Document Type : Original Article

Authors

1 Department of Environmental Health Engineering, School of Health, Shiraz University of Medical Sciences, Shiraz, Iran

2 Shiraz University of Medical Sciences, Shiraz, Iran

3 Department of Medicine, University of Alberta, Edmonton, AB, Canada

4 Department of Virology, Professor Alborzi Clinical Microbiology Research Center, Namazi Hospital, Shiraz University of Medical Sciences, Shiraz, Iran

5 Research Center for Health Sciences, Institute of Health, Department of Environmental Health Engineering, School of Health, Shiraz University of Medical Sciences, Shiraz, Iran

Abstract

Background: Coronavirus disease (COVID-19) is an immensely transmissible viral infectious disease caused by Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2). This study aimed to assess the presence of SARS-CoV-2 in the indoor air, on the surfaces, and on the fomites of a COVID-19 referral hospital in Shiraz, Iran.
Methods: In this cross-sectional study, indoor air sampling was conducted utilizing a standard midget impinger containing 15 ml of viral transfer medium (VTM) equipped with a sampling pump with a flow rate of 10 L min-1 for 60 minutes. Surfaces and fomites were sampled using sterile polyester swabs. The realtime reverse transcription-polymerase chain reaction (rRT-PCR) was utilized to detect SARS-CoV-2.
Results: The RNA of SARS-CoV-2 was detected in about 41.2% indoor air and 32% swab samples. Four out of the six (66.7%) indoor air samples up to a distance of 2 meters from the patient’s bed in intensive care units (ICU-1, ICU-3), accident and emergency (A&E-2), and negative pressure rooms were positive for SARS-CoV-2 RNA. All air samples within 2 to 5 meters of the patient’s bed were negative.
Conclusion: This study’s results did not support the airborne SARS-CoV-2 transmission; However, it showed contamination of surfaces and fomites in the studied hospital’s wards.

Keywords

  1. Andersen KG, Rambaut A, Lipkin WI, Holmes EC, Garry RF. The proximal origin of SARS-CoV-2. Nat Med. 2020;26(4):450-2. doi: 10.1038/s41591-020-0820-9. PubMed PMID: 32284615; PubMed Central PMCID: PMC7095063.
  2. Hu B, Guo H, Zhou P, Shi ZL. Characteristics of SARS-CoV-2 and COVID-19. Nat Rev Microbiol. 2021;19(3):141-54. doi: 10.1038/s41579-020-00459-7. PubMed PMID: 33024307; PubMed Central PMCID: PMC7537588.
  3. Sanche S, Lin YT, Xu C, Romero-Severson E, Hengartner N, Ke R. High Contagiousness and Rapid Spread of Severe Acute Respiratory Syndrome Coronavirus 2. Emerg Infect Dis. 2020;26(7):1470-7. doi: 10.3201/eid2607.200282. PubMed PMID: 32255761; PubMed Central PMCID: PMC7323562.
  4. Shakoor A, Chen X, Farooq TH, Shahzad U, Ashraf F, Rehman A, et al. Fluctuations in environmental pollutants and air quality during the lockdown in the USA and China: two sides of COVID-19 pandemic. Air Qual Atmos Health. 2020;13(11):1-8. doi: 10.1007/s11869-020-00888-6. PubMed PMID: 32837622; PubMed Central PMCID: PMC7415015.
  5. Abdool Karim SS, de Oliveira T. New SARS-CoV-2 Variants - Clinical, Public Health, and Vaccine Implications. N Engl J Med. 2021;384(19):1866-8. doi: 10.1056/NEJMc2100362. PubMed PMID: 33761203; PubMed Central PMCID: PMC8008749.
  6. Azimi SS, Koohi F, Aghaali M, Nikbakht R, Mahdavi M, Mokhayeri Y, et al. Estimation of the basic reproduction number (0) of the COVID-19 epidemic in Iran. Med J Islam Repub Iran. 2020;34:95. doi: 10.34171/mjiri.34.95. PubMed PMID: 33315980; PubMed Central PMCID: PMC7722950.
