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Discrepancies between general practitioners' vaccination recommendations for their patients and practices for their children

  • Author Footnotes
    ∗ N. Agrinier and M. Le Maréchal contributed equally to this work.
    N. Agrinier
    Footnotes
    ∗ N. Agrinier and M. Le Maréchal contributed equally to this work.
    Affiliations
    Université de Lorraine, EA 4360 APEMAC, Nancy, France

    INSERM, CIC-1433 Epidémiologie clinique, CHRU de Nancy, Nancy, France
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  • Author Footnotes
    ∗ N. Agrinier and M. Le Maréchal contributed equally to this work.
    M. Le Maréchal
    Correspondence
    Corresponding author. M. Le Maréchal, Faculté de médecine de Nancy, EA 4360 APEMAC, 9 avenue de la forêt de Haye, 54505 Vandoeuvre-Lès-Nancy, France.
    Footnotes
    ∗ N. Agrinier and M. Le Maréchal contributed equally to this work.
    Affiliations
    Université de Lorraine, EA 4360 APEMAC, Nancy, France
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  • L. Fressard
    Affiliations
    INSERM, UMR_S912, Sciences Economiques & Sociales de la Santé et Traitement de l'Information Médicale (SESSTIM), Marseille, France

    Aix Marseille Université, UMR_S912, IRD, Marseille, France

    ORS PACA, Observatoire Régional de la Santé Provence-Alpes-Côte d'Azur, Marseille, France
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  • P. Verger
    Affiliations
    INSERM, UMR_S912, Sciences Economiques & Sociales de la Santé et Traitement de l'Information Médicale (SESSTIM), Marseille, France

    Aix Marseille Université, UMR_S912, IRD, Marseille, France

    ORS PACA, Observatoire Régional de la Santé Provence-Alpes-Côte d'Azur, Marseille, France

    INSERM, F-CRIN, I-Reivac (Innovative Clinical Research Network in Vaccinology), Paris, France
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  • C. Pulcini
    Affiliations
    Université de Lorraine, EA 4360 APEMAC, Nancy, France

    INSERM, UMR_S912, Sciences Economiques & Sociales de la Santé et Traitement de l'Information Médicale (SESSTIM), Marseille, France

    CHRU de Nancy, Service de Maladies Infectieuses et Tropicales, Nancy, France
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  • Author Footnotes
    ∗ N. Agrinier and M. Le Maréchal contributed equally to this work.
Open ArchivePublished:September 03, 2016DOI:https://doi.org/10.1016/j.cmi.2016.08.019

      Abstract

      Objectives

      The objectives of our study were to describe the vaccination recommendations by general practitioners (GPs) for their patients and practices for their children, and to identify any discrepancies between them.

      Methods

      Applying multiple correspondence analysis and agglomerative hierarchical cluster analysis to data from a 2014 cross-sectional survey of a national sample of GPs, we constructed a typology based on the patterns of associations between GPs' vaccine recommendations to their patients and practices to their own children's vaccinations.

      Results

      This study includes the 1038 GPs who reported that they had at least one child aged 2–25 years. Nearly half (47%, 482/1021) reported that all of their children were vaccinated against hepatitis B but that they did not always recommend that vaccine to patients; the same discordance was observed among 36% (369/1027) for the measles–mumps–rubella vaccine, 19% (194/1013) to 28% (290/1019) for routine and catch-up meningococcal C vaccination, and 27% (136/496) for the human papillomavirus vaccine. Cluster analysis showed that 37% (95% CI 33%–39%) of GPs reported an above-average rate of systematic vaccine recommendations for their patients, and most reported that all their children were vaccinated (low level of discordance), whereas 60% (95% CI 58%–64%) had a high level of discordance, that is, most reported that their children were vaccinated, but did not always recommend the same vaccines to their patients.

      Conclusions

      Many GPs do not report the same attitude concerning the vaccination of their children and their patients. The reasons underlying these discrepancies, possibly including vaccine hesitancy, should be investigated.

