Vaccine 24 (2006) 1786–1791

Influenza vaccine uptake in adults aged 50–64 years:Policy and practice in England 2003/2004

Carol Josepha,∗, Suzanne Elgoharia, Tom Nicholsb, Neville Verlanderb

a Respiratory Diseases Department, Health Protection Agency Centre for Infections,61 Colindale Avenue, London NW9 5EQ, UK

b Statistics, Modelling and Economics Department, Health Protection Agency Centre for Infections,61 Colindale Avenue, London NW9 5EQ, UK

Received 11 February 2005; received in revised form 29 September 2005; accepted 10 October 2005Available online 26 October 2005

Abstract

A small national study was carried out in England in 2003/2004 to ascertain the views of primary care trusts (PCTs) and general practitioners(GPs) on whether influenza immunisation should be extended to all people aged 50–64 years from the current recommendation of 65y ided vieww the studyp l personsa R( perceived ag or more ise local healths©

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ears or more. Results showed that as many primary care trusts would be in favour, as would not be in favour. A similarly divas expressed by general practitioners. Vaccine uptake rates for high-risk (HR) and low-risk (LR) adults aged 50–64 years inopulation were higher in those practices where the GP was in favour of a more inclusive policy of offering flu vaccine to alged 50 years or more, compared with those that did not favour this policy (60% versus 54% HR (p = 0.02) and 16% versus 11% Lp = 0.02)). Higher rates of vaccine uptake for low-risk patients aged 50–64 years were also reported from practices where GPsreater health benefit of immunisation for this age group. Although policy for recommending vaccine to all patients aged 50 yearsstablished elsewhere, opinion on whether such a policy should be adopted in England is currently divided amongst those providingervices.2005 Elsevier Ltd. All rights reserved.

eywords: Influenza; Immunisation; Vaccine uptake

. Introduction

Immunisation against influenza is the principal and mostffective way of reducing morbidity and mortality in those

or whom there is an increased risk of complications from theisease. In the United Kingdom, influenza vaccination is cur-ently recommended for people who fall into a medical riskategory or who are aged 65 years or more. In England, theolicy for influenza immunisation is made by the Departmentf Health who in turn are advised by a panel of leading med-

cal and scientific experts in respiratory disease treatment,ontrol and prevention.

∗ Corresponding author. Tel.: +44 208 327 7497; fax: +44 208 200 7868.E-mail address: carol.joseph@hpa.org.uk (C. Joseph).

In autumn 2000, the Department of Health for Englannounced a change to the existing policy for influeimmunisation and for the first time recommended thapatients aged 65 years or more regardless of underlyingical conditions should be offered vaccine[1]. Each year sincthen a national uptake target has been set for this grouevaluation of the new policy has also taken place thromonitoring the vaccine uptake. Four years of data areavailable and show the national target was reached inout of these four years. In 2003/2004 when the target70%, 71% of all patients aged 65 years or more werecinated against influenza. The success of this policy iswell established[2].

In contrast, flu vaccine uptake in the medically high-groups aged less than 65 years continues to remainbelow 50%, particularly in the younger age groups[3]. Many

264-410X/$ – see front matter © 2005 Elsevier Ltd. All rights reserved.oi:10.1016/j.vaccine.2005.10.024

C. Joseph et al. / Vaccine 24 (2006) 1786–1791 1787

authorities believe that a higher uptake of influenza vaccineshould be encouraged in people aged 50–64 years, regardlessof medical risk, firstly in order to protect them from the virus,secondly as a catch-all policy to increase coverage in thosewith undetected risk conditions, thirdly to get people used tohaving the vaccine before they become eligible for the age-based policy of universal immunisation from the age of 65years and fourthly to increase vaccine consumption which inturn will allow manufacturers to more easily expand produc-tion in the event of a high demand associated with pandemicinfluenza. However, the extent to which the views are sup-ported on the first three points by general practitioners (GPs)and those managing local health care services in primary caretrusts (PCTs) is unknown. A small questionnaire study wastherefore carried out to provide information in relation topolicy, practice and attitudes of health professionals for vac-cinating high-risk and low-risk people in the 50–64 years agegroup during the winter 2003–2004. PCTs in England wererequested to provide information on local policy, and GPs insome of these PCTs, their views and use of vaccine for thisage group.

