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Epidemiology and Surveillance

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Public Health Weekly Report 2020; 13(18): 1207-1216

Published online April 29, 2020

© The Korea Disease Control and Prevention Agency

Establishment of surveillance system and network for the evaluation of influenza vaccine effectiveness and estimation of influenza vaccine effectiveness in preventing influenza

Park Sun Young, Kim Jong Hee, Cho En Hi, Kim Woo Joo

Division of VPD control & NIP, Center for Infectious Disease Surveillance & Response, KCDC; Korea University

*교신저자 : wjkim@korea.ac.kr, 02-2626-3051

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) which permits unrestricted distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Sections

Since the beginning of the Korean National Immunization Program (NIP) of influenza for the elderly in 1997, the NIP of the influenza vaccine has been operated with the inclusion of children and a high vaccine coverage rate. However, there is a lack of a system of evaluation to estimate influenza vaccine effectiveness (IVE). Evaluation of IVE for preventing laboratory-confirmed influenza (LCI), hospitalization, and death and the estimation of averted disease burden of influenza by influenza vaccine are required for the introduction of a newer vaccine and establishment of a policy for the prevention and control of influenza. Thus, a well-constructed system for estimation of IVE is urgently needed.
In this study, a network for the surveillance of influenza and a system for the evaluation of IVE were established. IVE in preventing LCI was estimated during the 2018-2019 flu season. The study population comprised of 2,409 adults over 19 years of age and 6,026 children over 6 months of age. Among the adults, 377 subjects in the prospective study who were enrolled in hospitals joined a network for the surveillance and 2,032 subjects in the retrospective study were collected from the immunization registry (IR) and the health insurance review and assessment service data. Furthermore, of the 6,026 children over the age of 6 months, 62 children were in the prospective study and 5,964 children were in the retrospective study. Prospective studies (for adults: October 14, 2018-May 9, 2019 and for children: December 27, 2018-April 30, 2019) with test-negative case-control design (TND) and a retrospective study with case-control design in the 2018-2019 influenza season were performed.
Through the prospective test-negative case-control study, adjusted VE in preventing all influenza and A/H1N1 were estimated as 55.9% (95% CI, 1.6-80.3) and 66.4% (95% CI, 6.7-87.9), respectively in adults aged 19-49 years of age. In pediatrics (≤18 years), adjusted VE for prevention of all influenza was 48.5% (95% CI, -141.5-89.0).
In the retrospective case-control study, adjusted VE in preventing all influenza and A/H1N1 were estimated as 41.4% (95% CI, 11.0-61.4) and 39.9% (95% CI, 2.2-63.0), respectively, in adults aged 19-49 years. In pediatrics (≤18 years), adjusted VE for prevention of all influenza, influenza A and influenza B were estimated as 43.2% (95% CI, 33.3-51.6), 47.7% (95% CI, 36.9-56.7) and 28.3% (95% CI, 6.9-44.8), respectively.
Influenza vaccine effectiveness during the 2018-2019 flu season was considered to be significant, which is similar to reports from the United States and Europe.

Key words Influenza, the influenza-like illness (ILI), Influenza vaccine, National Immunization Program (NIP), Effectiveness evaluation, Prospective study designed with test-negative, case-control design (TND), Retrospective case-control study, laboratory-confirmed influenza (LCI)

Sections
Table 1.

Retrospective case-control design

Polymerase Chain Reaction (PCR)
PositiveNegativeNo test
Rapid Antigen Test (RAT)PositiveInfluenzaInfluenzaInfluenza
NegativeInfluenzaControlsControls
No testInfluenzaControls-

Table 2.

