SARS-CoV-2 reinfection with Omicron variant in Shaanxi Province, China: December 2022 to February 2023

The prevalence of SARS-CoV-2 reinfection remained relatively low during the pre-Omicron period of the COVID-19 pandemic [10‐11], but cases of reinfection rose substantially with the emergence of the Omicron variant, which quickly became dominant [7, 12‐13]. Conducting the reinfection study is crucial to understanding the natural history of SARS-CoV-2 infection among Shaanxi provincial residents after China adjusted the anti-COVID measures. Having a knowledge of the proportions of reinfection is important when evaluating the impact on the healthcare system, allowing hospitals to stock up on supplies and medical equipment in advance of the outbreak. Characterizing the association between reinfection and vaccination history could provide information about the efficacy of hybrid immunization against Omicron. In our study, widespread SARS-CoV-2 reinfections occurred across the Shaanxi province during the first Omicron-dominant wave between December 2022 and February 2023. We found that the reinfection rate increased significantly over time, reaching a peak of more than 20% among those who were infected nearly one year prior to the Omicron period. However, within 6 months after being previously infected with Omicron, we found a low probability of reinfection.

Many studies on SARS-CoV-2 reinfection have been conducted in different various countries and regions during the different stages of the COVID-19 pandemic. Omicron was first reported in South Africa in early November 2021, sparking epidemics in over 100 countries and overcrowding hospitals in several of them. In comparison with our study, the rate of reinfection in Vojvodina, Serbia was substantially lower, with 5.49% of the study population experiencing reinfection between March 2020 and January 2022 and with a significantly increased incidence of reinfection during the Omicron wave [14]. Although lower than those of Guangdong province, China (28.3%) [15], the pooled reinfection rates in our study (11.94%) were comparable to those of Jiangsu province (12.61%) [16] and Zhejiang province (12.82%) [17]. The several local outbreaks in Shaanxi province were contained inside a specific geographical region throughout two maximum incubation periods owing to the dynamic zero-COVID strategy, which also prevented the outbreaks from spreading to nearby provinces and areas. Other Chinese provinces have effectively stopped the spread of viral infections by implementing the same prevention and control strategies. Because outbreaks involving different virus strains have occurred at different times throughout the county, the results of related studies have varied [15‐17]. Nonetheless, the findings of past research show that individuals who were first infected with Omicron had a reduced rate of reinfection than those who were first infected with Delta or the original SARS-CoV-2 strain.

By the end of 2022, China was experiencing a sharp increase in COVID-19 infections. Following the relaxation of anti-COVID-19 measures, it is estimated that 82.4% of the country’s population was infected with Omicron between December 2022 and February 2023 [18]. Around December 25, 2022, the Chinese National Influenza Surveillance Network recorded a 60% positive rate [4]. During that time, SARS-CoV-2 was the predominant respiratory infectious disease in the nation. The rapid spread of infection put an undue burden on medical resources, making it difficult to acquire antigen testing reagents as well as causing a shortage of locations for nucleic acid testing in Shaanxi Province. As a result, certain COVID-19 infections could not be identified through antigen or nucleic acid testing. For this reason, we incorporated the following definition of reinfection in the survey: individuals with symptoms and an epidemiological history of SARS-CoV-2 infection but who failed to obtain a positive diagnostic result. Individuals who met these criteria were included in the study to ascertain whether reinfection had occurred.

Reinfections were more frequently reported among individuals between age 18 and 38 years who were first infected with Delta than among adults over age 60 years. This may be because younger people have more social contact and an increased likelihood of infection than older people. This group should be advised to use personal protection during subsequent epidemic waves. Similar to other studies [10, 15], medical workers were found to be more susceptible to reinfection than workers in other occupations. Medical personnel should implement efficient preventative measures at work because they have a significant risk of exposure to SARS-CoV-2.

According to published data, there were more asymptomatic carriers among Omicron-infected individuals than among those infected with other virus variants [19]. However, compared with the first infection episode, more patients who were previously infected with the Delta variant were more symptomatic. Many cities in Shaanxi Province implemented lockdown measures and carried out rounds of mass testing during the Delta outbreak that occurred between December 2021 and January 2022. With a positive SARS-CoV-2 nucleic acid test result, infected individuals were placed under quarantine and received prompt, efficient treatment. For this reason, more asymptomatic Delta infections were identified early on. Additionally, in accordance with a previously report [19], people infected with Omicron were less likely than those infected with Delta to experience a loss of smell or taste. Furthermore, BA.1 and BA.2 Omicron sublineages were responsible for several domestic infections prior to December 2022 in Shaanxi province, in the study we found the proportion of asymptomatic cases was comparable between first and second infection episodes among patients who were first infected with Omicron, which has not been previously reported.

We found the differences in clinical characteristics between first and second infections were small, and no correlation between vaccination and reinfection. In our study, more than 55% of the study population had received a booster dose of vaccine. Similarly, in a cohort study on the incidence of reinfection conducted in Shanghai, China, more than 60% of participants had received one booster dose. It also found that vaccination status was not significantly associated with reinfection [20]. Both studies pointed out the stronger capacity for vaccine breakthrough of emerging Omicron subvariants. Reinfection was not associated with an increased risk of COVID-19 hospitalization, as evidenced by our study that only two patients were hospitalized during their second infection in the study, which is consistent with the result of a systematic review [21]. However, this could be because of the study’s limited sample size in our study. Further research is needed to assess how well hybrid immunity can protect people aged 60 years or older or people with comorbidities.

The study has several limitations. First of all, because this was a retrospective study, an assessment of the SARS-CoV-2 symptoms and epidemiological exposure history in the study population identified nearly 40% of reinfections using a questionnaire survey but without a positive nucleic acid or antigen test. Therefore, recall bias could be present. Second, mass testing under China’s dynamic zero-COVID approach was replaced on December 8, 2022 by 10 New Prevention and Control Measures. Individuals were encouraged to purchase antigen test kits or undergo nucleic acid testing at a medical facility if deemed necessary. Thus, there may be an underestimation of reinfection in mild and asymptomatic cases, which can remain undetected if the patient does not visit a clinic or nucleic acid testing site. Third, a single variant was dominant during each local outbreak in Shaanxi province, and not all the infected patients underwent genotyping with whole genome sequencing, we were unable to compare the reinfection rates owing to various Omicron sub-variants. And patients’ serum antibody levels against COVID in Shaanxi province during December 2021 and October 2022 were insufficient to distinguish between reinfection based on the waning immunity and according to different SARS-CoV-2 subvariants.