Abstract
The Daegu-Gyeongbuk has experienced an upsurge in cases of SARS-CoV-2 reinfections that have been attributed to the Omicron. In preparation for implementing preventative and control measures against reinfections, a study was conducted to analyze the incidence of suspected SARS-CoV-2 reinfections and the associated risk factors among patients with coronavirus disease 2019 (COVID-19), reported in Daegu-Gyeongbuk, from January 20, 2020, to December 31, 2022. The suspected SARS-CoV-2 reinfection rate in the region was 3.25% from the first suspected case in May 2021 until December 30, 2022. Notably, during the final four weeks of 2022 (4–31 December), the suspected SARS-CoV-2 reinfection rate increased to 13.60%. The study results indicated that the 6–11- and 12–17-year age groups (i.e., school students) had 1.65 times and 1.96 times higher risk of SARS-CoV-2 reinfection, respectively, compared with that in the 18–49-year age group. The at-risk elderly population, aged 60 years and above, also demonstrated a 1.19 times higher risk of SARS-CoV-2 reinfection than that in the 18-49-year age group. Additionally, the risk of SARS-CoV-2 reinfection decreased by 58% for fully vaccinated individuals, 40% for those vaccinated with the first booster, and 51% for those vaccinated with a third booster, compared with the risk in unvaccinated individuals. In conclusion, this study underscores the importance of regular administration of COVID-19 vaccines that have been modified according to the variants for school-aged children and elderly individuals aged 60 and above.
Keywords: Key words: COVID-19, Reinfection, Vaccine efficacy
Key messages
① What is known previously?
The Omicron variant has been associated with an increase in reinfection and a reduction in vaccine effectiveness.
② What new information is presented?
The risk of reinfection increased among school-aged children and the elderly population, aged over 60s. There were differences in reinfection risk depending on the number of vaccine doses received.
③ What are implications?
It is crucial to administer regularly modified COVID-19 vaccines to school-aged children and the elderly population, aged over 60s, to mitigate the impact of the viral variants.
Introduction
While the immunogenicity of vaccination has been reported to last for at least 6–8 months, the protective effect reduces due to the immune evasion response of the new variants of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) [1]. The first case of reinfection with SARS-CoV-2 was reported in August 2020 in Hong Kong. Research has shown that the recently prevalent Omicron variant increases the risk of reinfection and reduces the preventive effect of vaccination [2-4]. However, studies have also shown that vaccination produces higher titers of neutralizing antibodies than that from natural immunity. Additionally, studies have shown vaccination to be necessary even with a history of infection with SARS-CoV-2 as it reduces the risk of severe symptoms in the event of reinfection [5,6].
Recently, cases of reinfection with coronavirus disease 2019 (COVID-19) have increased in Gyeongsangbuk-do. However, the COVID-19 vaccination rate is low due to prolonged COVID-19 and high fatigue from vaccines. Therefore, it is important to identify and quantify the risk factors to establish an effective quarantine policy and increase public confidence in the policy. This study aimed to identify the status of presumed reinfection cases among COVID-19 patients reported in the Gyeongbuk region (Daegu and Gyeongbuk) between January 20, 2020, and December 31, 2022, and to analyze demographic characteristics and risk factors.
Methods
1. Methods
A cross-sectional study on the demographic characteristics of patients presumed to be reinfected with COVID-19 and a retrospective cohort study were conducted to analyze the correlation between sex, age, vaccination history, time of the first infection, and reinfection with COVID-19.
2. Patients
In the COVID-19 information management system of the Korea Disease Control and Prevention Agency, a case study was conducted on 2,583,266 confirmed cases of COVID-19 reported in Gyeongsangbuk-do from January 20, 2020, to December 31, 2022. The demographic information of patients with COVID-19, including sex, age, severe illness, and death, was obtained from the COVID-19 information management system, while the vaccination history was obtained from the COVID-19 vaccination management of the disease health integrated management system.
3. Case Definition
A presumed reinfection case is defined as a re-detection with COVID-19 after 90 days from the date of first confirmation regardless of symptoms, or a re-detection of COVID-19 after 45 days from the date of first confirmation with a history of exposure to symptoms or confirmed cases (or overseas travel history). Re-detection is defined as a case in which, after a COVID-19 patient is released from isolation (according to the quarantine release criteria), a polymerase chain reaction diagnostic test, rapid antigen test (for experts), or emergency screening test (with a product of emergency use authorization) reveals a positive result [7].
The time of infection was divided based on the period wherein each variant accounted for more than 50% of the weekly SARS-CoV-2 variant test as follows: pre-delta variant (before June 30, 2021); delta dominance (July 1, 2021, to January 15, 2022); BA.1 dominance (January 16, 2022–March 19, 2022); BA.2 dominance (March 20, 2022–July 23, 2022); and BA.5 dominance (July 24, 2022–December 30, 2022) [8].
4. Statistical Analysis
Through multivariate logistic regression analysis, the effects of sex, age, vaccination history, and the time of the first infection upon reinfection were confirmed. Statistical analysis was performed using SAS version 9.4 (SAS Institute Inc.).
Results
1. Status of Presumed Reinfection Cases
From January 20, 2020, to December 31, 2022, of the 2,583,266 confirmed cases of COVID-19 in Gyeongsangbuk-do, 83,922 were presumed reinfection cases, with an incidence rate of 3.25%. Of the presumed reinfection cases, 99.97% (83,899 cases) occurred during the Omicron variant dominance period, accounting for most of the COVID-19 infection period (Table 1). Among the confirmed cases of COVID-19 reported in Gyeongsangbuk-do, the reinfection rate was 3.25% from the first presumed reinfection case in May 2021 until December 30, 2022. When classified according to the period of dominance for each variant, the reinfection rate was 0.09% during the delta dominance period, 0.19% during the BA.1 dominance period, 0.57% during the BA.2 dominance period, and 7.90% during the BA.5 dominance period. In the last four weeks of 2022 (December 4, 2022 to December 31, 2022), the reinfection rate gradually increased to 13.60% (Figure 1). The overall COVID-19 reinfection rate in the Republic of Korea (ROK) was 0.35% by April 17, 2022. The reinfection rate before the Omicron dominance period was 0.10%, while the reinfection rate during the Omicron dominance period was 0.36%, approximately 3.6 times higher than before [9]. Regarding foreign cases, the reinfection rate was reported to be 2.96% in Italy (August 2021–March 2022) by Sacco et al. [10], 3.16% in France (March 2021–February 2022) by Bastard et al. [11], 5.19% in Denmark (January 2020–January 2022) by Nielsen et al. [12], 3.58% in South Africa (March 2020–February 2022) by Pulliam et al. [13], and 3.04% in Mexico City (March 2020–July 2022) by de Anda-Jauregui et al. [14]. Particularly, in a population-based study of each region, the reinfection rate during the Omicron dominance period was 11.50% in Iceland (December 2021–February 2022) by Eythorsson et al. [15], and 11.75% in Denmark (December 21–January 2022) by Nielsen et al. [12].
Table 1. Suspected severe acute respiratory syndrome coronavirus 2 reinfection cases in the Daegu-Gyeongbuk region during the period of variant epidemic (As of December 31, 2022).
| Characteristic | 2nd infection cases (suspected reinfection cases) | |||||
|---|---|---|---|---|---|---|
| Total | Wild type, Alpha & Beta variantsa) | Delta variantsb) | Omicron variants | |||
| BA.1c) | BA.2d) | BA.5e) | ||||
| Total | 83,922 (100.0) | 1 (0.00) | 22 (0.03) | 1,189 (1.42) | 5,468 (6.52) | 77,242 (92.04) |
| 1st infection cases | ||||||
| Wild type, Alpha&Beta variantsa) | 3,976 (4.74) | 1 (0.00) | 18 (0.02) | 604 (0.72) | 1,409 (1.68) | 1,944 (2.32) |
| Delta variantb) | 4,774 (5.69) | - | 4 (0.00) | 576 (0.69) | 1,540 (1.84) | 2,654 (3.16) |
| Omicron variant | ||||||
| BA.1c) | 38,096 (45.39) | - | - | 9 (0.01) | 1,687 (2.01) | 36,400 (43.37) |
| BA.2d) | 34,562 (41.18) | - | - | - | 832 (0.99) | 33,730 (40.19) |
| BA.5e) | 2,514 (3.00) | - | - | - | - | 2,514 (3.00) |
Values are presented as number (%). a)2020.1.20.–2021.7.24., b)2021.7.25.–2022.1.15., c)2022.1.16.–2022.3.19., d)2022.3.20.–2022.7.23., e)2022.7.24.–2022.12.31.
Figure 1. Weekly trend of the severe acute respiratory syndrome coronavirus 2 reinfection rate among coronavirus disease-19 confirmed cases in the Daegu-Gyeongbuk region.
Among the presumed reinfection cases in Gyeongsangbuk-do, 142 patients were seriously ill (including severe illness and death), with a severity rate of 0.17%, and 91 individuals died after reinfection, with a fatality rate of 0.11%. The severity and fatality rates of all COVID-19 confirmed cases in the ROK, as of September 3, 2022, were 0.20% and 0.12%, respectively, showing no significant differences from those of reinfection [9]. Medić et al. [16] reported that from March 2020 to October 21, Serbia’s COVID-19 reinfection severity rate was 1.08% and the fatality rate was 0.15%, which was lower than the initial infection severity rate (7.95%). However, a study by Nguyen et al. [17] reported no difference in the severity rate between the first COVID-19 infection and reinfection in France from March 2020 to August 2021.
2. Characteristics and Reinfection Rate
The reinfection rate by region was 3.34% (42,060 people) in Daegu, a metropolitan city, and was similar, at 3.16% (41,862 people), in Gyeongsangbuk-do, near the metropolitan city. The reinfection rate by sex was higher for females (3.48%) than for males (2.97%). Reinfection rates were the highest in the following age groups: 6–11 years (6.83%), 12–17 years (5.38%), and 80 years or older (5.24%) in Gyeongsangbuk-do (Table 2). The reason for the high reinfection rate in school-age children is attributed to the influence of group activities and asymptomatic infections in educational facilities such as schools and private institutes, as well as the low vaccination rate. According to Medić et al. [16], the COVID-19 reinfection rate in Serbia was higher for females (6.01%) than for males (4.90%). In addition, it was the highest at 8.26% in individuals who were in their 30s, followed by 7.29% in those in their 40s, 6.70% in those in their 20s, and 5.38% in those in their 50s. The reinfection rate according to vaccination history was the highest in the non-vaccination group (95.76%), followed by the groups that received the initial primary vaccine series (2.35%) and booster shots (0.16%), which was in line with the results of this study. Furthermore, Medić et al. [18] reported COVID-19 reinfection rates in children and adolescents, wherein the reinfection and asymptomatic rates were high in those aged 0–17 years during the Omicron dominance period, and the risk of reinfection was 1.3 times higher in the non-vaccination group than in the group that completed the first dose of vaccination.
Table 2. Incidence rate of suspected severe acute respiratory syndrome coronavirus 2 reinfection in the Daegu-Gyeongbuk region by sex and age (As of December 31, 2022).
| Characteristic | Daegu-Gyeongbuk | Daegu | Gyeongbuk | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| 1st infection | 2nd infection | Reinfection rate (%) | 1st infection | 2nd infection | Reinfection rate (%) | 1st infection | 2nd infection | Reinfection rate (%) | |||
| Total | 2,583,266 | 83,922 | 3.25 | 1,258,413 | 42,060 | 3.34 | 1,324,853 | 41,862 | 3.16 | ||
| Sex | |||||||||||
| Male | 1,186,134 | 35,268 | 2.97 | 561,300 | 17,024 | 3.03 | 624,834 | 18,244 | 2.92 | ||
| Female | 1,397,132 | 48,654 | 3.48 | 697,113 | 25,036 | 3.59 | 700,019 | 23,618 | 3.37 | ||
| Age group (yr) | |||||||||||
| 0–5 | 127,745 | 3,974 | 3.11 | 64,724 | 2,072 | 3.20 | 63,021 | 1,902 | 3.02 | ||
| 6–11 | 220,877 | 15,075 | 6.83 | 107,494 | 7,485 | 6.96 | 113,383 | 7,590 | 6.69 | ||
| 12–17 | 202,088 | 10,874 | 5.38 | 98,865 | 5,492 | 5.56 | 103,223 | 5,382 | 5.21 | ||
| 18–29 | 390,562 | 10,923 | 2.80 | 202,127 | 5,669 | 2.80 | 188,435 | 5,254 | 2.79 | ||
| 30–39 | 325,780 | 8,687 | 2.67 | 162,516 | 4,456 | 2.74 | 163,264 | 4,231 | 2.59 | ||
| 40–49 | 368,436 | 9,039 | 2.45 | 181,473 | 4,596 | 2.53 | 186,963 | 4,443 | 2.38 | ||
| 50–59 | 342,048 | 6,707 | 1.96 | 166,117 | 3,450 | 2.08 | 175,931 | 3,257 | 1.85 | ||
| 60–69 | 314,350 | 7,872 | 2.50 | 147,398 | 4,024 | 2.73 | 166,952 | 3,848 | 2.30 | ||
| 70–79 | 174,690 | 4,661 | 2.67 | 80,360 | 2,307 | 2.87 | 94,330 | 2,354 | 2.50 | ||
| ≥80 | 116,690 | 6,110 | 5.24 | 47,339 | 2,509 | 5.30 | 69,351 | 3,601 | 5.19 | ||
3. Risk Factors
To estimate risk factors for reinfection, sex, age, vaccination history, and time of the first infection were adjusted and analyzed. The risk of reinfection was 1.29 times higher in females than that in males. The risk of reinfection was 1.65 times and 1.96 times higher among school-age children aged 6–11 and 12–17 years, respectively than in those aged 18–49 years. Moreover, the risk of reinfection increased by 1.19 times in the high-risk group comprising those aged 60 years or older. The risk of reinfection according to COVID-19 vaccination history was reduced by 58% in the group that received the initial primary vaccine series, 40% in the group that received booster shots, and 51% in the group that received winter vaccination, compared to the non-vaccination group (Table 3). The 1.05-fold increase in the risk of reinfection in the group that received the fourth dose of vaccination compared to the non-vaccination group and the high risk of reinfection in the group that received the booster shots compared to the group that received the initial primary vaccine series may have been due to the low vaccine booster rate and the fact that inpatients at long-term care facilities and hospitals were prioritized for the booster shots. The increase in the risk of reinfection in school-age and old age is estimated to be due to the influence of group education environments such as schools and private institutes and co-living environments for high-risk groups such as long-term care facilities and hospitals, respectively. The low vaccine booster rate may also have contributed to the increase in the risk of reinfection. The decrease in the risk of reinfection with the increase in time of the first infection with SARS-CoV-2 could be a result of natural immunity. According to Piazza et al. [19], in Italy, the risk of reinfection increased by 1.11 times in females compared to males from September 21 to May 22. Furthermore, it increased by 1.22, 1.76, 1.66, and 1.52 times in the groups comprising those aged 0–19 years, 20–39 years, 40–59 years, and 80 years or older, respectively; it decreased by 38% and 20% in the group before 120 days from vaccination and group after 120 days from vaccination, respectively compared with the non-vaccination group. The finding that vaccination reduced the risk of reinfection was consistent with the results of this study. The difference in the high-risk age group from that of the ROK may have been influenced by social factors such as the unique educational environments and long-term care facilities and hospitals, as well as the country’s vaccine policy.
Table 3. Risk factors for suspected severe acute respiratory syndrome coronavirus 2 reinfection cases in the Daegu-Gyeongbuk region (As of December 31, 2022).
| Univariate | Multivariate | ||||||||
|---|---|---|---|---|---|---|---|---|---|
| Independent variable | β | OR | (95% CI) | p-value | β | OR | (95% CI) | p-value | |
| Sex | |||||||||
| Male | ref. | 1.000 | ref. | 1.000 | |||||
| Female | 0.168 | 1.183 | (1.166–1.199) | <0.001 | 0.257 | 1.293 | (1.274–1.311) | <0.001 | |
| Age group (yr) | |||||||||
| 0–5 | 0.389 | 1.475 | (1.430–1.522) | <0.001 | –0.221 | 0.802 | (0.772–0.832) | <0.001 | |
| 6–11 | 1.133 | 3.104 | (3.043–3.167) | <0.001 | 0.498 | 1.645 | (1.599–1.692) | <0.001 | |
| 12–17 | 0.679 | 1.973 | (1.927–2.020) | <0.001 | 0.675 | 1.964 | (1.914–2.016) | <0.001 | |
| 18–49 | ref. | 1.000 | ref. | 1.000 | |||||
| 50–59 | –0.311 | 0.733 | (0.714–0.753) | <0.001 | –0.307 | 0.735 | (0.715–0.756) | <0.001 | |
| ≥60 | 0.144 | 1.155 | (1.133–1.177) | <0.001 | 0.175 | 1.192 | (1.166–1.218) | <0.001 | |
| Vaccination | |||||||||
| Not vaccinated | ref. | 1.000 | ref. | 1.000 | |||||
| At least one dosea) | –1.067 | 0.344 | (0.322–0.367) | <0.001 | –1.273 | 0.280 | (0.262–0.299) | <0.001 | |
| Fully vaccinated | –1.045 | 0.352 | (0.345–0.359) | <0.001 | –0.839 | 0.432 | (0.421–0.444) | <0.001 | |
| 1st booster dose | –0.945 | 0.389 | (0.382–0.395) | <0.001 | –0.519 | 0.595 | (0.580–0.610) | <0.001 | |
| 2nd booster dose | –0.529 | 0.589 | (0.572–0.606) | <0.001 | 0.051 | 1.053 | (1.014–1.093) | <0.001 | |
| 3rd booster dose | –0.708 | 0.493 | (0.480–0.506) | <0.001 | –0.706 | 0.494 | (0.477–0.511) | <0.001 | |
| 1st infected period | |||||||||
| Wild type, Alpha & Beta variants | ref. | 1.000 | ref. | 1.000 | |||||
| Delta variant | –0.260 | 0.771 | (0.735–0.809) | <0.001 | –0.347 | 0.707 | (0.223–0.257) | <0.001 | |
| Omicron variant | |||||||||
| BA.1 | –1.650 | 0.192 | (0.185–0.199) | <0.001 | –1.848 | 0.158 | (0.293–0.307) | <0.001 | |
| BA.2 | –2.183 | 0.113 | (0.109–0.117) | <0.001 | –2.400 | 0.091 | (0.253–0.265) | <0.001 | |
| BA.5 | –4.778 | 0.008 | (0.008–0.009) | <0.001 | –4.957 | 0.007 | (0.007–0.007) | <0.001 | |
| Nagelkerke: R2=0.112 | |||||||||
OR=odds ratio; CI=confidence interval. a)At least one dose as an incomplete vaccination.
Discussion
As for the limitations of this study, first, the vaccination rate by age was not analyzed; therefore, the relationship between vaccination and the increased risk of reinfection in school-age children and older adults had to be presumed. Further analysis is required for accurate results. Second, the time variable was not considered in the risk factor analysis of COVID-19 reinfection. Only by considering the changes over time from initial infection with SARS-CoV-2 to reinfection can the effectiveness of vaccination in preventing reinfection and the effect of the time of the first infection could be more accurately identified. Therefore, the Cox proportional hazard model must be used to further analyze the risk factors for COVID-19 reinfection. Third, although there are various social factors such as the start of school and the start of vaccination, only the epidemiological characteristics according to the dominant variant were presented for the influence of the time of the infection upon reinfection. In the future, additional analyses on the relationship between social and policy factors and reinfection need to be undertaken in this regard.
Reinfection occurred even with multiple Omicron subvariants. It has been reported that natural immunity formed by BA.1 is less effective in preventing BA.4/5 infection than BA.2 infection. However, vaccine-induced immunity is equally effective in preventing BA.2 and BA.4/5 infections [20]. This study revealed that the risk of reinfection decreases with more doses of the vaccination, suggesting that it will be necessary to periodically provide improved COVID-19 vaccines according to the emergence of new variants for school-age children and those aged 60 years or older who live in groups.
Acknowledgments
None.
Declarations
Ethics Statement: Not applicable.
Funding Source: None.
Conflict of Interest: The authors have no conflicts of interest to declare.
Author Contributions: Conceptualization: TS. Data curation: SC, HP. Formal analysis: SC, CP. Investigation: SC, YHJ. Methodology: SC, MJH. Writing – original draft: SC. Writing – review & editing: TS.
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