Central Line Associated Bloodstream Infections in Critical Ill Patients during and before the COVID-19 Pandemic
Abstract
:1. Introduction
2. Materials and Methods
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Tabah, A.; Koulenti, D.; Laupland, K.; Misset, B.; Valles, J.; Bruzzi de Carvalho, F.; Paiva, J.A.; Cakar, N.; Ma, X.; Eggimann, P.; et al. Characteristics and determinants of outcome of hospital-acquired bloodstream infections in intensive care units: The EUROBACT International Cohort Study. Intensive Care Med. 2012, 38, 1930–1945. [Google Scholar] [CrossRef]
- Haddadin, Y.; Annamaraju, A.; Regunath, H. Central Line Associated Blood Stream Infections; StatPearls: St. Petersburg, FL, USA, 2022. [Google Scholar]
- Mohapatra, S.; Kapil, A.; Suri, A.; Pandia, M.P.; Bhatia, R.; Borkar, S.; Dube, S.K.; Jagdevan, A.; George, S.; Varghese, B.; et al. Impact of Continuous Education and Training in Reduction of Central Line-associated Bloodstream Infection in Neurointensive Care Unit. Indian J. Crit. Care Med. 2020, 24, 414–417. [Google Scholar] [CrossRef] [PubMed]
- Marschall, J.; Mermel, L.A.; Fakih, M.; Hadaway, L.; Kallen, A.; O’Grady, N.P.; Pettis, A.M.; Rupp, M.E.; Sandora, T.; Maragakis, L.L.; et al. Society for Healthcare Epidemiology of America. Strategies to prevent central line-associated bloodstream infections in acute care hospitals: 2014 update. Infect. Control Hosp. Epidemiol. 2014, 35, 753–771. [Google Scholar] [CrossRef]
- Weiner-Lastinger, L.M.; Pattabiraman, V.; Konnor, R.Y.; Patel, P.R.; Wong, E.; Xu, S.Y.; Smith, B.; Edwards, J.R.; Dudeck, M.A. The impact of coronavirus disease 2019 (COVID-19) on healthcare-associated infections in 2020: A summary of data reported to the National Healthcare Safety Network. Infect. Control Hosp. Epidemiol. 2022, 43, 12–25. [Google Scholar] [CrossRef] [PubMed]
- Rosenthal, V.D.; Duenas, L.; Sobreyra-Oropeza, M.; Ammar, K.; Navoa-Ng, J.A.; de Casares, A.C.; Machuca, L.; Ben-Jaballah, N.; Hamdi, A.; Villanueva, V.D.; et al. Findings of the International Nosocomial Infection Control Consortium (INICC), part III: Effectiveness of a multidimensional infection control approach to reduce central line-associated bloodstream infections in the neonatal intensive care units of 4 developing countries. Infect. Control Hosp. Epidemiol. 2013, 34, 229–237. [Google Scholar] [CrossRef] [PubMed]
- Lupia, T.; Scabini, S.; Pinna, S.M.; Di Perri, G.; De Rosa, F.G.; Corcione, S. 2019 novel coronavirus (2019-nCoV) outbreak: A new challenge. J. Glob. Antimicrob. Resist. 2020, 21, 22–27. [Google Scholar] [CrossRef]
- Petrilli, C.M.; Jones, S.A.; Yang, J.; Rajagopalan, H.; O’Donnell, L.; Chernyak, Y.; Tobin, K.A.; Cerfolio, R.J.; Francois, F.; Horwitz, L.I. Factors associated with hospital admission and critical illness among 5279 people with coronavirus disease 2019 in New York City: Prospective cohort study. BMJ 2020, 369, m1966. [Google Scholar] [CrossRef]
- Lansbury, L.; Lim, B.; Baskaran, V.; Lim, W.S. Co-infections in people with COVID-19: A systematic review and meta-analysis. J. Infect. 2020, 81, 266–275. [Google Scholar] [CrossRef]
