[en] Healthcare workers (HCWs) are known to be at higher risk of developing severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infections although whether these risks are equal across all occupational roles is uncertain. Identifying these risk factors and understand SARS-CoV-2 transmission pathways in healthcare settings are of high importance to achieve optimal protection measures. We aimed to investigate the implementation of a voluntary screening program for SARS-CoV-2 infections among hospital HCWs and to elucidate potential transmission pathways though phylogenetic analysis before the vaccination era. HCWs of the University Hospital of Liège, Belgium, were invited to participate in voluntary reverse transcriptase-polymerase chain reaction (RT-PCR) assays performed every week from April to December 2020. Phylogenetic analysis of SARS-CoV-2 genomes were performed for a subgroup of 45 HCWs. 5095 samples were collected from 703 HCWs. 212 test results were positive, 15 were indeterminate, and 4868 returned negative. 156 HCWs (22.2%) tested positive at least once during the study period. All SARS-CoV-2 test results returned negative for 547 HCWs (77.8%). Nurses (p < 0.05), paramedics (p < 0.05), and laboratory staff handling respiratory samples (p < 0.01) were at higher risk for being infected compared to the control non-patient facing group. Our phylogenetic analysis revealed that most positive samples corresponded to independent introduction events into the hospital. Our findings add to the growing evidence of differential risks of being infected among HCWs and support the need to implement appropriate protection measures based on each individual’s risk profile to guarantee the protection of both HCWs and patients. Furthermore, our phylogenetic investigations highlight that most positive samples correspond to distinct introduction events into the hospital.
Disciplines :
Immunology & infectious disease
Author, co-author :
El Moussaoui, Majdouline ; Université de Liège - ULiège > Département des sciences cliniques > Immunopathologie - Maladies infectieuses et médecine interne générale
Maes, Nathalie ; Université de Liège - ULiège > Département des sciences de la santé publique
Hong, Samuel L.
Lambert, Nicolas ; Centre Hospitalier Universitaire de Liège - CHU > > Service de neurologie
Bontems, Sébastien ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Bactériologie, mycologie, parasitologie, virologie et microbiologie
Defêche, Justine
Godderis, Lode
Molenberghs, Geert
Meuris, Christelle
Artesi, Maria ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Génétique humaine
Durkin, Keith ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Génétique humaine
Rahmouni, Souad ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
GREGOIRE, Céline ; Centre Hospitalier Universitaire de Liège - CHU > > Service d'hématologie clinique
BEGUIN, Yves ; Centre Hospitalier Universitaire de Liège - CHU > > Service d'hématologie clinique
MOUTSCHEN, Michel ; Centre Hospitalier Universitaire de Liège - CHU > > Service des maladies infectieuses - médecine interne
Dellicour, Simon
DARCIS, Gilles ; Centre Hospitalier Universitaire de Liège - CHU > > Service des maladies infectieuses - médecine interne
Lipsitch, M.; Swerdlow, D.L.; Finelli, L. Defining the epidemiology of COVID-19—Studies needed. N. Engl. J. Med. 2020, 382, 1194–1196. https://doi.org/10.1056/NEJMp2002125.
COVID-19 Surveillance Frequently Asked Questions. Sciensano. Available online: https://covid19.sciensano.be/sites/default/files/Covid19/COVID-19_FAQ_ENG_final.pdf (accessed on 20 December 2021).
Meurisse, M.; Lajot, A.; Dupont, Y.; Lesenfants, M.; Klamer, S.; Rebolledo, J.; Lernout, T.; Leroy, M.; Capron, A.; Van Bussel, J.; et al. One year of laboratory-based COVID-19 surveillance system in Belgium: Main indicators and performance of the laboratories. Arch. Belg. Public Health 2021, 79, 188. https://doi.org/10.1186/s13690-021-00704-2.
Iversen, K.; Bundgaard, H.; Hasselbalch, R.B.; Kristensen, J. H.; Nielsen, P. B.; Pries-Heje, M.; Knudsen, A.D.; Christensen, C. E.; Fogh, K.; Norsk, J. B.; et al. Risk of COVID-19 in health-care workers in Denmark: An observational cohort study. Lancet Infect. Dis. 2020, 20, 1401–1408. https://doi.org/10.1016/S1473-3099(20)30589-2.
