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. 2024 Nov 22;103(47):e40341. doi: 10.1097/MD.0000000000040341

Inactivation of β-coronavirus MHV-A59 by 2.8 GHz microwave

Yi Xiao a, Ruiyun Peng a, Haoyu Wang a, Hui Wang a, Ji Dong a, Kehui Wang b, Wei Liu b, Li Zhao a,*
PMCID: PMC11596339  PMID: 39809214

Abstract

From the severe acute respiratory syndrome coronavirus in 2003 to the severe acute respiratory syndrome coronavirus 2 in 2019, coronavirus has seriously threatened human health. Electromagnetic waves not only own high penetration and low pollution but also can physically resonate with the virus. Several studies have demonstrated that electromagnetic waves can inactivate viruses efficiently. However, there is still a lack of systemic studies to analyze the potential factors closely associated with the effectiveness of inactivation, such as pH, temperature, and so on. In this study, we evaluated the inactivation ability of a 2.8 GHz microwave (MW) on MHV-A59, a substitute virus for coronavirus. Moreover, the influences of environmental pH and temperature on inactivation abilities were also discussed. The results showed that the viral morphology was destroyed, and the infectivity of MHV-A59 was significantly decreased after exposure to a 2.8 GHz MW at a density of 100 mW/cm2. Furthermore, alteration of pH 8 could produce synergistic effects with MW on virus inactivation. And, it was also proved that MWs could inactivate viruses better at room temperature than that under lower environmental temperatures. These results suggested that electromagnetic wave has great promise to become an effective tool to eliminate coronavirus.

Keywords: coronavirus, infectivity, microwave, morphology, pH, temperature

1. Introduction

Coronaviruses are the largest RNA envelope viruses and can infect a variety of animal hosts, including humans, causing respiratory or intestinal infections.[1–4] In past decades, coronavirus has been becoming a serious public safety concern, with the outbreak of severe acute respiratory syndrome coronavirus (SARS-CoV) in 2003,[5–7] middle east respiratory syndrome coronavirus in 2012,[8,9] as well as the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in 2019.[10,11] Until December 16, 2023, 772,385,305 people were diagnosed with SARS-CoV-2 infection and 6987,209 people died from SARS-CoV-2 infection worldwide.[12] SARS-CoV-2 and other coronavirus spread quickly and have strong mutation ability. These properties enable the coronavirus to survive stably in both the host and the environment. Importantly, coronaviruses, such as SARS-CoV, MERS-CoV, and SARS-CoV-2, own high morbidity and mortality in human beings.[13–17] Therefore, it is urgent to develop efficient virus inactivation technologies to prevent the spread of viral spread and infection.

Some properties of traditional viral inactivation technologies, such as poor penetration of ultraviolet, environmental pollution of chemical disinfectants and ozone, and high cause of ionizing radiation, limited their application in the virus inactivation of coronaviruses.[18–23] The electromagnetic wave owns features of high penetration, low pollution, and uniform radiation, and they also can physically resonate with viruses.[18,24–30] In this paper, microwave (MW) is used to kill the coronavirus in order to provide new insight or reference for the inactivation of coronavirus.

MHV-A59 is an enveloped positive-strand RNA virus belonging to the coronavirus, β-coronavirus family and it has a similar structure to SARS-CoV-2.[31,32] S-band electromagnetic wave is a common electromagnetic wave frequency in daily life. In this study, we evaluated the virus inactivation effect of 2.8 GHz and 100 mW/cm2 MW on MHV-A59. And, the influence of environmental factors, such as pH and temperature on virus inactivation effects were also analyzed. These findings suggested that 2.8 GHz electromagnetic waves might be an effective tool for coronavirus inactivation.