      Keywords

      Introduction

      Recent decades have seen great reductions in vaccine-preventable diseases through routine vaccination programmes []. Nonetheless, vaccine hesitancy is increasing worldwide, both among the general population [
      • Larson H.J.
      • Cooper L.Z.
      • Eskola J.
      • Katz S.L.
      • Ratzan S.
      Addressing the vaccine confidence gap.
      ] and among health-care workers [
      • Suryadevara M.
      • Handel A.
      • Bonville C.A.
      • Cibula D.A.
      • Domachowske J.B.
      Pediatric provider vaccine hesitancy: an under-recognized obstacle to immunizing children.
      ,
      • Verger P.
      • Fressard L.
      • Collange F.
      • Gautier A.
      • Jestin C.
      • Launay O.
      • et al.
      Vaccine hesitancy among general practitioners and its determinants during controversies: a national cross-sectional survey in France.
      ].
      In France, official vaccination policy mandates some vaccines (diphtheria, tetanus and poliomyelitis) and recommends others [
      ]. Uptake of some vaccines is low or sub-optimal (see Supplementary material, Appendix S1) [], especially vaccines for hepatitis B (HepB), the second dose of measles–mumps–rubella (MMR), human papillomavirus (HPV) and meningococcal C (MenC) vaccines. A 2010 study by the French National Institute for Prevention and Health Education (INPES) showed that general practitioners' (GPs') confidence in vaccination was deteriorating: the percentage of GPs with an opinion very favourable to vaccination in general decreased from 85% in 1994, to 67% in 2010 [
      • Gautier A.
      Baromètre santé médecins généralistes 2009 [Internet].
      ]. This loss of confidence by GPs in vaccination is an important issue because they are the cornerstone of the French vaccination system. They are the health professionals seen most often by the general population as well as the most trusted source of information concerning vaccination [
      • Stefanoff P.
      • Mamelund S.-E.
      • Robinson M.
      • Netterlid E.
      • Tuells J.
      • Bergsaker M.A.R.
      • et al.
      Tracking parental attitudes on vaccination across European countries: the Vaccine Safety, Attitudes, Training and Communication Project (VACSATC).
      ], and they influence their patients' decisions about vaccination [
      • Gautier A.
      Baromètre santé médecins généralistes 2009 [Internet].
      ,
      • D’ Alessandro E.
      • Hubert D.
      • Launay O.
      • Bassinet L.
      • Lortholary O.
      • Jaffre Y.
      • et al.
      Determinants of refusal of A/H1N1 pandemic vaccination in a high risk population: a qualitative approach.
      ]. France has no school-based vaccination programme, and GPs prescribe 90% of the vaccines purchased here [
      ]. Parents must visit their GP or paediatrician to obtain prescriptions for their children's vaccines and then return to the physician for the vaccination after a visit to a community pharmacy to have the vaccine dispensed.
      These points show the need for a better understanding of GPs' practices concerning vaccination. One relevant but little-explored area is the consistency of GPs' practices towards their own children and their patients. Do some GPs vaccinate their own children but not recommend the same vaccines to their patients? Might they recommend vaccines to patients that they do not administer to their own children? To the best of our knowledge, only two studies have examined this topic; the first one, a cross-sectional questionnaire survey conducted by Posfay et al. in Switzerland in 2004 found that 93% of the 1017 surveyed physicians (paediatricians and other doctors) agreed with official vaccination recommendations and would apply them to their own children [
      • Posfay-Barbe K.M.
      • Heininger U.
      • Aebi C.
      • Desgrandchamps D.
      • Vaudaux B.
      • Siegrist C.-A.
      How do physicians immunize their own children? Differences among pediatricians and nonpediatricians.
      ]; however, this work did not compare GPs' vaccination behaviour for their patients and their own children. The second one is a very recently published survey conducted in 2013 in one French region, with a low response rate (12.5%), that compared vaccination behaviours of GPs for themselves, their children and their patients [
      • Killian M.
      • Detoc M.
      • Berthelot P.
      • Charles R.
      • Gagneux-Brunon A.
      • Lucht F.
      • et al.
      Vaccine hesitancy among general practitioners: evaluation and comparison of their immunisation practice for themselves, their patients and their children.
      ]. They found that vaccination coverage rates reported by GPs were higher for their children than for their patients for HepB (100% versus 87%), and higher for their patients than for their children for pneumococcal vaccine (90% versus 84%) and HPV vaccine (83% versus 74%).
      The objectives of our study were to describe GPs' vaccination recommendations for MMR, MenC, HepB and HPV for their patients and their practices for the corresponding vaccines for their children and to identify vaccination behaviour patterns for these vaccines. Finally, focusing on the concordance or discrepancy between vaccinations of their own children and recommendations to their patients, we sought to identify the factors associated with these patterns.

      Methods

      We conducted a cross-sectional survey on vaccination in a national panel of 1712 GPs in private practice in France, designed to collect data about GPs' medical practices and working conditions at regular intervals. The method we used to set up the panel has been described elsewhere in detail [
      • Verger P.
      • Fressard L.
      • Collange F.
      • Gautier A.
      • Jestin C.
      • Launay O.
      • et al.
      Vaccine hesitancy among general practitioners and its determinants during controversies: a national cross-sectional survey in France.
      ,
      • Le Maréchal M.
      • Collange F.
      • Fressard L.
      • Peretti-Watel P.
      • Sebbah R.
      • Mikol F.
      • et al.
      Design of a national and regional survey among French general practitioners and methodology of the first cross-sectional survey dedicated to vaccination.
      ].

       Population and sampling

      Between December 2013 and March 2014, we selected GPs by random sampling from the Ministry of Health's exhaustive database of health professionals in France. Sampling was stratified for gender, age and annual number of office consultations and house calls (workload), obtained from the exhaustive reimbursement database of the National Health Insurance Fund for each GP in 2012. Sampling was also stratified for the density of each GP's municipality of practice. The panel participation rate was 46%. Only GPs who had one or more children aged from 2 to 25 years were asked about their children's vaccinations and included in this study. The National Authority for Statistical Information (Commission Nationale de l'Information Statistique) approved the panel.

