Prevalence of influenza A (H1N1) seropositivity in unvaccinated healthcare workers in Scotland at the height of the global pandemic

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Ediburgh Research Explorer Prevalece of iflueza A (H1N1) seropositivity i uvacciated healthcare workers i Scotlad at the height of the global pademic Citatio for published versio: Smith, K, Warer, P,

1 Ediburgh Research Explorer Prevalece of iflueza A (H1N1) seropositivity i uvacciated healthcare workers i Scotlad at the height of the global pademic Citatio for published versio: Smith, K, Warer, P, Williams, LJ, Adamso, WE, Katikireddi, SV, Dewart, P, Carma, WF, Templeto, K, Deiso, FC & Mackezie, DG 2011, 'Prevalece of iflueza A (H1N1) seropositivity i uvacciated healthcare workers i Scotlad at the height of the global pademic' Joural of Evirometal ad Public Health, vol 2011, DOI: /2011/ Digital Object Idetifier (DOI): /2011/ Lik: Lik to publicatio record i Ediburgh Research Explorer Documet Versio: Publisher's PDF, also kow as Versio of record Published I: Joural of Evirometal ad Public Health Publisher Rights Statemet: Copyright 2011 Kate Smith et al. This is a ope access article distributed uder the Creative Commos Attributio Licese, which permits urestricted use, distributio, ad reproductio i ay medium, provided the origial work is properly cited. Geeral rights Copyright for the publicatios made accessible via the Ediburgh Research Explorer is retaied by the author(s) ad / or other copyright owers ad it is a coditio of accessig these publicatios that users recogise ad abide by the legal requiremets associated with these rights. Take dow policy The Uiversity of Ediburgh has made every reasoable effort to esure that Ediburgh Research Explorer cotet complies with UK legislatio. If you believe that the public display of this file breaches copyright please cotact opeaccess@ed.ac.uk providig details, ad we will remove access to the work immediately ad ivestigate your claim. Dowload date: 22. Apr. 2018

2 Hidawi Publishig Corporatio Joural of Evirometal ad Public Health Volume 2011, Article ID , 5 pages doi: /2011/ Research Article Prevalece of Iflueza A (H1N1) Seropositivity i Uvacciated Healthcare Workers i Scotlad at the Height of the Global Pademic Kate Smith, 1 Pamela Warer, 2 Lida J. Williams, 2 Walt E. Adamso, 3 S. Vittal Katikireddi, 1 Paul Dewart, 4 William F. Carma, 3 Kate Templeto, 5 Fioa C. Deiso, 6 ad D. Graham Mackezie 1 1 Public Health ad Health Policy, NHS Lothia, Waverley Gate, 2-4 Waterloo Place, Ediburgh EH1 3EG, UK 2 Cetre for Populatio Health Scieces, Medical School, Uiversity of Ediburgh, Teviot Place, Ediburgh EH8 9AG, UK 3 West of Scotlad Specialist Virology Cetre, Gartavel Geeral Hospital, Glasgow G12 0ZA, UK 4 St Joh s Hospital, Howde Road West, Livigsto, West Lothia EH54 6PP, UK 5 Royal Ifirmary Ediburgh, NHS Lothia, Ediburgh EH16 4SA, UK 6 MRC Cetre for Reproductive Health, Uiversity of Ediburgh, Quee s Medical Research Istitute, 47 Little Frace Crescet, Ediburgh EH16 4TJ, UK Correspodece should be addressed to D. Graham Mackezie, graham.mackezie@hslothia.scot.hs.uk Received 31 May 2011; Revised 7 August 2011; Accepted 7 August 2011 Academic Editor: Ivo Iavicoli Copyright 2011 Kate Smith et al. This is a ope access article distributed uder the Creative Commos Attributio Licese, which permits urestricted use, distributio, ad reproductio i ay medium, provided the origial work is properly cited. Backgroud. We set out to idetify the level of previous exposure to iflueza A (H1N1) i uvacciated healthcare workers (HCWs) at the peak of the pademic outbreak i the UK, with cotrol samples collected prior to the outbreak. Methods. Crosssectioal study (seroprevalece assessed before ad at pademic peak, with questioaire data collected at peak of outbreak) i HCWs i Scotlad. Results. The prevalece of seropositivity i 493 HCWs at pademic peak was 10.3, which was higher tha the prepademic level by 3.7 percetage poits (95 CI 0.3 to 7.3, P = 0.048). Seropositivity rates for frotlie ad ofrotlie HCWs were similar. Coclusio. At pademic peak, oly 10.3 of HCWs were seropositive for iflueza A (H1N1), sothe great majority were stillsusceptible to ifectio at the itroductio of the vacciatio programme. Few studies have reported o seroprevalece i uvacciated ad asymptomatic participats, so our fidigs may have relevace to the wider populatio. 1. Itroductio The susceptibility of healthcare workers (HCW) to iflueza is relevat i terms of sickess absece, productivity, ad oward trasmissio of ifectio from carer to patiet [1], a particular issue with a ovel iflueza strai. The first cases of 2009 pademic iflueza A (H1N1) were idetified i Scotlad i April 2009 [2]. We set out to determie the seroprevalece of atibodies agaist the virus i uvacciated HCWs i Lothia, south east Scotlad i Autum 2009 (after the first wave of ifectio, but before the expected icrease i cases over the witer period). It is ow clear that this was close to the peak of the outbreak i the Uited Kigdom (UK) [3]. 2. Materials ad Methods Betwee 29/10/2009 ad 4/11/2009 (at the time believed to be midpademic, but ow kow to have bee peak), uvacciated NHS Lothia employees ( = 505) were recruited withi days of the start of the HCW vacciatio programme ad prior to most HCWs beig vacciated. Recruitmet was maily from three acute teachig hospitals, with smaller umbers from a psychiatric hospital ad the Health Board headquarters. After givig iformed coset participats had a serum sample take ad completed a short questioaire recordig sex, age, occupatio, ad selfreported history of flu-like symptoms or illess sice the start of the pademic period (April 2009). Of the 505 recruited,

