Rapid In-Vitro Inactivation of Various SARS-CoV-2 Strains Using Ionizing Radiation: New Inactivation Patterns and Mechanistic Insights

Wei Wang , Xiaodi Zhang , Jiageng Yu , Tianhao Weng , Zhiyang Yu , Zhigang Wu , Danrong Shi , Sufen Zhang , Xiangyun Lu , Osama Alam , Dahang Shen , Qian Bao , Qingfu Ye , Lanjuan Li , Hangping Yao

Engineering ›› 2025, Vol. 54 ›› Issue (11) : 202 -214.

PDF (4309KB)
Engineering ›› 2025, Vol. 54 ›› Issue (11) : 202 -214. DOI: 10.1016/j.eng.2025.09.009
Article

Rapid In-Vitro Inactivation of Various SARS-CoV-2 Strains Using Ionizing Radiation: New Inactivation Patterns and Mechanistic Insights

Author information +
History +
PDF (4309KB)

Abstract

Ionizing radiation presents an important solution for virus inactivation. However, its efficacy for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) inactivation and the underlying mechanisms remain unclear. This study demonstrates radiosensitivity and radiation-induced biological changes in SARS-CoV-2 using 20 wild-type and mutant strains. The results show that 1.2 kGy of electron beam (E-beam) or 0.9 kGy of X-ray irradiation can eliminate 99.99% of SARS-CoV-2 particles. The Delta and various Omicron variants exhibit heightened sensitivity to radiation compared to the wild-type, showing nearly 99.99 % inactivation efficiency at 1.0 and 0.8 kGy. The relationship between irradiation dose and the logarithmic reduction in virus load adheres to a dose–response model, characterized by extremely narrow windows. Spike (S) protein disruption, rather than the commonly accepted nucleic acid cleavage, is identified as the primary inactivation mechanism (triggering a conformation transition of S protein from pre-fusion to post-fusion with minimal impact on nucleic acid integrity). This study introduces the concept of targeting critical proteins in coronavirus inactivation, offering valuable insight for infectious coronavirus disease control and vaccine development.

Keywords

SARS-CoV-2 / Ionizing irradiation / Virus inactivation / Molecular mechanism / Spike (S) protein

Cite this article

Download citation ▾
Wei Wang, Xiaodi Zhang, Jiageng Yu, Tianhao Weng, Zhiyang Yu, Zhigang Wu, Danrong Shi, Sufen Zhang, Xiangyun Lu, Osama Alam, Dahang Shen, Qian Bao, Qingfu Ye, Lanjuan Li, Hangping Yao. Rapid In-Vitro Inactivation of Various SARS-CoV-2 Strains Using Ionizing Radiation: New Inactivation Patterns and Mechanistic Insights. Engineering, 2025, 54(11): 202-214 DOI:10.1016/j.eng.2025.09.009

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Chu DK, Akl EA, Duda S, Solo K, Yaacoub S, Schunemann HJ, et al.Physical distancing, face masks, and eye protection to prevent person-to-person transmission of SARS-CoV-2 and COVID-19: a systematic review and meta-analysis.Lancet 2020; 395(10242):1973-1987.

[2]

La G Rosa, Bonadonna L, Lucentini L, Kenmoe S, Suffredini E.Coronavirus in water environments: occurrence, persistence and concentration methods—a scoping review.Water Res 2020; 179:115899.

[3]

Ye G, Lin H, Chen S, Wang S, Zeng Z, Wang W, et al.Environmental contamination of SARS-CoV-2 in healthcare premises.J Infect 2020; 81(2):e1-e5.

[4]

Prather KA, Wang CC, Schooley RT.Reducing transmission of SARS-CoV-2.Science 2020; 368(6498):1422-1424.

[5]

Cheng Y, Ma N, Witt C, Rapp S, Wild PS, Andreae MO, et al.Face masks effectively limit the probability of SARS-CoV-2 transmission.Science 2021; 372(6549):1439-1443.

[6]

Yisimayi A, Song W, Wang J, Jian F, Yu Y, Chen X, et al.Repeated Omicron exposures override ancestral SARS-CoV-2 immune imprinting.Nature 2024; 625(7993):148-156.

[7]

Zhao Y, Shi L, Jiang Z, Zeng N, Mei H, Lu Y, et al.The phenotype and prediction of long-term physical, mental and cognitive COVID-19 sequelae 20 months after recovery, a community-based cohort study in China.Mol Psychiatry 2023; 28(4):1793-1801.

[8]

Davis HE, McCorkell L, Vogel JM, Topol EJ.Long COVID: major findings, mechanisms and recommendations.Nat Rev Microbiol 2023; 21(3):133-146.

