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Viable mpox virus in the environment of a patient room

Open AccessPublished:March 16, 2023DOI:https://doi.org/10.1016/j.ijid.2023.03.016
Viable mpox virus in the environment of a patient room
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      Abstract

      We conducted a prospective environmental surveillance study to investigate the air, surface, dust and water contamination of a room occupied by a patient infected with mpox virus (MPXV) at various stages of the illness. The patient tested positive for MPXV from a throat swab and skin lesions. Environmental sampling was conducted in a negative pressure room with 12 unidirectional HEPA air changes per hour and daily cleaning of the surfaces. A total of 179 environmental samples were collected on days 7, 8, 13, and 21 of illness. Among the days of sampling, air, surface, and dust contamination showed highest contamination rates on day 7 and 8 of illness, with a gradual decline to the lowest contamination level by day 21. Viable MPXV was isolated from surfaces and dust samples and no viable virus was isolated from the air and water samples.

      Keywords

      Introduction

      The multi-country 2022 mpox virus (MPXV) outbreak continues to expand, leading the WHO Director General to declare mpox a global health emergency [
      WHO
      Multi-country monkeypox outbreak: situation update.
      World Health Organization. 2022; (accessed Jun. 30, 2022)
      https://www.who.int/emergencies/disease-outbreak-news/item/2022-DON396
      ]. MPXV has caused multiple outbreaks in traditionally endemic regions of central and western Africa, with a small number of imported cases and limited transmission documented outside these areas [
      • Bunge E.M.
      • et al.
      The changing epidemiology of human monkeypox—A potential threat? A systematic review.
      PLoS Negl Trop Dis. Feb. 2022; 16e0010141https://doi.org/10.1371/journal.pntd.0010141
      ]. With the decrease in herd immunity provided by Smallpox vaccination, human encroachment into forested area, increased global mobility and an increase in disease surveillance, the epidemiology of MPXV has changed over the years with increased cases [
      • Bunge E.M.
      • et al.
      The changing epidemiology of human monkeypox—A potential threat? A systematic review.
      PLoS Negl Trop Dis. Feb. 2022; 16e0010141https://doi.org/10.1371/journal.pntd.0010141
      ] and secondary attack rates [
      • Heymann D.L.
      • Szczeniowski M.
      • Esteves K.
      Re-emergence of monkeypox in Africa: a review of the past six years.
      Br Med Bull. Jan. 1998; 54: 693-702https://doi.org/10.1093/oxfordjournals.bmb.a011720
      ].
      Close wild animal contact in endemic areas and physical contact with infected individuals are known risk factors for MPXV human infections [
      • Heymann D.L.
      • Szczeniowski M.
      • Esteves K.
      Re-emergence of monkeypox in Africa: a review of the past six years.
      Br Med Bull. Jan. 1998; 54: 693-702https://doi.org/10.1093/oxfordjournals.bmb.a011720
      ]. Fomite-based transmission through contaminated linen and rooms occupied by infected patients has also previously been shown [
      • Vaughan A.
      • et al.
      Human-to-Human Transmission of Monkeypox Virus.
      Emerg Infect Dis. October 2018; 26 (Apr. 2020): 782-785https://doi.org/10.3201/eid2604.191164
      ]. Epidemiological evidence suggests that disease transmission in the current 2022 outbreak is mainly driven by direct physical contact [
      • Thornhill J.P.
      • et al.
      Monkeypox Virus Infection in Humans across 16 Countries.
      New England Journal of Medicine. Aug. 2022; 387 (April–June 2022): 679-691https://doi.org/10.1056/NEJMoa2207323
      ]. However, other possible modes of human-to-human transmission of MPXV have not been systematically investigated. For instance, the significance of prolonged throat positivity for MPXV even after the resolution of skin lesions [
      • Adler H.
      • et al.
      Clinical features and management of human monkeypox: a retrospective observational study in the UK.
      Lancet Infect Dis. Aug. 2022; 22: 1153-1162https://doi.org/10.1016/S1473-3099(22)00228-6
      ] in propagating mpox transmission remains unclear and could be further evaluation. This study aims to investigate the extent of viral contamination of the air, surface, dust and water environment of a room occupied by a patient with MPXV at various stages of illness.