- Chertow, D.S.; Memoli, M.J. Bacterial coinfection in influenza: A grand rounds review. JAMA 2013, 16, 275–282. [Google Scholar] [CrossRef]
- Stevens, M.P.; Doll, M.; Pryor, R.; Godbout, E.; Cooper, K.; Bearman, G. Impact of COVID-19 on traditional healthcare-associated infection prevention efforts. Infect. Control Hosp. Epidemiol. 2020, 41, 946–947. [Google Scholar] [CrossRef]
- Alsaffar, M.J.; Alsheddi, F.M.; Humayun, T.; Aldalbehi, F.Z.; Alshammari, W.H.S.; Aldecoa, Y.S.; Burhan, N.M.; El-Saed, A.; Tawfeeq, S.; Alanazi, K.H. Impact of COVID-19 pandemic on the rates of central line-associated bloodstream infection and catheter-associated urinary tract infection in an intensive care setting: National experience. Am. J. Infect. Control. 2023; 5, in press. [Google Scholar] [CrossRef]
- Fakih, M.G.; Bufalino, A.; Sturm, L.; Huang, R.H.; Ottenbacher, A.; Saake, K.; Winegar, A.; Fogel, R.; Cacchione, J. 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. [Google Scholar] [CrossRef] [PubMed]
- Pasquini, Z.; Barocci, J.; Brescini, L.; Candelaresi, B.; Castelletti, S.; Iencinellaa, V.; Mazzanti, S.; Procaccini, G.; Orsetti, E.; Pallottaa, F.; et al. Bloodstream infections in the COVID-19 era: Results from an Italian multi-centre study. Int. J. Infect. Dis. 2021, 111, 31–36. [Google Scholar] [CrossRef]
- 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, e24254. [Google Scholar] [CrossRef] [PubMed]
- 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, 7, 67. [Google Scholar] [CrossRef] [PubMed]
- Zand, F.; Vakili, H.; Asmarian, N.; Masjedi, M.; Sabetian, G.; Nikandish, R.; Shafiee, E.; Esfehani, A.T.; Azadi, F.; Dashti, A.S. Unintended impact of COVID-19 pandemic on the rate of catheter related nosocomial infections and incidence of multiple drug resistance pathogens in three intensive care units not allocated to COVID-19 patients in a large teaching hospital. BMC Infect. Dis. 2023, 23, 11. [Google Scholar] [CrossRef]
- Jabarpour, M.; Dehghan, M.; Afsharipour, G.; Hajipour Abaee, E.; Mangolian Shahrbabaki, P.; Ahmadinejad, M.; Maazallahi, M. The impact of Covid-19 outbreak on nosocomial infection rate: A case of Iran. Can. J. Infect. Dis. Med. Microbiol. 2021, 2021, 6650920. [Google Scholar] [CrossRef]
- Klimovsky, D.; Nemec, J.; Bouckaert, G. The COVID-19 Pandemic in the Czech Republic and Slovakia. Sci. Pap. Univ. Pardubic. Ser. D Fac. Econ. Adm. 2021, 29, 1320. [Google Scholar] [CrossRef]
- Centers for Disease Control and Prevention. National Healthcare Safety Network. Bloodstream Infection Event (Central-Line–Associated Bloodstream Infection and Non–Central-Line–Associated Bloodstream Infection). Updated January 2022. Available online: https://www.cdc.gov/nhsn/pdfs/pscmanual/4psc_clabscurrent.pdf (accessed on 10 April 2022).
- Public Health Authority of the Slovak Republic. Annual Report on the Activities of the Public Health Offices of the Slovak Republic according to Individual Departments of Public Health. 2021. Available online: https://www.uvzsr.sk/documents/362623/1023692/V%C3%BDro%C4%8Dna+spr%C3%A1va+o+%C4%8Dinnosti+%C3%BAradov+verejn%C3%A9ho+zdravotn%C3%ADctva+SR+2021.pdf/54416fd4-e509-72a4-9819-dd80285f5a03?t=1670364143367 (accessed on 17 June 2023).
