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What is the true burden of diphtheria, tetanus, pertussis and poliovirus in children aged 3–18 years in Asia? A systematic literature review.

Open AccessPublished:January 22, 2022DOI:https://doi.org/10.1016/j.ijid.2022.01.045

      HIGHLIGHTS

      • Vaccination reduces the burden of vaccine-preventable diseases and their mortality.
      • Booster doses of diphtheria-tetanus-pertussis and poliovirus vaccines in older children are recommended.
      • In Asia, outbreaks of diphtheria, tetanus, pertussis, and poliovirus have occurred.
      • This may be because of inadequate booster coverage or gaps in recommendations.
      • There is a public health need for booster vaccinations in older children.

      ABSTRACT

      Objectives

      In recent years, outbreaks and a rising incidence of diphtheria, tetanus, and pertussis have occurred in Asia, particularly in older children.

      Methods

      A systematic search of MEDLINE and Embase was conducted from January 2000 to October 2020 to identify the epidemiology of diphtheria, tetanus, pertussis, and poliomyelitis in children and adolescents (aged 3–18 years) in Asia. The results were then related to vaccination schedules, booster coverage rates, pertussis source of infection, and booster immunogenicity, as identified by a pragmatic review. The International Prospective Register of Systematic Reviews (PROSPERO) registration: #CRD42020222445.

      Results

      A total of 35 studies were included in this review. Limited data were reported on the epidemiology of diphtheria, tetanus, pertussis, and poliomyelitis. Data from studies reporting the incidence of diphtheria and pertussis exemplify the shift in epidemiology to older children/adolescents. Seroprevalence data suggest that immunity to pertussis and diphtheria is below the level of herd immunity in several Asian countries in this population.

      Conclusion

      The true burden of diphtheria, pertussis, and tetanus in children aged 3-18 years in Asia is unknown because of weak or absent nationwide surveillance systems. The available evidence highlights the inadequacies in immunity, either by gaps in a recommendation or suboptimal booster coverage, supporting the public health need for booster vaccinations in this population.

      Keywords

      Introduction

      Vaccination is an important public health intervention, reducing the burden of vaccine-preventable diseases (VPDs) and their associated mortality, particularly in children (
      • Rodrigues CMC
      • Plotkin SA
      Impact of Vaccines; Health, Economic and Social Perspectives.
      ). In 1977, the World Health Organization's (WHO) Expanded Program of Immunization set out global policies for immunization against diphtheria, pertussis, tetanus, measles, poliomyelitis, and tuberculosis (
      • Keya K
      • Chan C
      • Hayden G
      • Henderson R
      Expanded programme on immunization.
      ). Despite these global efforts, in recent years, there have been outbreaks and a rising incidence of diphtheria, tetanus, and pertussis in Asia (
      Aceh epidemiology group
      Outbreak of tetanus cases following the tsunami in Aceh Province.
      ;
      • Hara M
      • Fukuoka M
      • Tashiro K
      • et al.
      Pertussis outbreak in university students and evaluation of acellular pertussis vaccine effectiveness in Japan.
      ;
      • Karyanti MR
      • Nelwan EJ
      • Assyidiqie IZ
      • et al.
      Diphtheria epidemiology in Indonesia during 2010-2017.
      ;
      • Murhekar M
      Epidemiology of diphtheria in India, 1996-2016: implications for prevention and control.
      ;
      • Saito N
      • Dimapilis VO
      • Fujii H
      • et al.
      Diphtheria in Metro Manila, the Philippines 2006–2017: A Clinical, Molecular, and Spatial Characterization.
      ;
      • Takum T
      • Gara D
      • Tagyung H
      • Murhekar MV.
      ) and future resurgences are anticipated because of decreased vaccine coverage rates (VCRs) attributable to the COVID-19 pandemic (
      • Harris RC
      • Chen Y
      • Côte P
      • et al.
      Impact of COVID-19 on routine immunisation in South-East Asia and Western Pacific: Disruptions and solutions.
      ).
      Diphtheria, tetanus, pertussis, and poliomyelitis, including vaccine-associated paralytic polio (VAPP) and vaccine-derived poliovirus (VDPV), continue to be public health concerns, particularly in Southeast Asia, India, and Pakistan (

      World Health Organization (2020a) Immunization, Vaccines And Biologicals. Vaccine preventable diseases Vaccines monitoring system 2020 Global Summary Reference Time Series: PERTUSSIS. https://apps.who.int/immunization_monitoring/globalsummary/timeseries/tsincidencepertussis.html. Accessed 16 Jul 2021.

      ,

      World Health Organization (2020b) Immunization, Vaccines And Biologicals. Vaccine preventable diseases Vaccines monitoring system 2020 Global Summary Reference Time Series: POLIO. https://apps.who.int/immunization_monitoring/globalsummary/timeseries/tsincidencepolio.html. Accessed 15 Jul 2021.

      ,

      World Health Organization (2020c) Immunization, Vaccines And Biologicals. Vaccine preventable diseases Vaccines monitoring system 2020 Global Summary Reference Time Series: TETANUS (TOTAL). https://apps.who.int/immunization_monitoring/globalsummary/timeseries/tsincidencettetanus.html. Accessed 16 Jul 2021.

      ,

      World Health Organization (2020d) Immunization, Vaccines And Biologicals. Vaccine preventable diseases Vaccines monitoring system 2020 Global Summary Reference Time Series: DIPHTHERIA. https://apps.who.int/immunization_monitoring/globalsummary/timeseries/tsincidencediphtheria.html. Accessed 15 Jul 2021.

      ). Three doses of diphtheria-tetanus-pertussis (DTP) and poliovirus vaccines within the first year of age are recommended in National Immunization Programmes (NIPs) or scientific societies in most countries (
      • Galles NC
      • Liu PY
      • Updike RL
      • et al.
      Measuring routine childhood vaccination coverage in 204 countries and territories, 1980–2019: a systematic analysis for the Global Burden of Disease Study 2020, Release 1.
      ). However, vaccination coverage varies and in 2019, 75% of zero-vaccinated children lived in 14 countries, including India, Pakistan, the Philippines, and Indonesia (
      • Galles NC
      • Liu PY
      • Updike RL
      • et al.
      Measuring routine childhood vaccination coverage in 204 countries and territories, 1980–2019: a systematic analysis for the Global Burden of Disease Study 2020, Release 1.
      ). Consequently, WHO estimates show that over the past 5 years, diphtheria, pertussis, and tetanus were among the most frequently reported VPDs in children aged <5 years in Southeast Asia (

      World Health Organization (2020e) Global and regional immunization profile. South East Asia Region. https://www.who.int/immunization/monitoring_surveillance/data/gs_searprofile.pdf?ua=1.

      ).
      Even in children who have received the full primary series of DTP/poliovirus vaccines, challenges with sustained immunity exist. Immunity following a 3 or 4-dose primary vaccination wanes over time (
      • Nakayama T
      • Suga S
      • Okada K
      • Okabe N
      Persistence of Antibodies against Diphtheria, Tetanus, Pertussis, and Poliovirus Types I, II, and III Following Immunization with DTaP Combined with Inactivated Wild-Type Polio Vaccine (DTaP-wIPV).
      ;
      • Ohfuji S
      • Okada K
      • Mouri Y
      • et al.
      Effectiveness of four doses of pertussis vaccine during infancy diminished in elementary school age: A test-negative case-control study in Japan.
      ), with just 10% of children estimated to be immune to pertussis 8.5 years after the last primary dose (
      • McGirr A
      • Fisman DN
      Duration of pertussis immunity after DTaP immunization: A meta-analysis.
      ). To address this waning immunity, many countries have adopted preschool, school-age, and adolescent booster vaccinations for DTP-containing vaccines, with or without inactivated polio vaccine (IPV), in their NIPs. However, in some Asian countries, national surveillance systems are weak or absent and few countries report data on childhood and adolescent booster VCRs, often used as surrogate measures of protection (
      • Butt M
      • Mohammed R
      • Butt E
      • et al.
      Why have immunization efforts in Pakistan failed to achieve global standards of vaccination uptake and infectious disease control?.
      ;
      • Murhekar MV.
      • Bitragunta S
      • Hutin Y
      • et al.
      Immunization coverage and immunity to diphtheria and tetanus among children in Hyderabad, India.
      ). In countries that do report the data, case numbers are assumed to be underreported, partly because of the lack of active surveillance systems and adequate diagnostic facilities (
      • Son S
      • Thamlikitkul V
      • Chokephaibulkit K
      • et al.
      Prospective multinational serosurveillance study of Bordetella pertussis infection among 10- to 18-year-old Asian children and adolescents.
      ). Therefore, the burden of these diseases in children and adolescents in Asian countries remains unknown and is most likely underestimated. The literature review aimed to assess the epidemiology, burden, and mortality rate of diphtheria, pertussis, tetanus, and poliovirus infections among children aged 3 to 18 years in Asia.

      Methods

      Systematic and pragmatic methodology was used to identify evidence on the burden of diphtheria, tetanus, pertussis, and poliomyelitis in children and adolescents aged 3 to 18 years.

      Search strategy

      This study was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement (
      • Page MJ
      • McKenzie JE
      • Bossuyt PM
      • et al.
      The PRISMA 2020 statement: an updated guideline for reporting systematic reviews.
      ). The study protocol is published through the International Prospective Register of Systematic Reviews (PROSPERO #CRD42020222445). Searches for full-text reports were done in Ovid MEDLINE, MEDLINE In-Process Citations & Daily Update, and Embase, from January 2000–October 2020.
      The detailed search strategy is available in Supplementary Table S1. Reference lists of the published systematic reviews and relevant websites of the health authorities of the countries of interest were also searched.

      Eligibility criteria

      Full publications of observational studies (cohort and cross-sectional studies; case series were included for poliomyelitis, VAPP, and VDPV outcomes) published in any language from 2000 onward, reporting incidence, prevalence, or mortality of diphtheria, tetanus, pertussis, poliomyelitis because of the wild-polio virus (WPV), VAPP, or VDPV infection in children aged 3–18 years were included. Conference abstracts published within the last 2 years were also included. The geographic scope was Hong Kong, India, Indonesia, Japan, Malaysia, Pakistan, Philippines, Singapore, South Korea, Taiwan, Thailand, and Vietnam.

      Screening and abstraction process

      Two-stage screening (title/abstract and full-text screening), and data extraction were performed independently by 2 reviewers (LN and EA); disagreement was resolved by discussion. Included studies met the eligibility criteria. Studies were included if they were considered representative of the population of interest within the study location. Excluded studies were those whose population samples were based on rural communities, single cities/towns, single/multihospital or centers, specific ethnic groups, or studies that did not stratify results by age. Data on study characteristics and the outcomes of interest (incidence, prevalence, seroprevalence, mortality, VAPP, and VDPV) were extracted.

      Risk of bias and quality assessment

      The risk of bias was assessed by a single reviewer using a modified Newcastle-Ottawa scale (Supplementary File S1).

      Pragmatic review

      A pragmatic review was performed to identify vaccination schedules and VCRs of all the countries/regions of interest in the systematic review. Data on pertussis source of infection and booster immunogenicity were also identified. This process included a combination of electronic searches and free text searching of databases and relevant government and international organization websites.