      Methods

      We conducted longitudinal sampling of air, surfaces, water and dust in the room occupied by the MPXV patient on days 7, 8, 13, and 21 of illness. The patient is of Asian descent, age range between 40-45 years old, with no significant medical comorbidities and able to self-care and ambulate with no aid. The patient had mild to moderate symptoms with fever, lymphadenopathy and numerous vesico-pustular skin lesion but haemodynamically stable otherwise throughout the hospital admission. An additional air sampling was done on day 15. Supplementary Figure 1 illustrates the locations of environmental sampling. The patient was in an airborne infection isolation room (AIIR) at the National Centre for Infectious Diseases (NCID), Singapore. The AIIR room had 12 air changes/h, an average temperature of 23⁰C, relative humidity of 52-60% and an exhaust flow of 570 m3/h. The floor and high-touch surfaces in the patient's room and bathroom floor were cleaned daily with bleach 10,000 ppm. The swab used did not contain neutralizing agent for residual bleach. Room cleaning was only done after the environmental samples collected. The patient was on the bed during sampling except for 5 minutes when the study team needed to collect dust samples from the linen.
      We sampled the patient's room air using SASS3100 (Research International), Coriolis µ (Bertin Instruments) samplers, DustTrakTM DRX 8534, NIOSH BC-251 bioaerosol samplers and two SASS samplers (Supplementary Table S.1). Sterile nylon flocked swabs (Puritan UniTranz-RT, Puritan Medical Products) were used to collect surface samples. Dust samples from linen, room and bathroom floor surfaces were collected using vacuum socks (X-Cell-200, Midwest Filtration) fitted on a vacuum pump (Omega Plus HEPA Abatement Vacuum, Atrix international). Detailed orientation and distance of air sampler's placements, areas of surface swab samples, handling of dust sampling specimens, water sampling, sample quality control and transport as well as laboratory methods are further described in supplementary methods. Graphpad Prism was used to carry out statistical analyses.

