Abstract
Background
COVID-19 is believed to increase the risk of secondary health care–associated infections. The objective was to estimate the impact of COVID-l9 pandemic on the rates of central line–associated bloodstream infection (CLABSI) and catheter-associated urinary tract infections (CAUTIs) in the Ministry of Health hospitals across Saudi Arabia.
Methods
A retrospective analysis of prospectively collected CLABSI and CAUTI data over a period of 3 years (2019-2021) was done. The data were obtained from the Saudi Health Electronic Surveillance Network. All adult intensive care units in 78 Ministry of Health hospitals that contributed CLABSI or CAUTI data before (2019) and during (2020-2021) the pandemic were included.
Results
During the study, 1440 CLABSI events and 1119 CAUTI events were identified. CLABSI rates significantly increased in 2020-2021 compared with 2019 (2.50 versus 2.16 per 1000 central line days, P = .010). CAUTI rates significantly decreased in 2020-2021 compared with 2019 (0.96 versus 1.54 per 1000 urinary catheter days, P < .001).
Conclusions
COVID-19 pandemic is associated with increased CLABSI rates and reduced CAUTI rates. It is believed to have negative impacts on several infection control practices and surveillance accuracy. The opposite impacts of COVID-19 on CLABSI and CAUTI probably reflect the nature of their case definitions.
Key Words: Health care–associated infections, Urinary catheter, Infection control, Surveillance, Saudi Arabia, Intensive care unit
Background
Health care–associated infections (HAIs) are a major health care challenge due to their negative impact on patient outcomes and additional pressure on health care resources.1, 2, 3 For example, intensive care unit (ICU) patients with central line–associated bloodstream infection (CLABSI) have between 5% and 30% excess mortality and on average 2 weeks of extra length of stay.2, 3 Similarly, ICU patients with catheter-associated urinary tract infections (CAUTIs) have between 1% and 13% excess mortality and on average 2 weeks of extra length of stay.2, 3
COVID-19 pandemic has tremendously affected all components of the health care system, including reduced utilization of health care services.4 Although COVID-19 pandemic raised the public and professional attention to infection control,5 it had a negative impact on some infection control activities, such as surveillance and antimicrobial stewardship activities.6, 7, 8 Additionally, COVID-19 patients experienced a higher risk of secondary bacterial infections and HAIs due to prolonged illness, prolonged hospital stay, use of immunosuppressive medication, and increased device utilization.9, 10 Despite the strict implementation of infection control practices in most health care settings, some types of HAIs continued to rise in these facilities.11 This was especially important in HAIs caused by resistant bacteria.12
A number of studies compared the rates of CLABSI and CAUTI before and during the COVID-19 pandemic. The majority of these studies showed a significant increase in CLABSI rates13, 14, 15, 16 and nonsignificant decrease in CAUTI rates.13, 15 Other studies did not find a significant impact of the pandemic on the rates of device-associated HAIs.17, 18 There is a lack of national data determining the impact of COVID-19 pandemic on the HAI rates in Saudi Arabia and the Middle East. The objective of the current study was to estimate the impact of COVID-l9 pandemic on CLABSI and CAUTI rates in adult ICUs of Ministry of Health (MOH) hospitals across Saudi Arabia.
Methods
Setting
The study was conducted in the adult critical care units of MOH hospitals. MOH financially funds and administratively controls 284 hospitals with a total bed capacity of more than 43,000 beds. The rate of hospital beds in Saudi Arabia was 22.5 beds per 10,000 population at the start of the study.
Population
For the study, we obtained the data from the Saudi Health Electronic Surveillance Network (HESN) of MOH. For the sake of standardization and as per MOH policy, hospitals with more than 100 beds that have at least a critical care unit, and a microbiology laboratory with a full-time microbiologist were eligible to submit surveillance data to HESN. Therefore, 78 MOH hospitals that were submitting CALBSI and/or CAUTI data from adult ICUs to HESN during the study duration were included in the study. These hospitals were distributed in 20 regions of the Kingdom of Saudi Arabia. Hospitals that were not submitting surveillance data to HESN were not included. Hospitals that were submitting only pediatric and/or neonatal data were excluded (28 hospitals).