2. Methods

A multi-stage sampling process was used to select PCTsa ealthA itha ionsi on).S ran-d

udy.F ecteda f thef eralp forn smalld Mid-l outha veyst n too thiss GPs prac-t eightt rredt ion”o wasc

ber2 nzaa weres om-m tionc vant

lead person for influenza policy at the local level was askedto complete the questionnaire and return it by post in thepre-paid envelope provided. The second part of the studywas conducted in March 2004, when influenza activity hadceased. For the 30 PCTs involved, covering letters and ques-tionnaires were again sent to the same people but in addition,the influenza immunisation co-ordinator was asked to for-ward the part two questionnaire and a covering letter to eachof the general practices in their PCT. Only one response pergeneral practice was requested after which the questionnairewas to be returned to the PCT for forwarding to us. All datawere entered on to the computer using Epi Info 6[4] andanalysed in Stata 8[5].

3. Results

3.1. Policy study: Questionnaire 1

Fifty-one PCTs (85%) responded to the policy question-naire; 81% in the North, 75% in the Midlands and East, 90%in the South region and 100% in London.

PCT respondents were asked whether their PCT agreedwith or supported offering influenza vaccine to the followingpeople without medical risk and currently not in a risk grouprecommended for annual vaccine: children, young adultsa and5 nga sup-p –64y e sci-e is ast nda-t oft oulda e toa t thisv er-i f ther duc-t redg takea CTs( ther 9%g howt ups.A eirG insti cci-n ndi cticep f theP PCTf ged<

nd general practices. Firstly, 50% of the 28 Strategic Huthorities (SHAs) in England were randomly selected, wrandom sample being taken from each of four NHS reg

n England (North, Midlands and East, South and Londecondly, from the 14 SHAs selected, 60 PCTs wereomly selected from each of the four regions.

The 60 PCTs were used for the policy part of the strom these 60 PCTs, 30 PCTs were again randomly selnd again a random sample was taken from each o

our regions. The 30 PCTs yielded a total of 949 genractices to participate in the GP survey. After allowingon-response the achieved sample of PCTs was to aegree under representative of PCTs in the North and

ands and East and over representative of PCTs in the Snd in London. Weights are routinely used in sample sur

o correct estimates when the achieved sample is knowver or under sample certain groups and was applied inurvey before analysis was undertaken. Analysis of theurvey also used weights. In the event, none of the GPices in London returned the questionnaire. Thus, the what would have been given to London GPs was transfeo GPs from the South, effectively creating a “super-regut of London and the South regions before analysisompleted.

The policy part of the study was carried out in Octo003, at the beginning of the season for monitoring influectivity. Covering letters and copies of the questionnaireent to the Director of Public Health, the Consultant in Cunicable Disease Control and the influenza immunisa

o-ordinator in each of the 60 selected PCTs. The rele

ged 25–49 years or adults aged 50–64 years. Only 2%% supported offering vaccine to low-risk children or youdults respectively, and 18% reported that their PCTorted the offering of vaccine for low-risk adults aged 50ears. Of the 10 PCTS that gave this response, 7 gavntific evidence based on clinical or cost benefit analys

he reason. However, when told of the current recommeion in the USA and asked to give a personal view, 39%he PCT responders supported the view that the UK shlso adopt the USA recommendation of offering vaccinll persons aged 50 years or more; 33% did not supporiew and 28% were not sure. Of the 39% in favour of lowng the age for universal vaccination, 66% said that one oeasons for this support was that it would result in a reion in flu-related morbidity; 47% said that vaccine offeood protection; and 51% said that it would improve upmong high-risk younger age groups. The majority of P73%) offered advice to GPs on how to identify patients inisk groups for vaccine. Of those that did offer advice, 7ave advice on how to set up a disease register, 67% on

o monitor uptake and 65% on how to identify age grovery high proportion of all PCTs (81%) supported thPs in promoting the importance of immunisation aga

nfluenza, 74% through encouraging the setting up of vaation clinics, 59% helped with implementing funding a

ncentive schemes and 87% helped with auditing praerformance. Notwithstanding these reports, only 53% oCTs had established a data collection system in their

or monitoring the vaccine uptake in high-risk patients a65 years for the winter 2003/2004.

