Clinical outcomes of early remdesivir administration in hospitalized patients at high risk for severe COVID-19 during the Omicron wave

doi:10.21203/rs.3.rs-4957347/v1

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Clinical outcomes of early remdesivir administration in hospitalized patients at high risk for severe COVID-19 during the Omicron wave

https://doi.org/10.21203/rs.3.rs-4957347/v1

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Background

Early remdesivir administration in high-risk patients with coronavirus disease 2019 (COVID-19) is known to be effective in preventing the progression to severe disease. However, the effect of early remdesivir administration on Omicron variants, which are known to have decreased severity, remains unclear.

Methods

This study aimed to analyze the effects of early remdesivir administration during the Omicron wave in hospitalized patients. Electronic medical records of hospitalized patients with confirmed COVID-19 between February 2022 and February 2023 were reviewed. We included patients aged ≥18 years who had symptom onset within 7 days and had at least one risk factor for disease progression at the time of diagnosis. We compared the clinical outcomes between the early remdesivir administration group and the group not administered early remdesivir. The primary outcome was all-cause mortality within 28 days and the secondary outcome was the need for oxygen supplementation within 28 days. A total of 286 patients were enrolled, with 88 and 198 in the early and control groups, respectively. Results

Clinical outcomes, including all-cause mortality (3.4% vs. 6.1%, P = 0.556) and need for oxygen supplementation (15.9% vs. 14.6%, P= 0.783) within 28 days, were not significantly different between the two groups. Early remdesivir administration was not significantly associated with all-cause mortality (HR, 0.393; 95% CI: 0.109, 1.417; P = 0.154) or the need for oxygen supplementation (OR, 0.823; 95% CI: 0.389, 1.740; P = 0.610).

Conclusions

Considering the decline in the severity of the Omicron variant and the increased vaccination rate reported in previous studies, further studies are needed to establish new indications for the use of early remdesivir in the Omicron variant.

COVID-19

Omicron

Early remdesivir

severity

Coronavirus disease 2019 (COVID-19) caused by severe acute respiratory syndrome virus 2 (SARS-CoV-2), has rapidly spread worldwide since the end of 2019, resulting in a global pandemic. More than 775 million confirmed cases and more than 7.0 million deaths have been reported[1]. In many cases, COVID-19 has a mild spectrum of diseases, including non-pneumonia and mild pneumonia[2]. However, severe and critical cases were reported in 14% and 5% of the cases, respectively, according to a report from the Chinese Center for Disease Control and Prevention in the early 2020s. Although the variants of decreased severity and vaccination against COVID-19 reduced the progression to severe disease, patients with old age, multiple comorbidities, and specific underlying health conditions remain at an increased risk for severe disease[3, 4].

Remdesivir is an antiviral agent recommended by the World Health Organization (WHO) to prevent progression to severe disease in high-risk patients with COVID-19[5]. Remdesivir is an intravenous (IV) agent, whereas nirmatrelvir/ritonavir and molnupiravir are orally administered; therefore, it can be used when COVID-19 patients who are at risk of severe disease cannot swallow oral tablets for various reasons or when nirmatrelvir/ritonavir is contraindicated. In a randomized controlled trial (RCT), early remdesivir in outpatients with COVID-19 who had symptom onset within 7 days and had at least one risk factor for disease progression resulted in a substantially reduced risk of severe disease[6]. However, this RCT was conducted before the emergence of Omicron and its subvariants.

Omicron was first detected in South Africa in November 2021. It rapidly emerged as the dominant variant worldwide and evolved into several subvariants[7]. Omicrons are known to have high infectivity and the ability to evade immunity generated by prior variants or vaccinations; however, the risk of severe disease is lower than that of previous variants[3, 8, 9]. Despite this, older patients, those with multiple underlying diseases, and those with immunocompromised conditions remain at an increased risk of severe COVID-19 illness and death[4]. Although omicron has different characteristics compared to the previous variants, there is a lack of research on the effects of remdesivir during the Omicron wave. In addition, many studies on the effectiveness of early remdesivir administration have been conducted on outpatients. Remdesivir is an IV formulation that can be conveniently used in hospitalized patients who cannot take nirmatrelvir/ritonavir compared to outpatients. Therefore, in our study, we evaluated the effects of early remdesivir treatment in hospitalized patients infected with Omicron and its sub-variants.

