Meningococcal C glycoconjugate vaccine (MenCV) has been used in several countries since 1999. The objectives of this vaccination are to ensure direct protection of vaccinated individuals and indirect protection of the population by reducing the carriage and transmission of group C Neisseria meningitidis bacteria and thus to decrease mortality and morbidity because of invasive meningococcal C infections.1
In France, group C meningococcal infections accounted for 18% of all invasive meningococcal infections (IMIs) in 2012.2 Universal MenCV has been recommended in France since 2010 as a routine vaccination at 12 months of age and as a catch-up vaccination for children and young adults (2–24 years of age).3 MenCV coverage rates nonetheless remain low (64% at 2 years and 20.5% at 15–19 years in 2014).4 France does not have school-based vaccination programs, and general practitioners (GPs) prescribe 90% of all vaccines.5 Parents must make an appointment with their GP or pediatrician to obtain a vaccine prescription and then another appointment for the actual vaccination once they have gone to a community pharmacy to have the vaccine dispensed. There is no national program for notifications/reminders to parents about vaccinations according to the national schedule. The French situation for MenCV appears quite different from that in other European countries, where coverage rates are often >80%.1,6 The reasons explaining the low coverage rates in France are unknown.
To better understand French GPs’ perceptions, attitudes and practices regarding MenCV, we conducted a cross-sectional survey of a large representative nationwide sample of French GPs. Our objectives were (1) to assess GPs’ recommendations to their patients for MenCV; (2) to describe the GPs’ perceptions of its risks and benefits and of the barriers to vaccination; (3) to identify factors associated with their recommendations for this vaccine for 2 target groups, infants 12 months of age and children and young adults from 2 to 24 years of age.
MATERIALS AND METHODS
This work took advantage of a series of 5 national cross-sectional surveys of a representative panel of GPs in private practice designed to study their attitudes, perceptions and practices related to different medical topics. The first survey was dedicated to vaccination and was based on a telephone questionnaire. The methods used in this survey have been extensively described elsewhere.7,8
Enrollment took place between December 2013 and March 2014. The participants were selected by random sampling from the Ministry of Health’s exhaustive database of health professionals in France [the Répertoire Partagé des Professionnels de Santé (RPPS), combined healthcare workers repertory], from the population of 62,000 French GPs. Sampling was stratified by gender, age, workload and GP density in the municipality of practice. GPs with an exclusive practice of alternative medicine (eg, acupuncture, homeopathy and naturopathic medicine) or with fewer than 5 consultations/visits per week in 2012 were excluded. GPs who agreed to participate committed themselves to respond to the entire series of 5 surveys, 1 every 6 months for 2 and a half years. To limit any selection bias that might have resulted from particular opinions/attitudes, the specific topics of each survey were not mentioned to GPs before they were asked to participate.
Of the 5151 randomly selected GPs, 695 could not be contacted, and 732 were not eligible. Of the 3724 eligible GPs who were contacted, 1712 agreed to participate (46.0%, Fig. 1). GPs who refused to participate were more often men (P < 0.001), were old (P < 0.001) and had more consultations/visits in 2012 (P < 0.05). They reported 2 main reasons for refusal: lack of time (913/1660, 55%) and lack of interest in participating in a survey (516/1660, 31%). The National Council on Statistical Information approved the survey.
The questionnaire development included a literature review, a focus group with 7 GPs and discussions with experts in the field of vaccination (Supplemental Digital Content 1, http://links.lww.com/INF/C685). It collected information about (1) general attitudes toward vaccination; (2) GPs’ self-reported vaccination practices for themselves and their family; (3) GPs’ self-reported vaccine recommendations to their patients and (4) perceptions about the potential risks of certain vaccines.
The questionnaire was tested for clarity, length and face validity in a pilot study with 50 GPs.
Professional investigators conducted the interviews with computer-assisted telephone interview software (Catiopé, Soft-Concept, Lyon, France).
