Article Type: Original Article COVID-19 Pandemic, CLABSI .

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Infection Control & Hospital Epidemiology (2021), 1–6doi:10.1017/ice.2021.70Original ArticleCoronavirus disease 2019 (COVID-19) pandemic, central-line–associatedbloodstream infection (CLABSI), and catheter-associated urinary tractinfection (CAUTI): The urgent need to refocus on hardwiring preventioneffortsMohamad G. Fakih MD, MPH1,2, Angelo Bufalino PhD3, Lisa Sturm MPH1, Ren-Huai Huang PhD3,Allison Ottenbacher PhD3, Karl Saake MPH3, Angela Winegar PhD3, Richard Fogel MD1 and Joseph Cacchione MD11Clinical & Network Services, Ascension Healthcare, St Louis, Missouri, 2Wayne State University School of Medicine, Detroit, Michigan and 3Ascension DataScience Institute, Ascension Healthcare, St Louis, MissouriAbstractBackground: The coronavirus disease 2019 (COVID-19) pandemic has had a considerable impact on US hospitalizations, affecting processesand patient population.Objective: To evaluate the impact of COVID-19 pandemic on central-line–associated bloodstream infections (CLABSIs) and catheterassociated urinary tract infections (CAUTIs) in hospitals.Methods: We performed a retrospective study of CLABSIs and CAUTIs in 78 US 12 months before COVID-19 and 6 months duringCOVID-19 pandemic.Results: During the 2 study periods, there were 795,022 central-line days and 817,267 urinary catheter days. Compared to the period before theCOVID-19 pandemic, CLABSI rates increased by 51.0% during the pandemic period from 0.56 to 0.85 per 1,000 line days (P .001) and by62.9% from 1.00 to 1.64 per 10,000 patient days (P .001). Hospitals with monthly COVID-19 patients representing 10% of admissions hada National Health Safety Network (NHSN) device standardized infection ratio for CLABSI that was 2.38 times higher than hospitals with 5%prevalence during the pandemic period (P .004). Coagulase-negative Staphylococcus CLABSIs increased by 130% from 0.07 to 0.17 eventsper 1,000 line days (P .001), and Candida spp by 56.9% from 0.14 to 0.21 per 1,000 line days (P .01). In contrast, no significant changeswere identified for CAUTI (0.86 vs 0.77 per 1,000 catheter days; P .19).Conclusions: The COVID-19 pandemic was associated with substantial increases in CLABSIs but not CAUTIs. Our findings underscore theimportance of hardwiring processes for optimal line care and regular feedback on performance to maintain a safe environment.(Received 28 December 2020; accepted 10 February 2021)The coronavirus disease 2019 (COVID-19) pandemic has had aconsiderable impact on US healthcare, straining hospital resourcesand operations. By early December 2020, COVID-19 hospitalizations accounted for 14.5% of occupied inpatient beds.1 Caring forCOVID-19 patients requires more complex processes from diagnostic to safety measures, and it places tremendous pressure onhealthcare workers, from staffing challenges2 to risk of exposureand infection. In addition, the inpatient population has changed,3with a precipitous drop in elective surgical cases4 and an avoidanceof patients being admitted for other medical conditions resulting inAuthor for correspondence: Mohamad G. Fakih, E-mail: Mohamad.Fakih@ascension.org. Or Joseph Cacchione, E-mail: joseph.cacchione@ascension.orgCite this article: Fakih MG, et al. (2021). Coronavirus disease 2019 (COVID-19)pandemic, central-line–associated bloodstream infection (CLABSI), and catheter-associatedurinary tract infection (CAUTI): The urgent need to refocus on hardwiring preventionefforts. Infection Control & Hospital Epidemiology, https://doi.org/10.1017/ice.2021.70a higher case mix index (CMI) among our patient populations.Furthermore, COVID-19 patients often required close monitoringand higher levels of care, including ventilatory and critical caresupport.5Hospital-onset healthcare-associated infections (HAIs) arekey quality and safety metrics publicly reported in the acutecare space and linked to hospital reimbursement by theCenters for Medicare and Medicaid Services (CMS).6 Nationalefforts have been successfully implemented to reduce centralline–associated bloodstream infection (CLABSI)7 and catheter-associated urinary tract infection (CAUTI).8 We evaluatedthe impact of COVID-19 pandemic on the Centers for DiseaseControl and Prevention (CDC) National Healthcare SafetyNetwork (NHSN) CLABSI and CAUTI outcomes in 78 hospitalsof a large, multistate, healthcare system in the United States.Particularly, we examined changes in device utilization, CLABSI The Author(s), 2021. Published by Cambridge University Press on behalf of The Society for Healthcare Epidemiology of America. This is an Open Access article, distributed under theterms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium,provided the original work is properly cited.Downloaded from https://www.cambridge.org/core. 23 Apr 2021 at 07:10:32, subject to the Cambridge Core terms of use.