Design
A retrospective analysis of prospectively collected CLABSI and CAUTI data over a period of 3 years was done. The data were divided into 2 periods: before the start of the pandemic (2019) and during COVID-19 pandemic (2020 and 2021). This study includes all types of ICUs that conducted CLABSI and/or CAUTI surveillance before and during the pandemic. The outcomes studied were the numbers and rates of CLABSI and CAUTI.
Methods
The surveillance methodology was similar to the methods suggested by the US National Healthcare Safety Network (NHSN)19 and the Gulf Cooperation Council Center for Infection Control.20 The surveillance was an active, patient-based, prospective targeted surveillance that was done in specific ICUs for specific durations after a local infection risk assessment.
Data collection methods
The data were obtained from HESN, which is an integrated national electronic surveillance system that has several domains to uniformly monitor communicable diseases, disease epidemics, immunization, and HAIs across Saudi Arabia.21 It allows users at different hospitals to continually and uniformly report HAIs to the General Directorate of Infection Prevention and Control at Riyadh, Saudi Arabia. Infection preventionists collected the data on HAIs occurring in all patients admitted to the adult ICUs. The corresponding denominator data, consisting of specific patient days and device days, were collected and validated. The number of patients with a central line and/or urinary catheter inserted for any duration at the time of daily counting was considered central line days or urinary catheter days, respectively.
Statistical analysis
CLABSI rates (expressed per 1000 central line days) and CAUTI rates (expressed per 1000 urinary catheter days) were calculated for different types of ICUs by dividing the number of events by the device days of the same year and location. CLABSI and CAUTI rates were compared between 2020 and 2021 (individually and combined) and 2019 using the Z-test for event-time data. Additionally, standardized infection ratios (SIRs) and their 95% confidence intervals were calculated for each year separately after adjusting for differences in ICU types between the Saudi HESN and the US NHSN. SIRs were calculated by dividing the number of observed CLABSI or CAUTI events by their expected values.19 The expected values for CLABSI and CAUTI events were calculated using the published reports of NHSN.22 Additionally, the impacts of COVID-19 pandemic on CALBSI and CAUTI rates in large benchmarking datasets were graphically presented (Fig. 2). P values were two-tailed. P value<.05 was considered as significant. SPSS software (release 25.0, IBM Corp) was used for all statistical analyses.
Fig. 2.
Impact of COVID-19 on central line–associated bloodstream infection (CLABSI) and catheter-associated urinary tract infection (CAUTI) rates in the main benchmarking reports. Note: Benchmarking reports included reports published by the US National Healthcare Safety Network (NHSN), the International Nosocomial Infection Control Consortium (INICC) of developing countries, German National Reference Center for Surveillance of Nosocomial Infections (KISS), and Brazilian hospitals.
Results
During the 3 years of surveillance covering 601,079 central line days, a total of 1440 CLABSI events were identified: 395 in 2019, 522 in 2020, and 523 in 2021. As shown in Table 1, the overall CLABSI rates per 1000 central line days were 2.16 in 2019, 2.75 in 2020, and 2.29 in 2021. During the 3 years of surveillance covering 980,186 urinary catheter days, a total of 1119 CAUTI events were identified: 470 in 2019, 332 in 2020, and 317 in 2021. As shown in Table 2, the overall CAUTI rates per 1000 urinary catheter days were 1.54 in 2019, 1.07 in 2020, and 0.87 in 2021.
Table 1.