Li, R.; Xuyu, C.; Ying, W.; Wenwen, W.; Ling, Z.; Xiaodong, T. Risk Factors of Healthcare Workers with Coronavirus Disease 2019: A Retrospective Cohort Study in a Designated Hospital of Wuhan in China. Clin. Infect. Dis. 2020, 71, 2218–2221. https://doi.org/10.1093/cid/ciaa28.
Nguyen, L.H.; Drew, D.A.; Joshi, A.D.; Guo, G.G.; Ma, W.; Mehta, R.S. Risk of COVID-19 among frontline healthcare workers and the general community: A prospective cohort study. Epidemiology 2020, 6, 20084111. https://doi.org/10.1101/2020.04.29.20084111.
Lombardi, A.; Consonni, D.; Carugno, M.; Bozzi, G.; Mangioni, D.; Muscatello, A.; Castelli, V.; Palomba, E.; Cantù, A. P.; Ceriotti, F.; et al. Characteristics of 1573 healthcare workers who underwent nasopharyngeal swab testing for SARS-CoV-2 in Milan, 2020, Lombardy, Italy. Clin. Microbiol. Infect. 2020, 26, 1413.e9–1413.e13. https://doi.org/10.1016/j.cmi.2020.06.013.
Mo, Y.; Eyre, D.W.; Lumley, S.F.; Walker, T.M.; Shaw, R.H.; O’Donnell, D.; Butcher, L.; Jeffery, K.; Donnelly, C.A.; Oxford COVID Infection Review Team; et al. Transmission of community-and hospital-acquired SARS-CoV-2 in hospital settings in the UK: A cohort study. PLoS Med. 2021, 18, e1003816. https://doi.org/10.1371/journal.pmed.1003816.
Keeley, A.J.; Evans, C.; Colton, H.; Ankcorn, M.; Cope, A.; State, A.; Bennett, T.; Giri, P.; de Silva, T.I.; Raza, M. Roll-out of SARS-CoV-2 testing for healthcare workers at a large NHS Foundation Trust in the United Kingdom. Euro Surveill. Bull. Eur. Mal. Transm. 2020, 25, 2000433. https://doi.org/10.2807/1560-7917.ES.2020.25.14.2000433.
Sikkema, R.S.; Pas, S.D.; Nieuwenhuijse, D.F.; O’Toole, Á.; Verweij, J.; Van der Linden, A.; Chestakova, I.; Schapendonk, C.; Pronk, M.; Lexmond, P.; et al. COVID-19 in health-care workers in three hospitals in the south of the Netherlands: A cross-sectional study. Lancet Infect. Dis. 2020, 20, 1273–1280. https://doi.org/10.1016/S1473-3099(20)30527-2.
Abbas, M.; Robalo Nunes, T.; Martischang, R.; Zingg, W.; Iten, A.; Pittet, D.; Harbarth, S.. Nosocomial transmission and outbreaks of coronavirus disease 2019: The need to protect both patients and healthcare workers. Antimicrob. Resist. Infect. Control 2021, 10, 7. https://doi.org/10.1186/s13756-020-00875-7.
Hunter, E.; Price, D.A.; Murphy, E.; Van der Loeff, I.S.; Baker, K.F.; Lendrem, D.; Lendrem, C.; Schmid, M.L.; Pareja-Cebrian, L.; Welch, A.; et al. Experience of COVID-19 screening of health-care workers in England. Lancet 2020, 395, e77–e78. https://doi.org/10.1016/S0140-6736(20)30970-3.
Evans, S.; Agnew, E.; Vynnycky, E.; Stimson, J.; Bhattacharya, A.; Rooney, C.; Warne, B.; Robotham, J. The impact of testing and infection prevention and control strategies on within-hospital transmission dynamics of COVID-19 in English hospitals. Philos. Trans. R. Soc. Lond. 2021, 376, 20200268. https://doi.org/10.1098/rstb.2020.0268.
Hanrath, A.T.; Schim van der Loeff, I.; Lendrem, D.W.; Baker, K.F.; Price, D.A.; McDowall, P.; McDowall, K.; Cook, S.; Towns, P.; Schwab, U.; et al. SARS-CoV-2 Testing of 11,884 Healthcare Workers at an Acute NHS Hospital Trust in England: A Retrospective Analysis. Front. Med. 2021, 8, 636160. https://doi.org/10.3389/fmed.2021.636160.
