Vaccination coverage with seasonal and pandemic influenza vaccines in children in France, 2009–2010 season

Vaccine 29 (2011) 7075–7079

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Vaccination coverage with seasonal and pandemic influenza vaccines in children in France, 2009–2010 season Catherine Weil-Olivier a,1 , Bruno Lina b,∗,1 a

Université Paris 7 Diderot, Paris, France Laboratoire de Virologie EST des HCL, Centre National de Référence des virus influenzae, region Sud, CBPE, GHE, 59 bvd Pinel, 69677 BRON, & Virpath, UCBL, Université de Lyon, Lyon, France b

a r t i c l e

i n f o

Article history: Received 2 February 2011 Received in revised form 4 July 2011 Accepted 6 July 2011 Available online 4 August 2011 Keywords: Influenza vaccine Children Vaccine uptake Seasonal Pandemic

a b s t r a c t For a number of years now, GEIG, the Groupement d’Expertise et d’Information sur la Grippe (Influenza Expertise and Information Group) has conducted surveys to monitor seasonal trivalent vaccine uptake in France in adults. During the H1N1 pandemic in 2009, this survey was conducted to determine vaccination uptake for both pandemic and seasonal vaccines. An additional specific questionnaire was used to collect data on vaccination in children under 15 years of age. This additional study was carried out because pandemic vaccination (PV) was offered to the French population and children were listed as a priority target group by the national health authorities, whereas seasonal trivalent inactivated vaccines (TIV) are not recommended in children in France. Overall, we collected 2443 questionnaires on children, including children with underlying conditions (9.2%) for whom TIV vaccination was recommended. Overall, 17.9% of children (438/2443) received at least one shot of PV, compared to 3.4% (83/2443) who received at least one shot of TIV. PV uptake was statistically different between non at-risk and at-risk children (366/2218 [16.5%] vs. 71/225 [31.8%], p < 0.0001). This difference was even more significant in the subgroup of children with severe underlying diseases (42.7%, p < 0.0001). This confirms that despite the low overall PV uptake in the French population (9%), the specific recommendation for PV for children increased vaccine uptake in this specific population, suggesting that the disease burden of influenza in children is recognised by both practitioners and parents. The next few years will tell us whether TIV uptake in children increases as a consequence of the specific recommendations made for children during the 2009 pandemic wave, or whether it will return to the very low level of 3.4% observed before the pandemic. © 2011 Published by Elsevier Ltd.

1. Introduction The burden of disease of seasonal influenza in children is high [1]. In the light of increased hospital admissions, morbidity and mortality, some countries have implemented influenza vaccination in children [2]. In France, despite recognition of the impact of influenza, vaccination is not specifically recommended for this age group, except for frail children with underlying diseases [3–5]. In 2009–2010, A(H1N1)pdm 2009 was responsible for the first influenza pandemic of the 21st century [6]. Although the impact of this pandemic was debated, it was far from negligible. In the USA, the number of years of life lost (YLL) estimate for the 2009 pandemic was between an average H3N2 seasonal epidemic at the lower end and the 1968 H3N2 pandemic in 1968 adjusted to the

∗ Corresponding author. Tel.: +33 4721 29617. E-mail address: [email protected] (B. Lina). 1 On behalf of the GEIG (Groupement d’Expertise et d’Information sur la Grippe) Scientific Committee, Lyon, France. 0264-410X/$ – see front matter © 2011 Published by Elsevier Ltd. doi:10.1016/j.vaccine.2011.07.018