Study design

This retrospective cohort study was conducted to investigate the effect of early remdesivir administration in hospitalized patients with omicrons and their subvariants at Kangwon National University Hospital in Chuncheon, Korea. In Korea, the first case of the Omicron variant was identified in December 2021, and the Omicron variant rapidly replaced the Delta variant[10]. In February 2022, the Omicron variant accounted for 99.1% of all COVID-2019 cases in Korea. Electronic medical records of hospitalized patients with confirmed COVID-19 between February 2022 and February 2023 were reviewed, and clinical and laboratory data were collected. This study was approved by the Institutional Review Board and local Ethics Committee of Kangwon National University Hospital. (Approval no. 2024-07-018). Written informed consent was waived by Institutional Review Board and local Ethics Committee of Kangwon National University Hospital, due to the retrospective study.

Study population and outcomes

COVID-19 was confirmed using nucleic acid amplification tests at admission or during hospitalization. We included patients aged ≥ 18 years who had symptom onset within 7 days and had at least one risk factor for disease progression at diagnosis[6]. Risk factors included age > 60 years, hypertension, cardiovascular or cerebrovascular disease, diabetes mellitus, obesity (a body-mass index [BMI; the weight in kilograms divided by the square of the height in meters] of ≥ 30), immune compromise, chronic mild or moderate kidney disease, chronic liver disease, chronic lung disease, cancer, or sickle cell disease. Patients were excluded if they were receiving supplemental oxygen or were hospitalized in the intensive care unit (ICU) at the time of diagnosis. Patients were also excluded if they had previously received other antiviral agents or if their renal function was lower than the estimated glomerular rate(eGFR) 30.

The patients were divided into two groups according to whether remdesivir was administered or not. For patients who received early remdesivir, the intravenous remdesivir dose was 200 mg on day 1, followed by 100 mg on days 2 and 3[6]. The clinical outcomes of the two groups were compared. The primary outcome was all-cause mortality within 28 days and the secondary outcome was the need for oxygen supplementation within 28 days.

Statistical analysis

SPSS for Windows (ver. 26.0, Inc., Chicago, IL, USA) was used for statistical analysis. Baseline patient characteristics and clinical outcomes were compared between the early remdesivir and control groups. Student’s t-test was used for continuous variables, and chi-square or Fisher’s exact test was used for categorical variables. Statistical significance was defined as a two-sided P-value < 0.05. Cox regression analysis was performed to determine independent risk factors for all-cause mortality. Logistic regression analysis was used to evaluate risk factors for oxygen supply.

During the study period, 703 COVID-19 patients who had symptom onset within 7 days and had at least one risk factor for severe disease were evaluated at our hospital (Fig. 1). Among them, 86 patients treated with other antiviral agents, 121 patients with eGFR < 30 mL/min and 209 patients with severe disease requiring supplemental oxygen or ICU care at diagnosis were excluded. One patient who discontinued remdesivir because of side effects was also excluded. Therefore, 286 patients were enrolled in this study. Of these, 88 patients received early remdesivir (early remdesivir group), and 198 patients did not receive remdesivir (control group).

Figure 1. Flowdiagram of early Remdesivir group vs Control group in COVID-19 patients

Baseline characteristics and outcomes of the study population are summarized in Table 1. The mean age of the study population was 74.7 years, and females accounted for 45.1%. The mean BMI was 22.7 Kg/m². The most common underlying conditions were hypertension (57.3%), cerebrovascular disease (32.9%), diabetes mellitus (31.8%), and malignancies (25.9%). More than three COVID-19 vaccinations were received by 75.2% of patients COVID. There was no statistically significant difference between the early remdesivir and control groups in baseline characteristics, except for cerebrovascular disease. Cerebrovascular disease was 47.7% in the early remdesivir group and 26.3% in the control group (P < 0.001).