Pérez-Lago, L.; Martínez-Lozano, H.; Pajares-Díaz, J.A.; Díaz-Gómez, A.; Machado, M.; Sola-Campoy, P.J.; Herranz, M.; Valerio, M.; Olmedo, M.; Suárez-González, J.; et al. Overlapping of Independent SARS-CoV-2 Nosocomial Transmissions in a Complex Outbreak. mSphere 2021, 6, e0038921. https://doi.org/10.1128/mSphere.00389-21.
Braun, K.M.; Moreno, G.K.; Buys, A.; Somsen, E.D.; Bobholz, M.; Accola, M.A.; Anderson, L.; Rehrauer, W.M.; Baker, D.A.; Safdar, N.; et al. Viral sequencing reveals US healthcare personnel rarely become infected with SARS-CoV-2 through patient contact. Clin. Infect. Dis. 2021, 73, e1329–e1336.
Lenggenhager, L.; Martischang, R.; Sauser, J.; Perez, M.; Vieux, L.; Graf, C.; Cordey, S.; Laubscher, F.; Nunes, T.R.; Zingg, W.; et al. Occupational and community risk of SARS-CoV-2 infection among employees of a long-term care facility: An observational study. Antimicrob. Resist. Infect. Control 2022, 11, 51. https://doi.org/10.1186/s13756-022-01092-0.
Sikkens, J.J.; Buis, D.T.P.; Peters, E.;. Dekker, M.; Schinkel, M.; Reijnders, T.; Schuurman, A.R.; de Brabander, J.; Lavell, A.; Maas, J. J.; et al. Serologic Surveillance and Phylogenetic Analysis of SARS-CoV-2 Infection Among Hospital Health Care Workers. JAMA Netw. Open 2021, 4, e2118554. https://doi.org/10.1001/jamanetworkopen.2021.18554.
Leducq, V.; Jary, A.; Bridier-Nahmias, A.; Daniel, L.; Zafilaza, K.; Damond, F.; Goldstein, V.; Duval, A.; Blanquart, F.; Calvez, V.; et al. Nosocomial transmission clusters and lineage diversity characterized by SARS-CoV-2 genomes from two large hospitals in Paris, France, in 2020. Sci. Rep. 2022, 12, 1094. https://doi.org/10.1038/s41598-022-05085-2.
Lucey, M.; Macori, G.; Mullane, N.; Sutton-Fitzpatrick, U.; Gonzalez, G.; Coughlan, S.; Purcell, A.; Fenelon, L.; Fanning, S.; Schaffer, K. Whole-genome Sequencing to Track Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Transmission in Nosocomial Outbreaks. Clin. Infect. Dis. 2021, 72, e727–e735. https://doi.org/10.1093/cid/ciaa1433.
Francis, R.V.; Billam, H.; Clarke, M.; Yates, C.; Tsoleridis, T.; Berry, L.; Mahida, N.; Irving, W.L.; Moore, C.; Holmes, N.; et al. The Impact of Real-Time Whole-Genome Sequencing in Controlling Healthcare-Associated SARS-CoV-2 Outbreaks. J. Infect. Dis. 2022, 225, 10–18. https://doi.org/10.1093/infdis/jiab483.
Borges, V.; Isidro, J.; Macedo, F.; Neves, J.; Silva, L.; Paiva, M.; Barata, J.; Catarino, J.; Ciobanu, L.; Duarte, S.; et al. Nosocomial Outbreak of SARS-CoV-2 in a “Non-COVID-19” Hospital Ward: Virus Genome Sequencing as a Key Tool to Understand Cryptic Transmission. Viruses 2021, 13, 604. https://doi.org/10.3390/v13040604.
MacCannell, T.; Batson, J.; Bonin, B.; Astha, K.C.; Quenelle, R.; Strong, B.; Lin, W.; Rudman, S.L.; Dynerman, D.; Ayscue, P.; et al. Genomic Epidemiology and Transmission Dynamics of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) in Congregate Healthcare Facilities in Santa Clara County, California. Clin. Infect. Dis. 2022, 74, 829–835. https://doi.org/10.1093/cid/ciab553.
Meredith, L.W.; Hamilton, W.L.; Warne, B.; Houldcroft, C.J.; Hosmillo, M.; Jahun, A.S.; Curran, M.D.; Parmar, S.; Caller, L.G.; Caddy, S. L.; et al. Rapid implementation of SARSCoV-2 sequencing to investigate cases of health-care associated COVID-19: A prospective genomic surveillance study. Lancet Infect. Dis. 2020, 20, 1263–1271. https://doi.org/10.1016/S1473-3099(20)30562-4.