2018-2019 flu season influenza vaccine effectiveness (IVE) (prospective test-negative case-control study)

Vaccine (+)/Influenza (+) (%)Vaccine (+)/Influenza (-) (%)Adjusted VE(95% CI) (%)
For adult (n=377)
All influenza(n=298)(n=79)
Total157/298 (52.7)43/79 (54.4)48.3 (-4.6 to 74.5)
19-49 years30/106 (28.3)27/50 (54.0)55.9 (1.6 to 80.3)
50-64 years16/59 (27.1)4/14 (28.6)94.2 (-13.2 to 99.7)
≥65 years111/133 (83.5)12/15 (80.0)-312.6 (-4,857.7 to 65.7)
Influenza A(n=266)(n=79)
Total142/266 (53.4)43/79 (54.4)42.6 (-18.9 to 72.3)
19-49 years24/88 (27.3)27/50 (54.0)49.2 (-19.1 to 78.3)
50-64 years15/55 (27.3)4/14 (28.6)94.0 (-15.9 to 99.7)
≥65 years103/123 (83.7)12/15 (80.0)-310.7 (-4,802.8 to 65.6)
A/H1N1(n=108)(n=79)
Total48/108 (44.4)43/79 (54.4)52.7 (-13.9 to 80.4)
19-49 years12/48 (25.0)27/50 (54.0)66.4 (6.7 to 87.9)
50-64 years8/26 (30.8)4/14 (28.6)89.8 (-512.7 to 99.8)
≥65 years28/34 (82.4)12/15 (80.0)-243.5 (-15,336.3 to 92.4)
For pediatrics (≤18 years) (n=62)
All influenza(n=28)(n=34)
Total22/28 (78.6)30/34 (88.2)48.5 (-141.5 to 89.0)
Influenza A(n=22)(n=34)
Total17/22 (77.3)30/34 (88.2)46.1 (-170.9 to 89.3)

*Adjusted factor: sex, age, calendar month, hospital, underlying disease

Table 3.

2018-2019 flu season influenza vaccine effectiveness (IVE) (retrospective case-control study)

Vaccine (+)/Influenza (+) (%)Vaccine (+)/Influenza (-) (%)Adjusted VE (95% CI) (%)
For adult (n=2,032)
All influenza(n=786)(n=1,246)
Total230/786 (29.3)576/1,246 (46.2)17.9 (-6.5 to 36.7)
19-49 years47/486 (9.7)75/492 (15.2)41.4 (11 to 61.4)
50-64 years34/112 (30.4)72/219 (32.9)-17.1 (-105.6 to 33.3)
≥65 years149/188 (79.3)429/535 (80.2)-6.8 (-69 to 32.5)
Influenza A(n=652)(n=1,246)
Total208/652 (31.9)576/1,246 (46.2)11.9 (-17 to 33.7)
19-49 years36/373 (9.7)75/492 (15.2)39.9 (2.2 to 63.0)
50-64 years31/101 (30.7)72/219 (32.9)-28.5 (-135.6 to 29.9)
≥65 years141/178 (79.2)429/535 (80.2)-7.8 (-72.7 to 32.7)
For pediatrics (≤18 years) (n=5,694)
All influenza(n=1,637)(n=4,057)
Total1,112/1,637 (67.9)3,483/4,057 (85.9)43.2 (33.3 to 51.6)
Influenza A(n=1,084)(n=4,057)
Total711/1,084 (65.6)3,483/4,057 (85.9)47.7 (36.9 to 56.7)
Influenza B(n=553)(n=4,057)
Total401/553 (72.5)3,483/4,057 (85.9)28.3 (6.9 to 44.8)