- European Centre for Disease Prevention and Control. Point Prevalence Survey of Healthcare-Associated Infections and Antimicrobial Use in European Acute Care Hospitals, 2016–2017; ECDC: Stockholm, Sweden, 2023. Available online: https://www.ecdc.europa.eu/sites/default/files/documents/healthcare-associated--infections-antimicrobial-use-point-prevalence-survey-2016-2017.pdf (accessed on 17 June 2023).
- Centers for Disease Control and Prevention. The 2019 National and State Healthcare-Associated Infections (HAI) Progress Report. Available online: https://www.cdc.gov/hai/data/archive/2019-HAI-progress-report.html#2018 (accessed on 17 June 2023).
- Rosenthal, V.D.; Duszynska, W.; Ider, B.E.; Gurskis, V.; Al-Ruzzieh, M.A.; Myatra, S.N.; Gupta, D.; Belkebir, S.; Upadhyay, N.; Zand, F.; 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. [Google Scholar] [CrossRef]
- Baker, M.A.; Sands, K.E.; Huang, S.S.; Kleinman, K.; Septimus, E.J.; Varma, N.; Blanchard, J.; Poland, R.E.; Coady, M.H.; Yokoe, D.S.; et al. CDC Prevention Epicenters Program. The Impact of Coronavirus Disease 2019 (COVID-19) on Healthcare-Associated Infections. Clin. Infect. Dis. 2022, 74, 1748–1754. [Google Scholar] [CrossRef]
- Rosenthal, V.D.; Myatra, S.N.; Divatia, J.V.; Biswas, S.; Shrivastava, A.; Al-Ruzzieh, M.A.; Ayaad, O.; Bat-Erdene, A.; Bat-Erdene, I.; Narankhuu, B.; 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. [Google Scholar] [CrossRef]
- Lastinger, L.M.; Alvarez, C.R.; Kofman, A.; Konnor, R.Y.; Kuhar, D.T.; Nkwata, A.; Patel, P.R.; Pattabiraman, V.; Xu, S.Y.; Dudeck, M.A. 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. 2023, 44, 997–1001. [Google Scholar] [CrossRef] [PubMed]
- LeRose, J.; Sandhu, A.; Polistico, J.; Ellsworth, J.; Cranis, M.; Jabbo, L.; Cullen, L.; Moshos, J.; Samavati, L.; Chopra, T. 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. [Google Scholar] [CrossRef] [PubMed]
- Ben-Aderet, M.A.; Madhusudhan, M.S.; Haroun, P.; Almario, M.J.P.; Raypon, R.; Fawcett, S.; Johnson, J.; Girard, A.; Griner, T.; Sheffield, L.; et al. Characterizing the relationship between coronavirus disease 2019 (COVID-19) and central-line-associated bloodstream infection (CLABSI) and assessing the impact of a nursing-focused CLABSI reduction intervention during the COVID-19 pandemic. Infect. Control Hosp. Epidemiol. 2022, 44, 1108–1115. [Google Scholar] [CrossRef] [PubMed]
- Isonne, C.; Baccolini, V.; Migliara, G.; Ceparano, M.; Alessandri, F.; Ceccarelli, G.; Tellan, G.; Pugliese, F.; De Giusti, M.; De Vito, C.; et al. Comparing the Occurrence of Healthcare-Associated Infections in Patients with and without COVID-19 Hospitalized during the Pandemic: A 16-Month Retrospective Cohort Study in a Hospital Intensive Care Unit. J. Clin. Med. 2022, 11, 1446. [Google Scholar] [CrossRef]
