Population-level susceptibility, severity and spread of pandemic influenza: design of, and initial results from, a pre-pandemic and hibernating pandemic phase study using cross-sectional data from the Health Survey for England (HSE)

Background Assessing severity and spread of a novel influenza strain at the start of a pandemic is critical for informing a targeted and proportional response. It requires community-level studies to estimate the burden of infection and disease. Rapidly initiating such studies in a pandemic is diffic...

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Published inPublic health research (Southampton, England) Vol. 3; no. 6; pp. 1 - 24
Main Authors Fragaszy, Ellen B, Quinlivan, Mark, Breuer, Judith, Craig, Rachel, Hutchings, Stephanie, Kidd, Michael, Mindell, Jennifer, Hayward, Andrew C
Format Journal Article
LanguageEnglish
Published NIHR Journals Library 01.06.2015
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Abstract Background Assessing severity and spread of a novel influenza strain at the start of a pandemic is critical for informing a targeted and proportional response. It requires community-level studies to estimate the burden of infection and disease. Rapidly initiating such studies in a pandemic is difficult. The study aims to establish an efficient system allowing real-time assessment of population susceptibility, spread of infection and clinical attack rates in the event of a pandemic. Methods We developed and appended additional survey questions and specimen collection to the Health Survey for England (HSE) – a large, annual, rolling nationally representative general population survey recruiting throughout the year – to enable rapid population-based surveys of influenza infection and disease during a pandemic. Using these surveys we can assess the spread of the virus geographically, by age and through time. The data generated can also provide denominators for national estimates of case fatality and hospitalisation rates. Phase 1 : we compared retrospectively collected HSE illness rates during the first two infection waves of the 2009 pandemic with the Flu Watch study (a prospective community cohort). Monthly and seasonal age-specific rates of illness and proportion vaccinated were compared. Phase 2 : we piloted blood specimen and data collection alongside the 2012–13 HSE. We are developing laboratory methods and protocols for real-time serological assays of a novel pandemic influenza virus using these specimens, and automated programmes for analysing and reporting illness and infection rates. Phase 3 : during inter-pandemic years, the study enters a holding phase, where it is included in the yearly HSE ethics application and planning procedures, allowing rapid triggering in a pandemic. Phase 4 : once retriggered, the study will utilise the methods developed in phase 2 to monitor the severity and spread of the pandemic in real time. Results Phase 1 : the rates of reported illness during the first two waves in the HSE underestimated the community burden as measured by Flu Watch, but the patterns of illness by age and time were broadly comparable. The extent of underestimation was greatest for HSE participants interviewed later in the year compared with those interviewed closer to the pandemic. Vaccine uptake in the HSE study was comparable to independent national estimates and the Flu Watch study. Phases 2 and 3 : illness data and serological samples from 2018 participants were collected in the 2012–13 HSE and transferred to the University College London Hospital. In the 2013 HSE and onwards, this project was included in the annual HSE ethics and planning rounds. Conclusions The HSE’s underestimation of illness rates during the first two waves of the pandemic is probably due to recall bias and the limitation of being able to report only one illness when multiple illnesses per season can occur. Changes to the illness questions (reporting only recent illnesses) should help minimise these issues. Additional prospective follow-up could improve measurement of disease incidence. The representative nature of the HSE allows accurate measurements of vaccine uptake. Study registration This study is registered as ISRCTN80214280. Funding This project was funded by the NIHR Public Health Research programme and will be published in full in Public Health Research ; Vol. 3, No. 6. See the NIHR Journals Library website for further project information.
