Effects of the COVID-19 Pandemic on Incidence and Epidemiology of Catheter- Related Bacteremia, Spain Oriol Gasch, Laia Badia-Cebada, Joao Carmezim, Montserrat Vaqué, Virginia Pomar, Encarna Moreno, Anna Marrón, Emili Jiménez-Martínez, Maria José García-Quesada, Xavier Garcia-Alarcón, Dolors Domènech, Jordi Càmara, Marta Andrés, Judith Peñafiel, Rosario Porrón, Enric Limón, Esther Calbo, Miquel Pujol We compared hospital-acquired catheter-related bacte- acute care hospitals to modify their structural and remia (CRB) episodes diagnosed at acute care hospitals human resource organization (3); scheduled elective in Catalonia, Spain, during the COVID-19 pandemic in surgeries were cancelled, and healthcare workers had 2020 with those detected during 2007–2019. We com- to change their specific clinical roles to address the pared the annual observed and predicted CRB rates by abrupt increase in admissions of SARS-CoV-2–in- using the negative binomial regression model and calcu- fected patients. To reduce SARS-CoV-2 nosocomial lated stratified annual root mean squared errors. A total transmission, airborne and contact precaution mea- of 10,030 episodes were diagnosed during 2007–2020. sures were reinforced, personal protective equipment During 2020, the observed CRB incidence rate was was worn by healthcare providers, and strict hand 0.29/103 patient-days, whereas the predicted CRB rate hygiene measures were observed at most centers (4). was 0.14/103 patient-days. The root mean squared er- Hand hygiene is a cornerstone of healthcare-asso- ror was 0.153. Thus, a substantial increase in hospital- acquired CRB cases was observed during the COVID-19 ciated infection (HAI) prevention, and reductions in pandemic in 2020 compared with the rate predicted from Clostridioides difficile colitis incidence (5,6) and surgi- 2007–2019. The incidence rate was expected to increase cal-site infections (7,8) have been observed in different by 1.07 (95% CI 1–1.15) for every 1,000 COVID-19–re- settings during the COVID-19 pandemic. However, lated hospital admissions. We recommend maintaining reductions in other HAIs, such as catheter-associated all CRB prevention efforts regardless of the coexistence urinary tract infections, ventilator-associated pneu- of other challenges, such as the COVID-19 pandemic. monia, or catheter-related bacteremia (CRB) (9,10), were not observed. In addition, multidrug-resistant I n December 2019, the first cases of COVID-19 were reported in Wuhan, China (1). On March 11, 2020, the World Health Organization declared COVID-19 microorganisms were increasingly involved in these other HAIs (10–12). CRB is one of the most frequent HAIs (13,14) and a global pandemic because of the spread of SARS- represents a major health challenge because of its CoV-2 infections worldwide (2). Subsequent waves high association with illness and death (15,16). CRB related to the spread of different SARS-CoV-2 sero- is currently considered a leading safety concern in types forced healthcare systems and, specifically, healthcare settings and is a clinical practice quality Author affiliations: Universitat Autònoma de Barcelona, Barce- L’Hospitalet de Llobregat (E. Jiménez-Martínez, J. Càmara, lona, Spain (O. Gasch); Hospital Universitari Parc Taulí I3PT, M. Pujol); Hospital Germans Trias i Pujol, Badalona, Spain Sabadell, Spain (O. Gasch, L. Badia-Cebada, A. Marrón); (M.J. García-Quesada); Hospital Josep Trueta, Girona, Spain Institut d’Investigació Biomèdica de Bellvitge-IDIBELL, (X. Garcia-Alarcón, D. Domènech); Hospital Consorci de L’Hospitalet de Llobregat, Spain (J. Carmezim, J. Càmara, Terrassa, Terrassa, Spain (M. Andrés); VINCat, Barcelona J. Peñafiel, M. Pujol); Hospital de Barcelona, Barcelona (R. Porrón, E. Limón); Universitat de Barcelona, Barcelona (M. Vaqué); Hospital de la Santa Creu i Sant Pau, Barcelona (E. Limón); Hospital Universitari Mútua Terrassa, Terrassa (E. Calbo) (V. Pomar); Parc Sanitari Sant Joan de Déu, Sant Boi de Llobregat, Spain (E. Moreno); Hospital Universitari de Bellvitge, DOI: https://doi.org/10.3201/eid2811.220547 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 28, No. 11, November 2022 2181 RESEARCH indicator (17). For these reasons, CRB surveillance is identify habitual skin-colonizing microorganisms, mandatory