      Results

      Study identification

      A total of 1,967 records were identified; after de-duplication, 1,380 were screened by title and abstract; 212 were screened by full text; 3 were identified through hand searching; and 35 studies met inclusion criteria (Figure 1). A list of excluded studies is presented in Supplementary Table S2. Risk of bias data are presented in Supplementary Tables S34–S5.
      Figure 1
      Figure 1Flow of information through the different phases of the systematic review, adapted from Moher et al. (2009).
      The 35 studies reporting data in children aged 3–18 years were conducted in Japan (n = 7), India (n = 7), South Korea (n = 5), Indonesia (n = 4), Taiwan (n = 4), Thailand (n = 4), Singapore (n = 2). Pakistan (n = 1), and Asia (n = 1) (Table 1). No data were identified for Hong Kong, Malaysia, Philippines, and Vietnam.
      Table 1Study characteristics: burden of diphtheria, tetanus, pertussis, and polio in school-aged and adolescents in Asia
      Author/yearRegion, countryStudy designStudy periodSettingRepresentativenessN (% male)Age group(s)Disease reportedOutcomes reportedDiagnostic criteria, laboratory method
      (
      Aceh epidemiology group
      Outbreak of tetanus cases following the tsunami in Aceh Province.
      )
      IndonesiaSurveillance study30 December 2004−12 January 2005HospitalAceh province, outbreak after tsunami9 (56.0)5−14 yearsTetanusEpidemiologyClinical presentation
      (
      • Baba K
      • Okuno Y
      • Tanaka-Taya K
      • Okabe N
      Immunization coverage and natural infection rates of vaccine-preventable diseases among children by questionnaire survey in 2005 in Japan.
      JapanCross-sectionalJune and November 2005Nursery, kindergarten and elementary schoolsSchools across JapanNR4−12 yearsPertussisEpidemiologyNR
      (

      Bansiddhi H, Vuthitanachot V, Vuthitanachot C, et al (2015) Seroprevalence of antibody against diphtheria among the population inKhon Kaen Province, Thailand. Asia-Pacific J Public Heal 27:NP2712–NP2720. doi: 10.1177/1010539512450609.

      )
      ThailandSeroprevalence study2011CommunityKhon Kaen province48 (64.6)11−20 yearsDiphtheriaSeroprevalenceELISA
      (
      • Chang IF
      • Lee PI
      • Lu CY
      • et al.
      Resurgence of pertussis in Taiwan during 2009–2015 and its impact on infants.
      )
      TaiwanSurveillance study2003−2017CommunityNationwideNR5−9 yearsPertussisEpidemiologyClinical definition plus culture/PCR or epidemiological link to laboratory-confirmed case
      NR10−14 years
      (
      • Chatchatee P
      • Chatproedprai S
      • Warinsathien P
      • et al.
      Seroprevalence of tetanus antibody in the Thai population: A national survey.
      )
      ThailandSeroprevalence study2004HospitalNationwide118 (NR)5−9 yearsTetanusSeroprevalenceELISA
      91 (NR10−14 years
      79 (NR)15−19 years
      (
      • Choe YJ
      • Park YJ
      • Jung C
      • et al.
      National pertussis surveillance in South Korea 1955-2011: Epidemiological and clinical trends.
      )
      South KoreaSurveillance study1955−2011CommunityNationwideNR5−9 yearsPertussisEpidemiologyClinical definition or culture/PCR
      (
      • Chatchatee P
      • Chatproedprai S
      • Warinsathien P
      • et al.
      Seroprevalence of tetanus antibody in the Thai population: A national survey.
      )
      JapanSeroprevalence study2015-2016CommunityNationwide39 (NR)6−10 yearsTetanusSeroprevalenceELISA
      43 (NR)11−15 years
      34 (NR)16−20 years
      (
      • Deshpande JM
      • Bahl S
      • Sarkar BK
      • et al.
      Assessing population immunity in a persistently high-risk area for wild poliovirus transmission in India: A serological study in Moradabad, Western Uttar Pradesh.
      )
      IndiaSeroprevalence study30 October−21 November 2007Health facilityMoradabad44736−56 monthsWPV1SeroprevalenceNeutralisation assay
      WPV2
      WPV3
      (
      • Dravid MN
      • Joshi SA
      Resurgence of diphtheria in Malegaon & Dhule regions of north Maharashtra.
      )
      IndiaSurveillance study2005–2007Health facilityNorth Maharashtra42 (45.2)5–9 yearsDiphtheriaEpidemiologyLaboratory culture
      30 (53.3)10–14 years
      (
      • Hanvatananukul P
      • Prasarakee C
      • Sarachai S
      • et al.
      Seroprevalence of antibodies against diphtheria, tetanus, and pertussis among healthy Thai adolescents.
      )
      ThailandSeroprevalence studyJuly 2018− November 2018UniversityNorthern Thailand120 (48.6)11−15 yearsDiphtheriaPertussisTetanusSeroprevalenceELISA
      100 (48.6)16−20 years
      (
      • Hughes GJ
      • Mikhail AFW
      • Husada D
      • et al.
      Seroprevalence and Determinants of Immunity to Diphtheria for Children Living in Two Districts of Contrasting Incidence During an Outbreak in East Java.
      )
      IndonesiaSeroprevalence studyMarch 2013CommunityEast JavaNR6−10 yearsDiphtheriaSeroprevalenceELISA
      11−15 years
      (
      • Husada D
      • Puspitasari D
      • Kartina L
      • et al.
      Impact of a three-dose diphtheria outbreak response immunization in East Java, Indonesia, 6 months after completion.
      )
      IndonesiaSurveillance studyJanuary 2016 to June 2019Healthcare facilitiesEast Java7−21 (NR)7−<8 yearsDiphtheriaEpidemiologyLaboratory culture
      2−18 (NR)8−<9 years
      14−69 (NR)9−<19 years
      (
      • Hussain I
      • MacH O
      • Habib A
      • et al.
      Seroprevalence of Anti-polio Antibodies in Children from Polio High-risk Areas of Pakistan: A Cross-Sectional Survey 2015-2016.
      )
      PakistanSeroprevalence studyNovember 2015− March 2016CommunitySindh Province, Khyber Pakhtunkhwa Province, Punjab Province655 (55.6)3−4 yearsWPV1SeroprevalenceNeutralisation assay
      WPV2
      WPV3
      (
      • Ikematsu H
      • Kawai N
      • Yajima S
      A cross sectional survey measuring sero-incidence of pertussis infection among Japanese junior and senior high school students in 2013 and 2014.
      )
      JapanCross-sectional2013 and 2014 (paired sampling)SchoolGifu and Kagamihara1,017 (50.5)12−13 yearsPertussisSeroprevalence, EpidemiologyELISA
      1,146 (50.5)
      13−14 years
      83 (50.5)14−15 years
      523 (50.5)15−16 years
      474 (50.5)16−17 years
      (
      • Jafari H
      • Deshpande JM
      • Sutter RW
      • et al.
      Efficacy of inactivated poliovirus vaccine in India.
      )
      IndiaRCT (baseline data used)Not statedNot statedMoradabadNR (48.8)5 yearsWPV1SeroprevalenceNeutralisation assay
      WPV2
      NR (48.8)10 years
      WPV3
      (
      • Karyanti MR
      • Nelwan EJ
      • Assyidiqie IZ
      • et al.
      Diphtheria epidemiology in Indonesia during 2010-2017.
      )
      IndonesiaSurveillance study2010−2017CommunityNationwideNR5−9 yearsDiphtheriaEpidemiologyClinical definition plus culture/PCR
      NR10−14 years
      (
      • Kim HJ
      • Hwang S
      • Lee S
      • et al.
      A national cross-sectional study for poliovirus seroprevalence in the Republic of Korea in 2012: Implication for deficiency in immunity to polio among middle-aged people.
      )
      South KoreaSeroprevalence studyApril−November 2012HospitalNationwide236 (NR)6−10 yearsWPV1SeroprevalenceNeutralisation assay
      WPV2
      WPV3
      216 (NR)11−20 years
      (
      • Kuo CC
      • Hsieh YC
      • Huang YLYCYLC
      • et al.
      Seroepidemiology of pertussis among elementary school children in northern Taiwan.
      )
      TaiwanSeroprevalence studySeptember 2012−June 2013SchoolNorthern TaiwanNR6−7 yearsPertussisSeroprevalenceELISA
      NR7−8 years
      NR8−9 years
      NR9−10 years
      NR10−11 years
      NR11−12 years
      400 (NR)13−17 years
      (
      • Lee SY
      • Choi UY
      • Kim JS
      • et al.
      Immunoassay of pertussis according to ages.
      )
      South KoreaSeroprevalence studyJuly 2007−July 2008HospitalSeoul, Changwon, Cheonan, and Wonju100 (50)11−20 yearsPertussisSeroprevalenceELISA
      (
      • Lee SY
      • Han SB
      • Young Bae E
      • et al.
      Pertussis seroprevalence in korean adolescents and adults using anti-pertussis toxin immunoglobulin G.
      )
      South KoreaSeroprevalence studyJuly 2012− December 2012HospitalSeoul and Suwon198 (51.5)11−20 yearsPertussisSeroprevalenceELISA
      (
      • Lin YC
      • Yao SM
      • Yan JJ
      • et al.
      Epidemiological shift in the prevalence of pertussis in Taiwan: Implications for pertussis vaccination.
      )
      TaiwanSurveillance study1993-2004 (stratified by date)CommunityNationwideNR5−9 yearsPertussisEpidemiologyNR
      NR10−14 years
      (
      • Lu CY
      • Tsai HC
      • Huang YC
      • et al.
      A National Seroepidemiologic Survey of Pertussis among School Children in Taiwan.
      )
      TaiwanSeroprevalence study2013SchoolNationwideNR11−15 yearsPertussisSeroprevalenceELISA
      (
      • Mach O
      • Verma H
      • Khandait DW
      • et al.
      Prevalence of asymptomatic poliovirus infection in older children and adults in northern India: Analysis of contact and enhanced community surveillance, 2009.
      )
      IndiaSurveillance study2009CommunityBihar state, a polio endemic area2145−15 yearsWPV1EpidemiologyLaboratory testing of stool samples
      WPV3
      (
      • Moriuchi T
      • Otsuka N
      • Hiramatsu Y
      • et al.
      A high seroprevalence of antibodies to pertussis toxin among Japanese adults: Qualitative and quantitative analyses.
      )
      JapanSeroprevalence study2013−2014National Serum Reference Bank of the National Institute of Infectious DiseasesNationwide844−7 yearsPertussisSeroprevalenceELISA and neutralisation assay
      8410−14 years
      (
      • Murhekar MV
      • Kamaraj P
      • Kumar MS
      • et al.
      Immunity against diphtheria among children aged 5–17 years in India, 2017–18: a cross-sectional, population-based serosurvey.
      )
      IndiaSeroprevalence study2017−2018NationwideRepresentative of general population of India4,059 (NR)5−8 yearsDiphtheriaSeroprevalenceELISA
      4,265 (NR)9−17 years
      (
      • Ng Y
      • Chua LAV
      • Cui L
      • et al.
      Seroprevalence of vaccine-preventable diseases among children and adolescents in Singapore: Results from the National Paediatric Seroprevalence Survey 2018.
      )
      SingaporeSeroprevalence studyJanuary 2017− September 2018HospitalNationwideNR7−12 yearsDiphtheriaSeroprevalenceELISA
      NR13−17 yearsTetanus
      (
      • Paul Y
      Accuracy of the National Polio Surveillance Project data in Rajasthan.
      )
      IndiaSurveillance study2000Surveillance databaseRepresentative of Rajasthan3 (66.6)42−84 monthsPolio (type not specified)EpidemiologyLaboratory testing of stool samples
      20 (80.0)36−142 months
      VAPP
      (
      • Sangal L
      • Joshi S
      • Anandan S
      • et al.
      Resurgence of Diphtheria in North Kerala, India, 2016: Laboratory Supported Case-Based Surveillance Outcomes.
      )
      IndiaSurveillance studyMay 2016−November 2016VPD surveillance systemKerala state93 (58.1)5−10 yearsDiphtheriaEpidemiologyCulture/PCR
      161 (52.0)10−18 years
      (
      • Satoh H
      • Tanaka-Taya K
      • Shimizu H
      • et al.
      Polio vaccination coverage and seroprevalence of poliovirus antibodies after the introduction of inactivated poliovirus vaccines for routine immunization in Japan.
      )
      JapanSeroprevalence study2011−2015National Epidemiological SurveillanceNationwide315−3723−4 yearsWPV3SeroprevalenceNeutralisation assay
      (
      • Son S
      • Thamlikitkul V
      • Chokephaibulkit K
      • et al.
      Prospective multinational serosurveillance study of Bordetella pertussis infection among 10- to 18-year-old Asian children and adolescents.
      )
      AsiaCross-sectionalJuly 2013−June 2016HospitalLess than 100 subjects enrolled per country, data were collected from mostly university hospitals in metropolitan areas. Therefore, the data may not represent the general population.NR10−18 yearsPertussisEpidemiologyELISA
      (
      • Sung H
      • Jang MJ
      • Bae EY
      • et al.
      Seroepidemiology of tetanus in Korean adults and adolescents in 2012.
      )
      South KoreaSeroprevalence studyJuly 2012−December 2012HospitalSeoul and Gyeonggi199 (51.3)11−20 yearsTetanusSeroprevalenceELISA
      (
      • Wanlapakorn N
      • Ngaovithunvong V
      • Thongmee T
      • et al.
      Seroprevalence of Antibodies to Pertussis Toxin among Different Age Groups in Thailand after 37 Years of Universal Whole-Cell Pertussis Vaccination.
      )
      ThailandSeroprevalence studyMarch 2014− October 2014CommunitySeven provinces across Thailand147 (NR)11−20 yearsPertussisSeroprevalenceELISA
      (
      • Yasui Y
      • Mitsui T
      • Nishimura T
      • et al.
      School-age children and adolescents suspected of having been to be infected with pertussis in Japan.
      )
      JapanSeroprevalence study2013−2015Elementary and Junior High School, University, and Nursing SchoolNR2526−7 yearsPertussisSeroprevalenceELISA
      65312−13 years
      8618−19 years
      (
      • Yoneyama T
      • Sakae K
      • Baba J
      • et al.
      Surveillance of poliovirus-isolates in Japan.
      )
      JapanSurveillance study2000NRNationwide1 (0)3 yearsVPDV3EpidemiologyPCR
      ELISA, Enzyme-linked immunosorbent assay; NR, not reported, PCR, polymerase chain reaction; VAPP, vaccine-associated paralytic polio; VPD, vaccine preventable disease; VDPV3, vaccine-derived poliovirus type 3; pWPV1, wild poliovirus 1; WPV2, wild poliovirus 2; WPV3, wild poliovirus 3.