*Adjusted factor: sex, age, calendar month, hospital, underlying disease

Figure 1. Test-negative, case-control design study

References

Sections
  1. 신종인플루엔자 범 부처 사업단. 인플루엔자. 2016.
  2. 노지윤, 임수연, 송준영, 최원석, 박대원, 정혜원, 이재갑, 서유빈, 이진수, 위성헌, 김영근, 박경화, 정숙인, 김신우, 이선희, 정희진, 김우주. Estimates of the seasonal influenza vaccine effectiveness against laboratory-confirmed influenza among adults in South Korea, 2017∼2018 season: mid-season analysis. 2018년도 대한화학요법학회·대한감염학회 춘계학술대회
  3. 질병관리본부. 2017-2018절기 인플루엔자 국가예방접종 지원사업 관리지침.
  4. http://cdc.go.kr/CDC/together/CdcKrTogether0302.jsp?menuIds=HOME001-MNU1154-MNU0725-MNU0088&cid=75943
    Self
  5. 질병관리본부 예방접종관리과. 2018-2019절기 인플루엔자 국가예방접종 지원사업 계획. 2018.
  6. Evaluation of influenza vaccine effectiveness: a guide to the design and interpretation of observational studies. Geneva: World Health Organization; 2017.
    Self
  7. Kissling Esther, Rose Angela, Emborg Hanne-Dorthe, Gherasim Alin, Pebody Richard, Pozo Francisco, Trebbien Ramona, Mazagatos Clara, Whitaker Heather, Valenciano Marta, European IVE group. Interim 2018/19 influenza vaccine effectiveness: six European studies, October 2018 to January 2019. Euro Surveill. 2019;24(8):pii=1900121.
    CrossRef
  8. https://www.cdc.gov/vaccines/acip/meetings/downloads/slides-2018-06/flu-02-Flannery-508.pdf
    Self
  9. https://www.upmc.com/media/news/pitt-flu-vaccine-grant
    Self
  10. http://www.bccdc.ca/health-info/diseases-conditions/influenza/sentinel-network-spsn
    Self
  11. http://www.sarinet.org/sites/default/files/2017/day%201/MAY23%201545-1555%20PM%20Dr.%20Omeri%20SARInet%202017%20revelac-i%20NEO%20for%20distr.pdf
    Self

Epidemiology and Surveillance

Public Health Weekly Report 2020; 13(18): 1207-1216

Published online April 29, 2020

Copyright © The Korea Disease Control and Prevention Agency.

Establishment of surveillance system and network for the evaluation of influenza vaccine effectiveness and estimation of influenza vaccine effectiveness in preventing influenza

Park Sun Young, Kim Jong Hee, Cho En Hi, Kim Woo Joo

Division of VPD control & NIP, Center for Infectious Disease Surveillance & Response, KCDC; Korea University

Correspondence to:*교신저자 : wjkim@korea.ac.kr, 02-2626-3051

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) which permits unrestricted distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Since the beginning of the Korean National Immunization Program (NIP) of influenza for the elderly in 1997, the NIP of the influenza vaccine has been operated with the inclusion of children and a high vaccine coverage rate. However, there is a lack of a system of evaluation to estimate influenza vaccine effectiveness (IVE). Evaluation of IVE for preventing laboratory-confirmed influenza (LCI), hospitalization, and death and the estimation of averted disease burden of influenza by influenza vaccine are required for the introduction of a newer vaccine and establishment of a policy for the prevention and control of influenza. Thus, a well-constructed system for estimation of IVE is urgently needed.
In this study, a network for the surveillance of influenza and a system for the evaluation of IVE were established. IVE in preventing LCI was estimated during the 2018-2019 flu season. The study population comprised of 2,409 adults over 19 years of age and 6,026 children over 6 months of age. Among the adults, 377 subjects in the prospective study who were enrolled in hospitals joined a network for the surveillance and 2,032 subjects in the retrospective study were collected from the immunization registry (IR) and the health insurance review and assessment service data. Furthermore, of the 6,026 children over the age of 6 months, 62 children were in the prospective study and 5,964 children were in the retrospective study. Prospective studies (for adults: October 14, 2018-May 9, 2019 and for children: December 27, 2018-April 30, 2019) with test-negative case-control design (TND) and a retrospective study with case-control design in the 2018-2019 influenza season were performed.
Through the prospective test-negative case-control study, adjusted VE in preventing all influenza and A/H1N1 were estimated as 55.9% (95% CI, 1.6-80.3) and 66.4% (95% CI, 6.7-87.9), respectively in adults aged 19-49 years of age. In pediatrics (≤18 years), adjusted VE for prevention of all influenza was 48.5% (95% CI, -141.5-89.0).
In the retrospective case-control study, adjusted VE in preventing all influenza and A/H1N1 were estimated as 41.4% (95% CI, 11.0-61.4) and 39.9% (95% CI, 2.2-63.0), respectively, in adults aged 19-49 years. In pediatrics (≤18 years), adjusted VE for prevention of all influenza, influenza A and influenza B were estimated as 43.2% (95% CI, 33.3-51.6), 47.7% (95% CI, 36.9-56.7) and 28.3% (95% CI, 6.9-44.8), respectively.
Influenza vaccine effectiveness during the 2018-2019 flu season was considered to be significant, which is similar to reports from the United States and Europe.