in most countries (18–20). such as coagulase-negative staphylococci, Micrococ- In Catalonia, Spain, CRB surveillance is guided cus spp., Propionibacterium acnes, Bacillus spp., and Co- by the VINCat program of the Catalan Health Ser- rynebacterium spp. Positive bacterial cultures had to vice (21), which provides a surveillance system for be associated with clinical manifestations of infection, healthcare-associated nosocomial infections. The such as fever, chills, or hypotension, and absence of VINCat program was launched in 2006; the main any apparent alternative source of bloodstream in- objective of this program is to reduce the incidence fection (BSI). The conditions had to be accompanied of HAIs through continuous active monitoring and by >1 of the following criteria: >15 CFU per catheter implementation of preventive programs (21). During segment in semiquantitative cultures or >103 CFU recent decades, the incidence of healthcare-acquired per catheter segment in quantitative cultures that CRB has decreased in most hospitals, especially in detected the same microorganism found in periph- intensive care units (ICUs), because of the applica- eral blood cultures; quantitative blood cultures that tion of preventive measures (22,23). Some of the most detected the same microorganism and showed a dif- critical evidence-based preventive interventions have ference of >5:1 between the blood obtained from the been using appropriate barrier precautions and hand lumen of a venous catheter and that obtained from a hygiene before handling catheters, disinfecting skin peripheral vein by puncture; difference of >2 hours with chlorhexidine solutions, using appropriate cath- between positive bacterial cultures obtained from a eter materials, carefully selecting insertion sites that peripheral vein and the lumen of a venous catheter; avoid the femoral site, and withdrawing catheters presence of inflammatory signs or purulent secre- whenever possible (24). During the COVID-19 pan- tions in the insertion point or the subcutaneous tun- demic, adherence to some of these preventive mea- nel of a venous catheter (a culture of the secretion sures has notably affected HAI incidence rates (11); showing growth of the same microorganism detected however, the effect of COVID-19 on CRB incidence is in the blood cultures was also useful); and resolution not definitively known. The aim of this study was to of clinical signs and symptoms after catheter with- assess the effects of the COVID-19 pandemic on the drawal with or without appropriate antibiotic treat- incidence of hospital-acquired CRB. ment. For the clinical diagnosis of peripheral venous CRB, we required signs of phlebitis (induration, pain, Materials and Methods or signs of inflammation at the insertion point or the catheter route). Clinical Setting Bacteremia associated with the use of venous cath- Exclusion Criteria eters was continuously monitored under the VINCat We excluded patients if they were under 18 years of program. All nosocomial episodes of CRB diagnosed age, were outpatients, and had a hospital stay <48 in adult patients at each participating hospital were hours at the time of BSI detection. We also excluded prospectively followed and reported to the VINCat those who had CRB detected at an outpatient service program by infection control teams. CRB cases were or had CRB associated with arterial catheters. identified by daily evaluation of all patients with bac- teria-positive blood cultures. Microbiology Hospitals participating in the VINCat program Two sets of 2 blood samples from a peripheral vein are classified into 3 categories according to the num- were obtained from all patients with a suspected ber of beds available for hospitalization: >500 beds BSI. An additional blood sample was also obtained (group I), 200–499 beds (group II), and <200 beds through the catheter. When possible, the catheter tip (group III). Data from each hospital are continu- was cultured after removal. Blood samples were pro- ously monitored and presented in general clinical cessed at the microbiology laboratories of each center sessions. A public annual report is published on the in accordance with standard operating procedures. VINCat website (21). All microorganisms were identified by using