2. Methods

2.1. Cell culture and MHV-A59 propagation

17CL-1 cells and MHV-A59 were a gift from Wei Liu, the director of the Center for Disease Control and Prevention of PLA. 17CL-1 cells were grown in Dulbecco modified eagle medium (122448, Gibco, Waltham, MA) supplemented with 10% fetal bovine serum (10099-141, Gibco, Waltham, MA), and 1% penicillin–streptomycin solution (SV30010, HyClone, Pasching, Austria) at 37 °C, 5% CO2. To prepare MHV-A59, 17CL-1 cells confluently grown in 75 cm2 flasks. When the cells confluent to 90% to 100%, MHV-A59 virus was used for infection at 37 °C in a 5 % CO2. When the cytopathic effect (CPE) of the inoculated cells reached 75%, the viral supernatant was harvested. Then the virus was filtered by a 0.22 μm filtration membrane (SLGPR33RB, Mllex-GP, Darmstadt, Germany), and the virus supernatant was separated and stored at −80 °C.

2.2. MW wave exposure system

The MW radiation system has been described in previous studies.[33,34] Briefly, it is based on a Klystron amplifier model JD 2000 (Vacuum Electronics Research Institute, Beijing, China), and can produce a frequency of 2.8 GHz with a peak power density of 470 W/cm2, the pulse width is 500 ns and the average power density is 100 mW/cm2. MW energy is transmitted through rectangular waveguides and A16-dB standard-gain horn antennas to the electromagnetic shielding chamber, which is covered with 500 mm and 300 mm pyramid MW absorbers to reduce reflection. The MW radiation parameters used in this study were 2.8 GHz, 100 mW/cm2, the MHV-A59 was placed in the center of the radiation platform, and the distances between the antenna and the virus culture dish was 70 cm. The sham group received the same treatment, but the MW radiation source was turned off.

2.3. Viral infectivity analysis

The virus titer was determined using Median Tissue Culture Infective Dose Assay (TCID50). Briefly, 17CL-1 cells were seeded at a density of 1 × 104/100 μL/well in 96-well plates. 24 hours later, when 17CL-1 cells confluent to 90% to 100%, MHV-A59 suspension was serial diluted 10-fold by cell culture medium containing 5% fetal bovine serum, and then 200 µL serial diluted MHV-A59 suspension was added to 4 wells and incubated in 37 °C and 5% CO2 incubators for another 24 hours. The virus-induced CPE was counted, and the TCID50 was calculated by the Reed–Muench method. When the cell culture medium containing MHV-A59 was passaged 3 times, no CPE was found and the virus was considered to be completely inactivated.

2.4. Stability of MHV-A59 at room temperature

The air-conditioning temperature was set to 20 °C in an airtight room and the environmental temperature was confirmed 3 hours later. MHV-A59 was grouped into groups and placed in this environment for 15 and 30 minutes, with no treatment in the 0 minutes group, with 5 replicates per group. Then, the TCID50 was performed to assess the stability of the virus at room temperature.

2.5. Virus inactivation by MW radiation under different pH

Virus suspensions with pH of 2.0, 4.0, 8.0, and 12.0 were prepared using 3% hydrochloric acid (7647-01-0, Sinopharm Chemical Reagent Co., Ltd., Shanghai, China), 0.1 M/L sodium citrate (10007118, Sinopharm Chemical Reagent Co., Ltd., Shanghai, China), 0.2 M/L disodium hydrogen phosphate (D7292, Solarbio, China), and 0.5 M/L sodium hydroxide (1310-73-2, Sinopharm chemical reagent Co., Ltd., Shanghai, China). All prepared pH gradient viral samples (pH 2, 4, 8, and 12) were subjected to pH determination by a Pen pH meter (SANXIN, SX-610, China), and a repeated measure was conducted precisely at 24 hours after preparation, which was sealed and stored at 4 °C refrigerator to confirm the stability of the virus environment pH and virus infectivity. Firstly, the survival of the virus at different pH conditions was analyzed. Secondly, virus suspensions with different pH (n = 5) were exposed to MW radiation for 30 minutes to evaluate the effect of MW on virus inactivation, using sterile deionized water as control. The sham group received the same treatment at the same location for 30 minutes, but the MW source was turned off. Finally, viral suspensions were neutralized immediately after MW radiation, and the virus infectivity was analyzed by TCID50.