Table 1

Baseline characteristics and outcomes of the study population
Characteristics	Total (N = 286)	Early Remdesivir (N = 88)	Control (N = 198)	P value
Age (years), mean (SD)	74.7 (11.8)	75.2 (13.5)	74.5 (10.9)	0.697
Female, n (%)	129 (45.1)	35 (39.8)	94 (47.5)	0.227
BMI (Kg/m²), mean (SD)	22.7 (4.2)	22.1 (3.9)	22.9 (4.3)	0.110
Underlying comorbidities
Hypertension, n (%)	164 (57.3)	49 (55.7)	115 (58.1)	0.705
Diabetes mellitus, n (%)	91 (31.8)	25 (28.4)	66 (33.3)	0.409
Cerebrovascular disease, n (%)	94 (32.9)	42 (47.7)	52 (26.3)	< 0.001
Cardiovascular disease, n (%)	49 (17.1)	14 (15.9)	35 (17.7)	0.714
Chronic lung disease, n (%)	32 (11.2)	9 (10.2)	23 (11.6)	0.731
Chronic liver disease, n (%)	21 (7.3)	8 (9.1)	13 (6.6)	0.450
Malignancy, n (%)	74 (25.9)	27 (30.7)	47 (23.7)	0.216
Vaccination over 3 doses, n (%)	212/282 (75.2)	57/85 (67.1)	155/197 (78.7)	0.038
RT-PCR ct value, mean (SD)	20.3 (6.9)	20.0 (6.8)	20.3 (6.9)	0.687
Clinical outcomes
All-cause mortality, n (%)	15 (5.2)	3 (3.4)	12 (6.1)	0.566
Oxygen supply, n (%)	43 (15.0)	14 (15.9)	29 (14.6)	0.783

BMI, body mass index; CI, confidence interval; RT-PCR, reverse transcription polymerase chain reaction; SD, standard deviation

The clinical outcomes, including all-cause mortality and the need for oxygen supplementation within 28 days, were not significantly different between the two groups (Table 1). All-cause mortality was 3.4% in the early remdesivir group and 6.1% in the control group (P = 0.556). The number of patients requiring oxygen in the early remdesivir and control groups was 15.9% and 14.6% (P = 0.783), respectively.

Cox regression analysis was performed to identify risk factors associated with all-cause mortality (Table 2). In the univariate analysis, age (hazard ratio [HR], 1.055; 95% confidence interval [CI]: 1.002, 1.110; P = 0.042), BMI (HR, 0.836; 95% CI, 0.722, 0.969; P = 0.017), malignancy (HR, 3.410; 95% CI, 1.236, 9.403; P = 0.018) were significantly associated with all-cause mortality. Based on the multivariate analysis, age (HR, 1.061; 95% CI: 1.002, 1.124; P = 0.043), BMI (HR, 0.849; 95% CI: 0.725, 0.994; P = 0.041), malignancy (HR, 4.619; 95% CI: 1.618, 13.189; P = 0.004) were independent factors associated with all-cause mortality. Early remdesivir use was not significantly associated with all-cause mortality in univariate and multivariate analyses.

Table 2

Cox regression analysis for all-cause mortality
Variable	Univariate analysis		Multivariate analysis
Variable	HR (95% CI)	P value	HR (95% CI)	P value
Age (years)	1.055 (1.002–1.110)	0.042	1.061 (1.002–1.124)	0.043
Female	0.296 (0.084–1.051)	0.060
BMI (Kg/m²)	0.836 (0.722–0.969)	0.017	0.849 (0.725–0.994)	0.041
Underlying comorbidities
Hypertension	0.647 (0.235–1.785)	0.400
Diabetes mellitus	0.325 (0.073–1.438)	0.139
Cerebrovascular disease	0.142 (0.019–1.081)	0.059
Cardiovascular disease	2.516 (0.860–7.362)	0.092
Chronic lung disease	2.057 (0.580–7.288)	0.264
Chronic liver disease	0.892 (0.117–6.785)	0.912
Malignancy	3.410 (1.236–9.403)	0.018	4.619 (1.618–13.189)	0.004
Vaccination over 3 doses	0.368 (0.133–1.014)	0.053
RT-PCR ct value	1.034 (0.959–1.114)	0.384
Early remdesivir	0.558 (0.157–1.978)	0.366	0.393 (0.109–1.417)	0.154

BMI, body mass index; Ct, cycle threshold; CI, confidence interval; HR, hazard ratio; RT-PCR, reverse transcription polymerase chain reaction; SD, standard deviation