stan- dard microbiological techniques at each center. Definitions We defined catheter-related bacteremia as the detec- Statistical Analysis tion of bacterial growth in patient blood using a ve- We reported categorical variables as the number of nous catheter; >1 set of blood cultures were obtained cases and percentages and continuous variables as from a peripheral vein and 2 sets were obtained to means +SD or medians with interquartile ranges, 2182 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 28, No. 11, November 2022 Effects of COVID-19 on Catheter-Related Bacteremia Figure 1. Observed and predicted incidence rates of CRB during 2007–2020 in study of effects of the COVID-19 pandemic on incidence and epidemiology of CRB, Spain. We calculated the CRB incidence rate by dividing the total number of episodes of catheter-related bloodstream infections by the total number of hospital stays (patient- days) for each year from 2007 to 2020. We predicted incidence rates by using the negative binomial regression model and compared the predicted rates with observed rates for each year. CRB, catheter- related bacteremia. depending on whether the distribution was normal stratified analyses according to hospital ward, cath- or nonnormal. We assessed normality of variables eter type, catheter insertion site, catheter use, and graphically by using quantile-quantile and density type of identified microorganism. We reported the plots. We calculated the CRB incidence rate by divid- annual rate of CRBs diagnosed per 1,000 patient-days ing the total number of episodes of CRB by the total and the incidence rate ratio (IRR) and 95% CI for each number of hospital stays (patient-days) in 1 year. model. We focused the interpretation of the IRR on We used a negative binomial regression model the annual rate of increase or decrease. to assess the rate trend of CRBs diagnosed at VINCat We plotted and compared the annual CRB rates hospitals each year during 2007–2019. We used the observed during 2007–2020 and annual CRB rates number of admissions per year as the offset variable, predicted by our model. We calculated the aver- number of events as the dependent variable, and year age root mean squared error (RMSE) of the model as the main independent variable. We performed predictions for CRB rates during 2007–2019 and Table 1. Incidence rates of CRB per 1,000 patient-days in 2020 stratified by catheter characteristics and microorganisms in study of effects of the COVID-19 pandemic on incidence and epidemiology of catheter-related bacteremia, Spain* Category Observed rate Predicted rate Observed/predicted (95% CI) RMSE Location acquired ICU 1.62 0.48 3.42 (3.04–3.79) 1.147 Non-ICU 0.19 0.12 1.51 (1.37–1.65) 0.062 Catheter type CVC 0.16 0.06 2.54 (2.29–2.78) 0.094 PICVC 0.06 0.04 1.73 (1.46–2.00) 0.025 PVC 0.06 0.05 1.24 (1.06–1.43) 0.012 Catheter insertion site Arm/forearm 0.12 0.08 1.45 (1.29–1.60) 0.038 Jugular 0.09 0.03 2.64 (2.30–2.97) 0.056 Subclavian 0.04 0.02 1.88 (1.53–2.22) 0.020 Femoral 0.02 0.01 3.12 (2.27–3.96) 0.013 Catheter use Serum/medication 0.22 0.10 2.14 (1.97–2.31) 0.117 Hemodialysis 0.00 0.00 1.25 (0.51–1.99) 0.001 Parenteral nutrition 0.06 0.03 1.62 (1.36–1.89) 0.021 Microorganism Staphylococcus aureus 0.06 0.04 1.26 (1.06–1.46) 0.012 Coagulase-negative staphylococci 0.11 0.05 2.41 (2.14–2.68) 0.066 Gram-negative bacteria 0.04 0.03 1.69 (1.38–2.01) 0.017 Enterococcus sp. 0.03 0.01 5.41 (4.16–6.65) 0.022 Pseudomonas aeruginosa 0.01 0.01 2.20 (1.46–2.94) 0.007 Candida sp. 0.02 0.01 2.24 (1.59–2.90) 0.009 *We predicted expected rates of CRB by using negative binomial regression models and compared predicted rates with observed CRB rates in 2020. CRB, catheter-related bacteremia; RMSE, root mean squared error; ICU, intensive care unit; CVC, central vascular catheter; PICVC, peripherally inserted central vascular catheter; PVC, peripheral vascular catheter. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 28, No. 11, November 2022 2183 RESEARCH compared the RMSEs between the expected rate ac- We evaluated the conditions of application in cording to the model and observed rate in 2020. We all models and calculated the 95% CI for each esti- replicated these analyses after stratifying by hospital mator. We arbitrarily set the level of statistical sig- ward, catheter type, catheter insertion site, catheter nificance at 5%. We performed the analyses using use, and type of microorganism. the statistical package R version 4.0.3 (The R Project for Statistical Computing, https://www.r-project. org) for Windows. Ethical Considerations Participation in the VINCat program was voluntary, and data confidentiality was guaranteed. This study was evaluated and approved by the Parc Taulí Hospi- tal Research Ethics Committee, Sabadell, Spain. Results Study Periods During 2007–2020, a total of 10,030 nosocomial epi- sodes of CRB were diagnosed. Data from the 2007– 2019 period have been analyzed and described pre- viously (25). In summary, during 2007–2019, a total of 9,290 episodes of CRB were diagnosed. The mean annual incidence was 0.2 episodes/103 patient-days, 73.7% of episodes occurred in non-ICU wards, 62.7% of episodes were related to central vascular catheters, 24.1% of episodes were related to peripheral venous catheters, and 13.3% of episodes were related to pe- ripherally inserted central venous catheters (25). The incidence rate of CRB decreased substantially over the 2007–2019 study period (IRR 0.94, 95% CI 0.93– 0.96), especially in ICU wards. CRB episodes caused by central vascular catheters fell markedly (IRR 0.90, 95% CI 0.89–0.92), whereas those associated with pe- ripherally inserted catheters increased. In 2020, a total of 774 CRB episodes were diag- nosed at the participating hospitals. We determined that the incidence rate was 0.29 episodes/103 patient- days (Figure 1). Of 774 episodes, 297 (40.1%) were ac- quired in conventional medical wards, 127 (17.2%) in Figure 2. Observed and predicted incidence rates of CRB and number of CRB cases stratified by hospital ward, catheter type, surgical wards, and 316 (42.7%) in ICUs. We found and catheter use during 2007–2020 in study of effects of the that the catheters most frequently implicated in CRB COVID-19 pandemic on incidence and epidemiology of CRB, were central venous catheters (412 cases, 55.7%), pe- Spain. We calculated the CRB incidence rate by dividing the total ripheral catheters (169 cases, 22.8%), and peripherally number of episodes of catheter-related bloodstream infections inserted central venous catheters (159 cases, 21.5%). by the total number of patient-days for each year from 2007 to 2020. We predicted incidence rates by using the negative binomial Catheters causing CRB were located in the arm/fore- regression model and compared the predicted rates with observed arm (323 cases, 43.6%), jugular (237 cases, 32.0%), rates for each year. A) CRB incidence per 1,000 patient-days, subclavian (116 cases, 15.7%), or femoral (52 cases, stratified by the type of hospital ward. B) CRB incidence per 7.03%) sites. The catheters were used for medication 1,000 patient-days, stratified by the type of catheter used. C) and serum infusion (583 cases, 78.8%), parenteral nu- CRB incidence per 1,000 patient-days was stratified according to the reason for catheter use. CRB, catheter-related bacteremia; trition (146 cases, 19.7%), or hemodialysis (11 cases, ICU, intensive care unit; CVC, central vascular catheter; PICVC, 1.5%). The most frequent causes of CRB were coagu- peripherally-inserted central vascular catheter; PVC, peripheral lase-negative staphylococci (299 cases, 41.3%), Staph- vascular catheter; PN, parenteral nutrition; HD, hemodialysis. ylococcus aureus (155 cases, 21.4%), gram-negative 2184 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 28, No. 11, November 2022 Effects of COVID-19 on Catheter-Related Bacteremia Figure 3. COVID-19–related hospital admissions and CRB incidence rates in 2020 in study of effects of the COVID-19 pandemic on incidence and epidemiology of CRB, Spain. We compared the incidence rates for COVID-19- related hospital admissions with rates for CRB each month during 2020. We calculated the COVID-19 incidence rates by dividing the total number of COVID-19 admissions by the total number of patient-days. We calculated CRB incidence rates by dividing the total number of episodes of catheter-related bloodstream infections by the total number of patient-days. CRB, catheter-related bacteremia. enterobacteria (112 cases, 15.5%), enterococci (72 cas- In conventional surgical and medical wards, we es, 9.9%), Candida sp. (45 cases, 6.2%), and Pseudomo- found that the predicted incidence rate for CRB was nas aeruginosa (34 cases, 4.7%). 