1788 C. Joseph et al. / Vaccine 24 (2006) 1786–1791

Table 1GP practices by whether possible to calculate vaccine uptake rates

Number of GP practices

Neither vaccine uptake rate calculated 45Vaccine uptake rate calculated for HR

50–64 years, but not for LR 50–64years

13

Vaccine uptake rate calculated for LR50–64 years, but not for HR 50–64years

2

Vaccine uptake rate calculated forboth HR 50–64 years and LR50–64 years

155

Total number of responding GPpractices

215

3.2. General practice study: Questionnaire 2

A total of 215 GP practices (23%) responded. All 215came from just 20 of the 30 PCTs sampled for the secondpart of the study. The highest number was from the South(88), followed by 71 from the Midlands and East and 56from the North. None responded from the selected PCTS inthe London region. Of the GPs in the other three regions,35% responded from the South, 35% from the Midlandsand East and 18% from the North. The percentage of reg-istered patients aged 50–64 years in the high-risk group wasestimated as 21% from the data provided by 163 practices.Vaccine uptake data for high-risk and low-risk patients aged50–64 years were provided by 168 and 157 practices, respec-tively (Table 1).

Practices were asked if they had set up a reminder sys-tem last winter for offering vaccine to the <65 s high-riskpatients. Ninety percent reported that they had, the most com-mon form of which was by letter. Reminders to children <16years were sent less frequently than reminders to adults aged17–49 years (62% and 86%, respectively) and less frequentlythan reminders to older adults aged 50–64 years (95%). Whenasked if practices gave vaccine to any low-risk patients lastwinter, 93% replied in the affirmative. Of those that had, thevaccine was given to carers of patients (67%), on demand(64%) and for specific reasons, e.g. travel, by 14% of thep ealthb ofG -riska high-r

reda n 50y GPsb al ofb ed as riska

age-b 51%

agreed and 49% disagreed. (Unlike PCT respondents, GPswere not told about the current recommendation in the USA.)A reduction in flu-related work absenteeism was the mostfrequently cited reason for supporting the change in policy,followed by the view that an all-inclusive policy would cap-ture more patients in the high-risk groups.

In 33 practices where vaccine uptake among the high-riskpatients aged 50–64 years in 2003/2004 was <50%, logisticalreasons were not given as the cause. Instead GPs reported thatlack of demand and low perceptions of the severity of illnessby this patient group were the most common reasons for thelow-vaccine uptake. However, it was also reported that someGPs had historically focused their targeting on the >65 s atthe expense of the other risk groups.

In contrast, in 70 practices where vaccine uptake amongthe high-risk patients aged 50–64 years in 2003/2004 was>50%, good use of publicity and patient reminders, vacci-nation in previous years and vaccine recommended by thedoctor were all frequently reported reasons for the higheruptake.

3.3. Vaccine uptake rates in the 50- to 64-year-olds

In this study, mean vaccine uptake in 2003/2004 amonghigh-risk adults aged 50–64 years was calculated as 57%(95% Cl 53–60%, median rate 56%) and 13% (95% Cl1 ged5 eanu

e atG ratesin thate cineu thisg ortedb e not(

om-m ratesf ice,5 sa taker er lit-t reedo ntsa cticesw f fluv ver-sO xam-i nce(

nisa-t ages

ractices. When asked to express an opinion on the henefits of flu vaccine to high and low-risk adults, 56%Ps believed it offered a great deal of benefit to highdults under 50 years and 79% a great deal of benefit toisk adults aged 50–64 years.

Fifty-nine percent of GPs believed that flu vaccine offesmall health benefit to low-risk adults aged less tha

ears. For low-risk adults aged 50–64 years, 47% ofelieved it to offer a moderate benefit and 9% a great deenefit. Thirty-six percent of GPs believed vaccine offermall amount of benefit and 7% no benefit at all to low-dults aged 50–64 years.

GPs were almost equally divided as to whether theased policy should be lowered from 65 to 50 years;

0–16%, median rate 10%) among low-risk adults a0–64 years. For high and low risk combined, the mptake was 22% (Cl 19–25%, median rate 19%).