2000 population at the upper end [7]. In response to an emerging virus, pandemic planning was prepared in many countries, including France [8]. Among the actions to be implemented during the pandemic, vaccination was the cornerstone of the pandemic mitigation measures. Accordingly, and in the light of information collected from the countries that were first hit by A(H1N1)pdm 2009 in May, June and July 2009, pandemic vaccine purchases and recommendations were prepared in France in September 2009. The pandemic situation, with young children being at risk of frequent and severe influenza led to the introduction of specific vaccination recommendations that were different from the seasonal vaccine recommendations [8]. Children were high on the list of vaccine prioritisation [9] (Table 1). In France, influenza vaccination campaigns are carried out under the auspices of CNAM, the Caisse Nationale d’Assurance Maladie (National Health Insurance Fund). In September every year, CNAM posts out vaccine vouchers to be used by at-risk patients. This includes children with underlying conditions listed in the at-risk groups (Table 2). Using this voucher, patients can collect their vaccine (TIV) from the pharmacy and then see a doctor or nurse for

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Table 1 French recommendations for TIV in children. Seasonal vaccination is recommended to: People aged 6 months and over who have one of the following chronic conditions: Respiratory conditions, including asthma, bronchopulmonary dysplasia and cystic fibrosis. Severe congenital heart disease, severe heart failure and heart valve disease. Severe kidney disease, pure and primitive nephrotic syndromes. Sickle cell anaemia (homozygote and double heterozygote S/C), sickle cell -thalassemia. Diabetes with or without insulin when special diet is insufficient. Immune disorders (cellular, HIV positive patients: the indication for vaccination is assessed by the HCW in charge of the patient). People living in medium- or long-term care homes. Children and adolescents (between 6 months and 18 years of age) in need of prolonged acetyl-salicylic acid treatment. Cocooning strategy in the immediate household of infants less than 6 months of age with high risk factors for severe influenza, defined as follows: Premature babies, especially those with bronchopulmonary dysplasia sequelae. Congenital heart disease. Congenital immune disorder. Other lung disorders, neurological or neuromuscular disorders. Any other chronic disease.

immunisation. This system is efficient and has led to high vaccine coverage in target patient groups [10]. The seasonal vaccination campaign usually lasts 4 months, from October until the end of January. In 2009, because of the pandemic, seasonal vaccination was implemented earlier (September), to ensure wide immunisation with TIV prior to the switch to the pandemic vaccination when the monovalent pandemic vaccine (PV) would be available. For both vaccines, specific CNAM vouchers were prepared and posted to the groups for whom influenza immunisation was recommended. To determine the TIV coverage rate, a survey is conducted annually on behalf of GEIG just after the influenza season, using a procedure that has been implemented since 1992 [11]. This panel consists of 6000 individuals who are representative of the French population aged 15 years and over. This repeated analysis of vaccination coverage provides a comparison of the vaccination rates in different population categories over the years and shows the impact of changes in vaccination coverage [10,11]. Recently (since the 2006–2007 season), children have been included in the analysis. In March 2010, a survey was conducted by GEIG to determine the uptake of seasonal and pandemic influenza vaccines. This survey analysed vaccination uptake in France in both adults (15 years and over), and children of all ages. This study shows that as a result of the TIV and PV recommendations PV uptake was significantly higher in children compared with the adult population, and that in the child population PV uptake was significantly higher than TIV uptake. This result emphasizes that the general population acknowledged the fact that children were at risk Table 2 A/H1N1 MV vaccination priority groups; 2009–2010 season, France; from Ref. [12]. Population groups

Priority

Pregnant women from the beginning of the second trimester Family of infants under 6 months old (parents, siblings, adult guardian of the child including early childhood staff in charge of these infants: “cocooning” strategy) At-risk infants aged 6–23 months At-risk people aged 2–64 years Non at-risk infants aged 6–23 months At-risk people aged 65-years or older Non at-risk people aged 2–18 years Non at-risk people aged 19-years old or older

1 1

1 2 3 3 4 5

for frequent, severe influenza in the 2009 pandemic context, and accepted specific paediatric immunisation programmes to protect all children despite the lack of specific paediatric recommendations for seasonal influenza.