0.12 episodes/103 patient-days, and the observed rate was 0.19/103 patient-days in 2020 (O/P 1.51, Comparison of Observed and Expected Incidence Rates 95% CI 1.37–1.65). However, in ICUs, we predicted According to the case mix index observed during the incidence rate was 0.48 episodes/103 patient- 2007–2019, we predicted that the incidence rate for days, but the observed rate was 1.62/103 patient- CRB in 2020 was 0.14 episodes/103 patient-days. days in 2020 (O/P 3.42, 95% CI 3.04–3.79). The However, we observed 0.29 episodes/103 patient- average RMSE was 0.013 for conventional wards days (observed/predicted [O/P] ratio 2.10, 95% and 0.069 for ICUs during 2007–2019, whereas, in CI 1.95–2.25) in 2020. The RMSE was 0.015 during 2020, the RMSE was 0.062 for conventional wards 2007–2019 and 0.153 in 2020 (Figure 1). Disparities and 1.147 for ICUs (Table 1; Figure 2). between predicted and observed rates were con- We observed an incidence rate of 0.064 for CRB sistent among the different participating hospitals caused by peripheral catheters in 2020; the predicted (Appendix Figure 1, https://wwwnc.cdc.gov/EID/ rate according to the negative binomial regression article/28/11/22-0547-App1.pdf). model was 0.05 (O/P 1.24, 95% CI 1.06–1.43). When Table 2. Temporal evolution of COVID-19–related hospital admissions and catheter-related bacteremia incidence rates in study of effects of the COVID-19 pandemic on incidence and epidemiology of catheter-related bacteremia, Spain, 2020 Conventional ward ICU Total* Rate of COVID-19 CRB incidence Rate of COVID-19 CRB incidence Rate of COVID-19 CRB incidence Month admissions† rate‡ admissions† rate‡ admissions† rate‡ January 14.11 0.12 15.15 1.39 14.15 0.13 February 16.12 0.15 21.78 2.86 16.36 0.20 March 52.81 0.13 76.14 3.29 54.87 0.40 April 41.30 0.20 83.44 5.55 43.95 0.57 May 17.02 0.22 31.33 4.49 17.6 0.34 June 15.56 0.21 21.37 2.81 15.8 0.29 July 19.50 0.17 32.94 2.83 20.15 0.29 August 22.10 0.24 38.41 5.73 22.96 0.44 September 23.06 0.18 46.00 3.43 24.15 0.28 October 34.20 0.14 70.45 3.20 36.33 0.30 November 31.87 0.20 68.22 4.09 33.93 0.36 December 33.73 0.29 68.43 7.11 34.94 0.44 *Total rates for conventional plus ICU wards. ICU, intensive care unit; CRB, catheter-related bacteremia. †Values are COVID-19 admission rates per 100,000 patient-days. ‡Values are episodes of CRB per 1,000 patient-days. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 28, No. 11, November 2022 2185 RESEARCH binomial regression model according to catheter use and causative microorganisms. For hemodialysis, the observed CRB rate was 0.004, and the predicted rate was 0.003 (O/P 1.25, 95% CI 0.51–1.99). For parenteral nutrition, the observed CRB rate was 0.06, and the pre- dicted rate was 0.03 (O/P 1.62, 95% CI 1.36–1.89). For other uses, the observed CRB rate was 0.22, and the predicted rate was 0.10 (O/P 2.14, 95% CI 1.97–2.31); the last category increased most notably (Table 1; Fig- ure 2). Observed CRB rates were increased compared with predicted rates for all causative microorganisms, especially enterococci (O/P 5.41, 95% CI 4.16–6.65). Relationship between Monthly CRB Incidence Rates and SARS-CoV-2 Admissions The total number of hospital admissions and the pro- portion of patients affected by COVID-19 changed substantially during 2020 (Figure 3). We recorded more COVID-19–related admissions during Febru- ary–June in both conventional wards and ICUs (Table 2; Figure 3). The peak rate of COVID-19 hospital ad- Figure 4. Association between COVID-19–related hospital admissions and CRB incidence rate in 2020 in study of effects missions was 54.87 in March, and the lowest rate was of the COVID-19 pandemic on incidence and epidemiology of 14.15 in January. CRB, Spain. We calculated COVID-19 incidence rates by dividing Concomitantly, CRB incidence rates also varied the total number of COVID-19 admissions by the total number of during 2020, reaching a peak in April (0.57 episodes patient-days and CRB incidence rates by dividing the total number of CRB/103 admissions), followed by August and of episodes of catheter-related bloodstream infections by the total