Korth, J.; Wilde, B.; Dolff, S.; Frisch, J.; Jahn, M.; Krawczyk, A.; Trilling, M.; Schipper, L.; Cordes, S.; Ross, B.; et al. SARS-CoV-2 Seroprevalence in Healthcare Workers in Germany: A Follow-Up Study. Int. J. Environ. Res. Public Health 2021, 18, 4540. https://doi.org/10.3390/ijerph18094540=ancien17.
Jacob, J.T.; Baker, J.M.; Fridkin, S.K.; Lopman, B.A.; Steinberg, J.P.; Christenson, R.H.; King, B.; Leekha, S.; O’Hara, L.M.; Rock, P.; et al. Risk Factors Associated With SARS-CoV-2 Seropositivity Among US Health Care Personnel. JAMA Netw. Open 2021, 4, e211283. https://doi.org/10.1001/jamanetworkopen.2021.1283.
Nygren, D.; Norén, J.; De Marinis, Y.; Holmberg, A.; Fraenkel, C.J.; Rasmussen, M. Association between SARS-CoV-2 and exposure risks in health care workers and university employees—A cross-sectional study. Infect. Dis. 2021, 53, 460–468. https://doi.org/10.1080/23744235.2021.189281.
Wilkins, J.T.; Gray, E.L.; Wallia, A.; Hirschhorn, L.R.; Zembower, T. R.; Ho, J.; Kalume, N.; Agbo, O.; Zhu, A.; Rasmussen-Torvik; L.J.; et al. Seroprevalence and Correlates of SARS-CoV-2 Antibodies in Health Care Workers in Chicago. Open Forum Infect. Dis. 2020, 8, ofaa582. https://doi.org/10.1093/ofid/ofaa582.
Lai, X.; Wang, M.; Qin, C.; Tan, L.; Ran, L.; Chen, D.; Zhang, H.; Shang, K.; Xia, C.; Wang, S.; et al. Coronavirus Disease 2019 (COVID-2019) Infection Among Health Care Workers and Implications for Prevention Measures in a Tertiary Hospital in Wuhan, China. JAMA Netw. Open 2020, 3, e209666. https://doi.org/10.1001/jamanetworkopen.2020.9666.
Eyre, D.W.; Lumley, S.F.; O’Donnell, D.; Campbell, M.; Sims, E.; Lawson, E.; Warren, F.; James, T.; Cox, S.; Howarth, A.; et al. Differential occupational risks to healthcare workers from SARS-CoV-2 observed during a prospective observational study. eLife 2020, 9, e60675. https://doi.org/10.7554/eLife.60675.
Kahlert, C.R.; Persi, R.; Güsewell, S.; Egger, T.; Leal-Neto, O. B.; Sumer, J.; Flury, D.; Brucher, A.; Lemmenmeier, E.; Möller, J. C.; et al. Non-occupational and occupational factors associated with specific SARS-CoV-2 antibodies among hospital workers— A multicentre cross-sectional study. Clin. Microbiol. Infect. 2020, 27, 1336–1344. https://doi.org/10.1016/j.cmi.2021.05.014.
Rudberg, A.S.; Havervall, S.; Månberg, A.; Jernbom Falk, A.; Aguilera, K.; Ng, H.; Gabrielsson, L.; Salomonsson, A.C.; Hanke, L.; Murrell, B.; et al. SARS-CoV-2 exposure, symptoms and seroprevalence in healthcare workers in Sweden. Nat. Commun. 2020, 11, 5064. https://doi.org/10.1038/s41467-020-18848-0.
Gómez-Ochoa, S.A.; Franco, O.H.; Rojas, L.Z.; Raguindin, P.F.; Roa-Díaz, Z.M.; Wyssmann, B.M.; Guevara, S.; Echeverría, L.E.; Glisic, M., Muka, T. COVID-19 in Health-Care Workers: A Living Systemat-ic Review and Meta-Analysis of Prevalence, Risk Factors, Clinical Characteristics, and Outcomes. Am. J. Epidemiol. 2021, 190, 161–175. https://doi.org/10.1093/aje/kwaa191.
Steensels, D.; Oris, E.; Coninx, L.; Nuyens, D.; Delforge, M.L.; Vermeersch, P.; Heylen; L. Hospital-Wide SARS-CoV-2 Antibody Screening in 3056 Staff in a Tertiary Center in Belgium. JAMA 2020, 324, 195–197. https://doi.org/10.1001/jama.2020.11160.
