Abstract
Background: The rapid worldwide spread of the Omicron variant of SARS-CoV-2 has unleashed a new wave of COVID-19 outbreaks. The efficacy of molnupiravir, an approved drug, is still unknown in patients infected with the Omicron variant.
Objective: Evaluated the antiviral efficacy and safety of molnupiravir in patients infected with SARS-CoV-2 Omicron variant, with symptom duration within 5 days.
Methods: We conducted a randomized, controlled trial involving patients with mild or moderate COVID-19. Patients were randomized to orally receive molnupiravir (800 mg) plus basic treatment or only basic treatment for 5 days (BID). The antiviral efficacy of the drug was evaluated using reverse transcriptase polymerase chain reaction.
Results: Results showed that the time of viral RNA clearance (primary endpoint) was significantly decreased in the molnupiravir group (median, 9 days) compared to the control group (median, 10 days) (Log-Rank p = 0.0092). Of patients receiving molnupiravir, 18.42% achieved viral RNA clearance on day 5 of treatment, compared to the control group (0%) (p = 0.0092). On day 7, 40.79%, and 6.45% of patients in the molnupiravir and control groups, respectively, achieved viral RNA clearance (p = 0.0004). In addition, molnupiravir has a good safety profile, and no serious adverse events were reported.
Conclusion: Molnupiravir significantly accelerated the SARS-CoV-2 Omicron RNA clearance in patients with COVID-19.
Clinical Trial Registration: [chictr.org.cn], identifier [ChiCTR2200056817].
Introduction
The Omicron variant of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has rapidly replaced the Delta variant as the dominating SARS-CoV-2 variant, which has higher infectivity and stronger vaccine breakthrough ability (Chen et al., 2022; Saxena et al., 2022). Among the three lineages of Omicron: BA.1 (B.1.1.529.1), BA.2 (B.1.1.529.2), and BA.3 (B.1.1.529.3), BA.2 is rapidly increasing worldwide since January 2022 and has become a new dominating “variant of concern” in China (Cheng et al., 2022; World Health Organization, 2022). With the current surge of Omicron infections in China, both the absolute number of patients hospitalized with coronavirus disease 2019 (COVID-19) and the percentage of total COVID-19 hospitalizations have been increasing recently. Although the direct effects of SARS-CoV-2 Omicron variant on patients have been largely mild, the impact on people’s health is substantial due to the large number of infected individuals and potential virus-induced lung injury (He et al., 2021). Thus, an oral, effective, and direct-acting therapeutic is needed to block the transmission of SARS-CoV-2 Omicron variant.
Molnupiravir, a small-molecule drug, has been reported to have shown good anti-SARS-CoV-2 efficacy in phase II/III clinical trials (Jayk Bernal et al., 2021; Fischer et al., 2022). It has been approved by the United Kingdom MHRA and has received an Emergency Use Authorization from the FDA for the treatment of COVID-19. Recent studies have shown that molnupiravir could inhibits Omicron variant in vitro and in vivo (Rosenke et al., 2022; Takashita et al., 2022; Uraki et al., 2022). However, data on its efficacy and safety in the population infected with the Omicron variant is still lacking.
In this study, we performed a randomized, controlled study to evaluate the clinical efficacy of molnupiravir for COVID-19 patients infected with Omicron BA.2 at the Third People’s Hospital of Shenzhen. We endeavored to compare the antiviral efficacy between patients who were treated with molnupiravir plus basic treatment and those treated only with basic treatment. This study will provide practical insight for the treatment against SARS-CoV-2 Omicron variant infections.
Methods
Study Design
We conducted a randomized, controlled trial of molnupiravir in patients infected with Omicron variant (ChiCTR2200056817, chictr.org.cn). The protocol was reviewed and approved by the Medical Ethics Committee of the Third People’s Hospital of Shenzhen, and the trial was conducted in accordance with the Declaration of Helsinki and Good Clinical Practice guidelines of the International Conference on Harmonization. Molnupiravir was provided by HUAHAI Pharmaceutical.
From March 3 to 21 March 2022, patients with confirmed mild/moderate COVID-19 were admitted and enrolled at the Third People’s Hospital of Shenzhen. Eligible patients include male or nonpregnant females aged ≥18 years and ≤80 years, who were tested positive for SARS-CoV-2 Omicron variant and had initial onset of symptoms for ≤5 days prior to the day of treatment. Exclusion criteria included severe vomiting or intolerance of oral drugs for other reasons, pregnancy or lactation, patients retesting positive for COVID-19, and those who had received antibody therapy, plasma therapy, or other investigational drugs for SARS-CoV-2. All the patients provided a written informed consent.