       Data collection

      Professional investigators contacted panel members to ask them to participate in this survey. They then conducted interviews, using computer-assisted telephone interview software and a standardized questionnaire, developed after a review of the literature, qualitative interviews with ten GPs, and discussions with experts. We pilot-tested the questionnaire for clarity, length, and face validity among 50 GPs and modified it slightly before using it for the survey.
      The questionnaire (see Supplementary material, Appendix S2) collected information about GPs' professional characteristics, whether they reported that their own children were vaccinated against HPV, MMR, HepB or MenC, and the frequency at which they recommended these vaccines to their patients in four specific clinical situations chosen because the corresponding current vaccination coverage rates do not meet official French objectives (see Supplementary material, Appendix S1). These vaccines were recommended in all these situations according to French guidelines.

       Statistical analysis

      Because panel participants differed from non-participants for sex, age and workload [
      • Verger P.
      • Fressard L.
      • Collange F.
      • Gautier A.
      • Jestin C.
      • Launay O.
      • et al.
      Vaccine hesitancy among general practitioners and its determinants during controversies: a national cross-sectional survey in France.
      ], we weighted data to match the sample more closely to the national French GP population for these variables with SURVEY procedures (PROC SURVEYFREQ, PROC SURVEYLOGISTIC, SAS 9.4 statistical software). Participants and survey participants excluded because of having no children aged 2–25 years were compared for the main characteristics (gender, age, workload and type of practice).
      Bivariate analyses were performed to describe the relations between GPs' vaccine recommendations for their patients and practices for their own children for each of the four vaccines (MMR, HepB, MenC and HPV).
      Using multiple correspondence analysis and agglomerative hierarchical cluster analysis [
      • Antón-Ladislao A.
      • García-Gutiérrez S.
      • Soldevila N.
      • González-Candelas F.
      • Godoy P.
      • Castilla J.
      • et al.
      Visualizing knowledge and attitude factors related to influenza vaccination of physicians.
      ,
      • Kaufman L.
      • Rousseeuw P.J.
      Finding groups in data: an introduction to cluster analysis.
      ], we constructed a typology according to the patterns of associations between GPs' vaccine recommendations to their patients and practices for their own children's vaccinations for MMR, HepB and MenC. We excluded HPV vaccination because it concerned only GPs with daughters and so reduced the sample size to 538 participants. These analyses allowed us to identify and quantify the prevalence of various levels of discordance among GPs. Cluster analysis enables the study of the statistical proximity of individuals on the basis of the factors under study, without any preconceptions about possible relations between these factors [
      • Antón-Ladislao A.
      • García-Gutiérrez S.
      • Soldevila N.
      • González-Candelas F.
      • Godoy P.
      • Castilla J.
      • et al.
      Visualizing knowledge and attitude factors related to influenza vaccination of physicians.
      ]. Clustering implies that the distribution of the factors studied is not independent, but instead reflects their common features [
      • Antón-Ladislao A.
      • García-Gutiérrez S.
      • Soldevila N.
      • González-Candelas F.
      • Godoy P.
      • Castilla J.
      • et al.
      Visualizing knowledge and attitude factors related to influenza vaccination of physicians.
      ]. Hence, a classification procedure can uncover discordance at levels statistically defined according to criteria of similitude or distance. We used Ward's criterion as our clustering method: it links clusters on the basis of the degree of similarity between observations in the same cluster.
      We used the clusters that reflected some discordance between GPs as dependent variables and tested all their potential correlates with univariable and then multivariable binary logistic regression models. All analyses were based on two-sided p values, with statistical significance defined by p ≤0.05; they were conducted with SAS 9.4 statistical software (SAS Institute, Cary, NC, USA).

      Results

      Of the 1582 participants in the cross-sectional survey, 1038 (66%) reported that they had at least one child aged from 2 to 25 years and were therefore included in this study (Fig. 1). The response rate of GPs who had one or more children aged from 2 to 25 years old was also 92% (1038/1129). Compared with participating GPs without children, they were more often women (p <0.001), younger (p <0.001), and practiced more often with others (p <0.001) (Table 1).
      Fig. 1
      Fig. 1Flowchart of the general practitioners included in this nationwide French survey.
      Table 1Social, demographic and professional characteristics of the study population (French nationwide panel of general practitioners, weighted data); n (%)
      Survey participants with no children aged 2–25 years

