthcare centers ceased their HAI surveillance during 2020, the first year of the pandemic, due to the extreme workload demands associated with caring for the COVID-19 patient surge, coupled with marked reductions in staffing. Thus our current analyses are limited to a group of hospitals in just 7 LMICs. Thus, the findings of this paper cannot be generalized to represent the patterns of HAIs across a broader spectrum of LMICs. Furthermore, we focused solely on ACHs for these analyses; here again we are unable to extend our findings to other care settings for COVID-19 patients including critical access and long-term facilities. Finally, we didn't analyze if observed significant excess length of stay was the cause or the consequence of HAIs. This study is the first to provide a comprehensive look at the impact of COVID-19 on HAI incidence in LMICs. Significant increases were observed in overall mortality, CLABSIs, and mean LOS, along with a marginally significant rise in VAEs. The COVID-19 pandemic's first year-2020--marked an unprecedented time for hospitals, many of which were simultaneously challenged to confront an overwhelming patient caseload, deep and acute staffing shortages, austere care regimens, crisis standards of care, and rationing of life-saving devices and therapies, all of which impinged on the capabilities to maintain optimal infection prevention and control practices. Regular review of HAI surveillance data is critical for hospitals to rapidly detect any upward inflections in HAI rates, to identify gaps in prevention practices, and to implement effective interventions. Infection prevention programs should urgently reprioritize infection prevention practices in their facilities. Healthcare systems must improve contingency planning to foster resiliency and to withstand future public health emergencies. The funding for design, development, maintenance, technical support, data validation, and report generation of ISOS, and the activities carried out at INICC headquarters, were provided by the corresponding author, Victor D. Rosenthal. I have read and complied with the policy of the journal on ethical consent as stated in the Guide to Authors. 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