Logistic regression analysis was performed to evaluate the risk factors for oxygen supply (Table 3). In the univariate analysis, age (odds ratio [OR], 1.037; 95% CI: 1.005, 1.069; P = 0.025), BMI (OR, 0.881; 95% CI: 0.804, 0.965; P = 0.007), vaccination over three doses (OR, 0.417; 95% CI, 0.210, 0.829; P = 0.013) were significantly associated with the need for oxygen supplementation. In the multivariate analysis, BMI (OR, 0.908; 95% CI, 0.824, 1.000; P = 0.049), vaccination over three doses (OR, 0.412; 95% CI, 0.202, 0.839; P = 0.015) were significant risk factors for oxygen supply. Early remdesivir use was not significantly associated with the need for oxygen supplementation in univariate and multivariate analyses.

Table 3

Logistic regression for oxygen supply
Variable	Univariate analysis		Multivariate analysis
Variable	OR (95% CI)	P value	OR (95% CI)	P value
Age (years)	1.037 (1.005–1.069)	0.025	1.027 (0.994–1.061)	0.109
Female	0.606 (0.308–1.192)	0.147
BMI (Kg/m²)	0.881 (0.804–0.965)	0.007	0.908 (0.824–1.000)	0.049
Underlying comorbidities
Hypertension	0.832 (0.434–1.595)	0.580
Diabetes mellitus	1.327 (0.675–2.609)	0.411
Cerebrovascular disease	0.867 (0.429–1.751)	0.690
Cardiovascular disease	1.854 (0.861–3.995)	0.115
Chronic lung disease	1.353 (0.522–3.513)	0.534
Chronic liver disease	0.575 (0.129–2.563)	0.468
Malignancy	1.293 (0.634–2.636)	0.480
Vaccination over 3 doses	0.417 (0.210–0.829)	0.013	0.412 (0.202–0.839)	0.015
RT-PCR ct value	1.047 (0.991–1.106)	0.101
Early remdesivir	1.103 (0.551–2.207)	0.783	0.823 (0.389–1.740)	0.610

BMI, body mass index; CI, confidence interval; OR, odds ratio; RT-PCR, reverse transcription polymerase chain reaction; Ct, cycle threshold; SD, standard deviation

Our results showed that early remdesivir administration was ineffective in reducing mortality or the need for oxygenation in hospitalized patients at high risk of severe COVID-19 during the Omicron wave. This result is inconsistent with that of an RCT conducted on unvaccinated outpatients with the Omicron variant[6]. In that trial of 562 patients with mild to moderate COVID-19 who did not require oxygen, 3 days of remdesivir administration within 7 days of symptom onset reduced COVID-19–related hospitalization or death by 87%. However, no deaths were reported in either the remdesivir or control groups; therefore, the data cannot provide information regarding the effects of early remdesivir on death. This study was conducted before the Omicron variant, whereas ours was conducted in Omicron and its subvariants. A cohort study comparing the Delta and Omicron variants conducted in the UK reported that the hospitalization and death due to the Omicron variant compared to the Delta variant had HRs of 0.41 and 0.31, respectively[11]. The reduced severity of the Omicron variant may have influenced the observed effect of early remdesivir. Furthermore, this cohort study showed that vaccination could lower hospitalization and mortality rates for the Omicron variant. The previous RCT was conducted in unvaccinated patients; whereas in this study, 75.2% of patients received more than three doses of vaccine. These differences in vaccination status may have affected the outcomes. According to data from the WHO, 67% of the world's population was vaccinated with a complete primary series of COVID-19 vaccines as of November 2023[12].

Studies analyzing the effect of early remdesivir administration during the Omicron wave showed conflicting results. One study that analyzed the effect of early remdesivir administration in patients with hospital-acquired SARS-CoV-2 infection during the Omicron epidemic reported no significant differences in mortality[13]. Furthermore, there was no statistically significant difference in progression to severe disease. Another study analyzing the effect of remdesivir on mortality in 21,790 hospitalized COVID-19 patients in Switzerland from 2020 to 2022, including the Omicron period, reported that the early use of remdesivir increased mortality[14]. However, several studies conducted on outpatients during the Omicron period reported that early remdesivir administration effectively reduced the progression to severe disease requiring hospitalization[15–19]. Among these, two studies were conducted on organ transplant recipients[15, 16], and others included various patient groups, but at least more than 20% were immunocompromised or transplant recipients[17–19]. In our study, only one organ transplantation recipient was included (not shown in the table), although 25.9% of patients with malignancies were included. Owing to these differences in patient populations, early remdesivir administration may not have reduced the progression to severe disease in our study. We included high-risk patients with severe COVID-19, according to a previous RCT. However, considering the decline in disease severity and high vaccination rates, it is necessary to identify high-risk groups requiring early remdesivir therapy, such as transplant recipients and immunocompromised patients.

In our study, increased age, decreased BMI, and malignancy were independent factors associated with mortality. Statistically significant risk factors for progression to severe COVID-19, which requires oxygen supply, were age, BMI, and vaccination in the univariate analysis, and BMI and vaccination in the multivariate analysis. Vaccination with more than three doses played a defensive role in the progression to severe COVID-19. In previous studies, age was the most significant risk factor for mortality and severe disease[2, 20], and malignancy was a risk factor for severe events[21, 22]. However, unlike a meta-analysis involving 149 studies in which obesity was shown to be an independent factor in the poor prognosis of COVID-19[23], BMI was inversely correlated with mortality and progression to severe disease in our study. This can be explained by differences in the study population. In previous studies, the association between obesity and poor outcomes was strong in patients aged < 60 or 65[24–26]. The mean age in our study was 74.7 years, and most patients were elderly. In another study of COVID-19 hospitalized patients aged > 70, BMI and mortality showed an inverse correlation[27].

Our study had several limitations. First, this was a retrospective study conducted in one center, which may make it difficult to generalize the results and may have selection and information biases. Second, because this study included patients with various diseases, it may be difficult to apply the results to patients with specific diseases. Third, disease conditions other than COVID-19 may have affected the outcome because the study participants were confirmed to have COVID-19 at the time of hospitalization or during hospitalization. Fourth, because many previous studies were conducted on outpatients, hospital admission and mortality were set as clinical outcomes; however, this study was conducted on inpatients; therefore, oxygen administration and mortality were set as clinical outcomes. These differences may account for the variation in results between our study and previous studies.

In conclusion, using early remdesivir in hospitalized COVID-19 patients during the Omicron wave was ineffective in preventing disease progression to severity. Considering the decline in the severity of the Omicron variant and the increased vaccination rate reported in previous studies, further studies are needed to establish new indications for using early remdesivir in the Omicron variant.

COVID-19: Coronavirus disease 2019

SARS-CoV-2: Severe acute respiratory syndrome virus 2

WHO: World health organization

IV: Intravenous

RCT: Randomized controlled trial

BMI: Body-mass index

ICU: Intensive care unit

eGFR: estimated glomerular filtration rate

CI: Confidence interval

RT-PCR: Reverse transcription polymerase chain reaction

SD: Standard deviation

HR: Hazard ratio

OR: Odds ratio

Ct: Cycle threshold

Clinical trial number

Not applicable

Ethics declarations

Ethics approval and consent to participate

This study received approval from by Institutional Review Board and local Ethics Committee of Kangwon National University Hospital (Approval no. 2024-07-018). All methods were conducted according to relevant guidelines and regulations. Informed consent from participants were waived by Institutional Review Board and local Ethics Committee of Kangwon National University Hospital, due to the retrospective study.

Consent for publication

Not applicable

Data availability

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

Competing interests

The authors declare that they have no competing interests

Funding

Not applicable.

Author’s contributions

YeonJu La: Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Writing – original draft; Won Sup Oh: Conceptualization, Data curation, Supervision; Changhyup Kim: Data curation, Investigation; Myoung-nam Lim: Software, Validation; Yong Duk Jeon (Corresponding Author): Conceptualization, Methodology, Software, Resources, Supervision, Writing—Original Draft, Review & Editing.

Corresponding authors

Correspondence to Yong Duk Jeon

Acknowledgments

This study was supported by a 2023 Research Grant from Kangwon National University.

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No competing interests reported.

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Clinical outcomes of early remdesivir administration in hospitalized patients at high risk for severe COVID-19 during the Omicron wave

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