[9]

Harvey WT, Carabelli AM, Jackson B, Gupta RK, Thomson EC, Harrison EM, et al.SARS-CoV-2 variants, spike mutations and immune escape.Nat Rev Microbiol 2021; 19(7):409-424.

[10]

Cai YF, Zhang J, Xiao TS, Peng HQ, Sterling SM, Walsh RM, et al.Distinct conformational states of SARS-CoV-2 spike protein.Science 2020; 369(6511):1586-1592.

[11]

Yao H, Song Y, Chen Y, Wu N, Xu J, Sun C, et al.Molecular architecture of the SARS-CoV-2 virus.Cell 2020; 183(3):730-738.

[12]

Schrad JR, Abrah JSão, Cortines JR, Parent KN.Structural and proteomic characterization of the initiation of giant virus infection.Cell 2020; 181:1046-1061.e1046.

[13]

Gaidamakova EK, Myles IA, McDaniel DP, Fowler CJ, Valdez PA, Naik S, et al.Preserving immunogenicity of lethally irradiated viral and bacterial vaccine epitopes using a radio-protective Mn2+-peptide complex from Deinococcus.Cell Host Microbe 2012; 12(1):117-124.

[14]

Han S, Roy PK, Hossain MI, Byun KH, Choi C, Ha SD.COVID-19 pandemic crisis and food safety: implications and inactivation strategies.Trends Food Sci Technol 2021; 109:25-36.

[15]

Liu Y, Shao Y, Wang L, Lu W, Li S, Xu D, et al.Inactivation of porcine epidemic diarrhea virus with electron beam irradiation under cold chain conditions.Environ Technol Innov 2022; 27:102715.

[16]

Sanglay GC, Li J, Uribe RM, Lee K.Electron-beam inactivation of a norovirus surrogate in fresh produce and model systems.J Food Prot 2011; 74(7):1155-1160.

[17]

Benítez JS, Rodríguez CM, Casas AF.Disinfection byproducts (DBPs) in drinking water supply systems: a systematic review.Phys Chem Earth Parts ABC 2021; 123:102987.

[18]

Durante M, Schulze K, Incert i S, Francis Z, Zein S, Guzmán CA.Virus irradiation and COVID-19 disease, front phys-lausanne. 2020;8:565861.

[19]

Ruetalo N, Businger R, Schindler M.Rapid, dose-dependent and efficient inactivation of surface dried SARS-CoV-2 by 254 nm UV-C irradiation.Euro Surveill 2021; 26(42):2001718.

[20]

Deng LZ, Mujumdar AS, Pan Z, Vidyarthi SK, Xu J, Zielinska M, et al.Emerging chemical and physical disinfection technologies of fruits and vegetables: a comprehensive review.Crit Rev Food Sci Nutr 2020; 60(15):2481-2508.

[21]

Zucker I, Lester Y, Alter J, Werbner M, Yecheskel Y, Gal-Tanamy M, et al.Pseudoviruses for the assessment of coronavirus disinfection by ozone.Environ Chem Lett 2021; 19(2):1779-1785.

[22]

Smith TP, Flaxman S, Gallinat AS, Kinosian SP, Stemkovski M, Unwin HJT, et al.Temperature and population density influence SARS-CoV-2 transmission in the absence of nonpharmaceutical interventions.PNAS 2021; 118(25):e2019284118.

[23]

He X, Liu X, Li P, Cheng H, Li W, Li B, et al.A multi-stage green barrier strategy for the control of global SARS-CoV-2 transmission via cold chain goods.Engineering 2021; 9:13-16.

[24]

Aboubakr HA, Sharafeldin TA, Goyal SM.Stability of SARS-CoV-2 and other coronaviruses in the environment and on common touch surfaces and the influence of climatic conditions: a review.Transbound Emerg Dis 2021; 68(2):296-312.

[25]

Chin AW, Chu JT, Perera MR, Hui KP, Yen HL, Chan MC, et al.Stability of SARS-CoV-2 in different environmental conditions.Lancet Microbe 2020; 1(1):e10.

[26]

Bhatia SS, Pillai SD.Ionizing radiation technologies for vaccine development—a mini review.Front Immunol 2022; 13:845514.

[27]

Arvanitoyannis IS, Stratakos A, Tsarouhas P.Irradiation applications in vegetables and fruits: a review.Crit Rev Food Sci Nutr 2009; 49(5):427-462.

[28]

Farkas J, Mohácsi-Farkas C.History and future of food irradiation.Trends Food Sci Technol 2011; 22(2–3):121-126.