Jafari, Y.; Yin, M.; Lim, C.; Pople, D.; Evans, S.; Stimson, J.; Pham, T.M.; LSHTM CMMID COVID-19 Working Group; Read, J. M.; Robotham, J.V.; et al. Effectiveness of infection prevention and control interventions, excluding personal protective equipment, to prevent nosocomial transmission of SARS-CoV-2: A systematic review and call for action. Infect. Prev. Pract. 2021, 4, 100192. https://doi.org/10.1016/j.infpip.2021.100192.
COVID-19: Occupational Health and Safety for Health Workers, Interim Guidance 2 February 2021. Available online: https://hlh.who.int/docs/librariesprovider4/hlh-documents/covid-19---occupational-health-and-safety-for-health-workers.pdf?sfvrsn=581e60c6_5 (accessed on 20 December 2021).
Rivett, L.; Sridhar, S.; Sparkes, D.; Routledge, M.; Jones, N.K.; Forrest, S.; Young, J.; Pereira-Dias, J.; Hamilton, W.L.; Ferris, M.; et al. Screening of healthcare workers for SARS-CoV-2 highlights the role of asymptomatic carriage in COVID-19 transmission. eLife 2020, 9, e58728. https://doi.org/10.7554/eLife.58728.
Kasper, M.R.; Geibe, J.R.; Sears, C.L.; Riegodedios, A.J.; Luse, T.; von Thun, A.M.; McGinnis, M.B.; Olson, N.; Houskamp, D.; Fenequito, R.; et al. An Outbreak of Covid-19 on an Aircraft Carrier. N. Engl. J. Med. 2020, 383, 2417–2426. https://doi.org/10.1056/NEJMoa2019375.
Minh, B.Q.; Schmidt, H.A.; Chernomor, O.; Schrempf, D.; Woodhams, M.D.; von Haeseler, A.; Lanfear, R. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Mol. Biol. Evol. 2020, 37, 1530–1534. https://doi.org/10.1093/molbev/msaa015.
Tavaré, S. Some probabilistic and statistical problems in the analysis of DNA sequences. In Lectures on Mathematics in the Life Sciences; The American Mathematical Society: Providence, RI, USA, 1986; Volume 17, pp. 57–86.
Yang, Z. A space-time process model for the evolution of DNA sequences. Genetics 1995, 139, 993–1005.
Dellicour, S.; Durkin, K.; Hong, S.L.; Vanmechelen, B.; Martí-Carreras, J.; Gill, M.S. A Phylodynamic Workflow to Rapidly Gain Insights into the Dispersal History and Dynamics of SARS-CoV-2 Lineages. Mol. Biol. Evol. 2021, 38, 1608–1613. https://doi.org/10.1093/molbev/msaa284.
Bollen, N.; Artesi, M.; Durkin, K.; Hong, S.L.; Potter, B.; Boujemla, B.; Vanmechelen, B.; Martí-Carreras, J.; Wawina-Bokalanga, T.; Meex, C.; et al. Exploiting genomic surveillance to map the spatio-temporal dispersal of SARS-CoV-2 spike mutations in Belgium across 2020. Sci. Rep. 2021, 11, 18580. https://doi.org/10.1038/s41598-021-97667-9.
Lemey, P.; Rambaut, A.; Drummond, A.J.; Suchard, M.A. Bayesian phylogeography finds its roots. PLoS Comput. Biol. 2009, 5, e1000520. https://doi.org/10.1371/journal.pcbi.1000520.
Suchard, M.A.; Lemey, P.; Baele, G.; Ayres, D.L.; Drummond, A.J.; Rambaut, A. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 2018, 4, vey016. https://doi.org/10.1093/ve/vey016.
Rambaut, A.; Drummond, A.J.; Xie, D.; Baele, G.; Suchard, M.A. Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Syst. Biol. 2018, 67, 901–904. https://doi.org/10.1093/sysbio/syy032
Biorender. Available online: https://app.biorender.com/(accessed on 23 February 2022).
Martischang, R.; Iten, A.; Arm, I.; Abbas, M.; Meyer, B.; Yerly, S.; Eckerle, I.; Pralong, J.; Sauser, J.; Suard, J.C.; et al. Severe acute respiratory coronavirus virus 2 (SARS-CoV-2) seroconversion and occupational exposure of employees at a Swiss university hospital: A large longitudinal cohort study. Infect. Control Hosp. Epidemiol. 2021, 43, 326–333.