Rates of central line–associated bloodstream infection for different types of intensive care units between 2019 and 2021
| 2019 |
2020 |
2021 |
|||||||
|---|---|---|---|---|---|---|---|---|---|
| CL days | Events | Rate | CL days | Events | Rate | CL days | Events | Rate | |
| Burn | 1097 | 4 | 3.65 | 2054 | 5 | 2.43 | 1523 | 6 | 3.94 |
| Medical | 20,013 | 67 | 3.35 | 18,720 | 63 | 3.37 | 22,138 | 60 | 2.71 |
| Medical cardiac | 6663 | 15 | 2.25 | 7248 | 17 | 2.35 | 7439 | 13 | 1.75 |
| Medical surgical | 138,756 | 281 | 2.03 | 147,835 | 417 | 2.82 | 179,100 | 416 | 2.32 |
| Neurological | 30 | 0 | 0.00 | 169 | 0 | 0.00 | 365 | 0 | 0.00 |
| Neurosurgical | 2293 | 1 | 0.44 | 848 | 1 | 1.18 | 1245 | 2 | 1.61 |
| Respiratory | 1562 | 0 | 0.00 | 3107 | 17 | 5.47 | 3625 | 21 | 5.79 |
| Surgical | 2259 | 0 | 0.00 | 2542 | 0 | 0.00 | 3050 | 0 | 0.00 |
| Surgical cardiothoracic | 4304 | 6 | 1.39 | 3772 | 0 | 0.00 | 5129 | 5 | 0.97 |
| Trauma | 5894 | 21 | 3.56 | 3732 | 2 | 0.54 | 4567 | 0 | 0.00 |
| Total | 182,871 | 395 | 2.16 | 190,027 | 522 | 2.75 | 228,181 | 523 | 2.29 |
| 95% Confidence | 1.96-2.38 | 2.52-2.99 | 2.10-2.50 | ||||||
CL, central line.
Table 2.
Rates of catheter-associated urinary tract infections for different types of intensive care units between 2019 and 2021
| 2019 |
2020 |
2021 |
|||||||
|---|---|---|---|---|---|---|---|---|---|
| UC days | Events | Rate | UC days | Events | Rate | UC days | Events | Rate | |
| Burn | 1782 | 3 | 1.68 | 2706 | 2 | 0.74 | 2669 | 2 | 0.75 |
| Medical | 35,549 | 77 | 2.17 | 31,459 | 26 | 0.83 | 36,734 | 23 | 0.63 |
| Medical cardiac | 11,038 | 11 | 1.00 | 11,613 | 12 | 1.03 | 11,503 | 9 | 0.78 |
| Medical surgical | 234,752 | 346 | 1.47 | 244,898 | 284 | 1.16 | 289,506 | 267 | 0.92 |
| Neurological | 131 | 0 | 0.00 | 139 | 1 | 7.19 | 2 | 0 | 0.00 |
| Neurosurgical | 3470 | 5 | 1.44 | 1182 | 0 | 0.00 | 2421 | 1 | 0.41 |
| Respiratory | 2204 | 0 | 0.00 | 4736 | 5 | 1.06 | 5986 | 8 | 1.34 |
| Surgical | 3703 | 0 | 0.00 | 4177 | 0 | 0.00 | 4518 | 0 | 0.00 |
| Surgical cardiothoracic | 3908 | 2 | 0.51 | 3418 | 0 | 0.00 | 4473 | 1 | 0.22 |
| Trauma | 9089 | 26 | 2.86 | 5409 | 2 | 0.37 | 7011 | 6 | 0.86 |
| Total | 305,626 | 470 | 1.54 | 309,737 | 332 | 1.07 | 364,823 | 317 | 0.87 |
| 95% Confidence | 1.40-1.68 | 0.96-1.19 | 0.78-0.97 | ||||||
UC, urinary catheter.
As shown in Figure 1, the rates of CLABSI increased during the pandemic. Compared with the 2019 CLABSI rate (2.16 per 1000 central line days), the 2020 and 2021 rates increased (2.75 and 2.29 per 1000 central line days, respectively). The difference was significant in 2020 (P < .001) but not 2021 (P = .316). The same finding was observed using the 95% confidence intervals. The combined 2020-2021 CLABSI rate was significantly higher than the 2019 rate (2.50 versus 2.16 per 1000 central line days, P = .010). The rates of CAUTI decreased during the pandemic. Compared with the 2019 CAUTI rate (1.54 per 1000 urinary catheter days), the rates for 2020, 2021, and combined 2020-2021 were significantly lower (1.07, 0.87, and 0.96 per 1000 urinary catheter days, respectively, P < .001 for each). The same finding was observed using the 95% confidence intervals.
Fig. 1.
Rates of central line–associated bloodstream infection (CLABSI) and catheter-associated urinary tract infections (CAUTI) in all types of intensive care units between 2019 and 2021. Note: The P value of the Z-test was the testing rate difference relative to 2009.