  7. Moreno T, Pinto RM, Bosch A, Moreno N, Alastuey A, Minguillon MC, et al. Tracing surface and airborne SARS-CoV-2 RNA inside public buses and subway trains. Environ Int. 2021;147:106326. doi: 10.1016/j.envint.2020.106326. PubMed PMID: 33340987; PubMed Central PMCID: PMC7723781.
  8. Naddafi K, Jabbari H, Hoseini M, Nabizade R, Rahbar M, Yunesian M. Investigation of indoor and outdoor air bacterial density in Tehran subway system. J Environ Health Sci Eng. 2011.
  9. The Lancet Respiratory M. COVID-19 transmission-up in the air. Lancet Respir Med. 2020;8(12):1159. doi: 10.1016/S2213-2600(20)30514-2. PubMed PMID: 33129420; PubMed Central PMCID: PMC7598535.
  10. Park JE, Jung S, Kim A, Park JE. MERS transmission and risk factors: a systematic review. BMC Public Health. 2018;18(1):574. doi: 10.1186/s12889-018-5484-8. PubMed PMID: 29716568; PubMed Central PMCID: PMC5930778.
  11. Bin SY, Heo JY, Song MS, Lee J, Kim EH, Park SJ, et al. Environmental Contamination and Viral Shedding in MERS Patients During MERS-CoV Outbreak in South Korea. Clin Infect Dis. 2016;62(6):755-60. doi: 10.1093/cid/civ1020. PubMed PMID: 26679623; PubMed Central PMCID: PMC7108026.
  12. Kim SH, Chang SY, Sung M, Park JH, Bin Kim H, Lee H, et al. Extensive Viable Middle East Respiratory Syndrome (MERS) Coronavirus Contamination in Air and Surrounding Environment in MERS Isolation Wards. Clin Infect Dis. 2016;63(3):363-9. doi: 10.1093/cid/ciw239. PubMed PMID: 27090992; PubMed Central PMCID: PMC7108054.
  13. World Health Organization. Investigation of cases of human infection with Middle East respiratory syndrome coronavirus (‎‎ MERS-CoV)‎‎: interim guidance. World Health Organization; June 2018.
  14. World Health Organization. Middle East respiratory syndrome coronavirus (MERS-CoV) 11 March 2019 [Available from: https://www.who.int/news-room/fact-sheets/detail/middle-east-respiratory-syndrome-coronavirus-(mers-cov).
  15. World Health Organization. Modes of transmission of virus causing COVID-19: implications for IPC precaution recommendations: scientific brief, 27 March 2020. World Health Organization; 2020.
  16. Setti L, Passarini F, De Gennaro G, Barbieri P, Perrone MG, Borelli M, et al. Airborne Transmission Route of COVID-19: Why 2 Meters/6 Feet of Inter-Personal Distance Could Not Be Enough. Int J Environ Res Public Health. 2020;17(8). doi: 10.3390/ijerph17082932. PubMed PMID: 32340347; PubMed Central PMCID: PMC7215485.
  17. Scientific Brief. SARS-CoV-2 and Potential Airborne Transmission. cdc. org. Updated Oct. 5, 2020
  18. Godri Pollitt KJ, Peccia J, Ko AI, Kaminski N, Dela Cruz CS, Nebert DW, et al. COVID-19 vulnerability: the potential impact of genetic susceptibility and airborne transmission. Hum Genomics. 2020;14(1):17. doi: 10.1186/s40246-020-00267-3. PubMed PMID: 32398162; PubMed Central PMCID: PMC7214856.
  19. Li Y, Huang X, Yu IT, Wong TW, Qian H. Role of air distribution in SARS transmission during the largest nosocomial outbreak in Hong Kong. Indoor Air. 2005;15(2):83-95. doi: 10.1111/j.1600-0668.2004.00317.x. PubMed PMID: 15737151.