Associations between policy at PCT level and practicP level were investigated for effect on vaccine uptake

n high and low-risk adults aged 50–64 years (Table 2). A sig-ificant statistical association was found between PCTsstablished a data collection system for monitoring vacptake in the under 65 s high-risk and vaccine uptake inroup reported by GPs. An uptake rate of 60% was repy GPs who were monitored and 51% by those that werp = 0.005).

Offering advice to GPs on how to identify patients recended for flu vaccine made no difference to uptake

or high-risk patients aged 50–64 years (58% with adv5% without advice,p = 0.35). Similarly, for low-risk patientged 50–64 years with and without PCT advice, the upates were the same at 13% (p = 0.75). The vaccine uptakate in both high and low-risk patients was found to bele different in those general practices where the PCT agr supported the offering of flu vaccine to low-risk patieged 50–64 years, compared with those general prahere the PCT did not agree or support the offering oaccine to low-risk patients aged 50–64 years (57%us 57% HR (p = 0.86) and 15% versus 13% LR (p = 0.23)).ther associations between policy and practice were e

ned and none were found to be of statistical significaTable 2).

Practices that favoured lowering the age-based immuion policy from 65 to 50 years vaccinated higher percent

C. Joseph et al. / Vaccine 24 (2006) 1786–1791 1789

Table 2Associations between policy and influenza vaccine uptake rates for high-risk (HR) and low-risk (LR) patients aged 50–64 years

Comparison groups defined by “Policy”questionnaire sent to PCTs

Mean vaccine uptakerate HR 50–64 years

p-value HR Mean vaccine uptakerate LR 50–64 years

p-value LR

Q1(c)PCT agrees with or supports the offering offlu vaccine to LR 50–64 years

No 56.5% (n = 149)0.86

No 12.8% (n = 140)0.23Yes 56.8% (n = 19) Yes 15.1% (n = 17)

Q4Do you offer advice/support to GPs on howto identify patients in the different groupsrecommended for flu vaccination?

No 55.2% (n = 54)0.35

No 12.5% (n = 47)0.75

Yes 57.5%(n = 111) Yes 13.4% (n = 107)

Q5(a)Do you offer advice in how to setup anappropriate disease register forrecommended at-risk groups?

No 53.4% (n = 15)0.29

No 9.7%(n = 15)0.13

Yes 58.0% (n = 96) Yes 13.9% (n = 92)

Q5(b)Do you offer advice in how to identify agegroups?

No 54.7% (n = 31)0.43

No 10.6% (n = 31)0.28Yes 58.5% (n = 80) Yes 14.5% (n = 76)

Q5(c)Do you offer advice in how to monitoruptake?

No 58.8% (n = 34)0.65

No 14.7% (n = 33)0.63Yes 56.9% (n = 77) Yes 12.8% (n = 74)

Q5(d)(i) and(ii)

Do you offer advice in how to estimate theamount of vaccine required for HR and LR<65?

No 59.9% (n = 44)0.33

No 14.7% (n = 71)0.24

Yes 55.8% (n = 67) Yes 10.4% (n = 36)

Q6(a)Do you engage in flu immunisation activitieswith GPs (regular promotion ofimmunisation, e.g. newsletters)?

No 59.1%(n = 27)0.38

No 13.1% (n = 24) 0.99

Yes 56.1% (n = 141) Yes 13.0% (n = 133)

Q6(b)Do you engage in flu immunisation activitieswith GPs (meetings with GPs)?

No 58.2% (n = 83)0.30

No 13.6% (n = 77)0.75Yes 55.1%(n = 85) Yes 12.6% (n = 80)

Q6(c)Do you engage in flu immunisation activitieswith GPs (public health activities such aslocal adverts)?

No 55.8% (n = 27)0.76

No 13.8% (n = 25)0.81Yes 56.7% (n = 141) Yes 12.9% (n = 132)

Q6(d)Do you engage in flu immunisation activitieswith GPs (funding/incentive systems toincrease uptake)?