2and CAUTI events, the associated microbiology of these infections,and the impact on outcomes reflected by the NHSN standardizedinfection ratio.MethodsSettingThis study was a retrospective evaluation of CLABSI and CAUTIoutcomes in 78 hospitals from a single healthcare system over 2periods: before the COVID-19 pandemic (March 2019–February2020; 12 months) and during the COVID-19 pandemic(March–August 2020; 6 months). We evaluated whether increasesin CLABSI or CAUTI events occurred with the COVID-19 pandemic and whether the microbiology of the associated organismschanged.Relation between device-associated events and the COVID-19pandemicTo compare CLABSI and CAUTI outcomes before the COVID-19pandemic with those during the COVID-19 pandemic period, weevaluated CLABSI and CAUTI events as well as central-line andurinary catheter utilization reflected by their standardized utilization ratios (SURs). We also examined the prevalence of COVID-19admissions per month and its relationship to CLABSI and CAUTIevents. Hospitals were classified based on the number of beds aslarge ( 300), medium (100–300), or small ( 100). For each monthduring the pandemic period, hospitals were categorized as havinglow ( 5% of hospital admits), mid-level ( 5% to 10% of hospitaladmits), or high ( 10% of hospital admits) COVID-19 prevalence.The device standardized infection ratio (dSIR) and the populationSIR (pSIR) were compared for the 2 periods.9 The pSIR accountsfor changes in device use and its effect on infection events for apopulation. The pSIR is the ratio of observed events divided by predicted events based on the predicted device days for the same population. At the unit level, it may be calculated by multiplying thedSIR by the SUR.Mohamad G. Fakih et alset was used to identify patients admitted with COVID-19, including sociodemographic characteristics, laboratory results, andhealthcare utilization as captured in electronic health recordsand administrative data. The final data were deidentified andevaluated as aggregates. The study underwent institutional reviewboard evaluation and was deemed to be exempt from furtherreview.Statistical analysisWe used χ2 tests to evaluate the associations of the COVID-19pandemic with CLABSI and CAUTI events. Statistical significance was assessed as P .05, and analyses were performed usingR version 3.6.2 software (R Foundation for Statistical Computing,Vienna, Austria). These analyses were further stratified by eventsoccurring within or outside intensive care and by hospital size.Line utilization, predicted utilization, reported infections, andpredicted infections were calculated for SUR, dSIR, and pSIR.CLABSI dSIR, and CAUTI dSIR were calculated and comparedbased on monthly levels of COVID-19 admissions. The eventrates associated with organisms based on device days werecompared for periods before versus during the COVID-19pandemic.ResultsWe compared data from the 12 months before (March 2019–February 2020) and 6 months during (March–August 2020)COVID-19 pandemic in 78 hospitals in 12 states: 100 beds(n 21); 100–300 beds (n 29); and 300 beds (n 28).Overall, the study included 795,022 central-line days (utilization, 18.3%) and 817,267 urinary catheter days (utilization,18.4%). The SURs over the full 18 months of the study were0.89 for central lines and 0.80 for urinary catheters, and thedSIRs were 0.68 for CLABSI and 0.69 for CAUTI.MicrobiologyComparing device infection over the 2 periodsWe reviewed the associated organisms (up to 3 per CLABSI eventand up to 2 per CAUTI event) documented in the NHSN databasebefore and during the pandemic. Specifically, we looked atdifferences in proportions of gram-positive bacteria, gram-negative bacteria, and yeast over the 2 periods. We