      Diphtheria

      Four studies reported epidemiological data on diphtheria; 2 in India (
      • Dravid MN
      • Joshi SA
      Resurgence of diphtheria in Malegaon & Dhule regions of north Maharashtra.
      ;
      • Sangal L
      • Joshi S
      • Anandan S
      • et al.
      Resurgence of Diphtheria in North Kerala, India, 2016: Laboratory Supported Case-Based Surveillance Outcomes.
      ) and 2 in Indonesia (
      • Husada D
      • Puspitasari D
      • Kartina L
      • et al.
      Impact of a three-dose diphtheria outbreak response immunization in East Java, Indonesia, 6 months after completion.
      ;
      • Karyanti MR
      • Nelwan EJ
      • Assyidiqie IZ
      • et al.
      Diphtheria epidemiology in Indonesia during 2010-2017.
      ) (Table 2). Diphtheria surveillance data from Kerala, India (2016) found the majority of cases in the group aged 18–45 years (38%; 198/526), followed by the groups aged 10–18 years (31%; 161/526), and aged 5–10 years (18%; 93/526) (
      • Sangal L
      • Joshi S
      • Anandan S
      • et al.
      Resurgence of Diphtheria in North Kerala, India, 2016: Laboratory Supported Case-Based Surveillance Outcomes.
      ). In North Maharashtra, the age groups of 5–9 years and 10–14 years represented 33.3% (42/126) and 23.8% (30/126) of the total cases, respectively (
      • Dravid MN
      • Joshi SA
      Resurgence of diphtheria in Malegaon & Dhule regions of north Maharashtra.
      ). In Indonesia, similar numbers of diphtheria cases in 2018 and 2019 were reported in children aged ≥18 months to 7 years compared with children aged 7 to <19 years (2018: 106 vs 108 cases; 2019: 34 vs 23) (
      • Husada D
      • Puspitasari D
      • Kartina L
      • et al.
      Impact of a three-dose diphtheria outbreak response immunization in East Java, Indonesia, 6 months after completion.
      ). A second study from Indonesia in 2017 found the highest number of diphtheria cases in those aged 5–9 years (32.5% cases), followed by 1–4 years (19.1% cases) (
      • Karyanti MR
      • Nelwan EJ
      • Assyidiqie IZ
      • et al.
      Diphtheria epidemiology in Indonesia during 2010-2017.
      ).
      Table 2Studies reporting the epidemiology of diphtheria in school-aged children and adolescents
      Country, referenceData collection periodData sourceRepresentativenessSubgroupAge group (years)Case frequencyCase fatality rateVaccine detailsVaccination coverage/rate
      Indonesia (
      • Husada D
      • Puspitasari D
      • Kartina L
      • et al.
      Impact of a three-dose diphtheria outbreak response immunization in East Java, Indonesia, 6 months after completion.
      )
      January 2016 to June 2019Surveillance dataEast Java20187-<821NRDTPNot stratified by age.“Most were diagnosed in patients with incomplete immunisation”Average immunisation coverage (DTP III)
      Regular schedule for infants in Indonesia: DTP I (2 months), DTP II (3 months), DTP III (4 months), DTP IV (18 months). DTP, diphtheria–tetanus–pertussis-containing vaccine; NR, not reported
      for the whole province: 2016: 96.67%, 2017: 93.91%, 2018: 98.82%, 2019: 47.02%Average immunisation coverage (DTP IV)
      Regular schedule for infants in Indonesia: DTP I (2 months), DTP II (3 months), DTP III (4 months), DTP IV (18 months). DTP, diphtheria–tetanus–pertussis-containing vaccine; NR, not reported
      for the whole province: 2016: 74.26%, 2017: 76.99%, 2018: 98.93%, 2019: 38.62%
      20188-<918NRDTP
      20189-<1969NRDTP
      20197-<87NRDTP
      20198-<92NRDTP
      20199-<1914NRDTP
      Indonesia (
      • Karyanti MR
      • Nelwan EJ
      • Assyidiqie IZ
      • et al.
      Diphtheria epidemiology in Indonesia during 2010-2017.
      )
      2017Surveillance dataNationwideAge5-9185.8DTPNot stratified by age.Diphtheria-containing vaccine (not booster):67.7% in 200761.9% in 201075.6% in 201361.3% in 2019
      Age10-1486.5DTP
      Age15-1843.8DTP
      India (
      • Dravid MN
      • Joshi SA
      Resurgence of diphtheria in Malegaon & Dhule regions of north Maharashtra.
      )
      2005–2007Surveillance dataNorth MaharashtraAge5–930NRDTPNR, it was noted that ‘The disease was seen in non-immunized and partially immunized individuals, and in older children and adults’
      10–1442NRDTP
      India (
      • Sangal L
      • Joshi S
      • Anandan S
      • et al.
      Resurgence of Diphtheria in North Kerala, India, 2016: Laboratory Supported Case-Based Surveillance Outcomes.
      )
      May 2016 to November 2016Surveillance dataKerala stateAge5-1093NRDiphtheria-containing vaccine (no further details given)0 dose: 631 dose: 12 dose: 13 dose: 44 dose: 155 dose: 10Vaccinated against diphtheria ‘as per age’<5 years: 23%5–10 years: 11%In children aged <10 years, 31% had received three doses of primary vaccination and 68% were not vaccinated or their vaccination status was not known
      Age10-18161NR0 dose: 1351 dose: 72 dose: 33 dose: 44 dose: 455 dose: 8In age group of >10 years, 3% cases received five doses of diphtheria containing vaccine and 7% were partially immunised.
      a Regular schedule for infants in Indonesia: DTP I (2 months), DTP II (3 months), DTP III (4 months), DTP IV (18 months). DTP, diphtheria–tetanus–pertussis-containing vaccine; NR, not reported
      Six studies assessed the seroprevalence of diphtheria antibodies (Table 3). Two were conducted in Singapore (
      • Lai FY
      • Thoon KC
      • Ang LW
      • et al.
      Comparative seroepidemiology of pertussis, diphtheria and poliovirus antibodies in Singapore: Waning pertussis immunity in a highly immunized population and the need for adolescent booster doses.
      ;
      • Ng Y
      • Chua LAV
      • Cui L
      • et al.
      Seroprevalence of vaccine-preventable diseases among children and adolescents in Singapore: Results from the National Paediatric Seroprevalence Survey 2018.
      ) and Thailand (

      Bansiddhi H, Vuthitanachot V, Vuthitanachot C, et al (2015) Seroprevalence of antibody against diphtheria among the population inKhon Kaen Province, Thailand. Asia-Pacific J Public Heal 27:NP2712–NP2720. doi: 10.1177/1010539512450609.

      ;
      • Hanvatananukul P
      • Prasarakee C
      • Sarachai S
      • et al.
      Seroprevalence of antibodies against diphtheria, tetanus, and pertussis among healthy Thai adolescents.
      ), and 1 in India (
      • Murhekar MV
      • Kamaraj P
      • Kumar MS
      • et al.
      Immunity against diphtheria among children aged 5–17 years in India, 2017–18: a cross-sectional, population-based serosurvey.
      ) and Indonesia (
      • Hughes GJ
      • Mikhail AFW
      • Husada D
      • et al.
      Seroprevalence and Determinants of Immunity to Diphtheria for Children Living in Two Districts of Contrasting Incidence During an Outbreak in East Java.
      ). Four were based on nationwide data. Five studies used an enzyme-linked immunosorbent assay (ELISA) method and 1 used an in vitro Vero cell challenge neutralization assay (
      • Hughes GJ
      • Mikhail AFW
      • Husada D
      • et al.
      Seroprevalence and Determinants of Immunity to Diphtheria for Children Living in Two Districts of Contrasting Incidence During an Outbreak in East Java.
      ). In all studies, antibody concentrations of ≥0.1 IU/ml were used to define seroprotective levels, based on the accepted definition (

      Efstratiou A, Maple C (1994) Laboratory diagnosis of diphtheria. World Heal Organ Reg Off Eur.