- Tashkandi, N.; Aljuaid, M.; McKerry, T.; Alchin, J.; Taylor, L.; Catangui, E.J.; Mulla, R.; Sinnappan, S.; Nammour, G.; El-Saed, A.; 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. [Google Scholar] [CrossRef]
- Putekova, S.; Martinkova, J.; Urickova, A.; Kober, L.; Reichertova, S.; Plancikova, D.; Majdan, M. The impact of the COVID-19 pandemic on the health and working conditions of nurses and its implications for policies: A cross-sectional study in Slovakia. BMC Nurs. 2023, 22, 185. [Google Scholar] [CrossRef]
- Abelenda-Alonso, G.; Puig-Asensio, M.; Jiménez-Martínez, E.; García-Lerma, E.; Hornero, A.; Gutiérrez, C.; Torrecillas, M.; Tebé, C.; Pujol, M.; Carratalà, J. Impact of the coronavirus disease 2019 (COVID-19) pandemic on infection control practices in a university hospital. Infect. Control Hosp. Epidemiol. 2023, 44, 135–138. [Google Scholar] [CrossRef]
- Devrim, I.; Erdem, H.; El-Kholy, A.; Almohaizeie, A.; Logar, M.; Rahimi, B.A.; Amer, F.; Alkan-Ceviker, S.; Sonmezer, M.C.; Belitova, M.; et al. Analyzing central-line associated bloodstream infection prevention bundles in 22 countries: The results of ID-IRI survey. Am. J. Infect. Control. 2022, 50, 1327–1332. [Google Scholar] [CrossRef]
- Shukla, B.S.; Warde, P.R.; Knott, E.; Arenas, S.; Pronty, D.; Ramirez, R.; Rego, A.; Levy, M.; Zak, M.; Parekh, D.J.; et al. Bloodstream Infection Risk, Incidence, and Deaths for Hospitalized Patients during Coronavirus Disease Pandemic. Emerg. Infect. Dis. 2021, 27, 2588–2594. [Google Scholar] [CrossRef]
- Kumar, G.; Adams, A.; Hererra, M.; Rojas, E.R.; Singh, V.; Sakhuja, A.; Meersman, M.; Dalton, D.; Kethireddy, S.; Nanchal, R.; et al. Predictors and outcomes of healthcare-associated infections in COVID-19 patients. Int. J. Infect. Dis. 2021, 104, 287–292. [Google Scholar] [CrossRef]
- Sargin-Altunok, E.; Batirel, A.; Ersoz, Z.; Akay-Guven, D.; Ozturk-Aydemir, S. Does COVID-19 Increase the Risk of Central-Line-Associated Bloodstream Infections? Klimik J. 2022, 35, 191–195. [Google Scholar] [CrossRef]
- Afzal, A.; Gutierrez, V.P.; Gomez, E.; Mon, A.M.; Sarmiento, C.M.; Khalid, A.; Polishchuk, S.; Al-Khateeb, M.; Yankulova, B.; Yusuf, M.; et al. Bloodstream infections in hospitalized patients before and during the COVID-19 surge in a community hospital in the South Bronx. Int. J. Infect. Dis. 2022, 116, 43–46. [Google Scholar] [CrossRef] [PubMed]
- Almasaudi, S.B. Acinetobacter spp. as nosocomial pathogens: Epidemiology and resistance features. Saudi J. Biol. Sci. 2018, 25, 586–596. [Google Scholar] [CrossRef]