No 57.1%(n = 77)0.74

No 13.8% (n = 73)0.67Yes 56.1%(n = 91) Yes 12.5% (n = 84)

Q6(e)Do you engage in flu immunisation activitieswith GPs (encourage setting up ofvaccination clinics?)

No 59.0% (n = 34)0.31

No 12.3% (n = 31)0.81Yes 55.9% (n = 134) Yes 13.2% (n = 126)

Q6(f)Do you engage in flu immunisation activitieswith GPs (audit practiceperformance/achievement)?

No 58.3% (n = 15)0.28

No 16.0% (n = 14)0.49Yes 56.4% (n = 153) Yes 12.7% (n = 143)

Q7PCT established a data collectionsystem for monitoring the fluvaccine uptake in HR <65

No 51.4% (n = 46)0.005 N/AYes 60.1%(n = 98)

Comparison groups defined by“Practice” questionnaire sent to GPpractices

Mean vaccine uptakerate HR 50–64 years

p-value HR Mean vaccine uptakerate LR 50–64 years

p-value LR

Q1Practice set up asystem for remindingthe HR <65 patients toget vaccinated?

No 53.3% (n = 15)0.65 N/AYes 56.6% (n = 149)

Yes (mainly postalinvitations) 57.1%(n = 99)

0.63 N/A

Yes (mainly telephoneinvitations) 55.0%(n = 32)

0.80 N/A

Yes (other system forreminding) 55.6%(n = 72)

0.74 N/A

Q1Practice set up asystem for remindingthe HR 50–64-yearpatients to getvaccinated?

No 52.4% (n = 22)0.46 N/AYes 56.9% (n = 142)

Q2Practice set up special clinics forvaccinating HR patients separately fromclinics for those 65 or more?

No 55.9% (n = 142) 0.27 N/A

Yes 60.8% (n = 20)

Q3Did you give vaccineto any LR patients lastwinter?

N/ANo 7.4% (n = 7)

0.02Yes 12.9% (n = 147)

1790 C. Joseph et al. / Vaccine 24 (2006) 1786–1791

Table 2 (Continued )

Q4(c) and (d) GPs perceived healthprotective benefit influ vaccination for HRand LR 50–64 years

None –%(n = 0)

0.50

None 8.7% (n = 9)

0.09Small amount 62.4%(n = 2)

Small amount 10.1% (n = 50)

Mod amount 53.6%(n = 34)

Mod amount 13.7% (n = 71)

A great deal57.0%(n = 118)

A great deal 20.6% (n = 13)

Q5Are you in favour oflowering theage-based vaccinepolicy from 65 yearsto 50 years?

No 54.2% (n = 74)0.02

No 10.8% (n = 67)0.02Yes 60.4% (n = 76) Yes 15.5% (n = 72)

Table 3Associations between policy and whether GPs in favour of lowering the age-based vaccine policy from 65 years to 50 years

Comparison groups defined by “Policy”questionnaire sent to PCTs

Q5 GP in favour of lowering theage-based vaccine policy from 65 yearsto 50 years

p-value

Q3Do you think UK should offer fluvaccine to all persons aged 50years or more?

No 36.1% of GPs in favour (n = 36)0.11Yes 53.6% of GPs in favour (n = 56)

of both high and low-risk patients compared with practicesagainst a change in policy (60% versus 54% HR,p = 0.02 and16% versus 11% LR,p = 0.02).

Higher rates of vaccine uptake for low-risk patients aged50–64 years were reported from practices where GPs per-ceived a greater health benefit of immunisation for low-risk50- to 64-year-olds. Average uptake ranged from 21% in asmall number of practices where the GP perceived a great dealof benefit, 14% from practices where the GP perceived mod-erate benefit, 10% where the GP perceived a small amount ofbenefit and 9% where the GP perceived no benefit (trend testp = 0.09) (Table 2). GPs were more likely to agree to lower-ing the age-based vaccination policy from 65 to 50 years iftheir PCT was also in agreement (54% versus 36%,p = 0.11)(Table 3).