      ). In those aged 5−20 years, seroprotection levels ranged between 24.9%−100.0% (Table 3). Low levels of seroprotection were reported for India (24.9%–39.1%) and high levels were reported for Singapore (99.8%–100.0%). Mean antibody concentrations were reported in 4 studies and ranged from 0.05−0.74 IU/ml.
      Table 3Diphtheria seroprevalence and antibody titres in school-age children and adolescents
      Country, referenceRepresentativenessDateAge groupVaccination status of participantsN (% Male)Seroprevalence (%) [95% CI]GMT or GMC IU/ml [95% CI]
      India (
      • Murhekar MV
      • Kamaraj P
      • Kumar MS
      • et al.
      Immunity against diphtheria among children aged 5–17 years in India, 2017–18: a cross-sectional, population-based serosurvey.
      )
      Nationwide2017−20185−8 yearsNR4059 (NR)39.1 (33.5-44.9)0.10 (0.10-0.11)
      9−17 years4265 (NR)24.9 (20.9-29.5)0.05 (0.05-0.06)
      Indonesia (
      • Hughes GJ
      • Mikhail AFW
      • Husada D
      • et al.
      Seroprevalence and Determinants of Immunity to Diphtheria for Children Living in Two Districts of Contrasting Incidence During an Outbreak in East Java.
      )
      East Java20136−10 yearsNRNR82.0 (75.0, 89.0)NR
      11−15 yearsNR82.0 (75.0, 89.0)NR
      Singapore (
      • Lai FY
      • Thoon KC
      • Ang LW
      • et al.
      Comparative seroepidemiology of pertussis, diphtheria and poliovirus antibodies in Singapore: Waning pertussis immunity in a highly immunized population and the need for adolescent booster doses.
      )
      NationwideAugust 2008−July 20107−12 years91.0% received ≥3 DTP doses400 (NR)100.0 (99.1, 100.0)NR
      13−17 years400 (NR)99.8 (98.6, 100.0)NR
      Singapore (
      • Ng Y
      • Chua LAV
      • Cui L
      • et al.
      Seroprevalence of vaccine-preventable diseases among children and adolescents in Singapore: Results from the National Paediatric Seroprevalence Survey 2018.
      )
      NationwideJanuary 2017−September 20187−12 yearsNR400 (NR)97.3 (95.1, 98.5)NR
      13−17 years400 (NR)96.3 (93.9, 97.8)NR
      Thailand (

      Bansiddhi H, Vuthitanachot V, Vuthitanachot C, et al (2015) Seroprevalence of antibody against diphtheria among the population inKhon Kaen Province, Thailand. Asia-Pacific J Public Heal 27:NP2712–NP2720. doi: 10.1177/1010539512450609.

      )
      Northern Thailand201111−20 yearsNR48 (64.6)97.9 (89.1, 99.6)0.74 (0.58, 0.95)
      Thailand (
      • Hanvatananukul P
      • Prasarakee C
      • Sarachai S
      • et al.
      Seroprevalence of antibodies against diphtheria, tetanus, and pertussis among healthy Thai adolescents.
      )
      Northern ThailandJuly 2018−November 202011−20 years97.7% received 5 doses of DTwP and 2.3% received 5 doses of DTaP220 (48.6)50.0%0.45 (0.38, 0.53)
      CI, confidence interval; DTP, diphtheria-tetanus-pertussis containing vaccine; DTaP, diphtheria-tetanus-acellular pertussis containing vaccine; DTwP, diphtheria-tetanus-whole cell pertussis containing vaccine; GMC, geometric mean concentration; GMT, geometric mean titre; NR, not reported.

      Tetanus

      One study reported a tetanus outbreak in the Aceh province, Indonesia, 1 month after the 2004 tsunami (Table 4). Children aged 5–14 years accounted for 8.5% (9/106) of tetanus cases; 9 cases and 1 death were reported, giving a case fatality ratio of 11.1% (
      Aceh epidemiology group
      Outbreak of tetanus cases following the tsunami in Aceh Province.
      ).
      Table 4Studies reporting the epidemiology of tetanus in school-aged children and adolescents
      Country/region, referenceData collection periodData sourceRepresentativenessAge group (years)Case frequencyMortalityVaccine detailsVaccination coverage
      Indonesia (
      Aceh epidemiology group
      Outbreak of tetanus cases following the tsunami in Aceh Province.
      )
      December 2004 to January 2005Surveillance databaseAceh province, outbreak after tsunami5-1491/9NRNR
      NR, not reported.
      Four studies assessed seroprevalence of tetanus antibodies (Table 5); 2 were conducted in Thailand (
      • Chatchatee P
      • Chatproedprai S
      • Warinsathien P
      • et al.
      Seroprevalence of tetanus antibody in the Thai population: A national survey.
      ;
      • Hanvatananukul P
      • Prasarakee C
      • Sarachai S
      • et al.
      Seroprevalence of antibodies against diphtheria, tetanus, and pertussis among healthy Thai adolescents.
      ), and 1 in Singapore (
      • Ng Y
      • Chua LAV
      • Cui L
      • et al.
      Seroprevalence of vaccine-preventable diseases among children and adolescents in Singapore: Results from the National Paediatric Seroprevalence Survey 2018.
      ), and South Korea (
      • Sung H
      • Jang MJ
      • Bae EY
      • et al.
      Seroepidemiology of tetanus in Korean adults and adolescents in 2012.
      ). Two studies, in Singapore and Thailand, were based on national surveys (
      • Chatchatee P
      • Chatproedprai S
      • Warinsathien P
      • et al.
      Seroprevalence of tetanus antibody in the Thai population: A national survey.
      ;
      • Ng Y
      • Chua LAV
      • Cui L
      • et al.
      Seroprevalence of vaccine-preventable diseases among children and adolescents in Singapore: Results from the National Paediatric Seroprevalence Survey 2018.
      ). All 4 studies used the accepted minimum level of IgG antibody required for protection against tetanus (≥0.01 IU/mL) (
      • Roper MH
      • Wassilak SGF
      • Scobie HM
      • et al.
      Tetanus Toxoid.
      ) to define protection and an ELISA method. In those aged 5−20 years, seroprotective levels ranged between 84.3%−100.0%, and antibody concentrations ranged from 2.49−3.64 IU/ml. All subjects had antibody concentrations >0.01 IU/ml.
      Table 5Tetanus seroprevalence and antibody titres in school-age children and adolescents
      Country/region, referenceRepresentativenessDateAge groupVaccination status of participantsN (% male)Seroprevalence (%) [95% CI]GMT or GMC (IU/ml) [95% CI]
      Singapore (
      • Ng Y
      • Chua LAV
      • Cui L
      • et al.
      Seroprevalence of vaccine-preventable diseases among children and adolescents in Singapore: Results from the National Paediatric Seroprevalence Survey 2018.
      )
      NationwideJanuary 2017−September 20187−12 yearsNR400 (NR)84.3 (80.4, 87.5)NR
      13−17 years400 (NR)96.0 (93.6, 97.5)NR
      South Korea (
      • Sung H
      • Jang MJ
      • Bae EY
      • et al.
      Seroepidemiology of tetanus in Korean adults and adolescents in 2012.
      )
      Seoul and Gyeonggi provinceJuly 2012−December 201211−20 yearsNR199 (51.3)92.03.64 ± 7.21 (mean ± SD)
      Thailand (
      • Hanvatananukul P
      • Prasarakee C
      • Sarachai S
      • et al.
      Seroprevalence of antibodies against diphtheria, tetanus, and pertussis among healthy Thai adolescents.
      )
      Northern ThailandJuly 2018−November 202011−20 years97.7% received 5 doses of DTwP and 2.3% received 5 doses of DTaP217 (48.6)98.62.49 (2.14, 2.90)
      Thailand (
      • Chatchatee P
      • Chatproedprai S
      • Warinsathien P
      • et al.
      Seroprevalence of tetanus antibody in the Thai population: A national survey.
      )
      Nationwide20045−9 yearsNR118 (NR)<0.01 IU/ml: 0.00.01−0.9 IU/ml: 0.8>1 IU/ml: 99.23.64 (3.34, 3.96)
      10−14 years91 (NR)<0.01 IU/ml: 0.00.01−0.9 IU/ml: 0.0>1 IU/ml: 100.03.60 (NR)
      data taken from Figure.
      15−19 years79 (NR)<0.01 IU/ml: 0.00.01−0.9 IU/ml: 2.5>1 IU/ml: 97.53.55 (NR)*
      CI, confidence interval; DTaP, diphtheria-tetanus-acellular pertussis containing vaccine; DTwP, diphtheria-tetanus-whole cell pertussis containing vaccine GMC, geometric mean concentration; GMT, geometric mean titre; NR, not reported; SD, standard deviation.
      a data taken from Figure.