- Clarivet, B.; Grau, D.; Jumas-Bilak, E.; Jean-Pierre, H.; Pantel, A.; Parer, S.; Lotthé, A. Persisting transmission of carbapenemase-producing Klebsiella pneumoniae due to an environmental reservoir in a university hospital, France, 2012 to 2014. Euro Surveill. 2016, 21, 30213. [Google Scholar] [CrossRef] [PubMed]
- Venier, A.G.; Leroyer, C.; Slekovec, C.; Talon, D.; Bertrand, X.; Parer, S.; Alfandari, S.; Guerin, J.M.; Megarbane, B.; Lawrence, C.; et al. Risk factors for Pseudomonas aeruginosa acquisition in intensive care units: A prospective multicentre study. J. Hosp. Infect. 2014, 88, 103–108. [Google Scholar] [CrossRef]
- Baccolini, V.; D’Egidio, V.; De Soccio, P.; Migliara, G.; Massimi, A.; Alessandri, F.; Tellan, G.; Marzuillo, C.; De Vito, C.; Ranieri, M.V. Effectiveness over time of a multimodal intervention to improve compliance with standard hygiene precautions in an intensive care unit of a large teaching hospital. Antimicrob. Resist. Infect. Control 2019, 8, 92. [Google Scholar] [CrossRef]
Variable | Total (n = 803) | Before Pandemic (n = 339) | Pandemic (n = 464) | p-Value | Pandemic | p-Value | |
---|---|---|---|---|---|---|---|
Yes COVID-19 (n = 207) | Non COVID-19 (n = 257) | ||||||
No. of CLABSI n (%) | 45 (5.60) | 8 (2.36) | 37 (7.97) | <0.001 *B | 27 (13.04) | 10 (3.09) | <0.001 *B |
No. of Bed Days (M, SD, 95% CI) | 8385 (10.44 ± 11.22; 9.665–11.219) | 3098 (9.10 ± 11.11; 7.916–10.290) | 5299 (11.42 ± 11.20; 10.398–12.442) | <0.001 *A | 2857 (13.80 ± 11.11; 12.279–15.325) | 2442 (9.50 ± 10.93; 8.160–10.844) | <0.001 *A |
Central line days (M, SD, 95% CI) | 7803 (9.72 ± 12.55; 8.848–10.587) | 2848 (8.40 ± 12.72; 7.038–9.765) | 4955 (10.68 ± 12.32; 9.554–11.803) | <0.001 *A | 2647 (12.79 ± 11.67; 11.188–14.387) | 2308 (8.98 ± 12.59; 7.433–10.528) | <0.001 *A |
Central line utilization ratio (95% CI) | 0.93 (0.925–0.935) | 0.92 (0.909–0.928) | 0.94 (0.928–0.941) | <0.001 *A | 0.93 (0.916–0.936) | 0.95 (0.935–0.953) | 0.001 *A |
CLABSI/1000 CL-Days (95% CI) | 5.77 (4.313–7.707) | 2.81 (1.424–5.533) | 7.47 (5.423–10.270) | <0.001 *A | 10.20 (95 CL 7.02–14.8) | 4.33 (2.355–7.957) | <0.001 *A |
Variable | Variants | Total (n = 803) | CLABSI No (n = 758) | CLABSI Yes (n = 45) | p-Value |
---|---|---|---|---|---|
Age Me (IQR) | Years | 64 (21.50) | 64 (21.37) | 59 (17) | 0.032 **A |
Gender n (%) | 0 Male | 515 (64.13) | 485 (63.98) | 30 (66.67) | 0.715 B |
1 Female | 288 (35.87) | 273 (36.02) | 15 (33.33) | ||
Hospitalization Type n (%) | 0 Surgical | 371 (46.20) | 364 (48.02) | 7 (15.56) | <0.001 **B |
1 Medical | 432 (53.80) | 394 (51.98) | 38 (74.39) | ||
ICU Outcome n (%) | No | 528 (65.75) | 503 (66.36) | 25 (55.56) | 0.138 B |
Yes | 275 (34.25) | 255 (33.64) | 20 (44.44) | ||
COVID-19 n (%) | No | 596 (74.22) | 578 (76.25) | 18 (40.00) | <0.001 **B |
Yes | 207 (25.78) | 180 (23.75) | 27 (60.00) | ||