4. Discussion

Influenza vaccine is the most important means by whichinfluenza-related morbidity and mortality is reduced or pre-vented, and increasing vaccine uptake is a key public healthobjective in most countries. Immunisation of all persons aged50 years or more was recommended in USA in 2000[6]and in Canada universal immunisation for all people above6 months of age was introduced in 2004[7]. In England,t fori t thep idedo ptedh cludea ageg ationt year,

as well as logistic issues of organising vaccination clinics forthe additional cohort of patients.

The poor response rate by the GPs in the second halfof this study is a major limitation to interpretation of theresults. Non-response due to having never received the ques-tionnaire from the PCT occurred in one region and accountedfor 22% of the non-response rate. In the other three regions, itis unknown to what extent general practices did not respondbecause of work loads, a local policy of refusing to partici-pate in surveys of this type or because they may have beenperceived as giving less priority to vaccination policy com-pared with those that did respond. Also, the fact that only oneresponse was requested from each general practice may havecaused bias in those questions relating to GP opinions. Onecannot compare the non-responding practices with respond-ing practices or with information on general practices as awhole, for variables such as size of practice, demographicmake up of patients or vaccination policy since all respond-ing and non-responding practices were anonymised at thePCT level. Thus, the direction and magnitude of any overallbias that occurred cannot be determined with any certainty.

Where cost-benefit studies into immunisation of healthyworking adults have been carried out, most conclude thatcost savings are indirect and made in relation to a reductionin staff absenteeism from work rather than directly throughfewer hospitalisations and deaths as found in immunisationo yw tioni tweent d int ss int

thert sav-

he results of this small study into policy and practicemmunisation of people aged 50–64 years suggest thaarticipating PCTs and general practices are evenly divn the question of whether such a policy should be adoere. Speculated reasons for not supporting the policy inlack of perceived health benefit for vaccinating this

roup, and economic issues for general practices in relo estimating the amount of vaccine to purchase each

f the 65 s and over age group[8–10]. However, for healthorking adults the magnitude of the benefit of immunisa

n any one year depends on a close antigenic match behe circulating influenza virus strains and those includehe vaccine, and recorded high levels of influenza illnehe community[9].

Thus, in healthy younger age groups, the individual, rahan society benefits most from immunisation when cost

C. Joseph et al. / Vaccine 24 (2006) 1786–1791 1791

ings relate to avoiding lost productivity rather than reducedmedical care costs. In the case of pandemic influenza, vaccineproduction would have to be significantly increased to meetdemand. Manufacturers argue that annual increases of fluvaccine now would help meet this future target since muchof the machinery needed to meet the extra demand wouldalready be in place. Although this argument is neither linkedto cost-benefit or public health analyses, it does highlight thecomplexities of vaccine administration, supply and demand.

Increasing rates of hospitalisation begin to occur in peoplewith at risk conditions for influenza from the age of 45 years[11]. Recent estimates of the percentage of high-risk peopleaged 50–64 years range from 21% in Spain[12] to 29% in theUS[13], and 21% in this small study. When these percentagesare applied to national populations, denominators can be cal-culated for those who would benefit from receiving influenzaimmunisation and compared with the estimated number ofpeople vaccinated from the risk group. This small study inEngland included 215 practices, 163 of which were usedto calculate a registered population of 47,163 persons aged50–64 years at high risk for influenza. Of these persons, 57%were vaccinated in 2003/2004, leaving about 20,000 peoplefrom these practices with a chronic disease and unvaccinatedlast winter. When extrapolated to the whole population, thehigh number of unprotected persons in this age group is ofmajor concern. It is also recognised that many <65 s have ah nott seekv romi up.O too helpt ationb lly ifu ando

lowl ndm nzaa encen 50-t me,w un-t uceda cine

uptake in the <65 s high-risk groups would seem a prudentstep to take.

Acknowledgements

The United Kingdom Vaccine Industry Group providedan unconditional educational grant towards the costs of thisstudy. The aims and objectives of the study were supportedby the Department of Health, England.

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igh risk condition of which they are unaware, and doherefore appear in the at-risk denominator or activelyaccination. Thus, the true number that would benefit fmmunisation is likely to be much higher in this age groffering vaccine by age rather than by risk would helpvercome this issue in the 50–64 year olds and wouldo raise the absolute effectiveness of the recommendy increasing uptake in all susceptible people, especiaptake targets were set in line with those for the 65 sver.

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