      Pertussis

      Six studies reported data on the epidemiology of pertussis; 2 each in Japan (
      • Baba K
      • Okuno Y
      • Tanaka-Taya K
      • Okabe N
      Immunization coverage and natural infection rates of vaccine-preventable diseases among children by questionnaire survey in 2005 in Japan.
      ;
      • Ikematsu H
      • Kawai N
      • Yajima S
      A cross sectional survey measuring sero-incidence of pertussis infection among Japanese junior and senior high school students in 2013 and 2014.
      ) and Taiwan (
      • Chang IF
      • Lee PI
      • Lu CY
      • et al.
      Resurgence of pertussis in Taiwan during 2009–2015 and its impact on infants.
      ;
      • Lin YC
      • Yao SM
      • Yan JJ
      • et al.
      Epidemiological shift in the prevalence of pertussis in Taiwan: Implications for pertussis vaccination.
      ) and 1 in Asia (
      • Son S
      • Thamlikitkul V
      • Chokephaibulkit K
      • et al.
      Prospective multinational serosurveillance study of Bordetella pertussis infection among 10- to 18-year-old Asian children and adolescents.
      ) and South Korea (
      • Choe YJ
      • Park YJ
      • Jung C
      • et al.
      National pertussis surveillance in South Korea 1955-2011: Epidemiological and clinical trends.
      ) (Table 6). In Japan, the incidence of Bordetella pertussis infection in junior/high school students in 2013 was an estimated 0.103 cases per 100,000 person-years; ≥90% had completed 4 doses of vaccine by the age of 2 years (
      • Ikematsu H
      • Kawai N
      • Yajima S
      A cross sectional survey measuring sero-incidence of pertussis infection among Japanese junior and senior high school students in 2013 and 2014.
      ). A study of VPD in Japan, using a questionnaire survey in 2005 to investigate vaccination and infection history, reported an annual incidence rate of pertussis of 0.0%–0.1% in children aged 4–12 years, with approximately 80% having received ≥3 doses of DTP (
      • Baba K
      • Okuno Y
      • Tanaka-Taya K
      • Okabe N
      Immunization coverage and natural infection rates of vaccine-preventable diseases among children by questionnaire survey in 2005 in Japan.
      ). The incidence rate was higher in those aged 0–3 years (0.2%–0.6%), and 0–12 years (1.0%–1.1%) who had received only 1 DTP dose. A study of the epidemiology of pertussis in Taiwan analyzed data from 2003–2017 from the Taiwan Centers for Disease Control and annual surveillance reports of communicable diseases (
      • Chang IF
      • Lee PI
      • Lu CY
      • et al.
      Resurgence of pertussis in Taiwan during 2009–2015 and its impact on infants.
      ). The mean incidence rates of 1–4 years, 5–9 years, and 10–14 years were 0.46, 0.14, and 0.39 cases per 100,000 population, respectively, with the mean age 10–14 years incidence accounting for 12.4% of all cases. A second study conducted in Taiwan reported the incidence rate of pertussis between 2000–2004, with results indicating that the epidemiology of pertussis may have been changed by waning immunity (
      • Lin YC
      • Yao SM
      • Yan JJ
      • et al.
      Epidemiological shift in the prevalence of pertussis in Taiwan: Implications for pertussis vaccination.
      ). The incidence rates for those aged 5–9 years and 10–14 years ranged between 0.71–1.71 and 2.40–4.48 per 100,000 between 2000 and 2004, respectively (
      • Lin YC
      • Yao SM
      • Yan JJ
      • et al.
      Epidemiological shift in the prevalence of pertussis in Taiwan: Implications for pertussis vaccination.
      ). A multinational surveillance study of pertussis across 10 centers in Asia estimated the number of infections in children and adolescents (n = 1,802), aged 10–18 years between July 2013 to June 2016 (
      • Son S
      • Thamlikitkul V
      • Chokephaibulkit K
      • et al.
      Prospective multinational serosurveillance study of Bordetella pertussis infection among 10- to 18-year-old Asian children and adolescents.
      ). Within the 3-year timeframe, the estimated prevalence of pertussis was 4,828 per 100,000. In South Korea, national pertussis surveillance data reported that from 2001–2009, no cases of pertussis were reported in children aged 5–9 years and 10–14 years except for 2 cases in 2002 in children aged 5–9 years old. During 2010–2011, a shift in the age group was observed, 33.8% were young infants aged <3 months and 29.0% were adolescents/adults aged ≥15 years (
      • Choe YJ
      • Park YJ
      • Jung C
      • et al.
      National pertussis surveillance in South Korea 1955-2011: Epidemiological and clinical trends.
      ).
      Table 6Studies reporting the epidemiology of pertussis in school-aged children and adolescents
      Country/region, referenceData collection periodData sourceRepresentativenessSubgroupAge group (years)NEpidemiological measureFrequency/ rate
      Asia (
      • Son S
      • Thamlikitkul V
      • Chokephaibulkit K
      • et al.
      Prospective multinational serosurveillance study of Bordetella pertussis infection among 10- to 18-year-old Asian children and adolescents.
      )
      July 2013 to June 2016Convenience population sample from 10 centres in Asia: China (n=2), India (n=1), Japan (n=1), South Korea (n=1), Sri Lanka (n=2), Taiwan (n=2) and Thailand (n=1)Less than 100 subjects enrolled per country, data were collected from mostly university hospitals in metropolitan areas. Therefore, the data may not represent the general population.India10-18NREstimated
      Estimated prevalence rate, based on the number of B. pertussis infections calculated from the population of each country's children and adolescents aged 10 to 18 years multiplied by the pertussis seropositive rate (anti-PT IgG ≥62.5 IU/mL) (Son et al., 2019). DTP, diphtheria-tetanus-pertussis containing vaccine; DTaP, diphtheria-tetanus-acellular pertussis containing vaccine; DTwP, diphtheria-tetanus-whole cell pertussis containing vaccine; NR.
      prevalence rate
      6,091 per 100,000
      Japan10-18NR4,630 per 100,000
      Korea10-18NR2,158 per 100,000
      Taiwan10-18NR4,369 per 100,000
      Thailand10-18NR5,263 per 100,000
      Japan (
      • Ikematsu H
      • Kawai N
      • Yajima S
      A cross sectional survey measuring sero-incidence of pertussis infection among Japanese junior and senior high school students in 2013 and 2014.
      )
      Paired sampling from the same children in 2013 and 2014Paired blood sampling from students of 8 junior high (JHSs) and two senior high schools (HSs) in Gifu PrefectureRepresentative of high-school children in JapanNA12-171017Incidence rate10.3 per 1000 person years (32/3100)
      Japan (
      • Baba K
      • Okuno Y
      • Tanaka-Taya K
      • Okabe N
      Immunization coverage and natural infection rates of vaccine-preventable diseases among children by questionnaire survey in 2005 in Japan.
      )
      June and November 2005Questionnaire surveySchools across JapanAge group4-12NRIncidence rate0.0-0.1%
      South Korea (
      • Choe YJ
      • Park YJ
      • Jung C
      • et al.
      National pertussis surveillance in South Korea 1955-2011: Epidemiological and clinical trends.
      )
      1955-2011National surveillance dataNationwide20015-9NRReported cases0
      20025-9NR2
      20035-9NR0
      20045-9NR0
      20055-9NR0
      20065-9NR0
      20075-9NR0
      20085-9NR0
      20095-9NR0
      20105-9NR2
      20115-9NR4
      200110-14NR0
      200210-14NR0
      200310-14NR0
      200410-14NR0
      200510-14NR0
      200610-14NR0
      200710-14NR0
      200810-14NR0
      200910-14NR2
      201010-14NR1
      201110-14NR2
      Taiwan (
      • Chang IF
      • Lee PI
      • Lu CY
      • et al.
      Resurgence of pertussis in Taiwan during 2009–2015 and its impact on infants.
      )
      2003 - 2017National database (Taiwan Centers for Disease Control)NationwideAge group5-9NRIncidence rate0.14 per 100,000
      Age group10-14NR0.39 per 100,000
      20035-9NR0.21 per 100,000
      20045-9NR0.01 per 100,000
      20055-9NR0.07 per 100,000
      20065-9NR0.08 per 100,000
      20075-9NR0.00 per 100,000
      20085-9NR0.19 per 100,000
      20095-9NR0.32 per 100,000
      20105-9NR0.44 per 100,000
      20115-9NR0.37 per 100,000
      20125-9NR0.09 per 100,000
      20135-9NR0.00 per 100,000
      20145-9NR0.12 per 100,000
      20155-9NR0.20 per 100,000
      20165-9NR0.00 per 100,000
      20175-9NR0.00 per 100,000
      200310-14NR0.08 per 100,000
      200410-14NR0.42 per 100,000
      200510-14NR0.20 per 100,000
      200610-14NR0.00 per 100,000
      200710-14NR0.12 per 100,000
      200810-14NR0.60 per 100,000
      200910-14NR0.90 per 100,000
      201010-14NR0.32 per 100,000
      201110-14NR0.90 per 100,000
      201210-14NR0.22 per 100,000
      201310-14NR0.52 per 100,000
      201410-14NR0.70 per 100,000
      201510-14NR0.40 per 100,000
      201610-14NR0.10 per 100,000
      201710-14NR0.28 per 100,000
      Taiwan (
      • Lin YC
      • Yao SM
      • Yan JJ
      • et al.
      Epidemiological shift in the prevalence of pertussis in Taiwan: Implications for pertussis vaccination.
      )
      1993-2004National surveillance dataNationwide20005-9NRIncidence rate17.1 per million
      20015-9NR7.47 per million
      20025-9NR12.6 per million
      20035-9NR7.08 per million
      20045-9NR10.05 per million
      200010-14NR35.86 per million
      200110-14NR23.97 per million
      200210-14NR28.40 per million
      200310-14NR44.80 per million
      200410-14NR39.45 per million
      a Estimated prevalence rate, based on the number of B. pertussis infections calculated from the population of each country's children and adolescents aged 10 to 18 years multiplied by the pertussis seropositive rate (anti-PT IgG ≥62.5 IU/mL) (
      • Son S
      • Thamlikitkul V
      • Chokephaibulkit K
      • et al.
      Prospective multinational serosurveillance study of Bordetella pertussis infection among 10- to 18-year-old Asian children and adolescents.
      ).
      DTP, diphtheria-tetanus-pertussis containing vaccine; DTaP, diphtheria-tetanus-acellular pertussis containing vaccine; DTwP, diphtheria-tetanus-whole cell pertussis containing vaccine; NR.
      Eleven studies assessed the seroprevalence of pertussis antibodies (Table 7). Four were conducted in Japan (
      • Fumimoto R
      • Otsuka N
      • Kamiya H
      • et al.
      Seroprevalence of IgA and IgM antibodies to Bordetella pertussis in healthy Japanese donors: Assessment for the serological diagnosis of pertussis.
      ;