AbstractList Background Assessing severity and spread of a novel influenza strain at the start of a pandemic is critical for informing a targeted and proportional response. It requires community-level studies to estimate the burden of infection and disease. Rapidly initiating such studies in a pandemic is difficult. The study aims to establish an efficient system allowing real-time assessment of population susceptibility, spread of infection and clinical attack rates in the event of a pandemic. Methods We developed and appended additional survey questions and specimen collection to the Health Survey for England (HSE) – a large, annual, rolling nationally representative general population survey recruiting throughout the year – to enable rapid population-based surveys of influenza infection and disease during a pandemic. Using these surveys we can assess the spread of the virus geographically, by age and through time. The data generated can also provide denominators for national estimates of case fatality and hospitalisation rates. Phase 1 : we compared retrospectively collected HSE illness rates during the first two infection waves of the 2009 pandemic with the Flu Watch study (a prospective community cohort). Monthly and seasonal age-specific rates of illness and proportion vaccinated were compared. Phase 2 : we piloted blood specimen and data collection alongside the 2012–13 HSE. We are developing laboratory methods and protocols for real-time serological assays of a novel pandemic influenza virus using these specimens, and automated programmes for analysing and reporting illness and infection rates. Phase 3 : during inter-pandemic years, the study enters a holding phase, where it is included in the yearly HSE ethics application and planning procedures, allowing rapid triggering in a pandemic. Phase 4 : once retriggered, the study will utilise the methods developed in phase 2 to monitor the severity and spread of the pandemic in real time. Results Phase 1 : the rates of reported illness during the first two waves in the HSE underestimated the community burden as measured by Flu Watch, but the patterns of illness by age and time were broadly comparable. The extent of underestimation was greatest for HSE participants interviewed later in the year compared with those interviewed closer to the pandemic. Vaccine uptake in the HSE study was comparable to independent national estimates and the Flu Watch study. Phases 2 and 3 : illness data and serological samples from 2018 participants were collected in the 2012–13 HSE and transferred to the University College London Hospital. In the 2013 HSE and onwards, this project was included in the annual HSE ethics and planning rounds. Conclusions The HSE’s underestimation of illness rates during the first two waves of the pandemic is probably due to recall bias and the limitation of being able to report only one illness when multiple illnesses per season can occur. Changes to the illness questions (reporting only recent illnesses) should help minimise these issues. Additional prospective follow-up could improve measurement of disease incidence. The representative nature of the HSE allows accurate measurements of vaccine uptake. Study registration This study is registered as ISRCTN80214280. Funding This project was funded by the NIHR Public Health Research programme and will be published in full in Public Health Research ; Vol. 3, No. 6. See the NIHR Journals Library website for further project information.
Background: Assessing severity and spread of a novel influenza strain at the start of a pandemic is critical for informing a targeted and proportional response. It requires community-level studies to estimate the burden of infection and disease. Rapidly initiating such studies in a pandemic is difficult. The study aims to establish an efficient system allowing real-time assessment of population susceptibility, spread of infection and clinical attack rates in the event of a pandemic. Methods: We developed and appended additional survey questions and specimen collection to the Health Survey for England (HSE) – a large, annual, rolling nationally representative general population survey recruiting throughout the year – to enable rapid population-based surveys of influenza infection and disease during a pandemic. Using these surveys we can assess the spread of the virus geographically, by age and through time. The data generated can also provide denominators for national estimates of case fatality and hospitalisation rates. Phase 1: we compared retrospectively collected HSE illness rates during the first two infection waves of the 2009 pandemic with the Flu Watch study (a prospective community cohort). Monthly and seasonal age-specific rates of illness and proportion vaccinated were compared. Phase 2: we piloted blood specimen and data collection alongside the 2012–13 HSE. We are developing laboratory methods and protocols for real-time serological assays of a novel pandemic influenza virus using these specimens, and automated programmes for analysing and reporting illness and infection rates. Phase 3: during inter-pandemic years, the study enters a holding phase, where it is included in the yearly HSE ethics application and planning procedures, allowing rapid triggering in a pandemic. Phase 4: once retriggered, the study will utilise the methods developed in phase 2 to monitor the severity and spread of the pandemic in real time. Results: Phase 1: the rates of reported illness during the first two waves in the HSE underestimated the community burden as measured by Flu Watch, but the patterns of illness by age and time were broadly comparable. The extent of underestimation was greatest for HSE participants interviewed later in the year compared with those interviewed closer to the pandemic. Vaccine uptake in the HSE study was comparable to independent national estimates and the Flu Watch study. Phases 2 and 3: illness data and serological samples from 2018 participants were collected in the 2012–13 HSE and transferred to the University College London Hospital. In the 2013 HSE and onwards, this project was included in the annual HSE ethics and planning rounds. Conclusions: The HSE’s underestimation of illness rates during the first two waves of the pandemic is probably due to recall bias and the limitation of being able to report only one illness when multiple illnesses per season can occur. Changes to the illness questions (reporting only recent illnesses) should help minimise these issues. Additional prospective follow-up could improve measurement of disease incidence. The representative nature of the HSE allows accurate measurements of vaccine uptake. Study registration: This study is registered as ISRCTN80214280. Funding: This project was funded by the NIHR Public Health Research programme and will be published in full in Public Health Research; Vol. 3, No. 6. See the NIHR Journals Library website for further project information.