also comparedthe CLABSI rates of specific organisms before and during thepandemic.Compared to the pre–COVID-19 period, CLABSI rates increasedby 51.0% during the pandemic period from 0.56 to 0.85 per 1,000line days (P .001) and by 62.9% from 1.00 to 1.64 per 10,000patient days (P .001) (Table 1). This trend was mainly observedin the intensive care units (ICUs) where CLABSI rates increased by71.0% from 0.68 to 1.16 per 1,000 line days (P .001) and by 90.7%from 2.95 to 5.63 per 10,000 patient days (P .001). Larger hospitals ( 300 beds) were most affected, with 154 events during thepandemic period, increasing from 0.58 to 0.88 per 1,000 line days(P .001) and from 1.07 to 1.74 per 10,000 patient days (P .001).Medium-sized hospitals had similar increases in CLABSIs from0.54 to 0.82 per 1,000 line days (P .009) and from 0.95 to 1.61per 10,000 patient days (P .001). No significant changes weredetected in small hospitals.In contrast, overall CAUTI rates did not show any significantdifference between the pre–COVID-19 (0.86 per 1,000 catheterdays) and COVID-19 periods (0.77 per 1,000 catheter days; P .19).We detected no significant differences within the ICUs, but wedetected an improvement in CAUTI rates in the non-ICU settingfrom the pre–COVID-19 period normalized to catheter days (0.85per 1,000 catheter days) to the pandemic period (0.66 per 1,000catheter days; P .04). We detected no associated differences inCAUTI rates based on patient days in the non-ICUs.PopulationWe included hospitalized patients who had a central-line or a urinary catheter during their stay between March 2019 and August2020 reporting to the NHSN from 78 hospitals. All patients witha CDC NHSN–defined CLABSI or CAUTI event between March2019 and August 2020 were identified. The NHSN data includedpatients with events (CLABSIs and CAUTIs), device and patientdays over period of study, the type of unit where the eventsoccurred (ie, intensive care vs non–intensive care), and associatedmicroorganisms.Data sourcesThe CDC NHSN database was used to identify patients withCLABSIs and/or CAUTIs. The Ascension COVID-19 patient dataDownloaded from https://www.cambridge.org/core. 23 Apr 2021 at 07:10:32, subject to the Cambridge Core terms of use.

Infection Control & Hospital Epidemiology3Table 1. Central-Line–Associated Bloodstream Infection (CLABSI) and Catheter-Associated Urinary Tract Infection (CAUTI) Rates Before and During the COVID-19PandemicPre–COVID-19 (Mar 2019–Feb 2020)Pre–COVID-19 vsCOVID-19Relative Change,% (P Value)COVID-19 (Mar–Aug 2020)VariableObservedEventsDeviceDaysRate per1,000DeviceDaysPatientDaysRate per10,000PatientDaysObservedEventsDeviceDaysRate per1,000DeviceDaysPatientDaysRate per10,000PatientDaysRate per1,000DeviceDaysRate .00219257,8980.851,338,6831.6451.0( .001)62.9( .001)Intensive 5.6371.0( .001)90.7( 178135,8890.571,088,4150.7218.8 (.22)17.3 71,366,5581.53 10.2(.19) 0.3 (.97)Intensive 4.601.9 (.87)8.8 194142,0810.661,116,2900.84 21.8(.04) 16.2(.14)Table 2. SURs and SIRs for CLABSIs and CAUTIs Before and During the COVID-19 PandemicVariablePre–COVID-19 (Mar 2019–Feb ine SUR537,124609,7220.88Urinary catheterSUR546,952695,362ReportedInfectionsCLABSI dSIRabSURSIRCLABSI pSIRCOVID-19 (Mar–Aug 2020)Pre–COVID-19 vs COVID-19PredictedUtilizationRatioRelative Change,% (P Value)257,898279,1430.924.9 ( .001)0.79270,315319,9290.847.4% ( dictedInfectionsRatioRelative Change,% (P Value)3025200.582192520.8749.6 ( .001)Utilization3025930.512192720.8158.4 ( .001)CAUTI dSIRa4716600.712093250.64 9.8 (.21)b4718070.582093680.57 2.8 (.73)CAUTI pSIRNote. SUR, standardized utilization ratio; SIR, standardized infection ratio; CLABSI, central-line–associated bloodstream infection; CAUTI, catheter-associated urinary tract