      • Ikematsu H
      • Kawai N
      • Yajima S
      A cross sectional survey measuring sero-incidence of pertussis infection among Japanese junior and senior high school students in 2013 and 2014.
      ;
      • Moriuchi T
      • Otsuka N
      • Hiramatsu Y
      • et al.
      A high seroprevalence of antibodies to pertussis toxin among Japanese adults: Qualitative and quantitative analyses.
      ;
      • Yasui Y
      • Mitsui T
      • Nishimura T
      • et al.
      School-age children and adolescents suspected of having been to be infected with pertussis in Japan.
      ), 2 each in South Korea (
      • Lee SY
      • Choi UY
      • Kim JS
      • et al.
      Immunoassay of pertussis according to ages.
      ,
      • Lee SY
      • Han SB
      • Young Bae E
      • et al.
      Pertussis seroprevalence in korean adolescents and adults using anti-pertussis toxin immunoglobulin G.
      ), Taiwan (
      • Kuo CC
      • Hsieh YC
      • Huang YLYCYLC
      • et al.
      Seroepidemiology of pertussis among elementary school children in northern Taiwan.
      ;
      • Lu CY
      • Tsai HC
      • Huang YC
      • et al.
      A National Seroepidemiologic Survey of Pertussis among School Children in Taiwan.
      ), and Thailand (
      • Hanvatananukul P
      • Prasarakee C
      • Sarachai S
      • et al.
      Seroprevalence of antibodies against diphtheria, tetanus, and pertussis among healthy Thai adolescents.
      ;
      • Wanlapakorn N
      • Ngaovithunvong V
      • Thongmee T
      • et al.
      Seroprevalence of Antibodies to Pertussis Toxin among Different Age Groups in Thailand after 37 Years of Universal Whole-Cell Pertussis Vaccination.
      ), and 1 in Singapore (
      • Lai FY
      • Thoon KC
      • Ang LW
      • et al.
      Comparative seroepidemiology of pertussis, diphtheria and poliovirus antibodies in Singapore: Waning pertussis immunity in a highly immunized population and the need for adolescent booster doses.
      ). There are no well-accepted definitive serologic or laboratory correlates of protection against pertussis (
      • Liang JL
      • Tiwari T
      • Moro P
      • et al.
      Prevention of pertussis, tetanus, and diphtheria with vaccines in the United States: Recommendations of the Advisory Committee on Immunization Practices (ACIP).
      ) and all studies differed in their thresholds for seroprotection, the bacterial antigens detected, and units of measurement, precluding meaningful comparisons (Table 7). All studies used an ELISA-based technique to assess the bacterial antigens, anti-pertussis toxoid (anti-PT) IgG, anti-filamentous hemagglutinin (anti-FHA) IgG, or anti-B. pertussis IgA and IgM antibody concentration. Overall, in those aged 4−20 years, seroprevalence levels for anti-PT IgG ranged between 25.0%−73.0% and 74.8%−91.1% for anti-FHA IgG.
      Table 7Pertussis seroprevalence and antibody titres in school-age children and adolescents
      Country/region, referenceRepresentativenessDateAge groupVaccination status of participantsN (% Male)Definition of seroprotectionSeroprevalence (%) [95% CI]GMT or GMC [95% CI]
      95% CI reported unless otherwise stated. CI, confidence interval; DTP, diphtheria-tetanus-pertussis containing vaccine; DTaP, diphtheria-tetanus-acellular pertussis containing vaccine; GMC, geometric mean concentration; GMT, geometric mean titre; NR, not reported; NTU, Novagnost units; SD, standard deviation.
      Japan (
      • Fumimoto R
      • Otsuka N
      • Kamiya H
      • et al.
      Seroprevalence of IgA and IgM antibodies to Bordetella pertussis in healthy Japanese donors: Assessment for the serological diagnosis of pertussis.
      )
      Nationwide2015−20166−10 yearsNR39 (NR)Novagnost units (NTU): negative (<8.5 NTU), indeterminate (8.5–11.5 NTU) and positive (>11.5 NTU)anti-B. pertussis IgA: 5.1% anti-B. pertussis IgM: 30.8%anti-B. pertussis IgA, mean ± SD: 2.9 ± 2.2 NTU anti-B. pertussis IgM, mean ± SD: 7.7 ± 3.5 NTU
      11−15 yearsNR43 (NR)anti-B. pertussis IgA: 7.0%anti-B. pertussis IgM: 39.5%anti-B. pertussis IgA, mean ± SD: 3.6 ± 3.0 NTUanti-B. pertussis IgM, mean ± SD: 7.9 ± 3.2 NTU
      16−20 yearsNR34 (NR)anti-B. pertussis IgA: 8.8%anti-B. pertussis IgM: 26.5%anti-B. pertussis IgA, mean ± SD: 4.1 ± 3.2 NTUanti-B. pertussis IgM, mean ± SD: 7.3 ± 3.6 NTU
      Japan (
      • Yasui Y
      • Mitsui T
      • Nishimura T
      • et al.
      School-age children and adolescents suspected of having been to be infected with pertussis in Japan.
      )
      NR20146−7 years3−4 doses of DTaP252 (NR)Antibody titres of ≥10 EU/ml were considered positive, and <10 EU/ml were considered negativeAnti-PT: 47.1 (40.7, 53.6)Anti-FHA: 84.3 (79.1, 88.6)Anti-PT IgG: 18.3 EU/ml (15.5, 21.2)Anti-FHA IgG: 45.9 EU/ml (41.2, 50.6)
      201412−13 years3−4 doses of DTaP653 (NR)Anti-PT: 60.0 (56.0, 63.9)Anti-FHA: 91.1 (88.6, 93.2)Anti-PT IgG: 23.8 EU/ml (21.9, 25.8)Anti-FHA IgG: 55.0 EU/ml (52.3, 7.8)
      201318−19 years3−4 doses of DTaP86 (NR)Anti-PT: 73.0 (61.4, 82.6)Anti-FHA: 86.5 (76.5, 93.3)Anti-PT IgG: 29.3 EU/ml (23.0, 5.6)Anti-FHA IgG: 48.5 EU/ml (40.8–56.2)
      20156−7 years3−4 doses of DTaP252 (NR)Anti-PT: 37.4 (31.2, 43.9) Anti-FHA: 74.8 (68.8, 80.2)Anti-PT IgG: 13.5 EU/ml (11.1, 15.9)Anti-FHA IgG: 39.7 EU/ml (35.0, 44.0)
      201512−13 years3−4 doses of DTaP660 (NR)Anti-PT: 61.3 (57.3, 65.2)Anti-FHA: 86.1 (83.1, 88.8)Anti-PT IgG: 27.0 EU/ml (24.8, 9.3)Anti-FHA IgG: 58.3 EU/ml (55.0, 61.7)
      201518−19 years3−4 doses of DTaP114 (NR)Anti-PT: 75.7 (64.0, 85.2)Anti-FHA: 84.3 (73.6, 91.9)Anti-PT IgG: 8.9 EU/ml (31.0, 46.8)Anti-FHA IgG: 42.7 EU/ml (34.1, 51.2)
      Japan (
      • Moriuchi T
      • Otsuka N
      • Hiramatsu Y
      • et al.
      A high seroprevalence of antibodies to pertussis toxin among Japanese adults: Qualitative and quantitative analyses.
      )
      Nationwide2013−20144−7 yearsNR84 (NR)No definition statedanti-PT IgG at 25−<50 IU/mL: 57.1anti-PT IgG: 43.6 (29.2, 64.9) IU/mlanti-FHA IgG: 23.0 (6.4, 82.8) IU/ml
      10−14 yearsNR84 (NR)anti-PT IgG at 25−<50 IU/mL: 47.6anti-PT IgG: 54.1 (34.9, 83.6) IU/mlanti-FHA IgG: 29.9 (10.8, 82.3) IU/ml
      Japan (
      • Ikematsu H
      • Kawai N
      • Yajima S
      A cross sectional survey measuring sero-incidence of pertussis infection among Japanese junior and senior high school students in 2013 and 2014.
      )
      Gifu and Kagamihara2013 and 2014 (paired samples)12−13 years89.4% received 4 doses1017 (50.5)IgG PT of 100 EU/mL, change of IgG PT <100 EU/mL in 2013 to >100 EU/mL in 2014, and four fold-increase of IgG PT from 2013 to 2014NRAnti-PT IgG 2013: 17.4 (16.4–18.5) EU/mlAnti-PT IgG 2014: 16.8 (15.9–17.8) EU/ml
      13−14 years1146 50.5)NRAnti-PT IgG 2013: 17.0 (16.0–17.9) EU/mlAnti-PT IgG 2014: 17.1 (16.2–18.1) EU/ml
      14−15 years83 (50.5)NRAnti-PT IgG 2013: 13.3 (11.0–16.0) EU/mlAnti-PT IgG 2014: 17.7 (14.4–21.8) EU/ml
      15−16 years523 (50.5)NRAnti-PT IgG 2013: 20.7 (19.1–22.4) EU/mlAnti-PT IgG 2014: 20.5 (18.7–22.2) EU/ml
      16−17 years474 (50.5)NRAnti-PT IgG 2013: 19.0 (17.5–20.7) EU/mlAnti-PT IgG 2014: 20.6 (19.0–22.4) EU/ml
      Singapore (
      • Lai FY
      • Thoon KC
      • Ang LW
      • et al.
      Comparative seroepidemiology of pertussis, diphtheria and poliovirus antibodies in Singapore: Waning pertussis immunity in a highly immunized population and the need for adolescent booster doses.
      )
      NationwideAugust 2008−July 20107−12 years91.0% received ≥3 doses400(NR)IgG of ≥22 U/ml63.3 (58.4, 67.8)NR
      13−17 years400(NR)55.0 (50.1, 59.8)NR
      South Korea (
      • Lee SY
      • Choi UY
      • Kim JS
      • et al.
      Immunoassay of pertussis according to ages.
      )
      Seoul, Changwon, Cheonan, and WonjuJuly 2007−July 200811−20 yearsNR100 (50)anti-PT IgG titre>24 EU/mL53.0Mean ± SD anti-PT IgG: 46.91 ± 50.80 IU/ml
      South Korea (
      • Lee SY
      • Han SB
      • Young Bae E
      • et al.
      Pertussis seroprevalence in korean adolescents and adults using anti-pertussis toxin immunoglobulin G.
      )
      Seoul and SuwonJuly 2012− December 201211−20 yearsNR198 (51.5)anti-PT IgG titre>24 EU/mL38.9Anti-PT IgG mean ± SD: 31.2 ± 48.7 EU/ml
      Taiwan (
      • Kuo CC
      • Hsieh YC
      • Huang YLYCYLC
      • et al.
      Seroepidemiology of pertussis among elementary school children in northern Taiwan.
      )
      Northern TaiwanSeptember 2012−June 20136−7 years98.9% received ≥3 dosesNRNovatec units: The results were considered positive for titres >11 NTU, negative for titres below 9 NTU, and equivocal between 9 NTU and 11 NTU49.413.4 IU/ml
      7−8 yearsNR39.111.0 IU/ml
      8−9 yearsNR35.311.0 IU/ml
      9−10 yearsNR25.07.8 IU/ml
      10−11 yearsNR25.08.2 IU/ml
      11−12 yearsNR30.19.7 IU/ml
      Taiwan (
      • Lu CY
      • Tsai HC
      • Huang YC
      • et al.
      A National Seroepidemiologic Survey of Pertussis among School Children in Taiwan.
      )
      Nationwide20136−7 years6−11: 79.5% received 3 doses of DTP/DTaP12−15: 60.7% had 3 doses of DTP/DTaPNRNovatec units: The results were considered positive for titres >11 NTU, negative for titres below 9 NTU, and equivocal between 9 NTU and 11 NTU45.8NR
      7−8 yearsNR43.6NR
      8−9 yearsNR48.8NR
      9−10 yearsNR26.6NR
      10−11 yearsNR28.7NR
      11−12 yearsNR39.4NR
      12−13 yearsNR44.5NR
      13−14 yearsNR48.9NR
      14−15 yearsNR51.3NR
      Thailand (
      • Hanvatananukul P
      • Prasarakee C
      • Sarachai S
      • et al.
      Seroprevalence of antibodies against diphtheria, tetanus, and pertussis among healthy Thai adolescents.
      )
      Northern ThailandJuly 2018−November 202011−20 years97.7% received DTwP2.3% received DTaP220 (48.6)anti-Bordetella pertussis toxin IgG >5 IU/ml56.816.2 (14.1, 18.6) IU/ml
      Thailand (
      • Wanlapakorn N
      • Ngaovithunvong V
      • Thongmee T
      • et al.
      Seroprevalence of Antibodies to Pertussis Toxin among Different Age Groups in Thailand after 37 Years of Universal Whole-Cell Pertussis Vaccination.
      )
      Seven provinces across ThailandMarch 2014 −October 201411−20 years54.5−90.3% received 5 doses DTP147 (NR)>100 IU/ml indicative of acute pertussis infection or recent vaccination51.75.22 (4.01, 6.80) IU/ml
      a 95% CI reported unless otherwise stated. CI, confidence interval; DTP, diphtheria-tetanus-pertussis containing vaccine; DTaP, diphtheria-tetanus-acellular pertussis containing vaccine; GMC, geometric mean concentration; GMT, geometric mean titre; NR, not reported; NTU, Novagnost units; SD, standard deviation.