Author Quinlivan, Mark
Breuer, Judith
Hayward, Andrew C
Hutchings, Stephanie
Fragaszy, Ellen B
Craig, Rachel
Kidd, Michael
Mindell, Jennifer
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Cites_doi 10.1136/bmj.b2840
10.1371/journal.pone.0017074
10.1093/ije/dyr199
10.1371/journal.pmed.1000275
10.1136/bmj.b5213
10.1371/journal.pone.0011677
10.1016/S2213-2600(14)70034-7
10.1128/CVI.00368-08
10.1111/1469-0691.12477
10.1371/journal.pmed.1000207
10.1186/1471-2334-11-68
10.1128/CVI.05072-11
10.1371/journal.ppat.1003061
10.3310/hta14550-03
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References Craig (key20150701152716668_ref1-bib19) 2011
Garske (key20150701152716668_ref1-bib16) 2009; 339
Donaldson (key20150701152716668_ref1-bib10) 2009; 339
Monica Sethi (key20150701152716668_ref1-bib17) 2010
Baguelin (key20150701152716668_ref1-bib11) 2011; 6
Presanis (key20150701152716668_ref1-bib9) 2009; 6
Hine (key20150701152716668_ref1-bib4) 2010
key20150701152716668_ref1-bib5
Mindell (key20150701152716668_ref1-bib13) 2012; 41
Noah (key20150701152716668_ref1-bib15) 2009; 16
Brooks-Pollock (key20150701152716668_ref1-bib6) 2011; 11
Hayward (key20150701152716668_ref1-bib12) 2014; 2
Cauchemez (key20150701152716668_ref1-bib20) 2012; 8
Van Kerkhove (key20150701152716668_ref1-bib1) 2010; 7
Paolotti (key20150701152716668_ref1-bib7) 2014; 20
Hardelid (key20150701152716668_ref1-bib3) 2010; 14
Broberg (key20150701152716668_ref1-bib2) 2011; 18
Craig (key20150701152716668_ref1-bib14) 2011
Hadler (key20150701152716668_ref1-bib8) 2010; 5
Fateha Begum (key20150701152716668_ref1-bib18) 2010
References_xml – ident: key20150701152716668_ref1-bib5
– volume: 339
  start-page: b2840
  year: 2009
  ident: key20150701152716668_ref1-bib16
  article-title: Assessing the severity of the novel influenza A/H1N1 pandemic
  publication-title: BMJ
  doi: 10.1136/bmj.b2840
  contributor:
    fullname: Garske
– volume: 6
  start-page: e17074
  year: 2011
  ident: key20150701152716668_ref1-bib11
  article-title: Age-specific incidence of A/H1N1 2009 influenza infection in England from sequential antibody prevalence data using likelihood-based estimation
  publication-title: PLOS ONE
  doi: 10.1371/journal.pone.0017074
  contributor:
    fullname: Baguelin
– volume: 41
  start-page: 1585
  year: 2012
  ident: key20150701152716668_ref1-bib13
  article-title: Cohort profile: the health survey for England
  publication-title: Int J Epidemiol
  doi: 10.1093/ije/dyr199
  contributor:
    fullname: Mindell
– volume-title: Health Survey for England 2010. Volume 1: Respiratory Health
  year: 2011
  ident: key20150701152716668_ref1-bib19
  contributor:
    fullname: Craig
– volume: 7
  start-page: e1000275
  year: 2010
  ident: key20150701152716668_ref1-bib1
  article-title: Studies needed to address public health challenges of the 2009 H1N1 influenza pandemic: insights from modeling
  publication-title: PLOS Med
  doi: 10.1371/journal.pmed.1000275
  contributor:
    fullname: Van Kerkhove
– volume: 339
  start-page: b5213
  year: 2009
  ident: key20150701152716668_ref1-bib10
  article-title: Mortality from pandemic A/H1N1 2009 influenza in England: public health surveillance study
  publication-title: BMJ
  doi: 10.1136/bmj.b5213
  contributor:
    fullname: Donaldson
– volume: 5
  start-page: e11677
  year: 2010
  ident: key20150701152716668_ref1-bib8
  article-title: Case fatality rates based on population estimates of influenza-like illness due to novel H1N1 influenza: New York City, May–June 2009
  publication-title: PLOS ONE
  doi: 10.1371/journal.pone.0011677
  contributor:
    fullname: Hadler
– volume: 2
  start-page: 445
  year: 2014
  ident: key20150701152716668_ref1-bib12
  article-title: Comparative community burden and severity of seasonal and pandemic influenza: results of the Flu Watch cohort study
  publication-title: Lancet Respir Med
  doi: 10.1016/S2213-2600(14)70034-7