      Results

      We sampled the hospital room environment occupied by a patient admitted with skin lesions and an episode of fever. MPXV DNA was detected from a nasopharyngeal swab and swab of peri-anal lesions on the day of admission (Day 5 of illness). Most of the skin lesions were located on the buttocks (n=23), followed by the back (n=15) and extremities (n=2-4), with no new lesions reported during environmental sampling on day 13 and day 15 of illness. The clinical course was uneventful, and the patient was discharged on day 23. Details of the sampling schedule and the number of samples collected are provided in Supplementary Table S.1 and Table S.2.
      The overall degree of environmental contamination was compared across days of sampling. MPXV DNA detection in air samples appeared to be higher on day 7 of illness (100%, 4/4 samples positive, average 10 copies/L air) when compared to subsequent sampling days (i.e., day 8, 100%, 4/4 samples positive, average 3 copies/L air; day 13, 83.3%, 5/6 samples positive, average 1 copy/L air), with MPXV DNA concentration of less than 1 copies/L of air detected by day 21 of illness (40%, 2/5 samples positive) (Figures 1.A and 1.B). Similarly, MPXV DNA detection in surface swab samples was higher on day 8 of illness (72%, 18/25 samples positive, average 1.98 × 103 copies/swab) as compared to results from subsequent sampling days later in the course of illness; with comparatively lower detection on day 21 of illness (28%, 7/25 samples positive, average 5.5 × 102 copies/swab; Figure 1.C). A similar trend was observed for vacuumed dust samples, with higher viral load observed on day 7 of illness (average 2.12 × 107 copies/sample) as compared to subsequent sampling days, with comparatively lower detection on day 21 of illness (average 8.71 × 104 virus copies/sample) (Figure 1.D); all dust samples were positive for MPXV DNA across all days of sampling. Viable virus was isolated from four surface and dust samples from the patient's chair, toilet seat and linen (Table 1). Lastly, water from Sink P-traps were positive for MPXV DNA until day 13 of sampling.
      Figure 1
      Figure 1Environmental Contamination of Mpox Virus DNA. Virus DNA concentration (copies/L) detected in air using (A) Coriolis or SASS samplers across sampling days, and (B) NIOSH sampler on day 15 of disease. Line and error bars indicate mean and standard error of the mean (SEM). (C) Virus DNA concentration (copies/cm2) from swabs of environmental surfaces of patient room, toilet and anteroom across sampling days. Bar indicates median, + indicates mean. Box encompasses the interquartile range, and whiskers show the minimum to maximum values. (D) Virus DNA concentration (copies/sample) from dust samples across sampling dates.
      Table 1Mpox virus detection in the air, surface, water and dust of the room occupied by the infected patient
      Mpox virus detection in the air of the room occupied by the infected patient
      Days of illnessSymptoms reported by patientPatient's activities during samplingSampler typeDistance from patient's head (meter)Aerosol particle sizeAverage Gene Copies/ PCR ReactionAirborne Mpox virus concentration (copies/L of air)Virus Culture
      Day 7Formation of new vesiclesIn bed throughout sampling. Conversing over the phoneSASS
      Right side of the patient
      		0.9NA653811-
      SASS
      Left side of the patient
      		0.8NA47438-
      Coriolis
      Right side of the patient
      		0.9NA63911Negative
      Coriolis
      Left side of the patient
      		0.8NA4788Negative
      Day 8Formation of new vesiclesIn bed throughout sampling. Conversing over the phoneSASS
      Right side of the patient
      		0.9NA4921-
      SASS
      Left side of the patient
      		0.8NA4301-
      Coriolis
      Right side of the patient
      		0.9NA1896-
      Coriolis
      Left side of the patient
      		0.8NA2454Negative
      Day 13No new vesicles. Some scabs seenIn bed throughout sampling. Conversing over the phoneSASS
      Right side of the patient
      		0.9NA36<1-
      SASS
      Left side of the patient
      		0.8NA99<1-
      SASS-F2.5NA56<1-
      Coriolis
      Right side of the patient
      		0.9NA542-
      Coriolis
      Left side of the patient
      		0.8NA461Negative
      Coriolis-F2.5NANDND-
      Day 15No new vesicles. More scabs seen
      • -
        Around 2 hours were spent sitting on chair
      • -
        Around 1 hour was spent in bed
      • -
        Around 1 hour spent on exercise and walking around the room (Exercise on Yoga mat during first 30 mins and last 30 mins sampling)
      		SASS
      Right side of the patient
      		0.9NA5621-
      SASS
      Left side of the patient
      		0.8NA4501-
      SASS-F2.5NA3441-
      NIOSH
      First sampler on the right side
      		0.9> 4 μm886Negative
      1 -4 μmNDND-
      < 1 μmNDND-
      NIOSH