Table 3 shows the yearly SIRs of CLABSI and CAUTI. During the 3 years of the study, the CLABSI SIRs in HESN were 2.3-2.9 times higher as compared with NHSN while the CAUTI SIRs in HESN were 23%-56% lower as compared with NHSN. Similar to the crude CLABSI rates shown above, the CLABSI SIRs were higher in 2020, 2021, and combined 2020-2021 compared with 2019 (3.16, 2.67, and 2.82, respectively, versus 2.52). As shown in the confidence intervals, the increased CLABSI SIRs were significant (no overlap of confidence intervals) only in 2020. Similar to the crude CAUTI rates shown above, the CAUTI SIRs were lower in 2020, 2021, and combined 2020-2021 compared with 2019 (0.61, 0.50, and 0.53, respectively, versus 0.84). As shown in the confidence intervals, the reduced CAUTI SIRs were significant in 2020, 2021, and combined 2020-2021. Overall, the pandemic SIRs of CLABSI increased by 16% while the pandemic SIRs of CAUTI decreased by 36% after adjusting for the type of ICU relative to NHSN.
Table 3.
Standardized infection ratios (SIRs)* of central line–associated bloodstream infection (CLABSI) and catheter-associated urinary tract infections (CAUTI) between 2019 and 2021
| Observed events | Expected events | SIR | 95% LCI | 95% UCI | |
|---|---|---|---|---|---|
| CLABSI | |||||
| 2019 | 395 | 173.1 | 2.28 | 2.07 | 2.52 |
| 2020 | 522 | 179.9 | 2.90 | 2.66 | 3.16 |
| 2021 | 523 | 213.8 | 2.45 | 2.25 | 2.67 |
| 2020-2021 | 1045 | 393.7 | 2.65 | 2.50 | 2.82 |
| CAUTI | |||||
| 2019 | 470 | 614.3 | 0.77 | 0.70 | 0.84 |
| 2020 | 332 | 604.2 | 0.55 | 0.49 | 0.61 |
| 2021 | 317 | 713.2 | 0.44 | 0.40 | 0.50 |
| 2020-2021 | 649 | 1317.4 | 0.49 | 0.46 | 0.53 |
LCI, lower confidence interval; UCI, upper confidence interval.
Adjusted for the difference in the type of intensive care unit between the Saudi Health Electronic Surveillance Network and the US National Healthcare Safety Network.
Figure 2 shows the impact of COVID-19 on CLABSI and CAUTI rates in the main benchmarking reports.13, 14, 15, 16, 18 CLABSI rates increased during the pandemic in the studies of the International Nosocomial Infection Control Consortium of developing countries, the US NHSN, and Brazilian hospitals. The CLABSI increase was much higher in INICC (86%) and Brazilian hospitals (76%) than in NHSN hospitals (37% and 51%). CAUTI rates decreased during the pandemic in the International Nosocomial Infection Control Consortium and German National Reference Center for Surveillance of Nosocomial Infections hospitals (−6% to −13%), while the results were mixed in the NHSN hospitals (−10% and 9%).
Discussion
We report the impact of COVID-19 pandemic on CLABSI and CAUTI surveillance rates during the first 2 years of the pandemic in 78 MOH hospitals in Saudi Arabia. As far as we know, these national data are considered the first to examine such a topic in Saudi Arabia and the Middle East. The current findings showed that CLABSI rates were significantly increased by approximately 16% in 2020-2021 compared with the 2019 rates, before and after adjusting for the type of ICU. The current findings were consistent with previous studies done in multihospital systems.13, 14, 15, 16 For example, the increase in CLABSI rates in 2020/2021 compared with 2019 was 37%-51% in>3400 NHSN hospitals in the United States,13, 14 86% in 7 hospitals in 7 INNIC developing countries,15 and 76% in 21 Brazilian hospitals.16 With the exception of German hospitals,18 studies that failed to detect such increase in CLABSI rates were single-center studies, such as those done in Tunisia23 and Saudi Arabia.17
Several possible explanations have been reported in relation to the increase of CLABSI rates, including reduction of catheter care during insertion and maintenance by overwhelmed staff.6, 8, 24 For example, infection control staff experienced up to 500% increase in the number of infection control consultations during the pandemic, which primarily focused on COVID-19 isolations and exposures with marked reduction in the time allocated for surveillance or central line care.6, 8 Additionally, to meet the increasing care demands, quickly trained nurses were deployed to assist in the ICU care of COVID-19 patients.25 Moreover, the excess use of immunosuppressive drugs such as tocilizumab and steroids among patients with COVID-19 increased their susceptibility to infection including CLABSI.9, 26 Furthermore, as COVID-19 pandemic changed hospital admission policies with limited access to less severe cases, the increase of CLABSI rates could be due to the decrease in the denominator, which is primarily composed of patients with lower CLABSI risk.27 Furthermore, the preference of using the more-risky femoral catheter may have increased due to the fear of catheter insertion close to the mouth and respiratory secretions of the patients.27 Finally, COVID-19 patients may have had higher central line utilization due to the increased risk of acute renal injury that required dialysis and a prolonged ICU stay.27 Interestingly, the increasing impact of the pandemic on the CLABSI rates in the current study was higher in the first compared with the second year, which probably reflects the actual burden of the pandemic on an unprepared health care system in the first year.