  20. Booth TF, Kournikakis B, Bastien N, Ho J, Kobasa D, Stadnyk L, et al. Detection of airborne severe acute respiratory syndrome (SARS) coronavirus and environmental contamination in SARS outbreak units. J Infect Dis. 2005;191(9):1472-7. doi: 10.1086/429634. PubMed PMID: 15809906; PubMed Central PMCID: PMC7202477.
  21. Olsen SJ, Chang HL, Cheung TY, Tang AF, Fisk TL, Ooi SP, et al. Transmission of the severe acute respiratory syndrome on aircraft. N Engl J Med. 2003;349(25):2416-22. doi: 10.1056/NEJMoa031349. PubMed PMID: 14681507.
  22. Morawska L, Cao J. Airborne transmission of SARS-CoV-2: The world should face the reality. Environ Int. 2020;139:105730. PubMed PMID: 32294574; PubMed Central PMCID: PMC7151430.
  23. Zhang H, Li X, Ma R, Li X, Zhou Y, Dong H, et al. Airborne spread and infection of a novel swine-origin influenza A (H1N1) virus. Virol J. 2013;10(1):204. doi: 10.1186/1743-422X-10-204. PubMed PMID: 23800032; PubMed Central PMCID: PMC3700749.
  24. Setti L, Passarini F, De Gennaro G, Barbieri P, Perrone MG, Borelli M, et al. SARS-Cov-2RNA found on particulate matter of Bergamo in Northern Italy: First evidence. Environ Res. 2020;188:109754. doi: 10.1016/j.envres.2020.109754. PubMed PMID: 32526492; PubMed Central PMCID: PMC7260575.
  25. Liu Y, Ning Z, Chen Y, Guo M, Liu Y, Gali NK, et al. Aerodynamic analysis of SARS-CoV-2 in two Wuhan hospitals. Nature. 2020;582(7813):557-60. doi: 10.1038/s41586-020-2271-3. PubMed PMID: 32340022.
  26. Lednicky JA, Lauzardo M, Fan ZH, Jutla A, Tilly TB, Gangwar M, et al. Viable SARS-CoV-2 in the air of a hospital room with COVID-19 patients. Int J Infect Dis. 2020;100:476-82. doi: 10.1016/j.ijid.2020.09.025. PubMed PMID: 32949774; PubMed Central PMCID: PMC7493737.
  27. Li YH, Fan YZ, Jiang L, Wang HB. Aerosol and environmental surface monitoring for SARS-CoV-2 RNA in a designated hospital for severe COVID-19 patients. Epidemiol Infect. 2020;148:e154. doi: 10.1017/S0950268820001570. PubMed PMID: 32660668; PubMed Central PMCID: PMC7371847.
  28. Ong SWX, Tan YK, Chia PY, Lee TH, Ng OT, Wong MSY, et al. Air, Surface Environmental, and Personal Protective Equipment Contamination by Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) From a Symptomatic Patient. JAMA. 2020;323(16):1610-2. doi: 10.1001/jama.2020.3227. PubMed PMID: 32129805; PubMed Central PMCID: PMC7057172.
  29. Faridi S, Niazi S, Sadeghi K, Naddafi K, Yavarian J, Shamsipour M, et al. A field indoor air measurement of SARS-CoV-2 in the patient rooms of the largest hospital in Iran. Sci Total Environ. 2020;725:138401. doi: 10.1016/j.scitotenv.2020.138401. PubMed PMID: 32283308; PubMed Central PMCID: PMC7194859.
  30. Tabatabaeizadeh SA. Airborne transmission of COVID-19 and the role of face mask to prevent it: a systematic review and meta-analysis. Eur J Med Res. 2021;26(1):1. doi: 10.1186/s40001-020-00475-6. PubMed PMID: 33388089; PubMed Central PMCID: PMC7776300.
  31. Wilson NM, Norton A, Young FP, Collins DW. Airborne transmission of severe acute respiratory syndrome coronavirus-2 to healthcare workers: a narrative review. Anaesthesia. 2020;75(8):1086-95. doi: 10.1111/anae.15093. PubMed PMID: 32311771; PubMed Central PMCID: PMC7264768.