2. Materials and methods In March and April 2010 (for 6 weeks), a questionnaire leaflet to be self-completed was posted to the homes of 6000 French individuals, asking about their immunisation status against seasonal and pandemic influenza for the 2009–2010 season. This large panel belongs to the “Access Santé” permanent polling base, which is representative of the French resident population in terms of gender, age, occupation of head of household, region, habitat (size of the town/city) and number of individuals in the household. Data was weighted according to the characteristics of the French population aged 15 and over (Source: INSEEE employment survey 2002, with 2008 weighting). The same access panel is used every year. It consists of a list of 40,000 individuals, of whom 25% (10,000) are renewed each year. This panel is used to build the representative sample of 6000 individuals. Even though this panel is substantially renewed each year, it is possible that some individuals may have answered the survey more than once. In addition to the questions on their personal vaccination status, each adult respondent was also asked to fill in an additional questionnaire about vaccine uptake and the existence of risk factors for each of the children in their household. The children were divided into 3 age groups: 0–2, 3–5 and 6–14 years of age. These age groups were selected because of the specific recommendations introduced during the pandemic for children aged between 0 and 2, and to distinguish between children potentially attending nursery school [3–5] and those attending primary and secondary school [6–14]. The representativeness of the sample collected was retrospectively assessed using the quota method. In order to reduce the bias due to non-respondents and to infer estimations for the French population, the sociodemographic characteristics of the respondents were adjusted to the structure of the French population (INSEE, 2002, 2008 weighting). Computerised weighting was used in our analyses, based on the Raking Adjusted Statistic method, in order to compensate for any stratum under- or over-representation. Differences in proportions were compared with the z-test. Continuous variables were described by the mean and standard deviation (SD). Statistical analysis was carried out with a Student’s test (t-test); statistical significance was considered at p < 0.05 and p < 0.10, the latter value being acceptable in this type of test.

3. Results Among the 6000 questionnaires sent, 4775 people (79.6%) responded and 2443 complementary questionnaires about children in the household were obtained from among them. Information concerning vaccination rates was available for 2333 children; the number of non-respondents (110/2443) was evenly distributed among the child age groups [14/433 (3.2%), 20/548 (3.7%) and 76/1462 (5.2%) in the 0–2, 3–5 and 6–14-year-old age groups respectively (see Fig. 1)]. In this paediatric population, 225/2443 (9.2%) had underlying conditions for which TIV vaccination was recommended, including 57 with severe underlying conditions. According to the questionnaire, only 71.0% of these children received a vaccine voucher. The main underlying condition reported was asthma (193/225; 85.7%), including 168 mild and 25 severe or non-stabilized asthma cases. The remaining severe underlying conditions represented 32 children.

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Fig. 1. TIV and A(H1N1)pdm 2009 MV vaccination rate in children under 15 years of age; overall and by age group; 2009–10 season. Statistical analysis was carried out with a Student’s test.

Overall, 19.5% of the child population in this survey (476/2443) received at least one of the two vaccines (TIV or PV), 17.9% (438/2443) received at least one shot of PV, 3.4% (83/2443) at least one shot of TIV, and 1.8% (43/2443) at least one shot of both vaccines. These vaccination rates were not statistically different between the 0–2 years, 3–5 and 6–14 age groups (within the population of children who had received at least one shot of TIV or PV: comparing 0–2 years and 3–5 years p = 0.9047, comparing 0–2 years and 6–14 years p = 0.4904, comparing 3–5 years and 6–14 years p = 0.5468, Fig. 1). No significant difference was observed between the 2009–2010 TIV vaccination rates and those of the previous year (Fig. 2). Among the children with underlying conditions (225), 20.9% received at least one shot of seasonal TIV during the 2009–2010 season (Fig. 2). Among the 57 children in the severe underlying conditions group for whom TIV was recommended, the vaccination rate was 42.9% as compared to 36.8% during the previous season (p = 0.5065; Fig. 2). Among the 193 asthmatic children, 18.7% (36/193) received TIV, which represents a significant 5-point increase as compared to the previous season (p = 0.2405; Fig. 2). Among the non at-risk children (N = 2218), 145 were in families (6.5%) where a household cocooning strategy could be implep=0.5065 n = 2443