Because coverage rates for this vaccine are very different for infants (routine vaccination) and for patients 2–24 years of age (catch-up vaccination), we hypothesized that GPs’ behavior regarding MenCV is also different. Therefore, we treated those 2 questions as 2 separate dependent variables, in 2 different models: (1) “Do you recommend meningococcal C vaccine for infants aged 12 months?”; (2) “Do you recommend meningococcal C catch-up vaccine for ages 2–24 years old?”. The possible answers to both questions were “never,” “sometimes,” “often” or “always.”
For bivariate and multivariate analyses, we considered 6 adjustment variables: the 4 stratification variables (GPs’ gender, age, 2012 workload and local GP density) and 2 variables for professional characteristics: type of practice (solo or group) and occasional practice of alternative medicine.
Based on the literature and the plausibility of potential associations with the outcomes of interest, we considered 3 sets of factors as variables of interest.8–10 First were 6 variables about GPs’ attitudes regarding vaccination: their opinions concerning vaccination in general in their daily practice (more or less favorable); if they believe that it is their role to encourage patients to be vaccinated even if they are reticent; and the 4 scores described below. Second, we considered 6 variables concerning GPs’ perceptions related to this vaccine in particular: if they think the recommendation to vaccinate against meningococcal C meningitis is clear and their opinion about parents’ or patients’ barriers to MenCV vaccination, specifically, fear of serious or severe side effects from the vaccine, underestimation of the risk of contracting meningitis, (lack of) awareness of the severity of bacterial meningitis, expression of doubts about the vaccine’s efficacy and whether or not they had ever heard of this vaccine. The third set of variables concerned GPs’ practices and experiences: whether they had participated in any continuing medical education on the topic of infectious diseases and/or vaccination in the last 12 months; whether any of their patients had developed a serious health issue (ie, one which led to hospitalization and disability) potentially linked to vaccination; whether any patient had had bacterial meningitis in the last 5 years; and whether they had their own children vaccinated with MenCV.
Some variables were grouped together to compose scores. We constructed 4 different scores: (1) score of GPs’ trust in the reliability of information provided by institutional sources about the benefits and risks of vaccines (official trust score); (2) score of perception of vaccine risk (perceived vaccine risk score); (3) score of perception of vaccine utility (perceived utility score, a proxy for complacency) and (4) score of GPs’ self-efficacy regarding their ability to explain the benefits and risks of vaccines and adjuvants to their patients (self-efficacy score). Details for the score calculation are reported elsewhere and in the Supplemental Digital Content 2, http://links.lww.com/INF/C686.8
For the descriptive analysis, data were weighted to match the sample more closely to the national French GP population for age, gender, 2012 workload and local GP density (in the municipality of practice). Categorical variables were expressed as percentages.
Next, we performed bivariate analyses between the dependent variables and the explanatory variables, comparing groups with the χ2 test or Fisher exact test when needed.
Finally, we performed 2 multivariate analyses (1 for each dependent variable) using a logistic regression model adjusted for the 4 stratification variables (GPs’ age, gender, 2012 workload and local GP density), type of practice (solo or group) and the occasional practice of alternative medicine (yes/no). The collinearity between all variables was tested with generalized variance-inflation factors, as described by Fox and Monette.11 We used forward stepwise regression to select the variables for the model. All variables of interest with P < 0.2 in the bivariate analyses were considered eligible to enter the model as explanatory variables, and the 6 adjustment variables were forced into the model. Bivariate and multivariate analyses were run for all respondents with complete data (we excluded GPs with at least 1 item of missing data). At least 1 data item was missing for 12% (188/1582) of the respondents for the routine vaccination model and 11% (171/1582) for the catch-up vaccination model (Fig. 1).