infection;aDevice standardized infection ratio.bPopulation standardized infection ratio.Evaluating the changes in SUR and its effect ondSIR and pSIRpSIR was 0.58 and the pSIR during the pandemic was 0.57(P .73).Both central-line and urinary catheter SURs increased during thepandemic period. There was a 4.9% increase in central-line SURfrom 0.88 before the COVID-19 pandemic to 0.92 during the pandemic (P .001). Urinary catheter SUR increased by 7.4%, from0.79 before COVID-19 to 0.84 during the pandemic (P .001)(Table 2). The dSIR for CLABSI increased 49.6% during the pandemic, from 0.58 before COVID-19 to 0.87 during the pandemic(P .001). This change was more pronounced when we calculatedthe pSIR, which increased 58.4% from 0.51 before the pandemic to0.81 during the pandemic (P .001). For CAUTI, we detected nosignificant changes in dSIR; the pre–COVID-19 dSIR was 0.71 andthe dSIR during the pandemic was 0.64 (P .21). Nor did we detecta significant change in the pSIR for CAUTI; the pre–COVID-19Correlations between COVID-19 hospital prevalence, CLABSI,and CAUTI eventsDuring months when patients with active COVID-19 represented 10% of admissions, the CLABSI dSIR was 2.38 times higher(dSIR, 1.58) than in months when COVID-19 prevalence amonghospitalized patients was 5% (dSIR, 0.67; P .004) (Table 3). Wedetected no significant differences in CAUTI dSIR based onmonthly COVID-19 prevalence.CLABSI events and outcomes during the COVID-19 periodIn total, 219 CLABSI events occurred between March and August2020; of these, 52 (24%) occurred in patients hospitalized withDownloaded from https://www.cambridge.org/core. 23 Apr 2021 at 07:10:32, subject to the Cambridge Core terms of use.

4Mohamad G. Fakih et alTable 3. CLABSI and CAUTI Device SIRs and COVID-19 as a Proportion ofAdmissions During Pandemic PeriodMonthly COVID-19PrevalenceaCLABSIdSIRP ValueCAUTIdSIRP ValueHigh ( 10% of hospitaladmissions)1.58Reference0.61ReferenceMid ( 5%–10% of hospitaladmissions)1.09.050.70.55Low ( 5% of hospitaladmissions)0.67.0040.64.64Note. CLABSI, central-line–associated bloodstream infection; CAUTI, catheter-associatedurinary tract infection; SIR, standardized infection ratio.aPatient-based COVID-19 prevalence was available for 76 of 78 hospitals.COVID-19. Also, 2 additional patients were identified withCOVID-19 after their CLABSI event. The average time toCLABSI from COVID-19 diagnosis was 18.0 days (median,15.0). During the 6 months evaluated during the pandemic,18,048 patients diagnosed with COVID-19 were admitted tothe 76 of the 78 hospitals (with available data on patient-basedCOVID-19 prevalence), constituting 5.1% of all admissions.Proportionately, COVID-19 patients had 5 times more CLABSIevents than non–COVID-19 patients. A significant differencewas observed in mortality between patients with CLABSI forthose with COVID-19 (28 of 52, 53.8%) and without COVID19 (40 of 167, 24.0%) during that period (P .001).Microbiology associated with CLABSIs and CAUTIsOverall, 344 organisms were associated with CLABSI events and535 for CAUTI events in the 12 months before the COVID-19 pandemic, while 236 organisms were associated with CLABSI eventsand 237 organisms were associated with CAUTI events duringthe 6 months during the COVID-19 pandemic (Table 4). Grampositive CLABSIs increased by 80.6% from 0.27 to 0.48 eventsper 1,000 line days (P .001). Specifically, coagulase-negativeStaphylococcus CLABSIs increased by 130% from 0.07 to 0.17events per 1,000 line days (P .001), and Candida spp infectionsincreased by 56.9% from 0.14 to 0.21 per 1,000 line days (P .01).We did not observe any significant changes between the 2 periodsfor organisms associated with CAUTIs.DiscussionThe COVID-19 pandemic has had a disruptive