      (n = 544)
      Participants with

      children aged 2–25 years

      (n = 1038)
      p-value
      Rao–Scott chi-square test: survey, participants versus included population. *p ≤0.05, **p ≤0.01, ***p ≤0.001.
      Stratification variables
      Gender
       Male403 (74.1)669 (64.5)***
       Female141 (25.9)369 (35.6)
      Age (years)
       <5078 (14.4)469 (45.2)***
       50–58141 (25.8)420 (40.4)
       >58325 (59.8)149 (14.4)
      GP density in municipality of practice
       < –19.3% of national average147 (30.0)259 (25.0)
       Between –19.3% and +17.7% of national average262 (48.1)536 (51.7)
       > +17.7% of national average136 (25.0)243 (23.4)
      2012 workload
       <3067 procedures129 (23.8)220 (21.2)
       3067–6028 procedures264 (48.5)550 (53.0)
       >6028 procedures151 (27.7)268 (25.8)
      Professional characteristics
      Practice
       Group268 (49.3)656 (63.2)***
       Solo276 (50.7)382 (36.8)
      Occasional practice of alternative medicine
      Alternative medicine: e.g homeopathy, acupuncture (exclusive practice of alternative medicine was an exclusion criterion).
       No477 (87.7)914 (88.1)
       Yes67 (12.4)124 (11.9)
      CME on infectious diseases and vaccination in 2013
       No324 (59.5)574 (55.7)
       Yes220 (40.5)464 (44.7)
      Abbreviations: CME, continuing medical education; GPs, general practitioners.
      a Rao–Scott chi-square test: survey, participants versus included population. *p ≤0.05, **p ≤0.01, ***p ≤0.001.
      b Alternative medicine: e.g homeopathy, acupuncture (exclusive practice of alternative medicine was an exclusion criterion).
      A substantial proportion of GPs reported that all their children were vaccinated but that they did not always recommend those vaccines for their patients. This was the case for 36% (369/1027) of GPs for MMR for non-immunized adolescents or young adults (Table 2); 19% (194/1013 for 12-month-old infants) to 28% (290/1019, catch-up in 2- to 24-year-olds) for MenC vaccine; 47% (482/1021) for HepB vaccine for adolescents; and 27% (136/496) for HPV. The percentage of GPs who reported that they always recommended a vaccine to their patients but did not report having their children vaccinated for those vaccinations was much lower: 14% (144/1013) always recommended MenC for 12-month-old patients, but did not report that all of their children were vaccinated against this disease. This was the case for 5% (55/1019) for MenC for catch-up, 3% (31/1021) for HepB, <1% (8/1031) for MMR, and 3% (17/496) for HPV.
      Table 2General practitioners' vaccination recommendations to their patients compared to their practices for their own children (weighted data, n = 1038); n (%)
      Decision for their children
      All of them vaccinatedNone or only some of them vaccinated
      Frequency of vaccine recommendations to their patients
      MMR (to non-immune adolescents and young adults)
      11 missing values (4 for children's vaccination, 7 for vaccine recommendations).
       Always627 (61.1)8 (0.8)
       Not always (often, sometimes, or never)369 (35.9)23 (2.2)
      Meningococcal meningitis C (to ages 2–24 years; catch-up)
      19 missing values (14 for children's vaccination, 5 for vaccine recommendations).
       Always323 (31.7)55 (5.4)
       Not always290 (28.5)351 (34.5)
      Meningococcal meningitis C (to 12-month-old infants)
      25 missing values (14 for children's vaccination, 11 for vaccine recommendations).
       Always418 (41.3)144 (14.2)
       Not always194 (19.2)257 (25.4)
      Hepatitis B (to adolescents; catch-up)
      17 missing values (10 for children's vaccination, 7 for vaccine recommendations).
       Always309 (30.3)31 (3.0)
       Not always482 (47.2)199 (19.5)
      Human papillomavirus (to girls aged 11–14 years)
      42 missing values among the 538 GPs with daughters (34 for daughters' vaccination, 6 for vaccine recommendation, 2 for both).
       Always230 (46.4)17 (3.4)
       Not always136 (27.4)113 (22.8)
      Abbreviations: MMR, measles, mumps, and rubella.
      a 11 missing values (4 for children's vaccination, 7 for vaccine recommendations).
      b 19 missing values (14 for children's vaccination, 5 for vaccine recommendations).
      c 25 missing values (14 for children's vaccination, 11 for vaccine recommendations).
      d 17 missing values (10 for children's vaccination, 7 for vaccine recommendations).
      e 42 missing values among the 538 GPs with daughters (34 for daughters' vaccination, 6 for vaccine recommendation, 2 for both).
      The cluster analysis for the 1003 GPs identified three clusters according to GPs' vaccine recommendations for their patients and practices for their children (Table 3 and see Supplementary material, S3). The first cluster included 37% (95% CI 33%–39%) of the 1003 GPs. They reported an above-average rate of systematic vaccine recommendations for their patients, and most reported that all of their children were vaccinated against the three vaccines considered. This first cluster type is characterized by a low level of discordance. The second cluster included 60% (95% CI 58%–64%) of the 1003 GPs. Their discordance concerned especially the MMR vaccine: although all of them (100%) reported that all of their children had this vaccination, their MMR recommendations to their patients were substantially less consistent and less systematic than for the entire sample (high discordance cluster). They were more consistent for MenC and HepB, recommending both less often for their patients and reported that their children were less often vaccinated than the average in the sample. The third cluster (with a high frequency of no-vaccination behaviour) included only 3% (95% CI 2%–4%) of the GPs. Most reported that they never recommended vaccination to their patients and reported that their children were not vaccinated, except for MMR, which they nonetheless recommended to their patients and for which their children were much less often vaccinated than the other groups.
      Table 3Typology of general practitioners according to their vaccine practices for their own children and recommendations to their patients (agglomerative hierarchical cluster analysis, weighted data, n = 1003
      35 missing values.
      )
      Low level of discordance