  contributor:
    fullname: Hayward
– volume: 16
  start-page: 558
  year: 2009
  ident: key20150701152716668_ref1-bib15
  article-title: Qualification of the hemagglutination inhibition assay in support of pandemic influenza vaccine licensure
  publication-title: Clin Vaccine Immunol
  doi: 10.1128/CVI.00368-08
  contributor:
    fullname: Noah
– volume-title: The 2009 Influenza Pandemic. An Independent Review of the UK Response to the 2009 Influenza Pandemic
  year: 2010
  ident: key20150701152716668_ref1-bib4
  contributor:
    fullname: Hine
– volume-title: Seasonal Influenza Vaccine Uptake Among the 65 years and Over and Under 65 Years at Risk in England
  year: 2010
  ident: key20150701152716668_ref1-bib18
  contributor:
    fullname: Fateha Begum
– volume: 20
  start-page: 17
  year: 2014
  ident: key20150701152716668_ref1-bib7
  article-title: Web-based participatory surveillance of infectious diseases: the Influenzanet participatory surveillance experience
  publication-title: Clin Microbiol Infect
  doi: 10.1111/1469-0691.12477
  contributor:
    fullname: Paolotti
– volume: 6
  start-page: e1000207
  year: 2009
  ident: key20150701152716668_ref1-bib9
  article-title: The severity of pandemic H1N1 influenza in the United States, from April to July 2009: a Bayesian analysis
  publication-title: PLOS Med
  doi: 10.1371/journal.pmed.1000207
  contributor:
    fullname: Presanis
– volume: 11
  start-page: 68
  year: 2011
  ident: key20150701152716668_ref1-bib6
  article-title: Using an online survey of healthcare-seeking behaviour to estimate the magnitude and severity of the 2009 H1N1v influenza epidemic in England
  publication-title: BMC Infect Dis
  doi: 10.1186/1471-2334-11-68
  contributor:
    fullname: Brooks-Pollock
– volume: 18
  start-page: 1205
  year: 2011
  ident: key20150701152716668_ref1-bib2
  article-title: Seroprevalence to influenza A(H1N1) 2009 virus – where are we?
  publication-title: Clin Vaccine Immunol
  doi: 10.1128/CVI.05072-11
  contributor:
    fullname: Broberg
– volume-title: Pandemic H1N1 (Swine) Influenza Vaccine Uptake Amongst Patient Groups in Primary Care in England 2009/10
  year: 2010
  ident: key20150701152716668_ref1-bib17
  contributor:
    fullname: Monica Sethi
– volume: 8
  start-page: e1003061
  year: 2012
  ident: key20150701152716668_ref1-bib20
  article-title: Influenza infection rates, measurement errors and the interpretation of paired serology
  publication-title: PLOS Pathog
  doi: 10.1371/journal.ppat.1003061
  contributor:
    fullname: Cauchemez
– volume: 14
  issue: 55
  year: 2010
  ident: key20150701152716668_ref1-bib3
  article-title: Assessment of baseline age-specific antibody prevalence and incidence of infection to novel influenza A/H1N1 2009
  publication-title: Health Technol Assess
  doi: 10.3310/hta14550-03
  contributor:
    fullname: Hardelid
– volume-title: Health Survey for England 2010. Volume 2: Methods and Documentation
  year: 2011
  ident: key20150701152716668_ref1-bib14
  contributor:
    fullname: Craig
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Snippet Background Assessing severity and spread of a novel influenza strain at the start of a pandemic is critical for informing a targeted and proportional response....
Background: Assessing severity and spread of a novel influenza strain at the start of a pandemic is critical for informing a targeted and proportional...
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SubjectTerms data collection
epidemiology
health surveys
human
influenza
pandemics
public health
serology
surveillance
Title Population-level susceptibility, severity and spread of pandemic influenza: design of, and initial results from, a pre-pandemic and hibernating pandemic phase study using cross-sectional data from the Health Survey for England (HSE)
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