3,4

92,2

2294

2218

2057

2,4

1,6

0,9

95,8

93,5

225

236

20,9

16,2

4,4

1,8 20082009

All

Yes

67

42,9

36,8

57,1

63,2

193

207

18,7

14,3

81,3

85,7

20092010

20082009

97,2 79,1

20092010

57

p=0.2405

4,9

1,9

20092010

20082009

Non at-risk children

20092010

83,8

20082009

At-risk children

OF WHICH:

20092010

20082009

Children with severe underlying condition

Asthmatic children

No No response

Fig. 2. TIV coverage in children under 15 years of age; high-risk as listed in Table 1 versus non at-risk coverage rates; children with chronic conditions and asthma; 2009–2010 season. Statistical analysis was carried out with a Student’s test.

mented because of family member(s) with underlying conditions. 5.1% of these 145 children received at least one shot of TIV, as compared to 1.4% of the children (2073) in families where no members had underlying conditions (p < 0.001). PV uptake in all children, the non at-risk group and the at-risk group was 17.9% (438/2443), 16.5% (366/2218) and 31.8% (71/225) respectively (Fig. 3). This shows that vaccine uptake was significantly higher in children with underlying conditions (p < 0.0001). This difference was even more significant in the subgroup of children with severe underlying diseases (24/57, 42.7%; p < 0.0001). 4. Discussion Every year in France there is an estimated 2.2–4.6 million cases of seasonal influenza [22]. While mostly benign in healthy people, the morbidity and mortality in high risk groups (elderly, patients with underlying diseases) can be high [12]. Since the 1990s, the French recommendations for seasonal influenza have focused on high risk groups, as in most European Union Member States [2]. Recently, recommendations have been extended to all patients with asthma [3,13], and cocooning vaccination strategies have been recommended in households with children less than 6 months of age with an underlying condition [3]. However, there is no recommendation for child immunisation, unlike in some countries in North America and Europe [14,15]. According to our study, only 3.4% of the French paediatric population have received the TIV, while vaccine uptake can reach 30–42% in children in countries with a universal child immunisation policy [14]. The focus of vaccination on high-risk groups only (which represent 9.5% of children) explains the poor uptake in children and this is consistent with the data collected since 2007–2008 by GEIG (unpublished data), and similar to results published by Vaux et al. [21]. However, vaccine uptake in children with severe underlying diseases was high (43%), reaching up to 70% as reported in previous studies [15,21], whereas 26% of the French adult population was vaccinated with TIV during the 2009–2010 season (Fig. 1), the same level of TIV vaccination observed in 2008–2009, the highest level of TIV vaccination recorded so far. In 2009, the emergence of the A(H1N1)pdm 2009 virus was seen as a major pandemic threat for children. Hence, children were identified as a priority group for pandemic vaccination and practitioners were aware of the burden of disease, the high incidence and the increased risk of severe cases in the paediatric population, especially in school-age children. As this promotion of influenza vaccination in children was unusual, GEIG decided to carry out

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p=0.0000 Reminder of coverage rates among individuals aged 15 and older

11%

9%

17,9

16,5

13%

p=0.0000 20%

15% Yes

31,8

29,4 42,7

No No response

77,7

78,7 68,2

4,4

4,8

All

Non at-risk children

At-risk children

OF WHICH: n=

2443

2218

225

70,6 57,3

Children with seve re underlying conditions

57

Asthmatic children

193

Fig. 3. Children under 15 years of age; A(H1N1)pdm 2009 coverage rate in healthy and at-risk children as listed in Table 1, compared with overall adult coverage; 2009–2010 season. Statistical analysis was carried out with a Student’s test.