      (37.0%)
      High level of discordance

      (60.0%)
      High frequency of no-vaccination

      behaviour (3.0%)
      All
      MMR
      Recommendation to non-immune adolescents and young adults
       Never0.04.036.13.5
       Sometimes0.017.018.110.7
       Often20.825.118.423.3
       Always79.253.927.462.5
      Decision for their children
       None of them vaccinated0.00.073.42.2
       Some of them vaccinated0.00.026.60.8
       All of them vaccinated100.0100.00.097.0
      Meningococcal meningitis C
      Recommendation for 12-month-old infants
       Never0.023.166.015.8
       Sometimes0.236.420.622.6
       Often31.820.42.824.1
       Always68.020.110.637.5
      Recommendation for ages 2–24 years (catch-up)
       Never0.019.869.313.9
       Sometimes0.023.417.614.6
       Often0.025.60.015.4
       Always100.031.213.156.1
      Decision for their children
       None of them vaccinated12.342.492.932.8
       Some of them vaccinated0.011.70.07.0
       All of them vaccinated87.745.97.160.2
      Hepatitis B
      Recommendation to adolescents (catch-up)
       Never0.014.658.810.5
       Sometimes16.433.322.826.7
       Often34.827.08.829.3
       Always48.825.29.633.4
      Decision for their children
       None of them vaccinated6.917.969.815.4
       Some of them vaccinated0.010.911.66.9
       All of them vaccinated93.171.218.677.7
      Abbreviations: GPs, general practitioners; MMR, measles, mumps and rubella.
      a 35 missing values.
      Of the three clusters we identified, only the first two clusters were used as dependent variables. The third cluster, with the high frequency of no-vaccination behaviour, was excluded, because it concerned such a small proportion of GPs (3%).
      Multivariable logistic regression comparing the first two clusters (Table 4) showed that men, GPs who had solo practices, those occasionally practising alternative medicine, and those who were not favourable to vaccination in general were more prone to present high levels of discordance.
      Table 4Factors associated with general practitioners' discordance between vaccination practices for their children and vaccination recommendations to their patients (high discordance level cluster versus low discordance level cluster, binary logistic regressions, weighted data, n = 973
      65 GPs excluded because in the cluster with high frequency of no-vaccination behaviour (n = 30) or because of missing values about their discordance (n = 35).
      )
      Univariable

      regression
      Multivariable

      regression
      OR (95% CI)ORa (95% CI)
      Stratification variables
      Sex (ref. Female)
       Male1.63 (1.26–2.11)1.55 (1.16–2.07)
      Age (years) (ref. <50)
       50–581.36 (1.03–1.78)1.15 (0.86–1.54)
       >581.94 (1.23–3.04)1.54 (0.95–2.48)
      GP density in municipality of practice (ref. <–19.3% of national average)
       Between –19.3% and +17.7% of national average1.03 (0.77–1.39)1.08 (0.78–1.48)
       >+17.7% of national average1.24 (0.86–1.78)1.30 (0.89–1.91)
      2012 workload (ref. <3067 consultations/visits)
       3067–6028 consultations/visits0.88 (0.62–1.24)0.97 (0.66–1.41)
       >6028 consultations/visits0.86 (0.58–1.25)0.79 (0.52–1.20)
      Professional characteristics
      Practice (ref. Other)
       Solo1.61 (1.22–2.11)1.41 (1.05–1.89)
      Occasional practice of alternative medicine
      Alternative medicine: e.g. homeopathy, acupuncture.
      (ref. No)
       Yes2.36 (1.44–3.89)1.81 (1.07–3.05)
      CME on infectious diseases and vaccination in 2013 (ref. No)
       Yes0.81 (0.63–1.06)0.92 (0.70–1.21)
      General opinion about vaccination
      Favourable to vaccination in general (ref. Yes)
       No2.63 (1.78–3.88)2.25 (1.49–3.40)
      Nagelkerke R20.08
      Bold represents significant OR and 95% CI.
      Abbreviations: CME, continuing medical education; GPs, general practitioners; OR, odds ratio; ORa, adjusted OR.
      a 65 GPs excluded because in the cluster with high frequency of no-vaccination behaviour (n = 30) or because of missing values about their discordance (n = 35).
      b Alternative medicine: e.g. homeopathy, acupuncture.

      Discussion

       Key results

      More than half of the GPs reported discordances in their vaccination recommendations for their patients and their practices for their own children; the most frequent type of discrepancy, by far, concerned GPs who reported that their children were vaccinated, but who did not systematically recommend the same vaccines to their patients. Men, those who practice alone, those occasionally practising alternative medicine, and those not favourable to vaccination in general were more likely to present a high level of discordance.
      The cluster analysis identified three different GP vaccination profiles (Table 3): (a) GPs with a low level of discordance, who reported that their children were vaccinated and recommended vaccination to their patients; (b) GPs with a high level of discordance; and (c) GPs with a low level of vaccination, for both their children and the patients. The prevalence (3%) of the latter is similar to the prevalence of GPs reporting unfavourable opinions of vaccination in previous French surveys (2.5%) [
      • Gautier A.
      Baromètre santé médecins généralistes 2009 [Internet].
      ].