3 2 Joural of Evirometal ad Public Health 493 employees were aged betwee 16 ad 65 years ad had complete iformatio (laboratory results ad questioaire respose). It is these 493 respodets who have bee used i all aalyses reported here. Serology specimes were tested for atibodies to iflueza A (H1N1) i the West of Scotlad Specialist Virology Cetre, Glasgow, usig microeutralisatio assays at a dilutio of 1 : 40 as previously described [4]. I additio a set of age- ad sex-matched blood samples ( = 471) were obtaied from stored serology specimes collected from HCWs for occupatioal health purposes durig 2008 (i.e., prepademic), ad these were also tested. Chi-squared test with Yates cotiuity correctio was used to compare seropositive prevalece i pre- ad peak pademic samples ad logistic regressio aalysis to examie the associatio of seropositivity with risk group classificatio. ThestudywasapprovedbytheLocalRegioalEthicsCommittee. Sample size eeded was calculated as 500, to esure a pademic estimate of seropositivity with 95 cofidece iterval o wider tha ±3.5 percetage poits, assumig that the observed prevalece was Results The age ad sex profile for pre- ad peak pademic samples was similar to the overall hospital-based NHS Lothia workforce, ad 67 of pademic participats were classified as frotlie, the same as the overall HCW workforce. I the pademic sample the prevalece of seropositivity i HCWs was 10.3 (95 cofidece iterval (CI) 7.7 to 13.0). This seropositivity was higher tha prepademic HCW seropositivity rate by 3.7 percetage poits (95 CI 0.3 to 7.3 percetage poits, P = 0.048). The study was ot poweredtotestforvariatioiseropositivityratesacrossage bads, but the highest pademic rate observed was 17.4 i the yougest age bad (16 to 25 years old), whereas prepademic this age bad had early the lowest rate (4.3). However, the small umbers i the yougest age bad meas that the differece i seropositivity (pre versus pademic) was ot statistically sigificatly differet accordig to whether comparig withi those aged up to 25 years or over 25 years (P = 0.147). Occupatios were grouped ito frotlie cotact (allied health professioals, doctors, urses, midwives, ad studets) ad o-frotlie cotact (admiistrative, pharmacy, ad support staff icludig e.g., idividuals workig i laboratories or estates ). For pademic samples, seropositivity rates for frotlie ad o-frotlie HCWs were similar overall at 11.0 (95 CI 7.6 to 14.4) ad 9.1 (5.8 to 12.5), respectively. Iflueza-like symptoms i the precedig six moths were reported by 208 (42.2), ad 12.0 (95 CI 7.6 to 16.4) of them were seropositive, compared to 9.1 (95 CI 5.8 to 12.5) of those without recet symptoms (Table 1). A tred aalysis across three levels of risk (prepademic, pademic but o iflueza-like symptoms, pademic reportig symptoms) foud a statistically sigificat tred i seropositivity (P = 0.018), with a liear odds ratio of 1.39 (95 CI 1.06 to 1.84), suggestig that overall the odds of a () Up to 35 years 36 to 55 years 56 to 65 years Overall Age bad Prepademic Pademic, o flu symptoms Pademic+flusymptoms Figure 1: Seropositivity separately for peakpademic ad prepademic samples, with peakpademic samples subdivided accordig to report or ot of iflueza-like symptoms ( = 208, 285, 471, resp.), overall ad by age bad. positive laboratory result icreased by 39 for each move from oe risk category to the ext higher category. Figure 1 shows overall seropositivity for the three risk categories ad across age bads. 4. Discussio To our kowledge, this is the first study i the UK to quatify the level of seropositivity to iflueza A (H1N1) i uvacciated HCWs pre- ad peak pademic. Our fidigs have importat implicatios both for uderstadig the spread of iflueza A (H1N1) ad for plaig ad delivery of future pademic iflueza vacciatio programmes. Previous vacciatio is idistiguishable from previous ifectio o microeutralisatio testig, so our active recruitmet of uvacciated participats for the pademic samples avoids the limitatio of other studies which did ot have full documetatio of vacciatio status, may of which relied o discarded laboratory samples, samples from blood doors or patiets [4 7]. Otherstudies havelooked at a sigle time poit [4], icludig oe study of HCWs (from Taiwa) [8], whichmeasthatitisotpossibletocompare prepademic immuity observed i other studies [6]. Our study icluded pre- ad pademic samples which allowed us to compare peak pademic seropositivity agaist the rate about 9 moths before the start of the pademic. The oly other HCW study coducted pre- ad midpademic that we have idetified (from Sigapore) used a differet assessmet of serocoversio, requirig a 4-fold rise i titre from baselie, so a direct compariso with our fidigs is ot possible [9]. Elder has reported previously that there is little idicatio of icreased susceptibility to seasoal iflueza by occupatioal group, icludig healthcare [1]. Accordigly, i the absece of a more geeral study of seroprevalece i uvacciated adults of workig age, our estimate of