Patients were randomly grouped (2:1) into molnupiravir (n = 80) and control groups (n = 36) using a random number table. Molnupiravir (800 mg twice per day) were administered orally for 5 days in the hospital. In addition, all patients received the same basic treatment, which consisted of vitamin C, lianhuaqingwen granule, and nasal irrigation. Pharyngeal swab was collected every other day to determine the antiviral effect of molnupiravir against SARS-CoV-2 using RT-PCR. Adverse events were monitored throughout the study period.
Antiviral Efficacy
The primary endpoint was the time of viral RNA clearance measured using RT-PCR analysis of pharyngeal swab. The time of viral RNA clearance was defined as the number of days it took to have a negative viral RNA test result post-randomization (two consecutive times or 24 h at two intervals). Samples were tested for detection of ORF1ab and N genes. A negative RT-PCR result was confirmed only when all test results were reported negative (Ct > 35). The secondary antiviral efficacy endpoint included the percentage of patients who were negative for SARS-CoV-2 infectious virus on days 5, 7, and 10.
Statistical Analyses
The measurement data conforming to non-normal distribution were exhibited as median, and the Wilcoxon rank-sum test was used for comparison between groups. Meanwhile, the count data were exhibited as cases (%), and comparisons between groups were made using the chi-square test. A p value <0.05 was considered statistically significant. Time of viral RNA clearance was summarized using the Kaplan-Meier methodology, and log-rank test was used for comparison of the efficacy between treatments. The percentage of patients who were negative for viral RNA was summarized and compared between groups using Fisher’s exact test.
Results
Patient Demographics and Clinical Characteristics
From March 3 to 21 March 2022, 116 patients were randomly grouped, with 108 receiving molnupiravir or only basic treatment (Figure 1). The patients randomized to the control and molnupiravir groups were well matched. Baseline characteristics were generally similar across the groups, and baseline laboratory test results were well balanced (Table 1).
FIGURE 1
CONSORT diagram for this trial.
TABLE 1
| Characteristics | Molnupiravir (n = 77) | Control (n = 31) | p value |
|---|---|---|---|
| Median age (range) | 39 (20, 63) | 42 (22, 61) | 0.363 |
| Male | 43/77 (55.8%) | 17/31 (54.8%) | 0.924 |
| Median BMI (IQR) | 23.44 (21.17, 26.04) | 23.34 (21.45, 25.65) | 0.873 |
| Presenting symptoms | |||
| Fever | 32/77 (41.6%) | 9/31 (29.0%) | 0.225 |
| Maximum body temperature, C (mean, range) | 38.6 (37.8, 39.5) | 38.2 (37.5, 39) | 0.061 |
| Two or more symptomsa | 59/77 (76.6%) | 24/31 (77.4%) | 0.929 |
| One underlying disease# | 15/77 (19.5%) | 5/31 (16.1%) | 0.685 |
| Two or more underlying disease | 3/77 (3.9%) | 2/31 (6.5%) | 0.567 |
| Disease severity | |||
| Severe | 0 | 0 | |
| Moderate | 3/77 (3.9%) | 1/31 (3.2%) | 1.000 |
| Mild | 74/77 (96.1%) | 30/31 (96.8%) | 1.000 |
| Virus nucleic acid | |||
| ORF gene, median (IQR) | 18.35 (16.78, 22.32) | 18.19 (16.63, 22.44) | 0.638 |
| N gene, median (IQR) | 17.98 (15.68, 21.24) | 17.51 (15.13, 21.43) | 0.865 |
| Vaccination | |||
| Two doses | 22/77 (28.6%) | 11/31 (35.5%) | 0.833 |
| Three doses | 48/77 (62.3%) | 18/31 (58.1%) | 0.851 |
| Laboratory results | |||
| WBC (× 109/L) | 5.37 (4.43, 7.14) | 5.88 (4.53, 7.13) | 0.543 |
| LYM (× 109/L) | 1.21 (0.85, 1.72) | 1.22 (0.88, 1.55) | 0.760 |
| HB (g/L) | |||
| AST (U/L) | 29 (22.9, 33.35) | 30.2 (34.1, 25.2) | 0.852 |
| ALT (U/L) | 22 (14.5, 33.5) | 23 (14, 31) | 0.794 |
| CK (U/L) | 76 (49, 112.5) | 70 (54.5, 116.75) | 0.981 |
| CK-MB (ng/ml) | 0.219 (0.219, 0.410) | 0.219 (0.219, 0.250) | 0.424 |
| LDH (U/L) | 168 (147.5, 187) | 178 (154, 197) | 0.288 |
| IL-6 (pg/ml) | 4.6 (2.34, 8.56) | 7.30 (3.27, 12.18) | 0.059 |
| CRP (mg/L) | 7.35 (2.80, 11.66) | 7.00 (3.28, 15.77) | 0.508 |
| Bun (mmol/L) | 3.86 (3.34, 4.75) | 4.43 (3.26, 5.05) | 0.347 |
| Cr (μmol/L) | 73.6 (59.85, 94) | 72.1 (56.1, 83.45) | 0.288 |
| CD4 cells (count/μL) | 447.5 (310.75, 611.75) | 537 (328.5, 664.5) | 0.336 |
| CD8 cells (count/μL) | 299.5 (173, 416.25) | 363 (236, 507) | 0.232 |
| Abnormal CT scan features | 3/77 (3.9%) | 1/31 (3.2%) | 1.000 |
Patient demographics and clinical characteristics at baseline.