[29]

Tian Y, Wang Z, Cao S, Liu D, Zhang Y, Chen C, et al.Connective tissue inspired elastomer-based hydrogel for artificial skin via radiation-indued penetrating polymerization.Nat Commun 2024; 15(1):636.

[30]

Hasanain F, Guenther K, Mullett WM, Craven E.Gamma sterilization of pharmaceuticals—a review of the irradiation of excipients, active pharmaceutical ingredients, and final drug product formulations.PDA J Pharm Sci Technol 2014; 68(2):113-137.

[31]

Morozov VN, Mukhin AN, Kolyvanova MA, Belousov AV, Bushmanov YA, Grebennikova TV, et al.Radiation inactivation of coronavirus infection pathogen by the example of transmissible gastroenteritis virus.Biophysics (Oxf) 2021; 66(4):589-595.

[32]

Roque J, Santos P, Margaca FMA, Caeiro MF, Cabo VS.Inactivation mechanisms of human adenovirus by E-beam irradiation in water environments.Appl Microbiol Biotechnol 2022; 106(9–10):3799-3809.

[33]

Brahmakshatriya V, Lupiani B, Brinlee JL, Cepeda M, Pillai SD, Reddy SM.Preliminary study for evaluation of avian influenza virus inactivation in contaminated poultry products using electron beam irradiation.Avian Pathol 2009; 38(3):245-250.

[34]

Praveen C, Jesudhasan PR, Reimers RS, Pillai SD.Electron beam inactivation of selected microbial pathogens and indicator organisms in aerobically and anaerobically digested sewage sludge.Bioresour Technol 2013; 144:652-657.

[35]

Jeong MI, Lee EJ, Park SY, Kim MR, Park SR, Moon Y, et al.Assessment of human norovirus inhibition in cabbage kimchi by electron beam irradiation using RT-qPCR combined with immunomagnetic separation.J Food Sci 2021; 86(2):505-512.

[36]

Feldmann F, Shupert WL, Haddock E, Twardoski B, Feldmann H.Gamma irradiation as an effective method for inactivation of emerging viral pathogens.Am J Trop Med Hyg 2019; 100(5):1275-1277.

[37]

Elliott LH, McCormick JB, Johnson KM.Inactivation of lassa, marburg, and ebola viruses by gamma irradiation.J Clin Microbiol 1982; 16(4):704-708.

[38]

Leung A, Tran K, Audet J, Lavineway S, Bastien N, Krishnan J.In vitro inactivation of SARS-CoV-2 using gamma radiation.Appl Biosaf 2020; 25(3):157-160.

[39]

Luo Z, Ni K, Zhou Y, Chang G, Yu J, Zhang C, et al.Inactivation of two SARS-CoV-2 virus surrogates by electron beam irradiation on large yellow croaker slices and their packaging surfaces.Food Control 2023; 144:109340.

[40]

Wang Z, Liang Z, Wei R, Wang H, Cheng F, Liu Y, et al.Quantitative determination of the electron beam radiation dose for SARS-CoV-2 inactivation to decontaminate frozen food packaging.Virol Sin 2022; 37(6):823-830.

[41]

Yao H, Lu X, Chen Q, Xu K, Chen Y, Cheng M, et al.Patient-derived SARS-CoV-2 mutations impact viral replication dynamics and infectivity in vitro and with clinical implications in vivo.Cell Discov 2020; 6(1):761.

[42]

Song Y, Yao H, Wu N, Xu J, Zhang Z, Peng C, et al.In situ architecture and membrane fusion of SARS-CoV-2 Delta variant.Proc Natl Acad Sci USA 2023; 120(18):e2213332120.

[43]

Tamura K, Stecher G, Kumar S.MEGA11: molecular evolutionary genetics analysis version 11.Mol Biol Evol 2021; 38(7):3022-3027.

[44]

Nguyen LT, Schmidt HA, von A Haeseler, Minh BQ.IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies.Mol Biol Evol 2015; 32(1):268-274.

[45]

Abolaban FA, Djouider FM.Gamma irradiation-mediated inactivation of enveloped viruses with conservation of genome integrity: potential application for SARS-CoV-2 inactivated vaccine development.Open Life Sci 2021; 16(1):558-570.

[46]

Liu KK, Shan CX.Viral inactivation by irradiation rays.Light Sci Appl 2023; 12(1):72.

[47]

Farkas J.Physical methods of food preservation.M. Doyle, L. Beuchat (Eds.), Food microbiology: fundamentals and frontiers (3rd ed.), ASM Press, Washington, DC 2007; 685-712.