       Interpretation of the results

      This comparison of GPs' vaccination recommendations for their patients and practices for their own children (Table 2) provides some insight into barriers to vaccination. Depending on the vaccine, 30% (HepB) to 61% (MMR) of the GPs both reported that all of their children were vaccinated and always recommended the vaccine to their patients. We hypothesize that those GPs are convinced of the efficacy and safety of these vaccines, shown by their reported attitude towards their children's vaccinations, and that they perceive few patient barriers regarding these vaccines because they always recommended them to their patients. On the other hand, 2% (MMR) to 35% (MenC) of the GPs both reported that none or only some of their children were vaccinated and did not always recommend the vaccine to their patients. These GPs might be somewhat hesitant toward these vaccines and might not trust these vaccines.
      The most frequent type of discrepancy, by far, concerned GPs who reported that their children were vaccinated, but did not systematically recommend the same vaccines to their patients. The most striking example in our survey is the HepB vaccine: 77% of GPs reported that all their children were vaccinated, but only a third always recommended this vaccine to adolescent patients. We hypothesize that most GPs are convinced of the efficacy and the safety of this vaccine, since 77% reported that their children were vaccinated, but that barriers prevent some from recommending this vaccine to their patients. Killian et al. found in their survey the same finding, since HepB vaccine coverage rate reported by GPs was higher for their children (100%), than for their patients (87%, p <0.001) [
      • Killian M.
      • Detoc M.
      • Berthelot P.
      • Charles R.
      • Gagneux-Brunon A.
      • Lucht F.
      • et al.
      Vaccine hesitancy among general practitioners: evaluation and comparison of their immunisation practice for themselves, their patients and their children.
      ]. Numerous patient-related barriers exist. The first is due to reluctance about this vaccine, which is very controversial in France (due to the media-driven controversy claiming that it can cause multiple sclerosis [
      • André F.E.
      Vaccinology: past achievements, present roadblocks and future promises.
      ]). Moreover, all of the numerous more general vaccine-hesitancy concerns apply to this vaccine, including but not limited to doubts about its efficacy and worries about the risks of vaccination [
      • Mills E.
      • Jadad A.R.
      • Ross C.
      • Wilson K.
      Systematic review of qualitative studies exploring parental beliefs and attitudes toward childhood vaccination identifies common barriers to vaccination.
      ], fear of an immune overload [
      • Hulsey E.
      • Bland T.
      Immune overload: parental attitudes toward combination and single antigen vaccines.
      ], philosophical or religious opinions [
      • Larson H.J.
      • Cooper L.Z.
      • Eskola J.
      • Katz S.L.
      • Ratzan S.
      Addressing the vaccine confidence gap.
      ], beliefs that there are other methods to prevent disease [
      • Mills E.
      • Jadad A.R.
      • Ross C.
      • Wilson K.
      Systematic review of qualitative studies exploring parental beliefs and attitudes toward childhood vaccination identifies common barriers to vaccination.
      ], financial reasons (cost of vaccines); and fever or acute disease at the time the vaccination is scheduled [
      • Szilagyi P.G.
      • Rodewald L.E.
      • Humiston S.G.
      • Raubertas R.F.
      • Cove L.A.
      • Doane C.B.
      • et al.
      Missed opportunities for childhood vaccinations in office practices and the effect on vaccination status.
      ]. There are also barriers related to the GP: difficulties in convincing some vaccine-hesitant patients to be immunized [
      • Luthy K.E.
      • Beckstrand R.L.
      • Peterson N.E.
      Parental hesitation as a factor in delayed childhood immunization.
      ], forgetting to recommend the vaccine to adolescents, who rarely come for planned vaccination consultations, but consult most often for acute care visits [
      • Wong C.A.
      • Taylor J.A.
      • Wright J.A.
      • Opel D.J.
      • Katzenellenbogen R.A.
      Missed opportunities for adolescent vaccination, 2006-2011.
      ], lack of time during the consultation [
      • Mollema L.
      • Staal J.M.
      • van Steenbergen J.E.
      • Paulussen T.G.
      • de Melker H.E.
      An exploratory qualitative assessment of factors influencing childhood vaccine providers’ intention to recommend immunization in the Netherlands.
      ], organizational issues, such as difficulties in accessing the vaccination record or lack of systematic vaccine reminders [
      • Pulcini C.
      • Massin S.
      • Launay O.
      • Verger P.
      Knowledge, attitudes, beliefs and practices of general practitioners towards measles and MMR vaccination in southeastern France in 2012.
      ]. These GP barriers do not exist for their own children.
      Vaccine hesitancy on the GPs' part may therefore explain part, but not all, of the vaccination behaviours observed among GPs in this study. Vaccine hesitancy is defined as delay in acceptance of vaccination, or refusal, or even acceptance with doubts about its safety and benefits, with all these behaviours and attitudes varying according to context, vaccine and personal profile, despite the availability of vaccine services [
      • Verger P.
      • Fressard L.
      • Collange F.
      • Gautier A.
      • Jestin C.
      • Launay O.
      • et al.
      Vaccine hesitancy among general practitioners and its determinants during controversies: a national cross-sectional survey in France.
      ,
      ]. The link here between hesitancy and discordance is possible, as being unfavourable to vaccine in general (one component of vaccine hesitancy) was independently associated with a high level of discordance. Vaccine hesitancy is known to reduce the ability of GPs to be good vaccination advocates [
      • Verger P.
      • Fressard L.
      • Collange F.
      • Gautier A.
      • Jestin C.
      • Launay O.
      • et al.
      Vaccine hesitancy among general practitioners and its determinants during controversies: a national cross-sectional survey in France.
      ], and it can have several reasons. GPs may have doubts about the vaccine because it is new and they prefer to wait for further studies on its safety and efficacy [
      • Katz-Sidlow R.J.
      • Sidlow R.
      A look at the pediatrician as parent: experiences with the introduction of varicella vaccine.
      ]. They may question the utility of some vaccines. Some express safety concerns about combined vaccines [
      • Posfay-Barbe K.M.
      • Heininger U.
      • Aebi C.
      • Desgrandchamps D.
      • Vaudaux B.
      • Siegrist C.-A.
      How do physicians immunize their own children? Differences among pediatricians and nonpediatricians.
      ] or consider the incidence of the vaccine-targeted disease too low for any risk [
      • Posfay-Barbe K.M.
      • Heininger U.
      • Aebi C.
      • Desgrandchamps D.
      • Vaudaux B.
      • Siegrist C.-A.
      How do physicians immunize their own children? Differences among pediatricians and nonpediatricians.
      ] or think that children are vaccinated against too many diseases [
      • Verger P.
      • Fressard L.
      • Collange F.
      • Gautier A.
      • Jestin C.
      • Launay O.
      • et al.
      Vaccine hesitancy among general practitioners and its determinants during controversies: a national cross-sectional survey in France.
      ]. They may prefer infection-driven than vaccine-induced immunity [
      • Posfay-Barbe K.M.
      • Heininger U.
      • Aebi C.
      • Desgrandchamps D.
      • Vaudaux B.
      • Siegrist C.-A.
      How do physicians immunize their own children? Differences among pediatricians and nonpediatricians.
      ]. GPs can also lose confidence in vaccination, due to annual changes in vaccination schedules or vaccination policies [
      • Larson H.J.
      • Cooper L.Z.
      • Eskola J.
      • Katz S.L.
      • Ratzan S.
      Addressing the vaccine confidence gap.
      ], or differences in vaccination schedules between countries [
      ], or media controversies about the pharmaceutical industry concerning non-vaccine products (e.g. the Mediator® scandal in France, where the pharmaceutical industry was accused of not disclosing serious side effects to the public [
      • Mullard A.
      Mediator scandal rocks French medical community.
      ]), or serious failings in the pharmacovigilance system. Holman et al. also pointed out the continuing medical education knowledge gap as a barrier to vaccination [
      • Holman D.M.
      • Benard V.
      • Roland K.B.
      • Watson M.
      • Liddon N.
      • Stokley S.
      Barriers to human papillomavirus vaccination among US adolescents.
      ].