number of patient-days. We used linear regression analysis to December (0.44 episodes of CRB/103 admissions for determine the relationship between COVID-19–related hospital each month) (Table 2). We observed the lowest CRB admissions and the incidence of CRB. We found a positive rate at the beginning of the year (0.13 episodes of association between the incidence of COVID-19–related hospital CRB/103 admissions). admissions and incidence rate of CRB (R2 = 0.45). CRB, catheter- We observed an association between CRB and related bacteremia. COVID-19 incidence rate. The CRB incidence rate was expected to increase by 1.07 (IRR 1.07, 95% CI 1–1.15) central catheters were used, the observed rate for for every 1,000 COVID-19 admissions if all factors re- CRB was 0.16, and the predicted rate was 0.06 (O/P mained constant (Figure 4). 2.54, 95% CI 2.29–2.78). When peripherally inserted central catheters were used, the observed rate for Discussion CRB was 0.06, and the predicted rate was 0.04 (O/P We demonstrated that the COVID-19 pandemic in- 1.73, 95% CI 1.46–2.00). We observed increases in creased CRB incidence in 2020 in our hospitals in Cat- RMSEs in 2020 compared with the 2007–2019 pe- alonia, Spain. We found that months with the highest riod for peripheral catheters (0.012 vs. 0.007), cen- proportion of COVID-19 admissions were strongly tral catheters (0.094 vs. 0.008), and peripherally associated with increased CRB incidence. We also inserted central catheters (0.025 vs. 0.004) (Table 1; described the most critical CRB characteristics that Figure 2). In addition, we determined that the num- changed during the pandemic in 2020. Compared ber of observed CRB episodes in 2020 were higher with previous years, we observed increased CRB in- than predicted episodes depending on the location cidence in both ICUs and conventional wards in 2020. of the catheter; increased incidence was more pro- Other studies conducted around the same time nounced in catheters located in femoral (O/P 3.11, observed increased HAI incidence rates during 2020, 95% CI 2.27–3.96), jugular (O/P 2.64, 95% CI 2.30– especially in ICUs. Catheter-associated urinary tract 2.97), and subclavian (O/P 1.88, 95% CI 1.53–2.22) infections, ventilator-associated pneumonia, and sites (Table 1; Appendix Figure 2). CRB were the HAIs with the greatest increases (9–11). In 2020, we found increases in observed CRB in- In contrast, other HAIs, such as nosocomial-acquired cidence rates compared with rates predicted by the C. difficile colitis (5,6) or surgical-site infections (7,8, 2186 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 28, No. 11, November 2022 Effects of COVID-19 on Catheter-Related Bacteremia decreased during the same period. Of note, HAIs may Additional members of the Catalan Infection Control and be more frequently associated with patients receiving Antimicrobial Stewardship Program: Alfredo Jover, Dolors steroids or tocilizumab (26), although a specific asso- Castellana (Hospital Universitari Arnau de Vilanova, ciation with BSI was not observed (27). Lleida, Spain); Montserrat Olona, Antonia García Pino In most cases, the increased rates of CRB were (Hospital Universitari Joan XXIII, Tarragona, Spain); Josep likely associated with a lower adherence to specific Rebull Fatsini, M France Domènech (Hospital Verge de la preventive measures during the months when the Cinta, Tortosa, Spain); Miquel Pujol, Ana Hornero pandemic caused the most hospital admissions, de- (Hospital Universitari de Bellvitge, L’Hospitalet de spite the generalized reinforcement of contact pre- Llobregat, Spain); Joaquín López-Contreras, Engracia cautions and hand hygiene to reduce SARS-CoV-2 Fernández (Hospital de la Santa Creu i Sant Pau. nosocomial transmission. Of note, in our hospital Barcelona, Spain); Xavier Salgado, Dolors Domènech settings, alcohol-based product consumption for (Hospital Universitari Doctor Josep Trueta. Girona. hand hygiene during 2020 increased 2.4-fold over- Spain); Ana Lérida, Lydia Martin (Hospital deViladecans, all and 1.9-fold in ICUs compared with the previous Viladecans, Spain); Nieves Sopena, Irma Casas Garcia year, and a similar trend was observed in a hospital (Hospital Universitari Germans Tries i Pujol. Badalona. in Taiwan (28). Therefore, although