2.6. Virus inactivation by MW radiation under different temperatures

The viruses have divided the virus into 35 mm dishes with 1 mL each. They were divided into 4 groups, ice treated group, dry ice-treated group, room temperature group, and sham group. The virus sample in the ice-treated group and the dry ice-treated group were precooled in a foam box containing 1 kg ice and 500 g dry ice for 2 hours, respectively. MW-treated groups were radiated for 30 minutes by MW exposure system. In addition, an optical fiber system (THR-NC-1084C, FISO, CA) (Section 2.7) and portable digital thermometers (ALCBIO, ALC-ET, China) were used to real time monitor the temperature of the MHV-A59 culture medium during MW radiation. However, the dry ice-treated group was frozen for 10 minutes from the beginning of precooling to the end of radiation, which limited the measurement of temperature. Therefore, the temperature is tentatively set at 0 °C in this study. Finally, all viruses were tested for viral infectivity by TCID50.

2.7. Temperature measurement by optical fiber thermometer

During MW radiation, the temperature of the MHV-A59 medium was detected in real time by an optical fiber thermometer. Briefly, a 1 mm diameter hole was drilled at 5 mm of the top edge of the 35 mm Petri dish cover and put into the MW radiation room 4 hours earlier to eliminate the effect of room temperature on the temperature of the virus medium. Then the virus culture dish was fixed on the center of the MW radiation platform, and the metal-free optical fiber thermometer sensor was inserted into the base of the virus culture medium along the hole, and connected to the power supply for real-time temperature measurement. Temperature data are transmitted through optical fibers and recorded before, during, and after MW exposure.

2.8. Transmission electron microscopy

The morphology of MHV-A59 was detected by transmission electron microscopy (TEM) (HITACHI 7800, Japan) after negative staining. Briefly, samples of MHV-A59 were treated with 3% glutaraldehyde for 3 minutes. Then, 20 µL of MHV-A59 were dropped onto 200 mesh copper wire, and the virus suspension was removed with filter paper after 10 minutes. The samples were stained with 3% phosphotungstic acid for 2 to 3 minutes and the morphology was observed under TEM.

2.9. Statistical analysis

The data were expressed as mean ± standard deviation (x¯±s). SPSS software 25 was used for data analysis, and between-group differences were analyzed by one-way ANOVA with LSD test to compare differences between the 2 groups. A factorial design was used to analyze the effects of the other 2 factors. The P value of <.05 was considered statistically significant.

3. Results

3.1. The infectivity of the virus was stable at 20 °C for 30 minutes

To assess the stability of coronaviruses at room temperature, we exposed MHV-A59 to a 20 °C environment for 15 and 30 minutes. The infectivity of MHV-A59 was detected by TCID50 (Fig. 1A), and the morphology of infected cells was observed by microscope at 24 hours after MHV-A59 infection (Fig. 1B). Not hard to find, MHV-A59 maintains the infectivity after exposure to a 20 °C environment for 15 and 30 minutes. These results suggest that the infectivity of MHV-A59 was not affected after exposure to a 20 °C environment for 30 minutes.

Figure 1.

Figure 1.

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Infection infectivity of MHV-A59 after exposure to 20 °C environment. (A) MHV-A59 titers (20 °C, n = 5). (B) Morphological characteristics of 17CL-1 cells at serial dilutions at 24 hours after infections (scale bars = 50 μm). A one-way analysis of variance followed by LSD correction was used to compare multiple groups. NS = nonsignificant (P > .05).

3.2. MW radiation for 30 minutes damaged the infectivity and morphology of MHV-A59

To test the inactivation effect of MWs on MHV-A59, a specific MW radiation system was established, in which the MHV-A59 was placed in the center of the MW radiation platform (Fig. 2A). Our results showed that MW exposure for 30 minutes significantly decreased the virus infectivity (P < .05), but not for 15 minutes (Fig. 2B). Moreover, obvious virus morphological changes could be observed by TEM (Fig. 2C). Generally, part of the MHV-A59 envelope was damaged and the structure became incomplete after MW radiation for 15 and 30 minutes. Taken together, these data suggest that MWs can inactivate MHV-A59 and might though destructing the envelope of MHV-A59.