Pandemic COVID-19 n (%) | No | 339 (42.22) | 331 (43.67) | 8 (17.78) | <0.001 **B |
Yes | 464 (57.78) | 427 (56.33) | 37 (82.22) |
Microorganism CLABSI | Total N = 45 (%) | Pandemic COVID-19 Non 8 (%) | Pandemic COVID-19 Yes 37 (%) |
---|---|---|---|
Acinetobacter spp. | 10 (22.22) | 2 (25.00) | 8 (21.62) |
Candida albicans | 1 (2.22) | 1 (12.50) | - |
Coagulase-negative Staphylococci epidermidis | 5 (11.11) | 1 (12.50) | 4 (10.81) |
Enterobacter cloacae | 1 (2.22) | - | 1 (2.70) |
Enterococci spp. | 6 (13.33) | - | 6 (16.22) |
Escherichia coli | 2 (4.44) | - | 2 (5.41) |
Klebsiella pneumoniae | 9 (20.20) | 1 (12.50) | 8 (21.62) |
Pseudomonas aeruginosa | 8 (17.78) | 3 (37.50) | 5 (13.51) |
Streptococcus spp. | 3 (6.67) | - | 3 (8.81) |
Variable–Reference Variant | Estimate of the Logistic Regression Parameter | OR (95% Cl) | p-Value |
---|---|---|---|
Constant term | −3.058 | 0.047 (0.012–0.182) | <0.001 |
Patients’ days | 0.077 | 1.080 (1.057–1.103) | <0.001 |
COVID-19 | 1.702 | 5.485 (2.706–11.116) | <0.001 |
Age | −0.029 | 0.971 (0.949–0.993) | 0.011 |
CLABSI | COVID-19 | Pandemic COVID-19 | ICU Outcome | Observed Values No. of Patients | Expected Values No. of Patients | χ2 | p-Value |
---|---|---|---|---|---|---|---|
Non | Non | Non | Non | 247.00 | 156.17 | 7.268 | 0.000 |
Non | Non | Non | Yes | 84.00 | 81.34 | 0.295 | 0.384 |
Non | Non | Yes | Non | 187.00 | 213.76 | 1.830 | 0.034 |
Non | Non | Yes | Yes | 60.00 | 111.33 | 4.865 | 0.000 |
Non | Yes | Yes | Non | 69.00 | 74,.4 | 0.608 | 0.272 |
Non | Yes | Yes | Yes | 111.00 | 38.67 | 11.632 | 0.000 |
Yes | Non | Non | Non | 5.00 | 9.27 | 1.403 | 0.080 |
Yes | Non | Non | Yes | 3.00 | 4.83 | 0.832 | 0.203 |
Yes | Non | Yes | Non | 7.00 | 12.69 | 1.597 | 0.055 |
Yes | Non | Yes | Yes | 3.00 | 6.61 | 1.404 | 0.080 |
Yes | Yes | Yes | Non | 13.00 | 4.41 | 4.093 | 0.000 |
Yes | Yes | Yes | Yes | 14.00 | 2.30 | 7.725 | 0.000 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Hlinkova, S.; Moraucikova, E.; Lesnakova, A.; Strzelecka, A.; Littva, V. Central Line Associated Bloodstream Infections in Critical Ill Patients during and before the COVID-19 Pandemic. Healthcare 2023, 11, 2415. https://doi.org/10.3390/healthcare11172415
Hlinkova S, Moraucikova E, Lesnakova A, Strzelecka A, Littva V. Central Line Associated Bloodstream Infections in Critical Ill Patients during and before the COVID-19 Pandemic. Healthcare. 2023; 11(17):2415. https://doi.org/10.3390/healthcare11172415
Chicago/Turabian StyleHlinkova, Sona, Eva Moraucikova, Anna Lesnakova, Agnieszka Strzelecka, and Vladimir Littva. 2023. "Central Line Associated Bloodstream Infections in Critical Ill Patients during and before the COVID-19 Pandemic" Healthcare 11, no. 17: 2415. https://doi.org/10.3390/healthcare11172415