Cough, fatigue, loss of taste or smell, nasal congestion, runny nose, sore throat, myalgia, diarrhea, headache, chill, nausea or vomiting, dizziness, chest pain.
#Diabetes, hypertension, coronary heart disease, chronic liver disease, chronic kidney disease, chronic obstructive pulmonary disease, tumor.
IQR: interquartile range.
Antiviral Efficacy
A total of 107 patients in the cohort were included for the primary efficacy analysis. One patient in the molnupiravir group was excluded from the antiviral efficacy analysis because of a negative result in the viral RNA test less than 12 h after taking the medicine. The primary outcome of this study was the time of viral RNA clearance. The median time of viral clearance were 9 days (95% CI: 7–9 days) and 10 days (95% CI: 9–11 days) in the molnupiravir and control groups, respectively. The median time was significantly reduced in the molnupiravir group (log-rank p = 0.0092, Figure 2 and Table 2). This result indicates that molnupiravir can effectively accelerate viral RNA clearance in patients infected with the Omicron variant, which is consistent with the antiviral efficacy of molnupiravir in treatment of COVID-19 (Fischer et al., 2022).
FIGURE 2
Kaplan-Meier plot showing the time of viral RNA clearance in the molnupiravir and control groups.
TABLE 2
| Characteristics | Molnupiravir (n = 76) | Control (n = 31) | p value |
|---|---|---|---|
| Patients negative for viral RNA on day 5, n (%) | 14(18.42) | 0(0) | 0.0092 |
| Patients negative for viral RNA on day 7, n (%) | 31(40.79) | 2(6.45) | 0.0004 |
| Patients negative for viral RNA on day 10, n (%) | 58(76.32) | 16(51.61) | 0.02 |
| Median time for a negative viral RNA, days (95% CI) | 9(7–9) | 10(9–11) | 0.0092 |
Antiviral efficacy of molnupiravir.
The key secondary virological endpoint of this trial was the percentage of patients who were negative for viral RNA on days 5, 7, and 10 (Table 2). On day 5 of treatment, the percentage of patients who were negative for viral RNA was 18.42% in the molnupiravir group and 0% in the control group (p = 0.0092). The percentage of patients who were negative for viral RNA also increased to 40.79% on day 7 in the molnupiravir group compared to the control group (6.45%) (p = 0.0004). The percentage of patients negative for viral RNA remained significantly different between molnupiravir and control groups on day 10 of treatment (molnupiravir group: 76.32%; control group: 51.61%) (p = 0.02).
Safety
Three adverse events were reported in the molnupiravir group (Table 3). One patient (1.3%) had skin rash, and two patients (2.6%) had elevated levels of alanine transaminase. No grade 3 or higher adverse events were reported, and no adverse events led to the discontinuation of molnupiravir treatment.
TABLE 3
| Characteristic | Molnupiravir (n = 77) | Control (n = 31) | p value |
|---|---|---|---|
| Adverse events | |||
| Rash | 1 (1.3%) | 0 (0%) | 1.000 |
| Elevated ALT | 2 (2.6%) | 0 (0%) | 1.000 |
Summary of adverse events in the two groups.