      Poliovirus

      Three studies reported epidemiological data for poliomyelitis; 2 were conducted in India (
      • Mach O
      • Verma H
      • Khandait DW
      • et al.
      Prevalence of asymptomatic poliovirus infection in older children and adults in northern India: Analysis of contact and enhanced community surveillance, 2009.
      ;
      • Paul Y
      Accuracy of the National Polio Surveillance Project data in Rajasthan.
      ) and 1 in Japan (
      • Yoneyama T
      • Sakae K
      • Baba J
      • et al.
      Surveillance of poliovirus-isolates in Japan.
      ) (Table 8). Data from the polio-endemic areas of Uttar Pradesh and Bihar, India, in 2009, show that 1.4% and 0.9% of children aged 5–15 years were WPV1 and WPV3 positive, respectively (
      • Mach O
      • Verma H
      • Khandait DW
      • et al.
      Prevalence of asymptomatic poliovirus infection in older children and adults in northern India: Analysis of contact and enhanced community surveillance, 2009.
      ). A study of acute flaccid paralysis (AFP) surveillance in Rajasthan during 2000 reported 20 AFP cases that could be considered paralytic polio (asymmetric paralysis after the febrile episode) in children aged 3 to 3.5 years and 3 cases of AFP that could be considered VAPP in children aged 3.5 to 7 years (
      • Paul Y
      Accuracy of the National Polio Surveillance Project data in Rajasthan.
      ). One case of VDPV3 was reported in Japan in the year 2000 in a child aged 3 years (
      • Yoneyama T
      • Sakae K
      • Baba J
      • et al.
      Surveillance of poliovirus-isolates in Japan.
      ).
      Table 8Studies reporting the epidemiology of poliovirus in school-aged children and adolescents
      Country/region, referenceData collection periodData sourceRepresentativenessPathogenAge groupNN with diseaseVaccine detailsVaccination coverageVaccination rate
      India (
      • Mach O
      • Verma H
      • Khandait DW
      • et al.
      Prevalence of asymptomatic poliovirus infection in older children and adults in northern India: Analysis of contact and enhanced community surveillance, 2009.
      )
      2009Regional surveillance dataBihar state, a polio endemic areaWPV15-15 years2143 (1.4%)NRNRNR
      WPV35-15 years2142 (0.9%)NRNRNR
      India (
      • Paul Y
      Accuracy of the National Polio Surveillance Project data in Rajasthan.
      )
      2000AFP surveillance data from RajasthanRepresentative of RajasthanPoliomyelitis (type unspecified)36-142 monthsNR20OPV0-16 dosesNR
      VAPP42-84 monthsNR3OPV9-12 dosesNR
      Japan (
      • Yoneyama T
      • Sakae K
      • Baba J
      • et al.
      Surveillance of poliovirus-isolates in Japan.
      )
      2000National surveillance dataNationalVDPV33 years11NRVaccinated (no further details given)100%
      AFP, acute flaccid paralysis; NR, not reported; OPV, oral polio vaccine; VAPP, vaccine-activated associated paralytic poliomyelitis; VDPV, Vaccine-derived poliomyelitis; WPV, wild poliovirus
      Six studies assessed the seroprevalence of poliovirus antibodies (Table 9). Two were conducted in India (
      • Deshpande JM
      • Bahl S
      • Sarkar BK
      • et al.
      Assessing population immunity in a persistently high-risk area for wild poliovirus transmission in India: A serological study in Moradabad, Western Uttar Pradesh.
      ;
      • Jafari H
      • Deshpande JM
      • Sutter RW
      • et al.
      Efficacy of inactivated poliovirus vaccine in India.
      ), and 1 each in Japan (
      • Satoh H
      • Tanaka-Taya K
      • Shimizu H
      • et al.
      Polio vaccination coverage and seroprevalence of poliovirus antibodies after the introduction of inactivated poliovirus vaccines for routine immunization in Japan.
      ), Pakistan (
      • Hussain I
      • MacH O
      • Habib A
      • et al.
      Seroprevalence of Anti-polio Antibodies in Children from Polio High-risk Areas of Pakistan: A Cross-Sectional Survey 2015-2016.
      ), Singapore (
      • Lai FY
      • Thoon KC
      • Ang LW
      • et al.
      Comparative seroepidemiology of pertussis, diphtheria and poliovirus antibodies in Singapore: Waning pertussis immunity in a highly immunized population and the need for adolescent booster doses.
      ), and South Korea (
      • Kim HJ
      • Hwang S
      • Lee S
      • et al.
      A national cross-sectional study for poliovirus seroprevalence in the Republic of Korea in 2012: Implication for deficiency in immunity to polio among middle-aged people.
      ). Three were based on nationwide data (
      • Kim HJ
      • Hwang S
      • Lee S
      • et al.
      A national cross-sectional study for poliovirus seroprevalence in the Republic of Korea in 2012: Implication for deficiency in immunity to polio among middle-aged people.
      ;
      • Lai FY
      • Thoon KC
      • Ang LW
      • et al.
      Comparative seroepidemiology of pertussis, diphtheria and poliovirus antibodies in Singapore: Waning pertussis immunity in a highly immunized population and the need for adolescent booster doses.
      ;
      • Satoh H
      • Tanaka-Taya K
      • Shimizu H
      • et al.
      Polio vaccination coverage and seroprevalence of poliovirus antibodies after the introduction of inactivated poliovirus vaccines for routine immunization in Japan.
      ). Four out of the 5 studies used the gold-standard neutralization assay (
      • Weldon WC
      • Steven Oberste M
      • Pallansch MA
      Standardized methods for detection of poliovirus antibodies.
      ), and 1 study (
      • Lai FY
      • Thoon KC
      • Ang LW
      • et al.
      Comparative seroepidemiology of pertussis, diphtheria and poliovirus antibodies in Singapore: Waning pertussis immunity in a highly immunized population and the need for adolescent booster doses.
      ) used an ELISA-based method. Four studies defined seroprotection as a concentration of poliovirus neutralizing antibodies ≥1:8, and 1 defined seropositivity as levels ≥12 U/ml (
      • Lai FY
      • Thoon KC
      • Ang LW
      • et al.
      Comparative seroepidemiology of pertussis, diphtheria and poliovirus antibodies in Singapore: Waning pertussis immunity in a highly immunized population and the need for adolescent booster doses.
      ). Overall, in children and adolescents aged 3−17 years, seroprevalence levels for type 1 poliovirus ranged from 93.2%−100.0%, type 2 poliovirus 93.9%−100.0%, and type 3 poliovirus 58.3%−93.9%. In Singapore, the seroprevalence rate for poliomyelitis (all types) was ≥93.3%.
      Table 9Poliovirus seroprevalence and antibody titres in school-age children and adolescents
      Country/region, referenceRepresent-ativenessDateAge groupVaccination status of participantsN (% Male)Type 1Type 2Type 3
      % SP (95% CI)Antibody titres% SP (95% CI)Antibody titres% SP (95% CI)Antibody titres
      India (
      • Deshpande JM
      • Bahl S
      • Sarkar BK
      • et al.
      Assessing population immunity in a persistently high-risk area for wild poliovirus transmission in India: A serological study in Moradabad, Western Uttar Pradesh.
      )
      Moradabad30 October to 21 November 200736−59 monthsMedian of 18 (13–18) mOPV1 doses, 14 (6–24) tOPV doses, and 5 (1–5) mOPV3 doses447 (NR)99.0−100.0Reciprocal median titre: 72497.0 (95.0, 98.0)Reciprocal median titre: 36293.0 (91.0, 95.0)362
      India (
      • Jafari H
      • Deshpande JM
      • Sutter RW
      • et al.
      Efficacy of inactivated poliovirus vaccine in India.
      )
      Northern IndiaOctober to December 20115 yearsNRNR (48.8)100.0 (98.9, 100.0)NR95.4 (92.5, 97.4)NR97.5 (95.2, 98.9)NR
      10 yearsNR (48.1)99.7 (98.3, 100.0)NR97.2 (94.7, 98.7)NR92.2 (88.7, 94.9)NR
      Japan (
      • Satoh H
      • Tanaka-Taya K
      • Shimizu H
      • et al.
      Polio vaccination coverage and seroprevalence of poliovirus antibodies after the introduction of inactivated poliovirus vaccines for routine immunization in Japan.
      )
      Data extracted from figure. CI, confidence interval; GMT, geometric mean titre; IPV, inactivated poliovirus; NR, not reported; OPV, oral polio vaccine; SP, seroprevalence.
      Nationwide2011−20153 years≥1 dose of polio-containing vaccine: 97.4−100.0%2011: 372 (NR)2012: 315 (NR)2013: 321 (NR)2014: 339 (NR)2015: 331 (NR)2011: 100.02012: 96.82013: 97.32014: 96.82015: 97.8NR2011: 97.22012: 98.42013: 96.82014: 98.42015: 100.0NR2011: 69.92012: 71.52013: 72.82014: 77.62015: 93.9NR
      4 years2011: 97.82012: 97.82013: 100.02014: 94.62015: 99.5NR2011: 93.92012: 99.62013: 96.82014: 94.32015: 100.0NR2011: 61.82012: 70.32013: 61.42014: 76.02015: 72.8NR
      Pakistan (
      • Hussain I
      • MacH O
      • Habib A
      • et al.
      Seroprevalence of Anti-polio Antibodies in Children from Polio High-risk Areas of Pakistan: A Cross-Sectional Survey 2015-2016.
      )
      Six polio high-risk districts in Pakistan2015−20163−4 years55.9% fully immunised655 (55.6)99.0−100.0NR91.0−100.0NR92.0−100.0NR
      Singapore (
      • Lai FY
      • Thoon KC
      • Ang LW
      • et al.
      Comparative seroepidemiology of pertussis, diphtheria and poliovirus antibodies in Singapore: Waning pertussis immunity in a highly immunized population and the need for adolescent booster doses.
      )
      Nationwide7−12 years91.0% received ≥3 DTP doses400 (NR)93.3 (90.4–95.3) (all types)
      August 2008−July 201013−17 years400 (NR)94.3 (91.5–96.1) (all types)
      South Korea (
      • Kim HJ
      • Hwang S
      • Lee S
      • et al.
      A national cross-sectional study for poliovirus seroprevalence in the Republic of Korea in 2012: Implication for deficiency in immunity to polio among middle-aged people.
      )
      NationwideApril−November 20126−10 years82.6% fully immunised with IPV; 82.2% fully immunised with OPV236 (NR)93.2GMT (95% CI): 372.8 (295.9, 449.7)96.6GMT (95% CI): 470.2 (383.0, 557.4)87.7GMT (95% CI): 280.8 (213.5, 348.1)
      11−20 years216 (NR)80.183.0 (59.4, 106.7)92.1107.1 (81.9, 132.2)58.338.2 (27.6, 48.9)
      a Data extracted from figure. CI, confidence interval; GMT, geometric mean titre; IPV, inactivated poliovirus; NR, not reported; OPV, oral polio vaccine; SP, seroprevalence.

      Pragmatic review

      To support the interpretation of the findings of the systematic literature review, a pragmatic review was used to identify information on vaccination schedules, booster VCRs, source of pertussis infection, and booster immunogenicity. Boosters for tetanus and diphtheria are recommended in all countries except Pakistan; boosters are less common for pertussis (10 countries) and IPV (7 countries). Some recommendations are by medical societies and not included in the NIP. Data can be found in Supplementary File S2.