The current finding showed that CAUTI rates were significantly decreased by approximately 37% in 2020-2021 compared with the 2019 rates unlike CLABSI. Similar to the current findings but to a less extent, COVID-19 pandemic was associated with 6%-13% reduction in CAUTI rates in multicentered studies in the United States, Germany, and 7 developing countries.13, 15, 18 On the other hand, some studies reported no change17, 23 or even an increase28 in CAUTI during the COVID-19 pandemic. Interestingly, the increase and decrease in these studies did not reach statistical significance. The decrease in CAUTI rates observed in the current study may be explained by several reasons. For example, several hospitals limited surgical and elective admissions during the first year of the pandemic, which may have reduced the number of CAUTI-susceptible patients.13 As COVID-19 patients are more susceptible to develop secondary infections, they were prescribed more antibiotics, which may have masked the required CAUTI threshold for bacteriuria.13, 29 Additionally, the rate of urine culture may have been reduced to minimize the exposure to COVID-19 patients.13 Interestingly, the opposite impacts of COVID-19 on CLABSI and CAUTI probably reflect the nature of their case definitions. Unlike CLABSI, developing CAUTI is dependent on culturing practices and the level of preexisting bacteriuria rather than catheter maintenance.13, 30
Our study has several strengths and some limitations. The main strength is the fact that we used standardized national data obtained from different ICUs in 78 MOH hospitals covering all the 20 regions of Saudi Arabia over a period of 3 years. We presented the results using both rates and SIR. However, because of using standardized surveillance data collection tools, there was a lack of data to adjust the finding for disease severity and other risk factors of HAIs. Using a retrospective design, causal relationship cannot be confirmed. Nevertheless, these limitations are inherent in surveillance design and unlikely to significantly impact the current study findings.
Conclusions
In conclusion, we report increased CLABSI rates and reduced CAUTI rates during the first 2 years of the COVID-19 pandemic as compared with the prepandemic year. COVID-19 pandemic is believed to have negative impacts on several infection control practices and surveillance accuracy. The opposite impacts of COVID-19 on CLABSI and CAUTI probably reflect the nature of their case definitions. Unlike CLABSI, developing CAUTI is dependent on culturing practices and the level of preexisting bacteriuria rather than catheter maintenance. These national data are thought to be the first to elaborate on such a topic in Saudi Arabia and the Middle East.
Acknowledgments
The authors would like to thank the General Directorate of Infection Prevention and Control, Infection Control Practitioners, Regional Coordinators, and Health Electronic Surveillance Network Team at Ministry of Health, Riyadh, Kingdom of Saudi Arabia.
Footnotes
Conflicts of interest: There is no coflict of interest from all authors.
Ethics approval: The study obtained all required approvals from the Institutional Review Board of King Fahad Medical City, Riyadh.