       Strengths and limitations

      Our work brings original findings and was based on a large sample selected from an exhaustive list of French GPs, which strengthens its representativeness. We used multiple correspondence analysis and agglomerative hierarchical cluster analysis, which are validated methods for identifying and quantifying the prevalence of various levels of discordance among GPs.
      This work also has some limitations. First of all, the GPs included may differ from those not included, even though the sample was representative of the French national GP population in terms of gender, age and 2012 workload. Nevertheless, the fact that weighting the data did not affect our results (data not shown) suggests that selection bias was negligible in our study. Moreover, although only 46% of the eligible GPs agreed to participate in the survey, this is a high response rate compared with other surveys, especially considering that GPs were committing themselves to complete five different surveys over two and a half years. We note that this study's cross-sectional design does not allow us to conclude on the existence of any causal links. In addition, the questions did not always involve strictly comparable clinical situations, for instance doctors were asked if they recommended HepB vaccination as catch-up for teenagers but whether their children aged 2–25 years were vaccinated against it. As shown in the study conducted by Wong et al., adolescents mainly see doctors for acute care visits [
      • Wong C.A.
      • Taylor J.A.
      • Wright J.A.
      • Opel D.J.
      • Katzenellenbogen R.A.
      Missed opportunities for adolescent vaccination, 2006-2011.
      ], whereas younger children have dedicated preventive visits. Finally, our data are self-reports of vaccination recommendations to patients and of their children's vaccinations, rather than real coverage. We also do not know if GPs' children were vaccinated by the GP him/herself, or by another physician.

       Perspectives

      The comparison of GPs' reported vaccination practices for their children and recommendations to their patients might help us to draw assumptions about GPs' reasons for non-vaccination and to distinguish those who do not trust the vaccine, from those who face patient-related barriers to vaccination. Further investigations are however needed to confirm our findings in other countries, and to explore the reasons underlying these vaccination behaviours and to assess whether these might be a marker of vaccine hesitancy.

      Acknowledgements

      We thank Jo Ann Cahn for her help in editing the manuscript. The first results of this work have been presented as an e-poster session at the European Congress of Clinical Microbiology and Infectious Diseases (ECCMID) in April 2016 and as an oral presentation at the French Congress of Infectious Diseases (JNI) in June 2016.

      Transparency declaration

      The authors declare no conflicts of interest.

      Funding

      Funding was received from DREES (convention n° 2101172809), INPES (convention n° 06 /13 -DAS) and IReSP (convention “Prévention Primaire 2013” n° PP-S1-14).

      Contributions to authorship

      NA and MLM drafted the article and approved the final version to be submitted. LF analysed and interpreted the data, revised the article for important intellectual content, and approved the final version to be submitted. PV supervised the conception and design of the study, the acquisition of data, revised the article for important intellectual content, and approved the final version to be submitted. CP participated in the conception and design of the study, the acquisition of data, drafted the article, revised the article for important intellectual content, and approved the final version to be submitted.