proper hand hy- Spain); Rafel Pérez, Encarna Maraver (Althaia Xarxa giene is necessary to prevent CRB and other HAIs, Asistencia, Manresa, Spain); Eva Palau, Pepi Serrats it is not sufficient to avoid HAIs if other measures (Clinica de Girona, Girona, Spain); José Antonio Martínez, are not performed during the insertion and care of Gemina Santana (Hospital Clínic i Provincial, Barcelona, vascular catheters. Specifically, since 2006, various Spain); Ana Martínez, Anna Martínez (Hospital de evidence-based bundles for CRB interventions have Campdevànol, Campdevànol, Spain); Lourdes Ferrer, been shown to reduce CRB, especially in the ICU M. José Moreno (Hospital Dos de Maig, Barcelona, Spain); setting. These bundles include handwashing, us- Esther Calbo, Carolina Porta (Hospital Mútua de Terrassa, ing full-barrier precautions, cleaning the skin with Terrassa, Spain); Alex Smithson (Hospital de l’Esperit Sant, chlorhexidine, avoiding the femoral site if possible, Barcelona, Spain); Maria de la Roca Toda, Teresa Aliu and removing unnecessary catheters (22,23). Among (Hospital de Palamos, Palamós, Spain); Susanna Camps, the different preventive measures, both hand hy- Montserrat Ortega (Corporació Sanitària Parc Taulí, giene and catheter insertion measures were associ- Sabadell, Spain); Vicens Diaz-Brito, Encarna Moreno ated with reduced incidence of CRB, and they were (Hospital Sant Joan de Déu, Sant Boi, Spain); Carme most effective when both measures were applied si- Agustí, Miquel Perea Garcia (Hospital de Sant Celoni, multaneously (24). Sant Celoni, Spain); Marta Andrés, Laura Grau Palafox The first limitation of our study is that hetero- (Hospital de Terrassa, Terrassa, Spain); Raquel Carrera, geneity of COVID-19 pandemic responses existed Anna Besolí (Consorci Hospitalari, Vic, Spain); Juan Pablo between hospitals, resulting in lack of data on ad- Horcajada, Cristina Gonzalez (Hospital del Mar/ herence to CRB preventive measures at each center. Esperança, Barcelona, Spain); Jordi Cuquet, Demelsa Maria Second, there was a lack of clinical information re- Maldonado López (Hospital General, Granollers, Spain); garding the presence of chronic diseases or clinical Rosa Benítez, Mirella Duch (Serveis Assistencials, conditions that might influence CRB incidence rates. Badalona, Spain); David Blancas, Esther Moreno However, the availability of a large number of CRB (Consorci Sanitari del Garraf, Vilanova, Spain); Naiara episodes diagnosed by standardized definitions is a Villalba, Sara Martínez (Hospital Sant Bernabé, Berga, strength that enables generalization of our observa- Spain); Àngels García Flores, Roser Ferrer (Hospital Sant tions. In addition, CRB incidence rates were adjusted Jaume, Calella, Spain); Josep Bisbe, Montse Blascó by patient-days rather than catheter-days, which en- (Hospital Sant Jaume, Olot, Spain); Antoni Castro Salom, abled surveillance of all types of catheters inserted in Ana Felisa López (Hospital Universitari Sant Joan, Reus, all hospital wards. Spain); Joan Espinach Alvarós, Àngels Perez (Hospital In 2020, substantial resources were allocated for Sant Joan de Deu, Martorell, Spain); David Castander, infection prevention to manage the SARS-CoV-2 out- Elisabet Calaf (Hospital Sant Pau i Santa Tecla, Tarragona, break, which also affected HAI prevention programs. Spain); Mercè Clarós (Hospital Sant Rafael, Barcelona, Because CRB is a key healthcare quality indicator Spain); Núria Bosch Ros (Hospital Sta. Caterina, Girona, (29), our observations stress the importance of main- Spain); Irene Montardit (Hospital Sta. Maria, Lleida, taining all prevention efforts, regardless of the coex- Spain); Roser Porta, Pilar De la Cruz Sol (Hospital istence of other challenges, such as the worldwide Universitari Quirón Dexeus, Barcelona, Spain); Mª Rosa COVID-19 pandemic. Coll Colell, Rosa García Penche Sanches (Hospital Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 28, No. 11, November 2022 2187 RESEARCH Universitari Sagrat Cor, Barcelona, Spain); Josep Maria References Tricas, Eva Redon (Fundació Privada Hopstital de 1. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features of patients infected with 2019 novel coronavirus in Mollet, Mollet, Spain); Montse Brugués (Consorci Sanitari Wuhan, China. Lancet. 