References
- 1.Zimlichman E., Henderson D., Tamir O., et al. Health care-associated infections: a meta-analysis of costs and financial impact on the US health care system. JAMA Intern Med. 2013;173:2039–2046. doi: 10.1001/jamainternmed.2013.9763. [DOI] [PubMed] [Google Scholar]
- 2.Rosenthal V.D., Duszynska W., Ider B.E., et al. International Nosocomial Infection Control Consortium (INICC) report, data summary of 45 countries for 2013-2018, Adult and Pediatric Units, Device-associated Module. Am J Infect Control. 2021;49:1267–1274. doi: 10.1016/j.ajic.2021.04.077. [DOI] [PubMed] [Google Scholar]
- 3.European Centre for Disease Prevention and Control. Incidence and attributable mortality of healthcare-associated infections in intensive care units in Europe, 2008–2012. ECDC; 2018. Accessed December 1, 2022. 〈https://www.ecdc.europa.eu/sites/default/files/documents/surveillance-report-HAI-Net-ICU-mortality-2008-2012.pdf〉.
- 4.Moynihan R., Sanders S., Michaleff Z.A., et al. Impact of COVID-19 pandemic on utilisation of healthcare services: a systematic review. BMJ Open. 2021;11 doi: 10.1136/bmjopen-2020-045343. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Shbaklo N., Lupia T., De Rosa F.G., Corcione S. Infection control in the era of COVID-19: a narrative review. Antibiotics. 2021;10(10):1244. doi: 10.3390/antibiotics10101244. PMID: 34680824; PMCID: PMC8532716. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Alsuhaibani M., Kobayashi T., McPherson C., et al. Impact of COVID-19 on an infection prevention and control program, Iowa 2020-2021. Am J Infect Control. 2022;50:277–282. doi: 10.1016/j.ajic.2021.11.015. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Tomczyk S., Taylor A., Brown A., et al. Impact of the COVID-19 pandemic on the surveillance, prevention and control of antimicrobial resistance: a global survey. J Antimicrob Chemother. 2021;76:3045–3058. doi: 10.1093/jac/dkab300. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Abelenda-Alonso G., Puig-Asensio M., Jiménez-Martínez E., et al. Impact of the coronavirus disease 2019 (COVID-19) pandemic on infection control practices in a university hospital. Infect Control Hosp Epidemiol. 2023;44(1):135–138. doi: 10.1017/ice.2022.118. Epub 2022 May 20. PMID: 35591775; PMCID: PMC9273732. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Kumar G., Adams A., Hererra M., et al. Predictors and outcomes of healthcare-associated infections in COVID-19 patients. Int J Infect Dis. 2021;104:287–292. doi: 10.1016/j.ijid.2020.11.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.de Macedo V., Santos G.S., Silva R.N., et al. Healthcare-associated infections: a threat to the survival of patients with COVID-19 in intensive care units. J Hosp Infect. 2022;126:109–115. doi: 10.1016/j.jhin.2022.05.013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Baker M.A., Sands K.E., Huang S.S., et al. The impact of coronavirus disease 2019 (COVID-19) on healthcare-associated infections. Clin Infect Dis. 2022;74:1748–1754. doi: 10.1093/cid/ciab688. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Gaspar G.G., Ferreira L.R., Feliciano C.S., et al. Pre- and post-COVID-19 evaluation of antimicrobial susceptibility for healthcare-associated infections in the intensive care unit of a tertiary hospital. Rev Soc Bras Med Trop. 2021;54 doi: 10.1590/0037-8682-0090-2021. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Fakih M.G., Bufalino A., Sturm L., et al. Coronavirus disease 2019 (COVID-19) pandemic, central-line–associated bloodstream infection (CLABSI), and catheter-associated urinary tract infection (CAUTI): the urgent need to refocus on hardwiring prevention efforts. Infect Control Hosp Epidemiol. 2022;43:26–31. doi: 10.1017/ice.2021.70. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Lastinger L.M., Alvarez C.R., Kofman A., et al. Continued increases in the incidence of healthcare-associated infection (HAI) during the second year of the coronavirus disease 2019 (COVID-19) pandemic. Infect Control Hosp Epidemiol. 2022:1–5. doi: 10.1017/ice.2022.116. Epub ahead of print. PMID: 35591782; PMCID: PMC9237489. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Rosenthal V.D., Myatra S.N., Divatia J.V., et al. The impact of COVID-19 on health care associated infections in intensive care units in low- and middle-income countries: International Nosocomial Infection Control Consortium (INICC) findings. Int J Infect Dis. 2022;118:83–88. doi: 10.1016/j.ijid.2022.02.041. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Porto A.P.M., Borges I.C., Buss L., et al. Healthcare-associated infections on the intensive care unit in 21 Brazilian hospitals during the early months of the coronavirus disease 2019 (COVID-19) pandemic: an ecological study. Infect Control Hosp Epidemiol. 2022;44(2):284–290. doi: 10.1017/ice.2022.65. Epub 2022 Mar 18. PMID: 35300742; PMCID: PMC8987658. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.AlAhdal A.M., Alsada S.A., Alrashed H.A., Al Bazroun L.I., Alshoaibi A. Impact of the COVID-19 pandemic on levels of device-associated infections and hand hygiene compliance. Cureus. 2022;14 doi: 10.7759/cureus.24254. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Geffers C., Schwab F., Behnke M., Gastmeier P. No increase of device associated infections in German intensive care units during the start of the COVID-19 pandemic in 2020. Antimicrob Resist Infect Control. 2022;11 doi: 10.1186/s13756-022-01108-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.National Healthcare Safety Network (NHSN). NHSN Patient Safety Component Manual. Januray 2018. Accesed January 1, 2021.
- 20.GCC Centre for Infection Control and Ministry of National Guard Health Affairs. Healthcare-associated Infections surveillance manual, 3rd edition; 2018. Accessed January 1, 2021.
- 21.Saudi Ministry of Health (MOH). Health Electronic Surveillance Network. 2020. Accessed September 1, 2020.
- 22.Dudeck M.A., Edwards J.R., Allen-Bridson K., et al. National Healthcare Safety Network report, data summary for 2013, Device-associated Module. Am J Infect Control. 2015;43:206–221. doi: 10.1016/j.ajic.2014.11.014. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Ghali H., Ben Cheikh A., Bhiri S., Khefacha S., Latiri H.S., Ben Rejeb M. Trends of healthcare-associated infections in a Tuinisian University Hospital and impact of COVID-19 pandemic. Inquiry. 2021;58 doi: 10.1177/00469580211067930. 469580211067930. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.LeRose J., Sandhu A., Polistico J., et al. The impact of coronavirus disease 2019 (COVID-19) response on central-line–associated bloodstream infections and blood culture contamination rates at a tertiary-care center in the Greater Detroit area. Infect Control Hosp Epidemiol. 2021;42:997–1000. doi: 10.1017/ice.2020.1335. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Tashkandi N., Aljuaid M., McKerry T., et al. Nursing strategic pillars to enhance nursing preparedness and response to COVID-19 pandemic at a tertiary care hospital in Saudi Arabia. J Infect Public Health. 2021;14:1155–1160. doi: 10.1016/j.jiph.2021.06.016. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Aldawood F., El-Saed A., Zunitan M.A., Alshamrani M. Central line-associated blood stream infection during COVID-19 pandemic. J Infect Public Health. 2021;14:668–669. doi: 10.1016/j.jiph.2021.01.017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.McMullen K.M., Smith B.A., Rebmann T. Impact of SARS-CoV-2 on hospital acquired infection rates in the United States: predictions and early results. Am J Infect Control. 2020;48:1409–1411. doi: 10.1016/j.ajic.2020.06.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Su C., Zhang Z., Zhao X., et al. Changes in prevalence of nosocomial infection pre- and post-COVID-19 pandemic from a tertiary hospital in China. BMC Infect Dis. 2021;21:693. doi: 10.1186/s12879-021-06396-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Fukushige M., Ngo N.H., Lukmanto D., Fukuda S., Ohneda O. Effect of the COVID-19 pandemic on antibiotic consumption: a systematic review comparing 2019 and 2020 data. Front Public Health. 2022;10 doi: 10.3389/fpubh.2022.946077. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Fakih M.G., Advani S.D., Vaughn V.M. Diagnosis of urinary tract infections: need for a reflective rather than reflexive approach. Infect Control Hosp Epidemiol. 2019;40:834–835. doi: 10.1017/ice.2019.98. [DOI] [PubMed] [Google Scholar]