      Appendix A. Supplementary data

      The following supplementary materials are available for this article:

      References

      1. Immunization summery [Internet]. UNICEF & WHO, 2012 ([cited 2016 August 12]. Available from:)
        • Larson H.J.
        • Cooper L.Z.
        • Eskola J.
        • Katz S.L.
        • Ratzan S.
        Addressing the vaccine confidence gap.
        Lancet. 2011; 378: 526-535
        • Suryadevara M.
        • Handel A.
        • Bonville C.A.
        • Cibula D.A.
        • Domachowske J.B.
        Pediatric provider vaccine hesitancy: an under-recognized obstacle to immunizing children.
        Vaccine. 2015; 33: 6629-6634
        • Verger P.
        • Fressard L.
        • Collange F.
        • Gautier A.
        • Jestin C.
        • Launay O.
        • et al.
        Vaccine hesitancy among general practitioners and its determinants during controversies: a national cross-sectional survey in France.
        EBioMed. 2015; 2: 889-895
      2. Le Calendrier des vaccinations et les recommandations vaccinales 2015 selon l’avis du Haut Conseil de la santé publique [Internet]. Bulletin Epidémiologie Hebdomadaire, 2015 ([cited 2016 August 12]. Available from:)
      3. Couverture Vaccinale [Internet]. Institut de Veille Sanitaire, 2016 ([cited 2016 August 12]. Available from:)
        • Gautier A.
        Baromètre santé médecins généralistes 2009 [Internet].
        Institut National de Prévention et d'Education pour la Santé, 2011 ([cited 2016 August 12]. Available from:)
        • Stefanoff P.
        • Mamelund S.-E.
        • Robinson M.
        • Netterlid E.
        • Tuells J.
        • Bergsaker M.A.R.
        • et al.
        Tracking parental attitudes on vaccination across European countries: the Vaccine Safety, Attitudes, Training and Communication Project (VACSATC).
        Vaccine. 2010; 28: 5731-5737
        • D’ Alessandro E.
        • Hubert D.
        • Launay O.
        • Bassinet L.
        • Lortholary O.
        • Jaffre Y.
        • et al.
        Determinants of refusal of A/H1N1 pandemic vaccination in a high risk population: a qualitative approach.
        PloS One. 2012; 7: e34054
      4. Faciliter l’accès aux vaccinations en s’appuyant sur les Agences Régionales de Santé [Internet]. Ecole des Hautes Etudes en Santé Publique, 2013 ([cited 2016 August 12]. Available from:)
        • Posfay-Barbe K.M.
        • Heininger U.
        • Aebi C.
        • Desgrandchamps D.
        • Vaudaux B.
        • Siegrist C.-A.
        How do physicians immunize their own children? Differences among pediatricians and nonpediatricians.
        Pediatrics. 2005; 116: e623-e633
        • Killian M.
        • Detoc M.
        • Berthelot P.
        • Charles R.
        • Gagneux-Brunon A.
        • Lucht F.
        • et al.
        Vaccine hesitancy among general practitioners: evaluation and comparison of their immunisation practice for themselves, their patients and their children.
        Eur J Clin Microbiol Infect Dis. 2016; ([in press])
        • Le Maréchal M.
        • Collange F.
        • Fressard L.
        • Peretti-Watel P.
        • Sebbah R.
        • Mikol F.
        • et al.
        Design of a national and regional survey among French general practitioners and methodology of the first cross-sectional survey dedicated to vaccination.
        Med Mal Infect. 2015; 45: 403-410
        • Antón-Ladislao A.
        • García-Gutiérrez S.
        • Soldevila N.
        • González-Candelas F.
        • Godoy P.
        • Castilla J.
        • et al.
        Visualizing knowledge and attitude factors related to influenza vaccination of physicians.
        Vaccine. 2015; 33: 885-891
        • Kaufman L.
        • Rousseeuw P.J.
        Finding groups in data: an introduction to cluster analysis.
        John Wiley & Sons, Chichester2009
        • André F.E.
        Vaccinology: past achievements, present roadblocks and future promises.
        Vaccine. 2003; 21: 593-595
        • Mills E.
        • Jadad A.R.
        • Ross C.
        • Wilson K.
        Systematic review of qualitative studies exploring parental beliefs and attitudes toward childhood vaccination identifies common barriers to vaccination.
        J Clin Epidemiol. 2005; 58: 1081-1088
        • Hulsey E.
        • Bland T.
        Immune overload: parental attitudes toward combination and single antigen vaccines.
        Vaccine. 2015; 33: 2546-2550
        • Szilagyi P.G.
        • Rodewald L.E.
        • Humiston S.G.
        • Raubertas R.F.
        • Cove L.A.
        • Doane C.B.
        • et al.
        Missed opportunities for childhood vaccinations in office practices and the effect on vaccination status.
        Pediatrics. 1993; 91: 1-7
        • Luthy K.E.
        • Beckstrand R.L.
        • Peterson N.E.
        Parental hesitation as a factor in delayed childhood immunization.
        J Pediatr Health Care. 2009; 23: 388-393
        • Wong C.A.
        • Taylor J.A.
        • Wright J.A.
        • Opel D.J.
        • