Abstract
As a result of sentinel surveillance for outpatients influenza-like illness (ILI), seasonal influenza activity remains below national baseline from 13 weeks of 2020 to 8 weeks of 2023 and Inpatient surveillance results for acute respiratory infections has decreased by less than half compared to pre-coronavirus disease 2019 (COVID-19) pandemic. In the 2022–2023 season, the weekly ILI rate was above the national baseline of 4.9 per 1,000 outpatients and flu activity increased early in the 37th week of 2022. The number of hospitalized patients for parainfluenza virus infection increased rapidly from August to October 2021 and for human metapneumovirus infection have been slightly increasing after October 2022. These unusual patterns of respiratory viruses are presumed to be due to the ease of COVID-19 related social distancing and control measures.
Keywords: Influenza, Acute respiratory infections, Sentinel surveillance, Coronavirus disease 2019 pandemic
Key messages
① What is known previously?
Prior to the COVID-19 pandemic, the seasonal influenza epidemic was mainly reported in the winter season, from December to April.
② What new information is presented?
From the COVID-19 pandemic to the present (January 2020–January 2023), as Influenza-like illness rates were low for 2 years and 6 months, and exceptionally, the number of inpatients with parainfluenza virus since August 2021 and human metapneumovirus since October 2022 were increased.
③ What are implications?
During the COVID-19 pandemic, influenza like illness rates and acute respiratory infections decreased, but from the second half of 2022, respiratory viruses with seasonal characteristics such as influenza, respiratory syncytial virus, parainfluenza virus has showed seasonal epidemic pattern like before COVID-19 pandemic period.
Introduction
Influenza and acute respiratory infections are mainly transmitted through the human respiratory tract. These are designated as class 41) infectious diseases in accordance with the 2020 “Infectious Disease Control and Prevention Act (the Infectious Disease Prevention Act)” and being monitored with the sentinel surveillance systems.
In the Republic of Korea (ROK), the influenza sentinel surveillance system operates by gathering reports from sentinel sites designated in accordance with the Infectious Disease Prevention Act.
Influenza sentinel surveillance systems is operated with primary clinics which reports influenza-like illness (ILI)2) and laboratory surveillance system which collects respiratory specimens from the participating primary clinics. Influenza sentinel sites composed of primary clinics with departments of pediatrics, internal medicine, and family medicine, and the surveillance period is 52 weeks in total (or 53 weeks) in seasonal units (36 weeks in the current year to 35 weeks in the following year). Medical institutions designated as surveillance sites report the number of patients with ILI and the total number of visited patients on a weekly (or daily) basis through the Integrated Health and Disease Management System (http://is.kdca.go.kr). For laboratory surveillance, sentinel sites that wish to participate are designated among sentinel sites participating in ILI surveillance to collect patient samples, and metropolitan/provincial health and environment research institutes conduct diagnostic tests and compile the results.
These results of influenza sentinel surveillance are used to monitor whether the influenza rate is over the influenza threshold; if the influenza rate increases over the threshold3), the influenza epidemic alert is issued after external experts meeting. Laboratory surveillance results are used to monitor circulating influenza virus subtypes and genotypes.
Inpatient surveillance for influenza and acute respiratory infections (ARI) targets hospital-level sentinel sites with 200 or more beds, and the medical institutions participating in ARI surveillance report the number of patients hospitalized for influenza and acute respiratory infections among those visiting the institution on a weekly basis.
The surveillance results for influenza and acute respiratory infections are posted on the website of the Korea Disease Control and Prevention Agency (KDCA) every week as “Weekly Newsletter for Infectious Disease sentinel Surveillance4),” and related information is fed back to the sentinel sites, local governments, and related ministries.
Since January 2020, the global influenza incidence has remained at a very low level due to the coronavirus disease 2019 (COVID-19) pandemic, but it has gradually increased in the Northern Hemisphere since the summer of 2022. In particular, according to the Global Influenza Surveillance and Response System (GISRS) of the World Health Organization (WHO), it was reported that during the winter of 2022, influenza virus was showing a higher detection rate than the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) virus in some countries in the Northern Hemisphere [1].
This article summarizes the surveillance results through the influenza and acute respiratory infection surveillance system during the COVID-19 pandemic period (1st week of 2020 to 8th week of 2023), and compared the trends in the incidence of influenza and acute respiratory infections (nine types) before and after the pandemic.
Methods
During the COVID-19 pandemic, from the 1st week of 2020 to the 8th week of 2023, a sample surveillance system was operated for influenza and acute respiratory infections (nine types), and the surveillance results were analyzed. ILI cases per 1,000 outpatients was calculated by age based on the reports from the Integrated Health and Disease Management System, which were reported every Tuesday. ILI is defined as a case who presented with a fever of 38℃ and cough or sore throat. Surveillance of inpatients for influenza and acute respiratory infections confirmed the number of admitted reported to the Integrated Health and Disease Management System every week when diagnosed with the relevant infectious disease. The diagnostic criteria for reporting were based on the “Notice of Diagnostic Criteria for Reporting Infectious Diseases (KDCA Notice No. 2023-3)5),” and the number of patients with a confirmed infection was calculated according to the criteria. For the two types of bacteria, final patients were reported when bacterial isolates or specific genes were detected. The nine types of acute respiratory infections were caused by seven types of viruses (adenovirus [AdV)], human bocavirus [HBoV)], parainfluenza virus [PIV], respiratory syncytial virus [RSV], rhinovirus [RV], human metapneumovirus [HMPV], human coronavirus [HCoV]) and two types of bacteria (Mycoplasma pneumoniae and Chlamydophila pneumoniae).
Results
Influenza sentinel surveillance consists of sentinel sites, municipal and regional public health centers, health and environment research institutes, and KDCA (Figure 1). The current status of designation of influenza sentinel sites from 2020 to 2022 is shown in Table 1. During the COVID-19 pandemic, the influenza sentinel surveillance system has been operated, 195 institutions were designated and participated in clinical surveillance in 2022. Among these, 63 institutions participated in laboratory surveillance in 2022. In 2022, 219 institutions participated in hospital-level inpatient surveillance with 200 or more beds.
Figure 1. The influenza sentinel surveillance system in Korea.
KDCA=Korea Disease Control and Prevention Agency; RIPHE=Research Institute of Public Health and Environment; ILI=influenza-like illness, patients who having sudden fever over 38℃ and cough or sore throat.
Table 1. Sentinel institutions in Korean influenza surveillance, 2020–2022.
| Year | ILI surveillancea) | Laboratory surveillanceb) | ARIsurveillancec) |
|---|---|---|---|
| 2020 | 199 | 52 | 217 |
| 2021 | 199 | 52 | 219 |
| 2022 | 195 | 63 | 219 |
Values are presented as number. ILI=influenza-like illness; ARI=acute respiratory infections. a)Sentinel sites with departments of internal medicine, pediatrics, and family medicine; b)sentinel sites willing to participate among ILI reporting sentinel sites; c)general hospitals, hospital-level sentinel sites with more than 200 beds, public hospitals.
During the COVID-19 pandemic and after 2020, the ILI rates showed a different pattern from previous seasons. After the appearance of the SARS-CoV-2 virus in the ROK in January 2020, the ILI rates decreased sharply from the 8th week (8.5 patients), and there was no seasonal epidemic of influenza for a period of 2 years and 6 months until the 35th week of 2022 (4.3 patients), which was maintained at a low level (Figure 2). The KDCA issued an epidemic alert in the 37th week of 2022.
Figure 2. Weekly influenza-like illness rates during Korea’s COVID-19 pandemic period.
Upon comparing ILI rates with COVID-19 waves, ILI rates remained below the epidemic threshold from the 2nd wave (from August 2020), 3rd wave (from November 2020), 4th wave (from July 2021; during which the delta variant was prevalent), 5th wave (from January 2022; when the omicron variant was prevalent), and 6th wave (from July 2022). However, it started to rise gradually after September 2022, when the 6th wave ended, peaking in December (60.7 individuals in 53 weeks) and gradually decreasing. These trends were seasonal, similar to those before the COVID-19 pandemic (Figure 2).
The ILI rates was high among children aged from 1 to 6 years, 7 to 12 years, and 13 to 18 years, during 2017 and 2018, prior to the COVID-19 pandemic. During the 2018–2019 season, high ILI rates was observed among elementary, middle, and high school students; however, during the 2022–2023, the age groups of 7 to 12 years and 13 to 18 years showed a higher rates than in the 2017–2018 season (Figure 3).
Figure 3. Weekly influenza-like illness consultation rates by age group.
As a result of ARI surveillance, the number of inpatients for RSV and RV was relatively high during the winter season from 2017 to the 8th week of 2023; however, from 2020 to 2022, the number decreased to less than half than that in the winter season (Figure 4).
Figure 4. The number of hospital inpatients by respiratory viruses.
Many hospitalized patients with the HMPV were observed from spring to early summer, but there were almost none during the COVID-19 pandemic; the number of hospitalized patients increased once between October 2022 and November 2022. As for the PIV, which led to many hospitalizations at around the same time, the number of inpatients demonstrated an unusual sharp increase from August 2021 to October 2021, and inpatient outbreak have been occurred since October 2022 (Figure 5).
Figure 5. The number of hospital inpatients for parainfluenza virus and human metapneumovirus infection.
On comparing the number of patients hospitalized for influenza and acute respiratory infections by year, the number of hospitalized patients after the COVID-19 pandemic (2020–2022) decreased compared to the pre-pandemic period (2017–2019). AdV decreased the most by 86.9%, and influenza decreased by 84.9%. While Mycoplasma pneumoniae decreased by 83.4%, Chlamydia pneumoniae decreased by 14.2%, showing the smallest decrease after the COVID-19 pandemic (Table 2).
Table 2. The number of hospital inpatients for influenza virus and acute respiratory infections .
| Year | Influenza | Acute respiratory infections | |||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| Total | Rhino virus |
Respiratory syncytial virus | Adenovirus | Parainfluenza virus | Human metapneumovirus | Human boca virus |
Human coronavirus | Mycoplasma | Chlamydia | ||
| 2017 | 8,723 | 70,442 | 21,467 | 14,450 | 6,663 | 7,971 | 4,388 | 4,581 | 3,825 | 6,902 | 195 |
| 2018 | 23,583 | 93,402 | 25,896 | 16,227 | 13,627 | 10,586 | 7,052 | 5,446 | 7,084 | 7,225 | 259 |
| 2019 | 14,000 | 101,083 | 29,653 | 11,897 | 15,162 | 12,804 | 6,951 | 6,426 | 4,376 | 13,479 | 335 |
| 2020 | 8,435 | 24,260 | 7,307 | 4,390 | 2,283 | 707 | 782 | 1,309 | 3,303 | 4,004 | 175 |
| 2021 | 206 | 18,004 | 6,929 | 743 | 1,092 | 4,415 | 34 | 3,216 | 126 | 1,265 | 184 |
| 2022 | 2,713 | 32,439 | 8,646 | 8,405 | 1,656 | 3,763 | 3,461 | 3,004 | 1,673 | 1,591 | 240 |
| P1 | 46,306 | 264,927 | 77,016 | 42,574 | 35,452 | 31,361 | 18,391 | 16,453 | 15,285 | 27,606 | 789 |
| 2017–2019 | |||||||||||
| P2 | 7,009 | 86,449 | 24,755 | 18,090 | 4,647 | 12,660 | 7,114 | 9,345 | 4,575 | 4,586 | 677 |
| 2020–2022 | |||||||||||
| P1 on P2 (%) | △84.9 | △67.4 | △67.9 | △57.5 | △86.9 | △59.6 | △61.3 | △43.2 | △70.1 | △83.4 | △14.2 |
Values are presented as number. P1=period 1; P2=period 2.
Discussion
During the COVID-19 pandemic, the incidence of respiratory infection decreased worldwide, and in the ROK, the number of reported cases of national notifiable infectious diseases, excluding COVID-19, continued to decrease (182,570 in 2019; 105,990 in 2020; and 99,405 in 2021). In particular, the number of patients with class 2 respiratory infectious diseases decreased by 22.1% (from 64,607 in 2020 to 49,943 in 2021) due to the mask waring mandates and the implementation of social distancing. In the case of influenza and acute respiratory infections, the incidence of influenza was lower than the seasonal epidemic threshold for a period of 2 years and 6 months with no epidemics in the communities. The number of hospitalized patients with acute respiratory infections also decreased by 25.8% (from 24,260 in 2020 to 18,004 in 2021) [2].
Overseas, no seasonal influenza epidemic was observed during the COVID-19 pandemic from January 2020 to 2022. In few other countries, the outbreaks of RSV and PIV infections, which show seasonal characteristics, occurred later than usual [3,4].
After the omicron variant became prevalent, influenza virus A (H3N2) was detected in July 2022 and the influenza A virus was mainly detected until January 2023, like the past seasonal pattern [5]. In addition, in the ARI surveillance, the number of RSV and PIV tended to show seasonal pattern for a certain period of time, although lower than that of the past. The number of hospitalization has increased from spring to early summer before 2020 due to HMPV; however, in 2022, the number of hospitalized patients increased around October, showing an unusual pattern.
These results show that after the beginning of 2020, person-to-person contact decreased sharply due to the strictly enforced COVID-19 related social distancing measures but increased again after social distancing gradually eased from the winter of 2021. In particular, in the children, the accumulation of susceptible populations that have never been exposed to the respiratory viruses might have contributed to the increase of the overall cases.
This study analyzed the sentinel surveillance results, and may not represent the overall situations in ROK, although it is very unlikely given the structure of the sentinel surveillance systems. In addition, when interpreting the trends from sentinel sites, strong non-pharmaceutical interventions during COVID-19 pandemic period has to be considered.
In conclusion, a stable and systematic surveillance system should be implemented because the epidemic patterns of influenza and acute respiratory infections have changed after the COID-19 pandemic. The KDCA will provide surveillance outcomes to general public as well as medical societies in a timely manner as we step out of COVID-19 pandemic period.
Acknowledgments
None.
1) 「감염병의 예방 및 관리에 관한 법률」 제2조(정의)에 따라, “제4급감염병”이란 제1급부터 제3급감염병 외에 유행 여부를 조사하기 위하여 표본감시 활동이 필요한 감염병을 말한다.
2) 인플루엔자 의사환자(ILI): 38℃ 이상의 갑작스러운 발열과 더불어 기침 또는 인후통을 보이는 환자
3) 인플루엔자 유행기준: 과거 3년간 비유행 기간 인플루엔자 의사환자 분율+2×표준편차
4) 다운로드위치: 질병관리청 홈페이지(www.kdca.go.kr) > 간행물ㆍ통계 > 통계 > 감염병발생정보 > 표본감시주간소식지
5) 「감염병 신고를 위한 진단기준 고시」 (시행 2023. 2. 15., 질병관리청고시 제2023-3호)에 따름
1) In accordance with Article 2 (Definition) of the “Infectious Disease Control and Prevention Act” Class 4 Infectious Disease: Infectious diseases other than those in Class 1 to Class 3 that require sample surveillance activities to investigate whether they are prevalent.
2) ILI: Patients with sudden fever of 38℃ or higher and cough or sore throat
3) Influenza epidemic threshold: average ILI of non-epidemic period for the last 3 years+2×standard deviation
4) Korea Disease Control and Prevention Agency (www.kdca.go.kr) > Publications/Statistics > Statistics > Infectious Disease Outbreak Information > Sample Surveillance Weekly Newsletter
5) In accordance with the “Notification of Diagnostic Criteria for Reporting Infectious Diseases” (Enforced on February 15, 2023; Korea Disease Control and Prevention Agency No. 2023-3)
Declarations
Ethics Statement: Not applicable.
Funding Source: None.
Conflict of Interest: The authors have no conflicts of interest to declare.
Author Contributions: Conceptualization: JC. Data curation: YS. Formal analysis: SK. Writing – original draft: JC. Writing – review & editing: IK, JG.
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