2020;395:497–506. https://doi.org/ de l’Anoia, Igualada, Spain); Laura Linares, Maria Cusco 10.1016/S0140-6736(20)30183-5 (Hospital Comarcal de l’Alt Penedés, Vilafranca, Spain); 2. World Health Organization. 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Bhargava A, Riederer K, Sharma M, Fukushima EA, About the Author Johnson L, Saravolatz L. High rate of multidrug-resistant organisms (MDROs) among COVID-19 patients presenting Dr. Gasch is a clinician, associate of the Infectious Diseases with bacteremia upon hospital admission. Am J Infect Control. Service at the Corporació Sanitària Parc Taulí (Sabadell), 2021;49:1441–2. https://doi.org/10.1016/j.ajic. 2021.08.010 and a member of the infection control team of the 13. Zarb P, Coignard B, Griskeviciene J, Muller A, institution. He is an associate professor in the Faculty of Vankerckhoven V, Weist K, et al.; National Contact Points for the ECDC pilot point prevalence survey; Hospital Contact Medicine at Autonomous University of Barcelona, Spain, Points for the ECDC pilot point prevalence survey. The and his research interests are focused on the study of European Centre for Disease Prevention and Control (ECDC) bloodstream infections and infective endocarditis. pilot point prevalence survey of healthcare-associated 2188 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 28, No. 11, November 2022 Effects of COVID-19 on Catheter-Related Bacteremia infections and antimicrobial use. Euro Surveill. national multimodal intervention to prevent catheter-related 2012;17:20316. https://doi.org/10.2807/ese.17.46.20316-en bloodstream infection in the ICU: the Spanish experience. 14. Zingg W, Metsini A, Balmelli C, Neofytos D, Behnke M, Crit Care Med. 2013;41:2364–72. https://doi.org/10.1097/ Gardiol C, et al. National point prevalence survey on CCM.0b013e3182923622 healthcare-associated infections in acute care hospitals, 24. van der Kooi T, Sax H, Pittet D, van Dissel J, Switzerland, 2017. 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Council recommendation of 9 June Simonetti A, Coloma A, et al. Immunomodulatory therapy, 2009 on patient safety, including the prevention and risk factors and outcomes of hospital-acquired bloodstream control of healthcare associated infections [cited 2022 infection in patients with severe COVID-19 pneumonia: a Sep 21]. https://op.europa.eu/en/publication-detail/-/ Spanish case-control matched multicentre study publication/8ae80abf-31cd-4577-b0be-4f2fe108f6f9 (BACTCOVID). Clin Microbiol Infect. 2021;27:1685–92. 19. Centers for Disease Control and Prevention. National Health- https://doi.org/10.1016/j.cmi.2021.06.041 care Safety Network (NHSN) patient safety component 28. Lo SH, Lin CY, Hung CT, He JJ, Lu PL. The impact of manual. 2022 January [cited 2022 Sep 21]. https://www.cdc. universal face masking and enhanced hand hygiene gov/nhsn/pdfs/pscmanual/pcsmanual_current.pdf for COVID-19 disease prevention on the incidence of 20. Centers for Disease Control and Prevention. Current HAI hospital-acquired infections in a Taiwanese hospital. progress report. 2020 National and state healthcare-associ- Int J Infect Dis. 2021;104:15–8. https://doi.org/10.1016/ ated infections progress report [cited 2022 Sep 21]. https:// j.ijid.2020.12.072 www.cdc.gov/hai/data/portal/progress-report.html 29. World Health Organization. Global patient safety action 21. Catalan Health Service. VINCat program [cited 2022 Sep 21]. plan 2021–2030 [cited 2022 Sep 21]. https://www.who.int/ https://catsalut.gencat.cat/ca/proveidors-professionals/ teams/integrated-health-services/patient-safety/policy/ vincat global-patient-safety-action-plan 22. Pronovost P, Needham D, Berenholtz S, Sinopoli D, Chu H, Cosgrove S, et al. An intervention to decrease catheter- Address for correspondence: Oriol Gasch, Hospital Parc Taulí de related bloodstream infections in the ICU. N Engl J Med. Sabadell, Institut d’Investigació i Innovació Parc Taulí (IL3PT), 2006;355:2725–32. https://doi.org/10.1056/NEJMoa061115 23. Palomar M, Álvarez-Lerma F, Riera A, Díaz MT, Torres F, Universitat Autònoma de Barcelona, 08208 Sabadell, Spain; Agra Y, et al.; Bacteremia Zero Working Group. Impact of a email: ogasch@tauli.cat Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 28, No. 11, November 2022 2189