      Second sampler on the right side
      		0.9> 4 μm312Negative
      1 -4 μmNDND-
      < 1 μmNDND-
      NIOSH
      First sampler on the left side
      		0.8> 4 μm403Negative
      1 -4 μmNDND-
      < 1 μmNDND-
      NIOSH
      Second sampler on the left side Dashes ‘-‘, not done/not tested; NA, not applicable; ND, not detected; All controls were negative; PPE, personal protective equipment.
      		0.8> 4 μm292Negative
      1 -4 μmNDND-
      < 1 μmNDND-
      Day 21SASS
      Right side of the patient
      		0.9NA44<1-
      SASS
      Left side of the patient
      		0.8NA53<1-
      SASS-F2.5NANDND-
      Coriolis
      Right side of the patient
      		0.9NANDND-
      Coriolis
      Left side of the patient
      		0.8NANDND-
      Mpox virus detection on surfaces of the room occupied by an infected patient
      LocationDay of illness
      Day 7Day 8Day 13Day 21
      Average Gene Copies/Gene Copies/ cm2Virus CultureAverage Gene Copies/Gene Copies/ cm2Virus CultureAverage Gene Copies/Gene Copies/ cm2Virus CultureAverage Gene Copies/Gene Copies/ cm2Virus Culture
      PCR ReactionPCR ReactionPCR ReactionPCR Reaction
      Patient's room
      Floor2691.01 × 103-5752.16 × 103-2,5369.51 × 103NegativeNDND-
      Overbed table5643.76 × 103Negative2081.39 × 103-5613.74 × 103-513.38 × 102-
      Bed rails115344-3821.15 × 103-1875.61 × 102-NDND-
      Control panelsNDND-609.07 × 102-466.92 × 102-NDND-
      Call bellNDND-2091.25 × 104-1951.17 × 104-694.12 × 103-
      Bedside locker569.30 × 101-1292.15 × 102-2854.75 × 102-NDND-
      Patient's chair1094.10 × 102-19047.14 × 103Positive2238.37 × 102-NDND-
      Switches over the bed203.04 × 102-1191.78 × 103-891.34 × 103-NDND-
      StethoscopeNDND-171.01 × 103-1197.15 × 103-1026.10 × 103-
      PPE racks (unused)NDND-1001.50 × 103-588.69 × 102-1562.34 × 103-
      Sink-external surface209.80 × 101-1145.70 × 102-1,1595.80 × 103Negative994.97 × 102-
      Sink-internal surfaceNDND-2301.53 × 103Negative4272.85 × 103-442.94 × 102-
      Glass windowNDND-NDND-381.43 × 102-NDND-
      Sliding doorNDND-311.15 × 102-238.70 × 101-NDND-
      Bathroom
      Door handle684.05 × 102-2421.45 × 103-2011.21 × 103-NDND-
      Toilet seat6652.22 × 103Positive7982.66 × 103-5261.75 × 103-227.20 × 101-
      Support handrails1303.91 × 102-882.63 × 102-2868.57 × 102-NDND-
      Sink-external surface1688.40 × 102-6073.03 × 103-2821.41 × 103-NDND-
      Sink-internal surface966.39 × 102-15081.01 × 104Negative18,3021.22 × 105NegativeNDND-
      Anteroom
      FloorNDND-NDND-NDND-NDND-
      Sink-external surfaceNDND-NDND-NDND-NDND-
      Sink-internal surfaceNDND-NDND-NDND-NDND-
      Sliding door- to roomNDND-NDND-NDND-NDND-
      Sliding door- to corridorNDND-NDND-NDND-NDND-
      Clean corridor
      FloorNDND-NDND-NDND-NDND-
      Mpox virus detection in water and vacuumed dust sample
      Days of illnessSample typeAverage Gene Copies/ PCR ReactionCopies/ mL waterCopies / SampleVirus culture
      Day 7Water: Sink P-trap, patient's room373.00 × 101NA-
      Water: Sink P-trap, bathroom14,60811.69 × 103NA-
      Vacuum sock- linen4,219NA2.53 × 105Positive
      Vacuum sock- room floor6,837NA4.10 × 106Negative
      Vacuum sock- toilet floor98,989NA5.94 × 107Negative
      Day 8Water: Sink P-trap, patient's room--NA-
      Water: Sink P-trap, bathroom423.40 × 101NA-
      Vacuum sock- linen23,685NA1.42 × 107Positive
      Vacuum sock- room floor765NA4.59 × 104Negative
      Vacuum sock- toilet floor2,451NA1.47 × 106Negative
      Day 13Water: Sink P-trap, patient's room1,6481.32 × 103NA-
      Water: Sink P-trap, bathroomNDNDNA-
      Vacuum sock- linen453NA2.72 × 104Negative
      Vacuum sock- room floor851NA5.10 × 105Negative
      Vacuum sock- toilet floor159NA9.54 × 104-
      Day 21Water: Sink P-trap, patient's roomNDNDNA-
      Water: Sink P-trap, bathroomNDNDNA-
      Vacuum sock- linen47NA2.83 × 103-
      Vacuum sock- room floor382NA2.29 × 105-
      Vacuum sock- toilet floor49NA2.94 × 104-
      R Right side of the patient
      L Left side of the patient
      R-1 First sampler on the right side
      R-2 Second sampler on the right side
      L-1 First sampler on the left side
      L-2 Second sampler on the left sideDashes ‘-‘, not done/not tested; NA, not applicable; ND, not detected; All controls were negative; PPE, personal protective equipment.
      Results for air sampling are summarized by sampler types and date of collection in Table 1. Of note, we observed no significant change (p>0.05) in the concentration of particle matter of >4μm before and after the air samplers were turn on (Supplementary Figure S.2), but increased number of particles during activities such as opening of doors (Supplementary Figure S.3). Similarly, results for environmental surface swabs, dust samples and water from Sink P-traps are summarized by sampling sites and the date of collection in Table 1.