      Discussion

      Children and adolescents are an important target age group for booster vaccinations. This comprehensive literature review evaluating the VPD burden in this population in Asia identified significant evidence gaps where limited data are reported specifically for this population. For comparison, this review focused on several countries/regions with different economic statuses and levels of infectious disease burden. Most of the studies identified in this review were from Japan, India, and South Korea, with substantial data gaps. No data were reported for Hong Kong, Malaysia, and Vietnam. Thus, the main finding of this review is the lack of robust data. Consequently, it is difficult to accurately assess the burden of diphtheria, pertussis, and tetanus in Asia and to gauge the effectiveness of the different immunization campaigns. These findings are aligned with those of a recent systematic literature review assessing the epidemiology, burden, and mortality of pertussis in school-age children, adolescents, and adults in Asia (
      • Macina D
      • Evans KE
      Bordetella pertussis in School-Age Children, Adolescents, and Adults: A Systematic Review of Epidemiology, Burden, and Mortality in Asia.
      ). Nonetheless, the scarce data suggest diphtheria and pertussis remain a significant burden in children aged ≥5 years in these regions.
      Public health surveillance informs disease prevention and few countries in Asia have such systems in place. VPD national surveillance systems were identified in Hong Kong, Japan, the Philippines, Singapore, South Korea, and Taiwan. However, there was wide variation in the reporting systems, some stratified by age, others reporting for the overall population, and often with incomplete data sets. Similarly, few countries reported data on booster VCRs or seroprevalence rates which are important in assessing the success of vaccination programs (
      • Butt M
      • Mohammed R
      • Butt E
      • et al.
      Why have immunization efforts in Pakistan failed to achieve global standards of vaccination uptake and infectious disease control?.
      ). In this review, only Japan, Singapore, and Taiwan publicly reported VCRs based on national surveillance data, underscoring the difficulties in measuring the effectiveness of different country's immunization campaigns. Therefore, where national surveillance data exist, the data should be made publicly available, and in those countries where the data does not exist, certain diseases should be prioritized, with laboratory and clinical case definitions, and perhaps, sentinel surveillance should be started before launching a nationwide program (

      World Health Organization (2006) Setting priorities in communicable disease surveillance. http://www.who.int/csr/resources/publications/surveillance/WHO_CDS_EPR_LYO_2006_3/en/. Accessed 12 Jan 2022.

      ).
      Across the different NIPs and scientific recommendations, clear differences emerged in booster schedules. At school-entry age, neither Singapore nor Pakistan recommend a booster vaccine as part of the NIP (

      Government of Pakistan (2018) Immunization Schedule – Expanded Program on Immunization, Pakistan.

      ; ). In Japan, there is a voluntary recommendation for DTP-IPV booster doses at age 5−6 years, which is not state-funded (

      Japan Pediatric Society (2020) Vaccination Schedule chart – SEMI- Sapporo English Medical Interpreters.

      ). No recommendations for an adolescent booster were identified for Pakistan, Taiwan, or Vietnam. Adolescent boosters comprised DT (Japan), tetanus booster (Malaysia), Tdap (Hong Kong, Singapore, South Korea), or Tdap/Td (Indonesia, the Philippines, Thailand). The NIP in India includes Td, and although the Indian Academy of Pediatrics recommends the Tdap vaccine at 12–14 years, it is not state-funded and the level of uptake is unclear (
      • Kasi SG
      • Shivananda S
      • Marathe S
      • et al.
      Indian Academy of Pediatrics (IAP) Advisory Committee on Vaccines and Immunization Practices (ACVIP): Recommended Immunization Schedule (2020–21) and Update on Immunization for Children Aged 0 Through 18 Years.
      ).
      Based on this review, in Japan, Malaysia, and Singapore, pertussis and poliovirus vaccinations are complete in children by 2 years of age. Data from nationwide seroprevalence studies in Japan () and Singapore (
      • Lai FY
      • Thoon KC
      • Ang LW
      • et al.
      Comparative seroepidemiology of pertussis, diphtheria and poliovirus antibodies in Singapore: Waning pertussis immunity in a highly immunized population and the need for adolescent booster doses.
      ) show evidence of waning pertussis immunity over time, despite high coverage of DTP3/DTP4 (;
      World Health Organization
      WHO World Health Organization: Immunization, Vaccines And Biologicals.
      ). Globally, a resurgence of pertussis in developed regions has occurred (
      • Clark TA
      ;
      • Gulland A
      Teenagers and newborn babies in England and Wales may get pertussis jab as cases continue to rise.
      ), with an epidemiological shift toward older children and adolescents (
      • Hara M
      • Fukuoka M
      • Tashiro K
      • et al.
      Pertussis outbreak in university students and evaluation of acellular pertussis vaccine effectiveness in Japan.
      ;
      • Ikematsu H
      • Kawai N
      • Yajima S
      A cross sectional survey measuring sero-incidence of pertussis infection among Japanese junior and senior high school students in 2013 and 2014.
      ). Pertussis often remains undiagnosed in adolescents and adults, because of atypical presentation or mild disease and lack of awareness (
      • Bamberger ES
      • Srugo I
      What is new in pertussis?.
      ). Consequently, the incidence in these populations is likely underestimated; a pan-Asian serosurveillance study found that 1 in 20 adolescents aged 10−18 years had serologic evidence of recent pertussis infection, irrespective of vaccination status (
      • Son S
      • Thamlikitkul V
      • Chokephaibulkit K
      • et al.
      Prospective multinational serosurveillance study of Bordetella pertussis infection among 10- to 18-year-old Asian children and adolescents.
      ). This highlights the need for an increased awareness of clinicians in terms of diagnosis and educating policymakers/parents on the importance of boosters. Continued circulation of pertussis leaves infants vulnerable to severe disease and up to 50.0% of pertussis transmission to infants is likely because of older siblings (
      • Chang IF
      • Lee PI
      • Lu CY
      • et al.
      Resurgence of pertussis in Taiwan during 2009–2015 and its impact on infants.
      ). A US modeling study predicted that a single booster vaccination in children aged 5−10 years would reduce infant infections by 23% (
      • De Cellès MD
      • Magpantay FMG
      • King AA
      • Rohani P
      The impact of past vaccination coverage and immunity on pertussis resurgence.
      ). In contrast to Singapore, Taiwan recommends a booster at school-entry age, but not at adolescence (

      Taiwan Centers for Disease Control (2019) Current Immunization Schedule in Taiwan.

      ). Data presented here confirm previous studies showing the waning of immunity occurring later in adolescents despite high VCRs of 96.5% at school-entry age (

      Taiwan Ministry of Health and Welfare (2021) 10540-02-02 Statistics on the completion rate of various vaccinations-Census and Statistics Department. https://dep.mohw.gov.tw/DOS/cp-1730-2981-113.html. Accessed 15 Apr 2021.

      ). In Taiwan, adolescents account for 12.4% of cases of pertussis, highlighting the inadequacies of pertussis control with the current recommendations (
      • Chang IF
      • Lee PI
      • Lu CY
      • et al.
      Resurgence of pertussis in Taiwan during 2009–2015 and its impact on infants.
      ).
      Diphtheria seroprevalence rates varied, where data were available. In Singapore, seroprevalence rates were high (>95%) (
      • Ng Y
      • Chua LAV
      • Cui L
      • et al.
      Seroprevalence of vaccine-preventable diseases among children and adolescents in Singapore: Results from the National Paediatric Seroprevalence Survey 2018.
      ), likely attributable to diphtheria vaccination being mandated by law in children under the age of 2 years, and DTaP vaccination is required for school entry (

      Ministry of Education Singapore (2020) Primary 1 registration guides.

      ; ). In contrast, in India, despite recommendations of a DTwP/DTaP booster at 5−6 years, and Td boosters at 10 and 16 years, less than a third of children aged 5−17 years were immune to diphtheria in 2017−2018 (
      • Murhekar MV
      • Kamaraj P
      • Kumar MS
      • et al.
      Immunity against diphtheria among children aged 5–17 years in India, 2017–18: a cross-sectional, population-based serosurvey.
      ). Although no data exist on booster coverage, this low seroprevalence is likely because of the low uptake of primary vaccines/boosters, despite NIP recommendations. As has been noted with pertussis, with the wide adoption of the childhood schedule and booster, there has been a shift in diphtheria cases to older children and adolescents (
      • Maramraj KK
      • Latha MLK
      • Reddy R
      • et al.
      Addressing reemergence of diphtheria among adolescents through program integration in india.
      ;
      • Murhekar M
      Epidemiology of diphtheria in India, 1996-2016: implications for prevention and control.
      ). In India, diphtheria transmission is expected to continue until the immunity gap is bridged through adequate vaccine coverage. The available data suggest that adequate levels of immunity toward poliovirus and tetanus have been largely achieved and should be maintained.
      This review has several limitations. First, data from the gold standard for polio reporting, The Global Polio Eradication Initiative (
      GPEI
      Global Polio Eradication Initiative.
      ), were not included, owing to not stratifying by age, potentially missing valuable data for Pakistan, a country in which poliovirus remains endemic. Equally, by focusing only on those aged 3–18 years, potential trends/data from the overall population may have been missed. The identified studies were heterogeneous in study design, time period, and demographics, and often had incomplete vaccination status, precluding any comparisons between countries with and without boosters. Similarly, the lack of complete nationwide epidemiological or seroprevalence data across time periods, in addition to limited data on VCRs, made it unfeasible to identify temporal trends on VPD burden. In addition, there were no data from Hong Kong, Malaysia, and Vietnam, with limited data from the other regions of interest, again precluding comparisons. Scientific guidelines recommending boosters in older children were identified in the absence of inclusion in the NIPs in Japan, Malaysia, and the Philippines; it is unknown if these recommendations are implemented in clinical practice and to what extent. The lack of up-to-date nationwide VCRs and/or seroprevalence data, coupled with the sparse epidemiological data available for this specific population makes it difficult to draw robust conclusions.
      In conclusion, the available evidence supports the public health need for booster vaccinations in older children. Evidence indicates that inadequacies in immunity arose by way of 2 mechanisms, either by gaps in recommendations or suboptimal booster dose coverage. The findings of this comprehensive review are twofold. First, they highlight the need to implement or strengthen existing nationwide surveillance systems to allow for collection of robust data to assess vaccination campaign success. Second, they show that there is a need for targeted research such as national seroprevalence studies, retrospective analyses of cases in reference centers, and cross-sectional studies to determine laboratory-confirmed cases based on clinical presentation in sentinel centers across different countries to understand the burden of these VPDs more accurately in relation to booster vaccination recommendations and coverage in children and adolescents in Asia.

      Contributors

      LN, EA, and JCVZ conceived and designed this study. LN and EA performed initial screening, a review of full texts for eligibility, and extracted the data. LN and EA conducted the data analysis. LN, EA, JCZV, CH, MRK, AOL, and BS conducted the data interpretation. LN and EA drafted the final manuscript and prepared the tables and figures. JCZV, CH, MRK, AOL, and BS provided critical analysis and made revisions of the manuscript and important intellectual contributions. All authors reviewed the manuscript before final submission.

      Declaration of competing interests

      AOL, MRK, and BS declare they have no competing interests. LN and EA received consulting fees from Sanofi Pasteur. JCZV and CH are Sanofi employees and may hold shares and/or stock options in the company.

      Role of the funding source

      The review was funded by Sanofi Pasteur. The funder contributed to its design, data interpretation, and drafting of the manuscript. All authors had full access to all of the data in the study and can take responsibility for the integrity of the data and the accuracy of the data analysis.

      Ethical approval

      Concerning ethical aspects, this study was conducted through a literature review, without subject identification, ensuring individual confidentiality and anonymity.

      Acknowledgments

      We are grateful to Sheila Harvey for conducting a quality assessment and Rebecca Harris for reviewing the protocol and manuscript outline.

      Appendix. Supplementary materials

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