Figure 2.

Figure 2.

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Microwave exposure decreases the infectivity and damages the morphology of MHV-A59. (A) Microwave radiation schematic. (B) Changes of MHV-A59 infectivity after microwave exposure for different times (n = 5). (C) Morphological changes of the MHV-A59 before and after microwave exposure. One-way analysis of variance followed by LSD correction was used to compare multiple groups. *P < .05.

3.3. Slight pH alteration of virus suspensions to 8.0 enhance the sensitivity of MHV-A59 to MW radiation

The growth environments are critical for the survival and propagation of viruses. Here, we analyzed the influence of the pH of the virus culture medium on the virus inactivation ability of the 2.8 GHz MW. MHV-A59 at different pH conditions was prepared 24 hours before MW exposure and stored at 4 °C (Fig. 3A). Immediately after exposure to the MW for 30 minutes, the pH of virus suspensions was monitored both before and immediately after MW radiation (Fig. 3B). And, the virus suspensions with different pH were neutralized before TCID50 analysis. Our results showed that the infectivity of MHV-A59 decreased significantly after MW radiation at different pH (P < .001, Fig. 3C). In highly acidic solutions and highly alkaline solutions, the infectivity of MHV-A59 was reduced even without MW exposure. For example, the titers of MHV-A59 were decreased by 3 to 4 lgTCID50/0.2 mL at pH 2.0, and completely inactivated at pH 12 (P < .001). However, no significant alteration could be observed at pH 4.0 and 8.0 (Fig. 3C). Interestingly, a slight alteration of pH to 8.0 did not decrease the virus activation but enhanced the sensitivity of virus suspension to MW (P < .05, Fig. 3C). These results suggested that a slight alteration of the pH to 8.0 produced a synergistic effect with MW exposure on virus inactivation (P < .05, Fig. 3C). In conclusion, the effects of MWs on virus inactivation are closely related to the pH of virus suspensions.

Figure 3.

Figure 3.

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Slight pH alteration to 8.0 enhances the sensitivity of MHV-A59 to microwave radiation. (A) Schematic diagram of virus preparation process with different pH. (B) The changes in pH value of virus suspension with different pH gradients 24 hours before radiation and immediately after radiation (n = 5). (C) Changes of infectivity of MHV-A59 after exposure to microwave at different pH (n = 5). Factorial design is used to analyze the interaction between 2 factors. One-way analysis of variance followed by LSD correction was used to compare multiple groups (***, comparison with Sham group, P < .001; ###, comparison with pH group, P < .001; +++, comparison with MW group, P < .001).

3.4. The effect of MW on virus inactivation at room temperature is better than that at a lower temperature

To analyze the influence of environmental temperature on the virus inactivation by MW radiation, the MHV-A59 suspensions were treated with ice and dry ice, and then MHV-A59 suspensions with different temperatures were exposed to MW (Fig. 4A and B). Our data showed that MW radiation significantly decreased MHV-A59 infectivity (P < .001, Fig. 4C and E) for 30 minutes at 20 °C. However, the infectivity of MHV-A59 in ice and dry-ice-treated groups is much stronger, suggesting lower temperature reduced the virus inactivation ability by 2.8 GHz MW (Fig. 4D and E). We also monitored the temperature of virus suspensions during MW radiation (Fig. 4F). Our results showed that an increase of 17.51 °C was observed for room temperature samples (Fig. 4F and G), and the temperature of ice-cooling samples raised from 3.5 °C before radiation to 4.5 °C immediately after exposure. In conclusion, the inactivation effects on MHV-A59 by 2.8 GHz MW at room temperature are better than that at lower temperatures. And, thermal effects of MW radiation might be a potential mechanism for virus inactivation.

Figure 4.

Figure 4.