Clinical Outcomes
The duration of fever, time of symptom alleviation and laboratory test results were collected to evaluate the overall health condition associated with COVID-19. At baseline, patients in the molnupiravir and control groups matched well in all presentation indicators, with no significant difference. In the laboratory test before discharge, all test values of patients recovered to the normal range, and no significant difference was observed between the groups (Table 4). The median time to alleviate COVID-19 symptoms between the molnupiravir and control groups was not statistically significant (5 days vs. 7 days, p = 0.499), and the results were consistent with previously published studies (Fischer et al., 2022). In addition, the median time of fever duration was not statistically between the two groups, although the duration of fever was reduced by 2 days in the molnupiravir group compared to the control group (1 day vs. 3 days, p = 0.096).
TABLE 4
| Characteristics | Molnupiravir (n = 77) | Control (n = 31) | p value |
|---|---|---|---|
| Fever duration, days (median, IQR) | 1 (1, 2) | 3 (1, 3) | 0.096 |
| Symptoms alleviating time, days (median, IQR) | 5 (3.75, 7) | 7 (3, 7) | 0.499 |
| Laboratory test before discharge | |||
| AST (U/L) | 22.9 (21.4, 30.2) | 25.5 (20.2, 28.7) | 0.630 |
| ALT (U/L) | 21 (12.5, 36.5) | 19 (13, 26) | 0.847 |
| CK (U/L) | 43 (31, 73) | 37 (31, 69) | 0.425 |
| CK-MB (ng/ml) | 0.219 (0.291, 0.360) | 0.219 (0.219, 0.3) | 0.543 |
| LDH (U/L) | 168 (136, 181) | 156 (147, 174) | 0.917 |
| IL-6 (pg/ml) | 1.49 (1.49, 1.69) | 1.57 (1.49, 3.28) | 0.145 |
| CRP (mg/L) | 1.46 (0.66, 3.11) | 1.00 (0.33, 6.79) | 0.975 |
| Bun (mmol/L) | 4.63 (3.75, 5.01) | 4.13 (3.34, 5.21) | 0.555 |
| Cr (μmol/L) | 62 (56.3, 89.6) | 67.5 (52.8, 72.1) | 0.555 |
Clinical outcomes associated with COVID-19.
Discussion
As of 22 March 2022, 470,839,745 confirmed COVID-19 cases were recorded, including 6,092,933 deaths, and a total of 10,925,055,390 doses of vaccine had been administered worldwide. The emerging Omicron variant of SARS-CoV-2 is highly infectious and has a stronger vaccine breakthrough ability against antibodies provided by existing vaccines, thus it is the dominating SARS-CoV-2 variant globally (Arora et al., 2022). The current effective tools to fight COVID-19 outbreaks are vaccination and small-molecule oral drug therapy. The main role of marketed COVID-19 vaccines is to reduce symptomatic infection and prevent severe illness. Unfortunately, no clinical trial on small-molecule oral medicine as treatment against COVID-19 caused by Omicron variant is available. Molnupiravir has been approved for marketing in the United Kingdom for the treatment of adults with mild to moderate COVID-19 and has been granted emergency use authorization from FDA (Food and Drug Administration, 2021; Merck, 2021).
In our study, we found that molnupiravir was effective in treating COVID-19 caused by Omicron variant infection, with few adverse effects. Compared to basic treatment, molnupiravir treatment significantly reduced viral load in pharyngeal swabs and accelerated viral RNA clearance in patients with COVID-19. In the completed phase 2A trial of molnupiravir, the median time of viral RNA clearance was 14 days in the molnupiravir group and 15 days in the control group (p = 0.013) (Fischer et al., 2022). In this study, the median time of viral RNA clearance in the molnupiravir group and the control group were 9 days and 10 days, respectively (p = 0.0092). This difference may be due to two possible reasons, as follows: 1) reduced replication capacity and pathogenicity of the Omicron variant compared to the other variants (Shuai et al., 2022), and 2) more than 90% of the patients enrolled in this trial received at least two doses of COVID-19 vaccine (molnupiravir group: 90.9%; control group: 93.6%). In the vaccination population, most of the patients received the inactivated vaccine (Sinavac), only 7.1 and 6.9% patients received other vaccines (BNT162b2 or Zifivax) in molnupiravir and control groups, respectively (Supplmentary Table S1). We have checked the neutralization antibody titers for all the vaccination patients and found that there was no significant difference on neutralization antibody titer between two groups (p = 0.521) (Supplementary Table S2). In term of T cell immunity, there was no significant difference in T cells (CD4 and CD8 cells) counts, as shown in Table 1. These results indicate that molnupiravir administration based on widespread vaccination may be more effective in responding to outbreaks caused by the Omicron variant.