Keywords: Influenza, the influenza-like illness (ILI), Influenza vaccine, National Immunization Program (NIP), Effectiveness evaluation, Prospective study designed with test-negative, case-control design (TND), Retrospective case-control study, laboratory-confirmed influenza (LCI)

Body

Table 1 . Retrospective case-control design.

Polymerase Chain Reaction (PCR)
PositiveNegativeNo test
Rapid Antigen Test (RAT)PositiveInfluenzaInfluenzaInfluenza
NegativeInfluenzaControlsControls
No testInfluenzaControls-

Table 2 . 2018-2019 flu season influenza vaccine effectiveness (IVE) (prospective test-negative case-control study).

Vaccine (+)/Influenza (+) (%)Vaccine (+)/Influenza (-) (%)Adjusted VE(95% CI) (%)
For adult (n=377)
All influenza(n=298)(n=79)
Total157/298 (52.7)43/79 (54.4)48.3 (-4.6 to 74.5)
19-49 years30/106 (28.3)27/50 (54.0)55.9 (1.6 to 80.3)
50-64 years16/59 (27.1)4/14 (28.6)94.2 (-13.2 to 99.7)
≥65 years111/133 (83.5)12/15 (80.0)-312.6 (-4,857.7 to 65.7)
Influenza A(n=266)(n=79)
Total142/266 (53.4)43/79 (54.4)42.6 (-18.9 to 72.3)
19-49 years24/88 (27.3)27/50 (54.0)49.2 (-19.1 to 78.3)
50-64 years15/55 (27.3)4/14 (28.6)94.0 (-15.9 to 99.7)
≥65 years103/123 (83.7)12/15 (80.0)-310.7 (-4,802.8 to 65.6)
A/H1N1(n=108)(n=79)
Total48/108 (44.4)43/79 (54.4)52.7 (-13.9 to 80.4)
19-49 years12/48 (25.0)27/50 (54.0)66.4 (6.7 to 87.9)
50-64 years8/26 (30.8)4/14 (28.6)89.8 (-512.7 to 99.8)
≥65 years28/34 (82.4)12/15 (80.0)-243.5 (-15,336.3 to 92.4)
For pediatrics (≤18 years) (n=62)
All influenza(n=28)(n=34)
Total22/28 (78.6)30/34 (88.2)48.5 (-141.5 to 89.0)
Influenza A(n=22)(n=34)
Total17/22 (77.3)30/34 (88.2)46.1 (-170.9 to 89.3)

*Adjusted factor: sex, age, calendar month, hospital, underlying disease.

Table 3 . 2018-2019 flu season influenza vaccine effectiveness (IVE) (retrospective case-control study).