  32. Ram K, Thakur RC, Singh DK, Kawamura K, Shimouchi A, Sekine Y, et al. Why airborne transmission hasn't been conclusive in case of COVID-19? An atmospheric science perspective. Sci Total Environ. 2021;773:145525. doi: 10.1016/j.scitotenv.2021.145525. PubMed PMID: 33940729; PubMed Central PMCID: PMC7984961.
  33. Jaafari J, Dehghani MH, Hoseini M, Safari GH. Investigation of hospital solid waste management in Iran. World Review of Science, Technology and Sustainable Development. 2015;12(2):111-25. doi: 10.1504/WRSTSD.2015.073820.
  34. Bahl P, Doolan C, de Silva C, Chughtai AA, Bourouiba L, MacIntyre CR. Airborne or droplet precautions for health workers treating COVID-19? J Infect Dis. 2020. doi: 10.1093/infdis/jiaa189. PubMed PMID: 32301491; PubMed Central PMCID: PMC7184471.
  35. Adams JG, Walls RM. Supporting the Health Care Workforce During the COVID-19 Global Epidemic. JAMA. 2020;323(15):1439-40. doi: 10.1001/jama.2020.3972. PubMed PMID: 32163102.
  36. Sim MR. The COVID-19 pandemic: major risks to healthcare and other workers on the front line. Occup Environ Med. 2020;77(5):281-2. doi: 10.1136/oemed-2020-106567. PubMed PMID: 32238444.
  37. Nguyen LH, Drew DA, Graham MS, Joshi AD, Guo C-G, Ma W, et al. Risk of COVID-19 among front-line health-care workers and the general community: a prospective cohort study. Lancet Glob Health. 2020;5(9):e475-e83. doi: 10.1016/s2468-2667(20)30164-x. PubMed PMID: 32745512; PubMed Central PMCID: PMC7491202.
  38. Pourdowlat G, Panahi P, Pooransari P, Ghorbani F. Prophylactic recommendation for healthcare workers in COVID-19 pandemic. Front Med. 2020;4(2s):e39-e.
  39. Gharehchahi E, Mahvi AH, Amini H, Nabizadeh R, Akhlaghi AA, Shamsipour M, et al. Health impact assessment of air pollution in Shiraz, Iran: a two-part study. J Environ Health Sci Eng. 2013;11(1):11. doi: 10.1186/2052-336X-11-11. PubMed PMID: 24499576; PubMed Central PMCID: PMC3776287.
  40. Shahsavani S, Hoseini M, Dehghani M, Fararouei M. Characterisation and potential source identification of polycyclic aromatic hydrocarbons in atmospheric particles (PM10) from urban and suburban residential areas in Shiraz, Iran. Chemosphere. 2017;183:557-64. doi: 10.1016/j.chemosphere.2017.05.101. PubMed PMID: 28570899.
  41. Dart A, Thornburg J. Collection efficiencies of bioaerosol impingers for virus-containing aerosols. Atmos Environt. 2008;42(4):828-32. doi: 10.1016/j.atmosenv.2007.11.003.
  42. Verreault D, Moineau S, Duchaine C. Methods for sampling of airborne viruses. Microbiol Mol Biol Rev. 2008;72(3):413-44. doi: 10.1128/MMBR.00002-08. PubMed PMID: 18772283; PubMed Central PMCID: PMC2546863.
  43. Vosoughi M, Karami C, Dargahi A, Jeddi F, Jalali KM, Hadisi A, et al. Investigation of SARS-CoV-2 in hospital indoor air of COVID-19 patients' ward with impinger method. Environ Sci Pollut Res Int. 2021;28(36):50480-8. doi: 10.1007/s11356-021-14260-3. PubMed PMID: 33956316; PubMed Central PMCID: PMC8100364.
  44. Lin X, Willeke K, Ulevicius V, Grinshpun SA. Effect of sampling time on the collection efficiency of all-glass impingers. Am Ind Hyg. 1997;58(7):480-8. doi: 10.1080/15428119791012577.