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Lower temperature reduces the virus inactivation by 2.8 GHz microwave radiation. (A and B) The schematic diagram of microwave radiation on virus suspensions with different temperatures. (C and D) The alteration of MHV-A59 infectivity before and after exposure to microwave exposure at different temperatures (n = 5). (E) The infectivity of MHV-A59 on 17CL-1 cells after exposure to microwave (scale bars = 50 μm). (F) Schematic diagram of real-time temperature measurement by fiber-optic thermometer during radiation. (G) Change of the temperature of virus culture medium during microwave exposure. One-way analysis of variance followed by LSD correction was used to compare multiple groups (***P < .001).

4. Discussion

In the past decades, the coronavirus pandemic has become more and more frequent, and the public health security system has been facing severe challenges.[15,16,25,35,36] Virus inactivation is critical to prevent the spread, infection, and pathogenicity of the virus. Traditional virus inactivation strategies have several limitations, such as poor penetration of ultraviolet, environmental pollution of chemical disinfectants and ozone, and high cause of ionizing radiation. Therefore, it is urgent to develop novel and efficient virus inactivation technologies.

Coronaviruses, such as SARS-CoV, middle east respiratory syndrome coronavirus, and SARS-CoV-2, can rapidly spread through air droplets, as well as person-to-person contact, and can induce severe infectious diseases. Moreover, coronaviruses such as SARS-CoV-2 can persist for 72 hours on the surfaces of plastic and stainless steel, which significantly increase the possibility of transmission and infection.[37] Therefore, it is necessary to establish an alternative model to study the biological characteristics, prevention methods, and therapy strategies of highly pathogenic coronaviruses. MHV-A59 is similar to SARS-CoV-2 in structure, biophysical properties, and genetic characteristics.[31,32,38] And, we confirmed that the virus infectivity of MHV-A59 could not be altered at room temperature for 30 minutes. Therefore, we used MHV-A59 as an alternative model to evaluate the inactivation ability of MWs on coronavirus infectivity.

Some studies have reported that the virus can be inactivated efficiently by electromagnetic waves at multiple frequencies.[28,29,39] In this study, we showed that the infectivity of MHV-A59 was decreased and the morphology of MHV-A59 was destroyed after radiation with 2.8 GHz, 100 mW/cm2 MW at room temperature for 30 minutes. However, the inactivation effect still needs to be improved. In addition, the mechanisms underlying MW-induced virus inactivation are still largely unexplored. Previous studies showed that the inactivation of viruses by electromagnetic waves is mainly attributed to the thermal effects, nonthermal effects, or physical resonance effects.[40–42] In this study, we found that the envelope of MHV-A59 was broken and its morphological structure was destroyed. Moreover, the infectivity of MHV-A59 was also decreased after 2.8 GHz MW radiation. Therefore, we concluded that the destruction of the envelope integrity of MHV-A59 might be one of the potential mechanisms for virus inactivation of MHV-A59 by 2.8 GHz MW. But at the same time does not exclude the participation of other factors inactivating the MHV-A59.

The environments, such as the pH of virus suspensions and environmental temperature, are pivotal for the survival and propagation of viruses. According to previous reports, both highly acidic and highly alkaline environments are unfriendly to viruses.[43,44] In this study, the stability of MHV-A59 under different pH conditions was monitored, and the virus infectivity decreased significantly under pH of 2.0 and 12.0. However, there was no significant change in virus suspensions with a pH of 4.0 or 8.0, which is consistent with the previously described stable survival of MHV-A59 at pH 4.0 to 7.0. Interestingly, a slight alteration of pH to 8.0 could not affect the infectivity of MHV-A59, but enhance the virus inactivation ability by 2.8 GHz MW radiation. These results suggested that the virus inactivation ability is closely related to the pH of the environment around the virus. Therefore, creating a weak alkaline environment could accelerate the inactivation of the virus by MW. These findings are not reported in other studies, it can further improve the efficiency of electromagnetic wave inactivation of virus, clear the best application of electromagnetic wave inactivation of virus conditions. This finding provides new insights and references for the study of inactivation of coronavirus.