Vaccine (+)/Influenza (+) (%)Vaccine (+)/Influenza (-) (%)Adjusted VE (95% CI) (%)
For adult (n=2,032)
All influenza(n=786)(n=1,246)
Total230/786 (29.3)576/1,246 (46.2)17.9 (-6.5 to 36.7)
19-49 years47/486 (9.7)75/492 (15.2)41.4 (11 to 61.4)
50-64 years34/112 (30.4)72/219 (32.9)-17.1 (-105.6 to 33.3)
≥65 years149/188 (79.3)429/535 (80.2)-6.8 (-69 to 32.5)
Influenza A(n=652)(n=1,246)
Total208/652 (31.9)576/1,246 (46.2)11.9 (-17 to 33.7)
19-49 years36/373 (9.7)75/492 (15.2)39.9 (2.2 to 63.0)
50-64 years31/101 (30.7)72/219 (32.9)-28.5 (-135.6 to 29.9)
≥65 years141/178 (79.2)429/535 (80.2)-7.8 (-72.7 to 32.7)
For pediatrics (≤18 years) (n=5,694)
All influenza(n=1,637)(n=4,057)
Total1,112/1,637 (67.9)3,483/4,057 (85.9)43.2 (33.3 to 51.6)
Influenza A(n=1,084)(n=4,057)
Total711/1,084 (65.6)3,483/4,057 (85.9)47.7 (36.9 to 56.7)
Influenza B(n=553)(n=4,057)
Total401/553 (72.5)3,483/4,057 (85.9)28.3 (6.9 to 44.8)

*Adjusted factor: sex, age, calendar month, hospital, underlying disease.

Figure 1. Test-negative, case-control design study

Fig 1.

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Figure 1.Test-negative, case-control design study
Public Health Weekly Report 2020; 13: 1207-1216

Table 1 . Retrospective case-control design.

Polymerase Chain Reaction (PCR)
PositiveNegativeNo test
Rapid Antigen Test (RAT)PositiveInfluenzaInfluenzaInfluenza
NegativeInfluenzaControlsControls
No testInfluenzaControls-

Table 2 . 2018-2019 flu season influenza vaccine effectiveness (IVE) (prospective test-negative case-control study).

Vaccine (+)/Influenza (+) (%)Vaccine (+)/Influenza (-) (%)Adjusted VE(95% CI) (%)
For adult (n=377)
All influenza(n=298)(n=79)
Total157/298 (52.7)43/79 (54.4)48.3 (-4.6 to 74.5)
19-49 years30/106 (28.3)27/50 (54.0)55.9 (1.6 to 80.3)
50-64 years16/59 (27.1)4/14 (28.6)94.2 (-13.2 to 99.7)
≥65 years111/133 (83.5)12/15 (80.0)-312.6 (-4,857.7 to 65.7)
Influenza A(n=266)(n=79)
Total142/266 (53.4)43/79 (54.4)42.6 (-18.9 to 72.3)
19-49 years24/88 (27.3)27/50 (54.0)49.2 (-19.1 to 78.3)
50-64 years15/55 (27.3)4/14 (28.6)94.0 (-15.9 to 99.7)
≥65 years103/123 (83.7)12/15 (80.0)-310.7 (-4,802.8 to 65.6)
A/H1N1(n=108)(n=79)
Total48/108 (44.4)43/79 (54.4)52.7 (-13.9 to 80.4)
19-49 years12/48 (25.0)27/50 (54.0)66.4 (6.7 to 87.9)
50-64 years8/26 (30.8)4/14 (28.6)89.8 (-512.7 to 99.8)
≥65 years28/34 (82.4)12/15 (80.0)-243.5 (-15,336.3 to 92.4)
For pediatrics (≤18 years) (n=62)
All influenza(n=28)(n=34)
Total22/28 (78.6)30/34 (88.2)48.5 (-141.5 to 89.0)
Influenza A(n=22)(n=34)
Total17/22 (77.3)30/34 (88.2)46.1 (-170.9 to 89.3)

*Adjusted factor: sex, age, calendar month, hospital, underlying disease.