4 Joural of Evirometal ad Public Health 3 Table 1: Seropositivity overall ad by age bad, separately for prepademic ad peak pademic samples. Age bad (years) Prepademic samples Peakpademic samples Overall Subdivided accordig to report of iflueza-like symptoms Reportig symptoms No symptoms reported Subgroup Subgroup Subgroup Subgroup Overall CI 4.3 to to to to 12.5

5 4 Joural of Evirometal ad Public Health pademic seropositivity is arguably the closest estimate to date of overall populatio prevalece i adults i the UK at that time. It is importat to remember the levels of ucertaity ad cocer that existed midpademic. I October 2009 the Scottish Chief Medical Officerotedaslowerspread tha aticipated [10]. However that same week the Uited States declared a iflueza A (H1N1) emergecy, with 1,000 deaths across 46 states ad questios about the ability to cope with a potetial surge i cases [11]. A week later Health Protectio Scotlad reported that iflueza A (H1N1) related hospitalisatios ad deaths i Scotlad cotiued to icrease [12]. Furthermore, the iflueza virus s ability to mutate ad trasfer geetic material betwee strais meat that a substatial icrease i cases over the witer iflueza seaso remaied a possibility. Our fidigs show that over the first six moths of the pademic the A (H1N1) strai was of limited virulece with oly aroud 4 of susceptible HCWs havig developed seropositivity despite 42 participats reportig flu-like symptoms i precedig moths. However, previous virulece is ot ecessarily a guide to future spread, particularly o the cusp of the iflueza seaso, ad our fidigs show that 90 HCWs were still susceptible to ifectio. These fidigs support the importace of vacciatio eve at the peak of a pademic (ad regardless of previous symptoms), cotrastig with fidigs of a large Eglish study that sampled patiets accessig health care betwee August ad September 2009 [6]. It has bee estimated that betwee 40 ad 50 of HCWs i the UK were vacciated for iflueza A (H1N1) by February April 2010 [13 15]; i Lothia the figure was 52 [16]. This high level of uptake i HCWs across the Uited Kigdom i the weeks followig this study meas that it would ot be feasible to estimate postpademic seropositivity amog uvacciated HCWs. Although i other studies performed towards the ed of the pademic period the seroprevalece reported betwee 20 ad 40 [4, 5, 7] was cosiderably higher tha we foud, there is ucertaity about vacciatio rates ad caveats about study populatio i these studies, as described above. Our study has a umber of potetial weakesses. We did ot recruit primary care staff. Self-selectio of participats ad the exclusio of HCWs who were targeted first by the vacciatio programme may have led to a uder- or overestimatio of the true level of ifectio with the virus for all HCWs i Lothia. Other studies have demostrated a greater icrease i seropositivity durig the pademic period i youger adults (16 to 25 years old) compared to older adults, both i high prevalece areas i the UK [4] ad amog blood doors i Australia [5]. While our study showed a similar patter of greater icrease i seropositivity i youger adults tha other age groups (Figure 1) it was ot powered to test such a iteractio hypothesis. These fidigs have importat implicatios for research ito future pademics. Havig iformatio o seroprevalece i uvacciated idividuals durig the pademic wouldhavebeeivaluableadmaybefeasibleiafuture pademic. Virology samples ca be stored idefiitely allowig compariso with samples take from previous years. Such iformatio would help idetify susceptible age groups, helpig the plaig of vacciatio campaigs durig the pademic. We therefore suggest that health protectio orgaisatios cosider collectig samples aually from a represetative pael of asymptomatic idividuals, selected ad powered to allow comparisos by age. 5. Coclusio I coclusio, our study shows that at pademic peak 10.3 of HCWs i Lothia, south east Scotlad, were seropositive for iflueza A (H1N1), so the great majority were still susceptible to iflueza A (H1N1) ifectio at the itroductio of the vacciatio programme. Coflict of Iterests The authors declare that there is o coflict of iterests. Ethical Approval This study was approved by the Lothia LREC (referece o. 09/S1102/44). Ackowledgmets Dr. Kirsty Dudas (Cosultat i Obstetrics ad Gyaecology, Royal Ifirmary Ediburgh, NHS Lothia), Eilidh Fletcher (Aalyst, Health Itelligece Uit, NHS Lothia), Adrew Deas ad Mairi McCulloch (Iformatio Services Divisio, NHS Natioal Services Scotlad). Sharo Camero ad colleagues at the Wellcome Trust Cliical Research Facility, Royal Ifirmary Ediburgh. The Chief Scietist Office, Scottish Govermet Health Directorates, for fudig this work ad providig support throughout the research. Refereces [1] A. G. Elder, Iflueza i workig populatios: a overview, Occupatioal Medicie, vol. 52, o. 5, pp , [2] E. McLea, R. G. Pebody, C. Campbell et al., Pademic (H1N1) 2009 iflueza i the UK: cliical ad epidemiological fidigs from the first few hudred (FF100) cases, Epidemiology ad Ifectio, vol. 138, o. 11, pp , [3] Epidemiological report of pademic (H1N1) 2009 i the UK April 2009 May 2010, Health Protectio Agecy, 2010, C/ [4] W. E. Adamso, S. Maddi, C. Robertso et al., 2009 pademic iflueza A(H1N1) virus i Scotlad: geographically variable immuity i Sprig 2010, followig the witer outbreak, Eurosurveillace, vol. 15, o. 24, [5] J. Mcvero, K. Laurie, T. Nola et al., Seroprevalece of 2009 pademic iflueza a (H1N1) virus i Australia blood doors, October December 2009, Eurosurveillace, vol. 15, o. 40, pp. 7 14, [6] E. Miller, K. Hoschler, P. Hardelid, E. Staford, N. Adrews, ad M. Zambo, Icidece of 2009 pademic iflueza A H1N1 ifectio i Eglad: a cross-sectioal serological study, The Lacet, vol. 375, o. 9720, pp , 2010.