  45. Campisano R, Hall K, Griggs J, Willison S, Reimer S, Mash H, et al. Selected analytical methods for environmental remediation and recovery (SAM) 2017. US Environmental Protection Agency, Washington, DC. 2017.
  46. World Health Organization. Surface sampling of coronavirus disease (‎ COVID-19)‎: a practical “how to” protocol for health care and public health professionals. World Health Organization; 2020.
  47. COVID LabCorp. RT-PCR test EUA Summary. Accelerated Emergency Use Authorization (EUA) Summary COVID-19 RT-PCR Test (Laboratory Corporation of America) Available online: www fda gov (accessed on 20 March 2020).
  48. World Health Organization. Laboratory testing for coronavirus disease 2019 (COVID-19) in suspected human cases: interim guidance, 2 March 2020. World Health Organization; 2020.
  49. Rao SN, Manissero D, Steele VR, Pareja J. A Systematic Review of the Clinical Utility of Cycle Threshold Values in the Context of COVID-19. Infect Dis Ther. 2020;9(3):573-86. doi: 10.1007/s40121-020-00324-3. PubMed PMID: 32725536; PubMed Central PMCID: PMC7386165.
  50. Karami C, Normohammadi A, Dargahi A, Vosoughi M, Zandian H, Jeddi F, et al. Investigation of SARS-CoV-2 virus on nozzle surfaces of fuel supply stations in North West of Iran. Sci Total Environ. 2021;780:146641. doi: 10.1016/j.scitotenv.2021.146641. PubMed PMID: 34030290; PubMed Central PMCID: PMC7981268.
  51. Somsen GA, van Rijn C, Kooij S, Bem RA, Bonn D. Small droplet aerosols in poorly ventilated spaces and SARS-CoV-2 transmission. Lancet Respir Med. 2020;8(7):658-9. doi: 10.1016/S2213-2600(20)30245-9. PubMed PMID: 32473123; PubMed Central PMCID: PMC7255254.
  52. Jayaweera M, Perera H, Gunawardana B, Manatunge J. Transmission of COVID-19 virus by droplets and aerosols: A critical review on the unresolved dichotomy. Environ Res. 2020;188:109819. doi: 10.1016/j.envres.2020.109819. PubMed PMID: 32569870; PubMed Central PMCID: PMC7293495.
  53. Chartier Y, Pessoa-Silva C. Natural ventilation for infection control in health-care settings. 2009.
  54. Nissen K, Krambrich J, Akaberi D, Hoffman T, Ling J, Lundkvist A, et al. Long-distance airborne dispersal of SARS-CoV-2 in COVID-19 wards. Sci Rep. 2020;10(1):19589. doi: 10.1038/s41598-020-76442-2. PubMed PMID: 33177563; PubMed Central PMCID: PMC7659316.
  55. Santarpia JL, Rivera DN, Herrera V, Morwitzer MJ, Creager H, Santarpia GW, et al. Transmission potential of SARS-CoV-2 in viral shedding observed at the University of Nebraska Medical Center. MedRxIV. 2020. doi: 10.1101/2020.03.23.20039446.
  56. Razzini K, Castrica M, Menchetti L, Maggi L, Negroni L, Orfeo NV, et al. SARS-CoV-2 RNA detection in the air and on surfaces in the COVID-19 ward of a hospital in Milan, Italy. Sci Total Environ. 2020;742:140540. doi: 10.1016/j.scitotenv.2020.140540. PubMed PMID: 32619843; PubMed Central PMCID: PMC7319646.
  57. Asadi S, Bouvier N, Wexler AS, Ristenpart WD. The coronavirus pandemic and aerosols: Does COVID-19 transmit via expiratory particles? Aerosol Sci Technol. 2020;0(0):1-4. doi: 10.1080/02786826.2020.1749229. PubMed PMID: 32308568; PubMed Central PMCID: PMC7157964.
  58. Stadnytskyi V, Bax CE, Bax A, Anfinrud P. The airborne lifetime of small speech droplets and their potential importance in SARS-CoV-2 transmission. Proc Natl Acad Sci U S A. 2020;117(22):11875-7. doi: 10.1073/pnas.2006874117. PubMed PMID: 32404416; PubMed Central PMCID: PMC7275719.