All analyses were based on 2-sided P values, with statistical significance defined by P < 0.05. They were conducted with R (version 3.0.3, R Foundation for Statistical Computing, Vienna, Austria) and the “ResourceSelection” package.12
Of the 1712 GPs who agreed to participate in the overall survey series, 1582 GPs (92%) responded to the first survey, focused on vaccination (Fig. 1). Their characteristics did not differ significantly from those of the GPs who agreed to participate but did not actually respond to this survey (130/1712). Respondents were mostly men (1076/1582, 68%) and in group practices (920/1582, 58%). About 12% (191/1582) of them occasionally practiced alternative medicine (Table 1).
Recommendations to Patients
For the routine vaccination, 52% of GPs (800/1547) reported always recommending MenCV for infants 12 months of age; 16% (246/1547) recommended it often; 17% (259/1547), sometimes; and 16% (242/1547), never. Recommendations were somewhat less frequent for the catch-up vaccination: 33% (523/1572) of GPs reported they always recommend it; 23% (368/1572), often; 26% (404/1572), sometimes; and 18% (277/1572), never.
Barriers to Vaccination
GPs perceived several parent-/patient-related barriers to vaccination: 72% (1094/1523) reported that parents had never heard of the vaccine; 69% (1049/1514), that parents underestimate the risk of contracting meningitis; 55% (838/1537), that they lack awareness of the seriousness of bacterial meningitis; 48% (718/1509), that they fear vaccine side effects; and 21% (320/1504), that they express doubts about its efficacy (Table 1).
Factors Independently Associated With Vaccine Recommendation
GPs recommended both routine and catch-up vaccination more frequently when they had had their children vaccinated with MenCV, when they thought that the official recommendations for vaccination against meningococcal C meningitis were clear and when they believed that vaccines in general are useful and safe. They also recommended the routine vaccination more often when they were very favorable to vaccination in general (Table 2). On the other hand, they recommended the catch-up vaccination more often when they thought patients/parents were unaware of the severity of meningitis (P = 0.012) and when they reported no doubts about the efficacy of MenCV in their patients (P = 0.015) (Table 3).
Our study is the first to address GPs’ perceptions, attitudes and behaviors related to meningococcal C vaccination in a large national sample in France. Five years after MenCV was recommended for all children, teenagers and young adults, only 52% (800/1547) and 33% (523/1572) of GPs reported always recommending it to patients 12 months and 2–24 years of age, respectively, and only 66% (659/993) of GPs with children vaccinated them with MenCV.
Influence of GPs’ Global Perceptions and Attitudes Toward Vaccination
Most of the factors independently associated with GPs’ recommendations to vaccinate their patients with MenCV applied to both routine and catch-up vaccinations. These common factors are known to be markers of vaccine hesitancy8: GPs’ failure to vaccinate their own children, doubts about vaccines’ utility and perception of vaccine-associated risks. The relative hesitancy French GPs report about MenCV may play a role in the suboptimal coverage rate in France.
GPs’ Recommendations of the Catch-up Vaccination Are Influenced by How Their Patients Perceive the Vaccine’s Benefit
Two specific factors were found to be associated with catch-up vaccination in multivariate analysis, and both involved the GPs’ perception of how patients see the vaccine’s benefits, in particular, doubting its efficacy or/and underestimating the severity of bacterial meningitis. MenCV, thus, appeared less routine for GPs for patients 2–24 years of age than for 12-month-olds. GPs may recommend vaccination on a case-by-case basis, influenced by their own and patients’/parents’ perception of risk of severe infection. IMIs are rare (incidence of 0.72/100,000 per year in France in 2014),13 and nationwide information and communication campaigns are crucial to raise awareness about this disease.
The French Exception?