this study. Our data showed that PV vaccine uptake in the paediatric population was 18%, significantly higher than TIV uptake (3%), and also significantly higher than the 11% PV uptake recorded in adults (p < 0.05). Similarly, in patients with underlying diseases, PV vaccine uptake was higher in children (32%) than in adults (13%, p < 0.0001, data not shown). This higher PV uptake in children, independent of age group, is a result of specific messages provided by health authorities and practitioners about the A(H1N1) burden of disease, mortality and morbidity observed in children. Vaccine sessions were held during the beginning of the pandemic wave (9 November), when the impact in the paediatric population was obvious. At the same time, different categories of frail patients, such as pregnant women and immunocompromised patients were given specific recommendations and their vaccine uptake was also high (data not shown). Media coverage about clinical impact and recommendations in specific fragile groups probably contributed to promoting vaccination in children and other fragile populations. The Ministry of Health anticipated excellent vaccine uptake, by up to 75% of the general population. However, the vaccination programme was impaired by public perception of the pandemic vaccine characterised by a lack of confidence [16–18]. The public (and some practitioners) perceived (i) a lack of transparency over the real disease burden, the reasons for prioritising target groups and the safety of the vaccines and (ii) uncertainties around burden estimations and related decisions [16–18]. Moreover, several anti-vaccine lobbies expressed a negative opinion via the Internet and other media on (i) the adjuvanted vaccines, (ii) the vaccine manufacturers, and (iii) national and international authorities such as WHO. This resulted in poor PV uptake in France and some other countries [19,20,25]. The official figure in France is a PV uptake of 9% (5,741,553 people vaccinated out of a population of 63.7 M). This is consistent with the results from our study. This survey was based on a self-completed questionnaire and hence has some limitations. It is possible that some individuals may have mixed TIV and PV in their answers. On the other hand, these possible errors are potentially counterbalanced by the large size of the panel, its stability over the years, and the experience gained from previous studies on TIV uptake. Overall, this study conducted in a panel representative of the French population provides a useful insight into both TIV and PV influenza vaccines, especially in children. The 18% PV uptake obtained in children needs to be seen in context. In France, the implementation of the PV encountered several hurdles. First, PV vaccination was mainly carried out in dedicated

vaccination venues (centres) scattered throughout the country. Some vaccinations were organised in schools and in hospitals. This vaccination strategy is unusual. Second, pandemic vaccines were approved and delivered at different times. The incremental availability of the vaccines over time required immunisation to be prioritised, as summarised in Table 1. This was poorly understood by the population. Third, the switch to a single-dose vaccination was difficult to explain, which added to the confusion. Despite these hurdles, the visible impact of the A(H1N1)pdm 2009 virus in the paediatric population was a strong motivator for PV uptake in children, and this was observed even more in children with underlying diseases. Overall, the latter paediatric population was fairly well vaccinated (43%) as compared to the general population (9%). The burden of pandemic influenza in children was visible for the general population. The question now is to see whether these figures (low PV vaccination in adults, high PV uptake in children, as compared to previous TIV vaccination coverage) may be a signal for changes in vaccine uptake in these specific populations. While increased vaccine uptake may be beneficial in terms of reducing the disease burden in children, lower vaccine uptake in at-risk patients may lead to increased morbidity and mortality in this frail population. 5. Conclusion In a large survey conducted on behalf of GEIG during the 2009–2010 pandemic period, TIV uptake was low in the paediatric French population (3–4%). However, 18% PV uptake was observed, higher than in the adult population, as a result of specific recommendations concerning morbidity and mortality young children. Moreover, PV uptake in children with underlying diseases was 43%. Although this can be seen as good uptake of vaccination in children, this rate of vaccination was significantly lower than that expected by the French authorities (75% uptake). The knowledge and experience gained during this pandemic will hopefully be of help in managing future large epidemics or pandemics more effectively, and this post pandemic year’s vaccination uptake will show the potential impact of this vaccination campaign on vaccine uptake in the coming years. We can assume that the severe cases observed in specific patient groups (i.e. pregnant women) may have changed thinking about influenza and favour vaccination is these specific groups. It is important to remember that influenza viruses changes constantly and the vaccine recommendations may also change. This evolution of the virus and disease perception reinforces the need for

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sustained monitoring of seasonal influenza vaccination campaigns, including those financed by industry, as others have suggested [24].

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