  59. Delikhoon M, Guzman MI, Nabizadeh R, Norouzian Baghani A. Modes of Transmission of Severe Acute Respiratory Syndrome-Coronavirus-2 (SARS-CoV-2) and Factors Influencing on the Airborne Transmission: A Review. Int J Environ Res Public Health. 2021;18(2):395. doi: 10.3390/ijerph18020395. PubMed PMID: 33419142; PubMed Central PMCID: PMC7825517.
  60. Ahlawat A, Wiedensohler A, Mishra SK. An Overview on the role of relative humidity in airborne transmission of SARS-CoV-2 in indoor environments. Aerosol Air Qual Res. 2020;20(9):1856-61. doi: 10.4209/aaqr.2020.06.0302
  61. Shahzad F, Shahzad U, Fareed Z, Iqbal N, Hashmi SH, Ahmad F. Asymmetric nexus between temperature and COVID-19 in the top ten affected provinces of China: A current application of quantile-on-quantile approach. Sci Total Environ. 2020;736:139115. doi: 10.1016/j.scitotenv.2020.139115. PubMed PMID: 32470687; PubMed Central PMCID: PMC7194057.
  62. Dogan B, Ben Jebli M, Shahzad K, Farooq TH, Shahzad U. Investigating the Effects of Meteorological Parameters on COVID-19: Case Study of New Jersey, United States. Environ Res. 2020;191:110148. doi: 10.1016/j.envres.2020.110148. PubMed PMID: 32877703; PubMed Central PMCID: PMC7456582.
  63. Iqbal N, Fareed Z, Shahzad F, He X, Shahzad U, Lina M. The nexus between COVID-19, temperature and exchange rate in Wuhan city: New findings from partial and multiple wavelet coherence. Sci Total Environ. 2020;729:138916. doi: 10.1016/j.scitotenv.2020.138916. PubMed PMID: 32388129; PubMed Central PMCID: PMC7194511.
  64. Yao Y, Pan J, Liu Z, Meng X, Wang W, Kan H, et al. No association of COVID-19 transmission with temperature or UV radiation in Chinese cities. European Respiratory Journal. 2020;55(5). doi: 10.1183/13993003.00517-2020. PubMed PMID: 32269084; PubMed Central PMCID: PMC7144256.
  65. He Z, Chin Y, Yu S, Huang J, Zhang CJP, Zhu K, et al. The Influence of Average Temperature and Relative Humidity on New Cases of COVID-19: Time-Series Analysis. JMIR Public Health Surveill. 2021;7(1):e20495. doi: 10.2196/20495. PubMed PMID: 33232262; PubMed Central PMCID: PMC7836910.
  66. Wang J, Tang K, Feng K, Lin X, Lv W, Chen K, et al. Impact of temperature and relative humidity on the transmission of COVID-19: a modelling study in China and the United States. BMJ Open. 2021;11(2):e043863. doi: 10.1136/bmjopen-2020-043863. PubMed PMID: 33597143; PubMed Central PMCID: PMC7893211.
  67. Sepulcri C, Dentone C, Mikulska M, Bruzzone B, Lai A, Fenoglio D, et al. The longest persistence of viable SARS-CoV-2 with recurrence of viremia and relapsing symptomatic COVID-19 in an immunocompromised patient – a case study. medRxiv. 2021:2021.01.23.21249554. doi: 10.1101/2021.01.23.21249554.
  68. Hu X, Ni W, Wang Z, Ma G, Pan B, Dong L, et al. The distribution of SARS-CoV-2 contamination on the environmental surfaces during incubation period of COVID-19 patients. Ecotoxicol Environ Saf. 2021;208:111438. doi: 10.1016/j.ecoenv.2020.111438. PubMed PMID: 33039873; PubMed Central PMCID: PMC7526608.
  69. Dargahi A, Jeddi F, Vosoughi M, Karami C, Hadisi A, Ahamad Mokhtari S, et al. Investigation of SARS CoV-2 virus in environmental surface. Environ Res. 2021;195:110765. doi: 10.1016/j.envres.2021.110765. PubMed PMID: 33497684; PubMed Central PMCID: PMC7826054.