The French situation regarding MenCV is quite different from the majority of other European countries, where coverage rates often exceed 90%, whereas it barely reaches 65% at 24 months in France.4 According to World Health Organization, 12/52 European countries have a MenCV coverage of 90% or less, including France.14
About half of the surveyed GPs reported that their patients feared side effects from this vaccine. This finding is surprising, for MenCV has not aroused controversy in the media in France, in contrast to the vaccines for human papillomavirus and hepatitis B. Doubts about the safety of the latter and strong media coverage of these controversies have led to insufficient coverage rates for human papillomavirus and hepatitis B vaccines in France.8,15
The organization of care may play a role in the low MenCV coverage rate. In France, childhood vaccination relies mainly on GPs and to a lesser extent on pediatricians. No letters are sent to parents to suggest they have the child vaccinated, and there are no reminders if a child misses 1 dose. On the contrary, some European countries with excellent coverage rates for MenCV have organized different systems of vaccination delivery. The United Kingdom uses a school-based vaccination program for MenCV16 and has a 90% coverage rate.6 In the Netherlands, where the MenCV coverage rate was 96% in 24-month-olds in 2012,17 children are vaccinated by public health doctors and nurses who see all children on a regular basis for routine monitoring. Each family receives an invitation for each vaccination included in the national vaccination program and a reminder if they fail to appear. In Ireland, the Health Service also sends parents letters to invite them to have the child vaccinated; coverage there is 97% for 24-month-olds.18 In the Flanders region of Belgium, coverage rates are 93% at 24 months and 87% for teenagers. Approximately 84% of the children/teenagers are vaccinated by public health service personnel, 12% by pediatricians and 4% by GPs, but the patients are free to choose.19 In the United States, quadrivalent vaccine is used for meningococcal vaccination, which includes MenCV. Meningococcal vaccination is mandatory in 28/50 states for elementary and secondary schools, and in 21/50 states, vaccination proof is mandatory to register in college, and US meningococcal vaccination coverage is 79% (from 46% in Mississippi, where no vaccination is mandatory, to 95% in Pennsylvania, where meningococcal vaccination is mandatory in elementary schools).20,21 In some Canadian provinces and territories, the public healthcare system administers immunization programs; infants and children receive their vaccinations at public health clinics. In other provinces and territories, vaccinations are primarily given by private physicians who order vaccines from local public health units. MenCV coverage in Canada is 89%.22,23
Our results finally suggest that the communication and information campaign for MenCV in France is insufficient, among both GPs and the public. Half the GPs (48%, 765/1580) reported that they found the recommendation for MenCV vaccination unclear, and this statement was associated in the multivariate analyses with a lower recommendation rate for both routine and catch-up MenCV. The French guidelines may appear somewhat complex, with general and specific recommendations for 5 different meningococcal vaccines24 (Supplemental Digital Content 3, http://links.lww.com/INF/C687). GPs might also have difficulty understanding why universal meningococcal vaccination in France uses MenCV, although most invasive infections are because of the serogroup B.13 The health authorities’ communication with the general public also appear inadequate, in view of the GPs’ reports about patients’ perceptions.
Strengths and Weaknesses of the Study
Our study provides original findings that may help to modify French vaccination policy to improve MenCV coverage rates. This work was based on a large sample that was randomly selected from the exhaustive list of French GPs, and results were weighted, which makes it highly representative. To limit any selection bias that might have resulted from particular opinions/attitudes, the specific topics of each survey were not mentioned to GPs before they were asked to participate in the survey. We compared the group of GPs with at least 1 item of missing data with the group with no missing data for age and gender and found no differences (results not shown).
Our work nonetheless has some limitations. First, only 46% (1712/3724) of the eligible GPs agreed to participate in the survey. Nonetheless, compared with other repeated surveys and bearing in mind that GPs agreed to participate in 5 surveys over 2.5 years, this response rate is high.25 Moreover, participants may differ from the nonparticipants even though the sample was representative of the French national GP population in terms of gender, age and 2012 workload. Weighting the data did not affect our results, however. Another potential weakness is that vaccine recommendation behavior was self-reported, which means that declaration or desirability biases cannot be excluded. However, questionnaire data have been shown to overestimate vaccination coverage rates by less than 10%,15 and self-reported coverage rates in hospital healthcare professionals have been shown to be a good proxy for recorded vaccination coverage.15 Finally, this is a cross-sectional study, which does not allow any causal inferences.