      Discussion

      In this study, swab and dust sampling showed extensive surface contamination of the hospital room occupied by a MPXV patient with the recovery of viable MPXV virus especially from chair, toilet seat and dust from bed linen. MPXV DNA was consistently detected in almost all air samplers, though they were not culturable. Surface, dust, and air contamination gradually declined after the first week of illness.
      Recovery of viable virus from the chair and toilet seat correlates with the location of skin lesions of the patient. As linens were changed daily, surfaces, room floors, and bathroom area were cleaned daily, the detection of MPXV DNA across sampling days showed continued viral shedding over the course of the illness. While environmental contamination has been reported in other recently published reports [
      • Nörz D.
      • et al.
      Evidence of surface contamination in hospital rooms occupied by patients infected with monkeypox.
      Eurosurveillance. June 2022; 27 (Jun. 2022)https://doi.org/10.2807/1560-7917.ES.2022.27.26.2200477
      ,
      • Atkinson B.
      • et al.
      Infection-competent monkeypox virus contamination identified in domestic settings following an imported case of monkeypox into the <scp>UK</scp>.
      Environ Microbiol. Oct. 2022; 24: 4561-4569https://doi.org/10.1111/1462-2920.16129
      ,
      • Gould S.
      • et al.
      Air and surface sampling for monkeypox virus in a UK hospital: an observational study.
      Lancet Microbe. Dec. 2022; 3: e904-e911https://doi.org/10.1016/S2666-5247(22)00257-9
      ], our study tracked virus shedding of the patient over time, with reduced levels of environmental contamination from the second week of illness onwards, coinciding with the period when the patient stops developing new lesions. Findings of viable viruses from surface swabs and dust samples support the possibility of fomite-based transmission, especially in the nosocomial [
      • Vaughan A.
      • et al.
      Human-to-Human Transmission of Monkeypox Virus.
      Emerg Infect Dis. October 2018; 26 (Apr. 2020): 782-785https://doi.org/10.3201/eid2604.191164
      ] and home settings. It highlights the importance of surface disinfection, especially of chairs, toilet seats and floors, and the need for precautions when handling linens.
      The daily detection of viral particles by all air samplers in an environment with 12 HEPA-filtered unidirectional air changes per hour, together with previous findings from the United Kingdom of potentially viable MPXV DNA suspended in air especially during certain activities [
      • Gould S.
      • et al.
      Air and surface sampling for monkeypox virus in a UK hospital: an observational study.
      Lancet Microbe. Dec. 2022; 3: e904-e911https://doi.org/10.1016/S2666-5247(22)00257-9
      ], underscores the possibility of aerosol-based transmission of MPXV. Our finding of viral material only in particles of >4μm sizes suggests that the possibility of breathing and/or talking being the source of the virus is low, as these activities were previously found to emit predominantly virus particles of <5um sizes [
      • Fennelly K.P.
      Particle sizes of infectious aerosols: implications for infection control.
      Lancet Respir Med. Sep. 2020; 8: 914-924https://doi.org/10.1016/S2213-2600(20)30323-4
      ]. On the other hand, the presence of viruses, including live virus, in dust samples suggests lesion shedding as the potential source of contaminated particles in the air.
      Notably, the detection of MPXV DNA from wastewater in the sink traps suggests that mpox could be discharged in wastewater and provides data for the possible utility of wastewater-based surveillance [
      WHO
      Multi-country monkeypox outbreak: situation update.
      World Health Organization. 2022; (accessed Jun. 30, 2022)
      https://www.who.int/emergencies/disease-outbreak-news/item/2022-DON396
      ,
      • Tiwari A.
      • et al.
      Monkeypox outbreak: Wastewater and environmental surveillance perspective.
      Science of The Total Environment. Jan. 2023; 856159166https://doi.org/10.1016/j.scitotenv.2022.159166
      ] of MPXV. Main limitations of this study include small sample size of one mpox patient, periodic sampling time instead of daily samplings that may or may not lead to limited numbers of viable virus cultured (16 of 179 samples). Our findings should be viewed in the context of a pilot study of one patient and larger cohort might be needed to adequately elucidate the transmission dynamics of mpox.