  70. Wan B, Zhang X, Luo D, Zhang T, Chen X, Yao Y, et al. On-site analysis of COVID-19 on the surfaces in wards. Sci Total Environ. 2021;753:141758. doi: 10.1016/j.scitotenv.2020.141758. PubMed PMID: 32898806; PubMed Central PMCID: PMC7434306.
  71. Dargahi A, Jeddi F, Ghobadi H, Vosoughi M, Karami C, Sarailoo M, et al. Evaluation of masks' internal and external surfaces used by health care workers and patients in coronavirus-2 (SARS-CoV-2) wards. Environ Res. 2021;196:110948. doi: 10.1016/j.envres.2021.110948. PubMed PMID: 33684411; PubMed Central PMCID: PMC7935683.
  72. Aydogdu MO, Altun E, Chung E, Ren G, Homer-Vanniasinkam S, Chen B, et al. Surface interactions and viability of coronaviruses. J R Soc Interface. 2021;18(174):20200798. doi: 10.1098/rsif.2020.0798. PubMed PMID: 33402019; PubMed Central PMCID: PMC7879773.
  73. Shahzad K, Shahzad U, Iqbal N, Shahzad F, Fareed Z. Effects of climatological parameters on the outbreak spread of COVID-19 in highly affected regions of Spain. Environ Sci Pollut Res Int. 2020;27(31):39657-66. doi: 10.1007/s11356-020-10551-3. PubMed PMID: 32827296; PubMed Central PMCID: PMC7442890.
  74. Riddell S, Goldie S, Hill A, Eagles D, Drew TW. The effect of temperature on persistence of SARS-CoV-2 on common surfaces. Virol J. 2020;17(1):145. doi: 10.1186/s12985-020-01418-7. PubMed PMID: 33028356; PubMed Central PMCID: PMC7538848.
  75. Fareed Z, Iqbal N, Shahzad F, Shah SGM, Zulfiqar B, Shahzad K, et al. Co-variance nexus between COVID-19 mortality, humidity, and air quality index in Wuhan, China: New insights from partial and multiple wavelet coherence. Air Qual Atmos Health. 2020;13:673-82. doi: 10.1007/s11869-020-00847-1. PubMed PMID: 32837610; PubMed Central PMCID: PMC7279636.
  76. Biryukov J, Boydston J, Dunning R, Yeager J, Wood S, Reese A, et al. Increasing temperature and relative humidity accelerates inactivation of SARS-CoV-2 on surfaces. mSphere. 2020;5(4). doi: 10.1128/mSphere.00441-20. PubMed PMID: 32611701; PubMed Central PMCID: PMC7333574.
  77. Chin A, Chu J, Perera M, Hui K, Yen H-L, Chan M, et al. Stability of SARS-CoV-2 in different environmental conditions. medRxiv. 2020.
  78. van Doremalen N, Bushmaker T, Morris DH, Holbrook MG, Gamble A, Williamson BN, et al. Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1. N Engl J Med. 2020;382(16):1564-7. doi: 10.1056/NEJMc2004973. PubMed PMID: 32182409; PubMed Central PMCID: PMC7121658.
  79. Harvey AP, Fuhrmeister ER, Cantrell ME, Pitol AK, Swarthout JM, Powers JE, et al. Longitudinal Monitoring of SARS-CoV-2 RNA on High-Touch Surfaces in a Community Setting. Environ Sci Technol Lett. 2021;8(2):168-75. doi: 10.1021/acs.estlett.0c00875. PubMed PMID: 34192125; PubMed Central PMCID: PMC7927285.
  80. Centers for Disease Control Prevention. Science brief: SARS-CoV-2 and surface (fomite) transmission for indoor community environments. Updated Apr; 2021
  81. World Health Organization. Transmission of SARS-CoV-2: implications for infection prevention precautions: scientific brief, 09 July 2020. World Health Organization; 2020.