This survey of a nationwide representative sample of 1582 French GPs shows that they did not systematically recommend MenCV to their patients. Our results suggest that a large nationwide information and communication campaign targeting both healthcare professionals and patients would be useful as a first-step intervention to clarify the meningococcal vaccine recommendations, to present the benefits of the vaccine and to explain why each child/teenager is at risk for potentially deadly IMIs. A better understanding of the underlying individual, structural and contextual determinants of vaccine hesitancy for MenCV is also needed to help change physicians’ behavior.26,27
We thank Jo-Ann Cahn for her help in editing the manuscript.
1. Pérez-Breva L, Villanueva RJ, Villanueva-Oller J, et al. Optimizing strategies for meningococcal C disease vaccination in Valencia (Spain). BMC Infect Dis. 2014;14:280–286.
2. Barret A, Deghmane A, Lepoutre A, et al. Invasive meningococcal disease in France in 2012: main epidemiological features. Bull Epidemiol Hebd. 2014;1–2:25–31.
3. Haut Conseil de la Santé Publique. Vaccination schedule and recommendations from the “Haut conseil de la santé publique” in France. Bull Epidemiol Hebd. 2010;14–15:121–172.
5. Ecole des Hautes Etudes en Santé Publique. Faciliter L’accès aux Vaccinations en S’appuyant sur les Agences Régionales de Santé. 2013. Available at: http://www.bdsp.ehesp.fr/Fulltext/469469/
. Accessed August 18, 2016.
6. Trotter CL, Maiden MCJ. Meningococcal vaccines and herd immunity: lessons learned from serogroup C conjugate vaccination programs. Expert Rev Vaccines. 2009;8:851–861.
7. Le Maréchal M, Collange F, Fressard L, et al. Design of a national and regional survey among French general practitioners and method of the first wave of survey dedicated to vaccination. Med Mal Infect. 2015;45:403–410.
8. Verger P, Fressard L, Collange F, et al. Vaccine hesitancy among general practitioners and its determinants during controversies: a national cross-sectional survey in France. EBioMedicine. 2015;2:891–897.
9. Pulcini C, Massin S, Launay O, et al. Factors associated with vaccination for hepatitis B, pertussis, seasonal and pandemic influenza among French general practitioners: a 2010 survey. Vaccine. 2013;31:3943–3949.
10. Pulcini C, Massin S, Launay O, et al. Knowledge, attitudes, beliefs and practices of general practitioners towards measles and MMR vaccination in southeastern France in 2012. Clin Microbiol Infect. 2014;20:38–43.
11. Fox J, Monette G. Generalized Collinearity Diagnostics. J Am Stat Assoc. 1992;87:178–183.
15. Collange F, Fressard L, Pulcini C, et al. General practitioners’ attitudes and behaviors toward HPV vaccination: a French national survey. Vaccine. 2016;34:762–768.
20. Immunization Action Coalition. State Mandates on Immunization and Vaccine-preventable Diseases. 2016. Available at: http://www.immunize.org/laws
. Accessed August 18, 2016.
21. Centers for Disease Control and Prevention. National, Regional, State, and Selected Local Area Vaccination Coverage Among Adolescents Aged 13–17 Years—United States, 2014. 2015. Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6429a3.htm
. Accessed August 18, 2016.
25. Joyce CM, Scott A, Jeon SH, et al. The “medicine in Australia: balancing employment and life (MABEL)” longitudinal survey–protocol and baseline data for a prospective cohort study of Australian doctors’ workforce participation. BMC Health Serv Res. 2010;10:50.
26. Henrikson NB, Opel DJ, Grothaus L, et al. Physician communication training and parental vaccine hesitancy: a randomized trial. Pediatrics. 2015;136:70–79.
27. MacDonald NE, Dubé E. Unpacking vaccine hesitancy among healthcare providers. EBioMedicine. 2015;2:792–793.
Keywords:Copyright © 2017 Wolters Kluwer Health, Inc. All rights reserved.
questionnaire; primary care; family physician; meningococcal C vaccination; general practitioner