Baker, J.M.; Nelson, K.N.; Overton, E.; Lopman, B.A.; Lash, T.L.; Photakis, M.; Jacob, J.T.; Roback, J.; Fridkin, S.K., Steinberg, J. P. Quantification of occupational and community risk factors for SARS-CoV-2 seropositivity among healthcare workers in a large U.S. healthcare system. Preprint. medRxiv 2020, 2020, 20222877. https://doi.org/10.1101/2020.10.30.20222877.
Modenese, A.; Casolari, L.; Rossi, G.; Della Vecchia, E.; Glieca, F.; D'Elia, C.; Garavini, D.; Righi, E.; Mariani, S.; Venturelli, L.; et al. Factors Associated with SARS-CoV-2 Infection Risk among Healthcare Workers of an Italian University Hospital. Healthcare 2021, 9, 1495. https://doi.org/10.3390/healthcare9111495.
McEllistrem, M.C.; Clancy, C.J.; Buehrle, D.J.; Singh, N.; Lucas, A.; Sirianni, V.; Decker, B.K. SARS-CoV-2 is associated with high viral loads in asymptomatic and recently symptomatic healthcare workers. PLoS ONE 2021, 16, e0248347. https://doi.org/10.1371/journal.pone.0248347.
Paltansing, S.; Sikkema, R.S.; De Man, S.J.; Koopmans, M.; Oude Munnink, B.B.; De Man, P. Transmission of SARS-CoV-2 among healthcare workers and patients in a teaching hospital in the Netherlands confirmed by whole-genome sequencing. J. Hosp. Infect. 2021, 110, 178–183. https://doi.org/10.1016/j.jhin.2021.02.005.
He, X.; Lau, E.; Wu, P.; Deng, X.; Wang, J.; Hao, X.; Lau, Y.C.; Wong, J.Y.; Guan, Y.; Tan, X.; et al. Temporal dynamics in viral shedding and transmissibility of COVID-19. Nat. Med. 2020, 26, 672–675. https://doi.org/10.1038/s41591-020-0869-5.
McMichael, T.M.; Currie, D.W.; Clark, S.; Pogosjans, S.; Kay, M.; Schwartz, N.G.; Lewis, J.; Baer, A.; Kawakami, V.; Lukoff, M.D.; et al. Public Health–Seattle and King County, EvergreenHealth, and CDC COVID-19 Investigation Team. Epidemiology of Covid-19 in a Long-Term Care Facility in King County, Washington. N. Engl. J. Med. 2020, 382, 2005–2011. https://doi.org/10.1056/NEJMoa2005412.
Migisha, R.; Ario, A.R.; Kwesiga, B.; Bulage, L.; Kadobera, D.; Kabwama, S.N.; Katana, E.; Ndyabakira, A.; Wadunde, I.; Byaruhanga, A.; et al. Risk perception and psychological state of healthcare workers in referral hospitals during the early phase of the COVID-19 pandemic, Uganda. BMC Psychol. 2021, 9, 195. https://doi.org/10.1186/s40359-021-00706-3.
McAlonan, G.M.; Lee, A.M.; Cheung, V.; Cheung, C.; Tsang, K.W.; Sham, P.C.; Chua, S.E.; Wong, J.G. Immediate and sustained psychological impact of an emerging infectious disease outbreak on health care workers. Canadian journal of psychiatry. Rev. Can. Psychiatr. 2007, 52, 241–247. https://doi.org/10.1177/070674370705200406.
Jones, N.K.; Rivett, L.; Sparkes, D.; Forrest, S.; Sridhar, S.; Young, J.; Pereira-Dias, J.; Cormie, C.; Gill, H.; Reynolds, N.; et al. Effective control of SARS-CoV-2 transmission between healthcare workers during a period of diminished community prevalence of COVID-19. eLife 2020, 9, e59391. https://doi.org/10.7554/eLife.59391.
Grassly, N.C.; Pons-Salort, M.; Parker, E.P.K. Role of Testing in COVID-19 Control. London, United Kingdom: Imperial College. 2020. Available online: https://www.imperial.ac.uk/media/imperial-college/medicine/mrc-gida/2020-04-23-COVID19-Report-16.pdf (accessed on 20 December 2021).