Environmental temperature is another important factor that can influence the survival of coronavirus. In general, cold conditions will be beneficial for the survival of the virus.[45–47] In this study, we confirmed that the inactivation efficiency of the 2.8 GHz MW on MHV-A59 at low temperatures is much weaker than that at room temperature. In addition, obvious temperature rise could be observed in virus suspensions at room temperature, but not in suspensions with lower temperature, during MW radiation, which indicated that thermal effects also might be a potential mechanism for MW-mediated virus inactivation. However, it is not completely excluded that other factors are involved in virus inactivation, such as physical resonance and other nonthermal effects. We speculated that a 2.8 GHz MW may inactivate MHV-A59 better at higher temperatures than at room temperature. In addition, the influences of environmental temperature on virus inactivation by electromagnetic waves might be due to the frequencies and power densities of electromagnetic waves, as well as the types of viruses.[27,29,30] For example, some researchers have proposed the existence of a structural resonance energy transfer effect between electromagnetic waves and viruses. This resonant mode can be used to inactivate the virus efficiently at a specific electromagnetic frequency and a power density, independent of the thermal effect.

5. Conclusion

In this study, we found that 2.8 GHz and 100 mW/cm2 MW exposure for 30 minutes decreased the infectivity and damaged the structures of MHV-A59. Moreover, a slight alteration of the pH of virus suspensions to 8.0 significantly increases the sensitivity of MHV-A59 to MW. And, lower temperature of virus suspensions reduced the virus inactivation ability of MW. Furthermore, thermal effects and destruction to the envelope of viruses might be the potential mechanisms for MW-mediated virus inactivation. In a word, our results might provide new insight into the application of mirowaves in the field of virus inactivation and provide potential help for the development of public health. In the future, we can start with the nonthermal effect of electromagnetic wave, including the physical resonance effect, to find a new and efficient virus inactivation technology.

Acknowledgments

We thank Xuelong Zhao at the Beijing Institute of Radiation Medicine, for assistance with the radiation of the virus. We thank Yong Zou at Beijing Institute of Radiation Medicine, for assistance with measurements of the temperature by optical fiber.

Author contributions

Conceptualization: Yi Xiao, Ruiyun Peng, Li Zhao.

Data curation: Yi Xiao.

Formal analysis: Yi Xiao, Ruiyun Peng, Haoyu Wang, Hui Wang, Ji Dong, Kehui Wang, Wei Liu, Li Zhao.

Funding acquisition: Ruiyun Peng, Li Zhao.

Investigation: Yi Xiao, Ruiyun Peng, Haoyu Wang, Hui Wang, Ji Dong, Kehui Wang, Wei Liu, Li Zhao.

Methodology: Yi Xiao, Ruiyun Peng, Haoyu Wang, Hui Wang, Ji Dong, Li Zhao.

Project administration: Ruiyun Peng, Li Zhao.

Software: Yi Xiao, Ruiyun Peng, Haoyu Wang, Hui Wang, Ji Dong, Kehui Wang, Wei Liu, Li Zhao.

Validation: Yi Xiao, Ruiyun Peng, Haoyu Wang, Hui Wang, Ji Dong, Kehui Wang, Wei Liu, Li Zhao.

Writing – original draft: Yi Xiao.

Writing – review & editing: Ruiyun Peng, Li Zhao.

Abbreviations:

CPE
cytopathic effect
MW
microwave
SARS-CoV
severe acute respiratory syndrome coronavirus
SARS-CoV-2
severe acute respiratory syndrome coronavirus 2
TCID50
median tissue culture infective dose assay
TEM
transmission electron microscopy

The authors have no funding and conflicts of interest to disclose.

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

How to cite this article: Xiao Y, Peng R, Wang H, Wang H, Dong J, Wang K, Liu W, Zhao L. Inactivation of β-coronavirus MHV-A59 by 2.8 GHz microwave. Medicine 2024;103:47(e40341).

Contributor Information

Yi Xiao, Email: yixx999@163.com.

Ruiyun Peng, Email: ruiyunpeng18@126.com.

Haoyu Wang, Email: 155369709@qq.com.

Hui Wang, Email: 155369709@qq.com.

Ji Dong, Email: djtiwj@163.com.

Kehui Wang, Email: 155369709@qq.com.

Wei Liu, Email: 931448189@qq.com.

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