[48]

Smolko EE, Lombardo JH.Virus inactivation studies using ion beams, electron and gamma irradiation.Nucl Instrum Methods Phys Res B 2005; 236(1–4):249-253.

[49]

Haddock E, Feldmann F, Shupert WL, Feldmann H.Inactivation of SARS-CoV-2 laboratory specimens.Am J Trop Med Hyg 2021; 104(6):2195-2198.

[50]

Kumar M, Mazur S, Ork BL, Postnikova E, Hensley LE, Jahrling PB, et al.Inactivation and safety testing of middle east respiratory syndrome coronavirus.J Virol Methods 2015; 223:13-18.

[51]

Wrapp D, Wang NS, Corbett KS, Goldsmith JA, Hsieh CL, Abiona O, et al.Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation.Science 2020; 367(6483):1260-1263.

[52]

Li F.Structure, function, and evolution of coronavirus spike proteins.Annu Rev Virol 2016; 3(1):237-261.

[53]

Huang Y, Yang C, Xu XF, Xu W, Liu SW.Structural and functional properties of SARS-CoV-2 spike protein: potential antivirus drug development for COVID-19.Acta Pharmacol Sin 2020; 41(9):1141-1149.

[54]

Cui T, Theuns S, Xie J, Van W den Broeck, Nauwynck HJ.Role of porcine aminopeptidase N and sialic acids in porcine coronavirus infections in primary porcine enterocytes.Viruses 2020; 12(4):402.

[55]

Walls AC, Park YJ, Tortorici MA, Wall A, McGuire AT, Veesler D.Structure, function, and antigenicity of the SARS-CoV-2 spike glycoprotein.Cell 2020; 181:281-292.

[56]

Zhang X, Wang F, Weng M, Cao M.Calculations of energy deposition and ionization in the 2019 novel coronavirus by electron beam irradiation.Radiat Phys Chem 2020; 177:109169.

[57]

Feng G, Liu L, Cui W, Wang F.Electron beam irradiation on novel coronavirus (COVID-19): a Monte–Carlo simulation.Chin Phys B 2020; 29(4):048703.

[58]

Chi X, Zhang X, Pan S, Yu Y, Shi Y, Lin T, et al.An ultrapotent RBD-targeted biparatopic nanobody neutralizes broad SARS-CoV-2 variants.Signal Transduct Target Ther 2022; 7(1):44.

[59]

Jung C, Kmiec D, Koepke L, Zech F, Jacob T, Sparrer KM, et al.Omicron: what makes the latest SARS-CoV-2 variant of concern so concerning?. J Virol, 96 (6) (2022)

[60]

Tao K, Tzou PL, Nouhin J, Gupta RK, de T Oliveira, Kosakovsky SL Pond, et al.The biological and clinical significance of emerging SARS-CoV-2 variants.Nat Rev Genet 2021; 22(12):757-773.

[61]

Rees-Spear C, Muir L, Griffith SA, Heaney J, Aldon Y, Snitselaar JL, et al.The effect of spike mutations on SARS-CoV-2 neutralization.Cell Rep 2021; 34(12):108890.

[62]

Elveborg S, Monteil VM, Mirazimi A.Methods of inactivation of highly pathogenic viruses for molecular, serology or vaccine development purposes.Pathogens 2022; 11(2):271.

[63]

Mykytyn AZ, Rissmann M, Kok A, Rosu ME, Schipper D, Breugem TI, et al.Antigenic cartography of SARS-CoV-2 reveals that Omicron BA.1 and BA.2 are antigenically distinct.Sci Immunol 2022; 7(75):eabq4450.

[64]

Wang Z, Li Z, Shi W, Zhu D, Hu S, Dinh PC, et al.A SARS-CoV-2 and influenza double hit vaccine based on RBD-conjugated inactivated influenza A virus.Sci Adv 2023; 9(25):eabo4100.

[65]

Toback S, Galiza E, Cosgrove C, Galloway J, Goodman AL, Swift PA, et al.Safety, immunogenicity, and efficacy of a COVID-19 vaccine (NVX-CoV2373) co-administered with seasonal influenza vaccines: an exploratory substudy of a randomised, observer-blinded, placebo-controlled, phase 3 trial.Lancet Respir Med 2022; 10(2):167-179.

[66]

Osunla A, Oloye F, Kayode A, Femi-Oloye O, Okiti A, Servos M, et al.The slow pandemic: emergence of antimicrobial resistance in the postadvent of SARS‐CoV‐2 pandemic.Glob Health Epidemiol Genom 2025; 2025(1):3172234.

AI Summary AI Mindmap
PDF (4309KB)

Supplementary files

Supplementary file for ENG-D-24-02010

9789

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/