      Acknowledgements

      We would like to thank the Ministry of Health, Singapore for their review of the manuscript. We also appreciate the nursing team at the National Centre of Infectious Diseases, and the Facilities, Safety and Quality Department at the Environmental Health Institute, for their support in sample collection and coordination. We would like to thank Dr Sean Ong for the graphics and Mr Pek Han Bin for his support in sample transfer.

      Declaration of interests

      The authors declare no competing interests

      Funding Sources

      This research is supported by the Singapore Ministry of Health's (MOH) National Medical Research Council (NMRC) under its NMRC Collaborative Grant: Collaborative Solutions Targeting Antimicrobial Resistance Threats in Health Systems (CoSTAR-HS) (CG21APR2005), NMRC Clinician Scientist Award (MOH-000276) and NMRC Clinician Scientist Individual Research Grant (MOH-CIRG18Nov-0034). The study is also internally funded by the National Environment Agency.

      Ethics statement

      Informed consent was obtained from the patient as part of the PROTECT study protocol (DSRB number: 2012/00917).
      This study was approved by the Environmental Health Institute's Management Committee (Project TS325), National Environment Agency.

      Associated content

      Supporting Information. Supplementary methods, figures and tables are found in the Supplementary file.

      Declaration of interests

      ☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
      ☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:

      References

        • WHO
        Multi-country monkeypox outbreak: situation update.
        World Health Organization. 2022; (accessed Jun. 30, 2022)
        https://www.who.int/emergencies/disease-outbreak-news/item/2022-DON396
        View in Article
        • Bunge E.M.
        • et al.
        The changing epidemiology of human monkeypox—A potential threat? A systematic review.
        PLoS Negl Trop Dis. Feb. 2022; 16e0010141https://doi.org/10.1371/journal.pntd.0010141
        View in Article
        • Heymann D.L.
        • Szczeniowski M.
        • Esteves K.
        Re-emergence of monkeypox in Africa: a review of the past six years.
        Br Med Bull. Jan. 1998; 54: 693-702https://doi.org/10.1093/oxfordjournals.bmb.a011720
        View in Article
        • Vaughan A.
        • et al.
        Human-to-Human Transmission of Monkeypox Virus.
        Emerg Infect Dis. October 2018; 26 (Apr. 2020): 782-785https://doi.org/10.3201/eid2604.191164
        View in Article
        • Thornhill J.P.
        • et al.
        Monkeypox Virus Infection in Humans across 16 Countries.
        New England Journal of Medicine. Aug. 2022; 387 (April–June 2022): 679-691https://doi.org/10.1056/NEJMoa2207323
        View in Article
        • Adler H.
        • et al.
        Clinical features and management of human monkeypox: a retrospective observational study in the UK.
        Lancet Infect Dis. Aug. 2022; 22: 1153-1162https://doi.org/10.1016/S1473-3099(22)00228-6
        View in Article
        • Nörz D.
        • et al.
        Evidence of surface contamination in hospital rooms occupied by patients infected with monkeypox.
        Eurosurveillance. June 2022; 27 (Jun. 2022)https://doi.org/10.2807/1560-7917.ES.2022.27.26.2200477
        View in Article
        • Atkinson B.
        • et al.
        Infection-competent monkeypox virus contamination identified in domestic settings following an imported case of monkeypox into the <scp>UK</scp>.
        Environ Microbiol. Oct. 2022; 24: 4561-4569https://doi.org/10.1111/1462-2920.16129
        View in Article
        • Gould S.
        • et al.
        Air and surface sampling for monkeypox virus in a UK hospital: an observational study.
        Lancet Microbe. Dec. 2022; 3: e904-e911https://doi.org/10.1016/S2666-5247(22)00257-9
        View in Article
        • Fennelly K.P.
        Particle sizes of infectious aerosols: implications for infection control.
        Lancet Respir Med. Sep. 2020; 8: 914-924https://doi.org/10.1016/S2213-2600(20)30323-4
        View in Article
        • Tiwari A.
        • et al.
        Monkeypox outbreak: Wastewater and environmental surveillance perspective.
        Science of The Total Environment. Jan. 2023; 856159166https://doi.org/10.1016/j.scitotenv.2022.159166
        View in Article

      Article info

      Publication history

      Accepted: March 7, 2023
      Received in revised form: March 7, 2023
      Received: December 21, 2022

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      DOI: https://doi.org/10.1016/j.ijid.2023.03.016

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