Based on the higher infectivity and reduced pathogenicity of the Omicron variant, it is more likely to result in a great deal of patients with mild COVID-19 or asymptomatic infections, rather than severe COVID-19. As a result, the clearance of viral RNA from patients and interruption of viral transmission are more relevant in the fight against Omicron variant infections. This clinical trial was outlined to assess the efficacy and safety of molnupiravir against the Omicron variant of SARS-CoV-2 and did not focus on evaluating clinical endpoints, such as symptom duration or length of hospitalization. Furthermore, recruitment was not limited to patients with risk factors of progressing to severe disease. Patients did not benefit from molnupiravir treatment in terms of duration of fever and symptoms alleviating time during the observation period. Another limitation is that asymptomatic individuals were not recruited into the trial. In this population, which was positive for viral RNA but has no characteristic symptoms, treatment with molnupiravir that exert a direct antiviral effect is equally relevant and may be more effective.
This study provides biological evidence to support the use of molnupiravir in accelerating viral RNA clearance in patients infected with the Omicron variant of SARS-CoV-2, potentially reducing viruses early transmission. The dynamic zero COVID-19 strategy is the most effective prevention and control strategy proposed and implemented in China during the COVID-19 epidemic. In the face of a new wave of COVID-19 outbreaks caused by the Omicron variant, small-molecule oral drug therapy will contribute to the implementation of the dynamic zero COVID-19 strategy and accelerate the end of the epidemic.
Statements
Data availability statement
The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.
Ethics statement
The studies involving human participants were reviewed and approved by the Medical Ethics Committee of the Third People’s Hospital of Shenzhen (No. 2022-034-02). The patients/participants provided their written informed consent to participate in this study.
Author contributions
RZ, SL, HL, WZ, and YL conceived the overall study and designed experiments. RZ, LP, DS, JL, GT, JP, XY, ML, CZ, JY, HW, and HL contributed to the data collection, analysis, and interpretation. RZ, LZ, and HL analyzed the data. YL, LZ, and WZ wrote and edited the manuscript. SL, WZ, and YL conceived and supervised the data analysis. All co-authors made important comments on the manuscript.
Funding
This research was supported by grants from the National Key Research and Development Project (2021YFC2300704) (WZ), Shenzhen Science and Technology Research and Development Project (JSGG20200207161928126) (YL) and in part from the National Science and Technology Major Projects (2018ZX09711003) (WZ).
Acknowledgments
Thanks to Qian Kang of Carelink Pharmaceutical Co., Ltd. for providing statistical analysis.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fphar.2022.939573/full#supplementary-material
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Summary
Keywords
Omicron variant, SARS-CoV-2, molnupiravir, antiviral efficacy, clinical trial
Citation
Zou R, Peng L, Shu D, Zhao L, Lan J, Tan G, Peng J, Yang X, Liu M, Zhang C, Yuan J, Wang H, Li S, Lu H, Zhong W and Liu Y (2022) Antiviral Efficacy and Safety of Molnupiravir Against Omicron Variant Infection: A Randomized Controlled Clinical Trial. Front. Pharmacol. 13:939573. doi: 10.3389/fphar.2022.939573
Received
09 May 2022
Accepted
31 May 2022
Published
15 June 2022
Volume
13 - 2022
Edited by
Qingbing Zheng, Xiamen University, China
Reviewed by
Xun Gui, Mabwell (Shanghai) Bioscience Co., Ltd., China
Yingying Su, Xiamen University, China
Yushan Jiang, Southern Medical University, China
Updates
Copyright
© 2022 Zou, Peng, Shu, Zhao, Lan, Tan, Peng, Yang, Liu, Zhang, Yuan, Wang, Li, Lu, Zhong and Liu.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Song Li, lis.lisong@gmail.com; Hongzhou Lu, luhongzhou@szsy.sustech.edu.cn; Wu Zhong, zhongwu@bmi.ac.cn; Yingxia Liu, szsy_lyx@szsy.sustech.edu.cn
†These authors have contributed equally to this work
This article was submitted to Respiratory Pharmacology, a section of the journal Frontiers in Pharmacology
Disclaimer
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.