Table 3 . 2018-2019 flu season influenza vaccine effectiveness (IVE) (retrospective case-control study).

Vaccine (+)/Influenza (+) (%)Vaccine (+)/Influenza (-) (%)Adjusted VE (95% CI) (%)
For adult (n=2,032)
All influenza(n=786)(n=1,246)
Total230/786 (29.3)576/1,246 (46.2)17.9 (-6.5 to 36.7)
19-49 years47/486 (9.7)75/492 (15.2)41.4 (11 to 61.4)
50-64 years34/112 (30.4)72/219 (32.9)-17.1 (-105.6 to 33.3)
≥65 years149/188 (79.3)429/535 (80.2)-6.8 (-69 to 32.5)
Influenza A(n=652)(n=1,246)
Total208/652 (31.9)576/1,246 (46.2)11.9 (-17 to 33.7)
19-49 years36/373 (9.7)75/492 (15.2)39.9 (2.2 to 63.0)
50-64 years31/101 (30.7)72/219 (32.9)-28.5 (-135.6 to 29.9)
≥65 years141/178 (79.2)429/535 (80.2)-7.8 (-72.7 to 32.7)
For pediatrics (≤18 years) (n=5,694)
All influenza(n=1,637)(n=4,057)
Total1,112/1,637 (67.9)3,483/4,057 (85.9)43.2 (33.3 to 51.6)
Influenza A(n=1,084)(n=4,057)
Total711/1,084 (65.6)3,483/4,057 (85.9)47.7 (36.9 to 56.7)
Influenza B(n=553)(n=4,057)
Total401/553 (72.5)3,483/4,057 (85.9)28.3 (6.9 to 44.8)

*Adjusted factor: sex, age, calendar month, hospital, underlying disease.

References

  1. 신종인플루엔자 범 부처 사업단. 인플루엔자. 2016.
  2. 노지윤, 임수연, 송준영, 최원석, 박대원, 정혜원, 이재갑, 서유빈, 이진수, 위성헌, 김영근, 박경화, 정숙인, 김신우, 이선희, 정희진, 김우주. Estimates of the seasonal influenza vaccine effectiveness against laboratory-confirmed influenza among adults in South Korea, 2017∼2018 season: mid-season analysis. 2018년도 대한화학요법학회·대한감염학회 춘계학술대회
  3. 질병관리본부. 2017-2018절기 인플루엔자 국가예방접종 지원사업 관리지침.
  4. http://cdc.go.kr/CDC/together/CdcKrTogether0302.jsp?menuIds=HOME001-MNU1154-MNU0725-MNU0088&cid=75943
    Self
  5. 질병관리본부 예방접종관리과. 2018-2019절기 인플루엔자 국가예방접종 지원사업 계획. 2018.
  6. Evaluation of influenza vaccine effectiveness: a guide to the design and interpretation of observational studies. Geneva: World Health Organization; 2017.
    Self
  7. Kissling Esther, Rose Angela, Emborg Hanne-Dorthe, Gherasim Alin, Pebody Richard, Pozo Francisco, Trebbien Ramona, Mazagatos Clara, Whitaker Heather, Valenciano Marta, European IVE group. Interim 2018/19 influenza vaccine effectiveness: six European studies, October 2018 to January 2019. Euro Surveill. 2019;24(8):pii=1900121.
    CrossRef
  8. https://www.cdc.gov/vaccines/acip/meetings/downloads/slides-2018-06/flu-02-Flannery-508.pdf
    Self
  9. https://www.upmc.com/media/news/pitt-flu-vaccine-grant
    Self
  10. http://www.bccdc.ca/health-info/diseases-conditions/influenza/sentinel-network-spsn
    Self
  11. http://www.sarinet.org/sites/default/files/2017/day%201/MAY23%201545-1555%20PM%20Dr.%20Omeri%20SARInet%202017%20revelac-i%20NEO%20for%20distr.pdf
    Self

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