6 Joural of Evirometal ad Public Health 5 [7] S.M.Zimmer,C.J.Crevar,D.M.Carteretal., Seroprevalece followig the secod wave of pademic 2009 H1N1 iflueza i Pittsburgh, PA, USA, PLoS Oe, vol. 5, o. 7, Article ID e11601, [8] Y. J. Cha, C. L. Lee, S. J. Hwag et al., Seroprevalece of atibodies to pademic (H1N1) 2009 iflueza virus amog hospital staff i a medical ceter i Taiwa, Joural of the Chiese Medical Associatio, vol. 73, o. 2, pp , [9] M. I. C. Che, V. J. M. Lee, W. Y. Lim et al., 2009 iflueza A(H1N1) serocoversio rates ad risk factors amog distict adult cohorts i Sigapore, Joural of the America Medical Associatio, vol. 303, o. 14, pp , [10] Chief Medical Officer Scotlad, Lauch date for the iflueza A(H1N1) vacciatio programme ad additioal details o vaccie dosage, CMO Letter 12, Scottish Govermet Health Directorate, 2009, [11] BBC News, US declares swie flu emergecy, BBC News Report, 2009, [12] Weekly iflueza situatio report (Icludig H1N1v), Health Protectio Scotlad, 2010, weekly-iflueza-sitrep pdf. [13] Pademic H1N1(Swie Flu) ad seasoal iflueza vaccie uptake amogst frotlie healthcare workers i Eglad 2009/2010, Departmet of Health, 2010, [14] Iflueza A H1N1v, Situatio Report umber 72, Scottish Govermet Resiliece Room, [15] NHS Laarkshire Director of Public Health Aual report 2009/2010, (chapter 3.1, Iflueza A (H1N1v) i Laarkshire), NHS Laarkshire, 2010, shire.org.uk/services/publichealth/directors-aual-report /Documets/Health20Protectio.pdf. [16] E. Fletcher, Iformatioal aalyst, NHS Lothia, Persoal commuicatio, 2011.

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