effect on the UShealthcare system, resulting in an abrupt drop in admissions formost common conditions and leading to a selective increase inseverity of illness among hospitalized patients.3 As a large UShealth system with 78 hospitals, we report our experience andthe outcomes related to 2 devices: central lines and urinary catheters. Our data show differing impacts of COVID-19 on the CDCNHSN–defined rates of CLABSI and CAUTI events. Based on central-line days, CLABSI rates increased by more than two-thirdswithin the ICUs, whereas the events per 10,000 patient days almostdoubled. Recent studies have reported large increases in CLABSIevents10 and a higher likelihood for secondary bloodstream infections in COVID-19 patients requiring intensive care.11 In anattempt to reduce healthcare worker exposure to patients and topreserve personal protective equipment, the frequency of contactwith patients may have changed during the pandemic. Moreover,patients admitted during the pandemic were more likely to requirecritical care support and to need it for a longer period of time,12potentially putting them at greater risk for CLABSI. The proportion of COVID-19 patients with CLABSI events was 5 times greaterthan for non–COVID-19 patients during the pandemic period.Additionally, the average time from COVID-19 diagnosis to developing CLABSI was 18 days, indicating that the CLABSI eventsoccurred in COVID-19 patients with prolonged hospitalization.Although the increases in CLABSI events did not reach statisticalsignificance in non–ICUs, we expect that similar challenges ininfection prevention were encountered.An integral risk-reduction strategy for CLABSI is anchoredin the optimal maintenance of the device.13 In the prepandemicperiod, CLABSI prevention strategies were hardwired at ourhospitals leading to a dSIR of 0.58, which outperformed thenational CDC NHSN CLABSI dSIR of 0.69 for 2019.14 The pandemic likely affected both the care of the line for COVID-19 andnon–COVID-19 hospitalized patients. Qualitative feedback frominfection prevention teams reported changes to routine CLABSIprevention practices in ICUs, such as less universal decolonization(eg, mupirocin administration and chlorhexidine bathing), alterations in line care due to intravenous pumps placed in hallways (eg,extension tubing used and less bedside checks on lines), line anddressing integrity gaps related to prone positioning of patients,opportunities in scrub-the-hub compliance, and increases in linedraws for blood cultures. Another variable potentially impactingCLABSI outcomes includes staffing changes responding toincreased patient volume on the units, such as the help of travelingclinicians not as familiar with standard unit prevention practices.Lastly, during the pre–COVID-19 period, “line rounds” were aroutine practice, ensuring that proper device selection, utilization,and bedside practices were being followed. The teams reported thatmany of those rounds stopped during the COVID-19 pandemicperiod due to competing priorities. On the other hand, with theless intense needs for indwelling urinary catheter device care,nominal changes in practice were reported, with the exceptionof some reports of increases in pan-culturing for febrile patients.In addition to the increases in the occurrence of CLABSI duringthe pandemic, we observed changes in the mi

Article Type: Original Article COVID-19 Pandemic, CLABSI, and CAUTI: The Urgent Need to Refocus on . for optimal line care, and regular feedback on performance to maintain a safe environment. . other medical conditions, resulting in a higher Case Mix Index (CMI) among our patient populations. Furthermore, COVID-19 patients often .

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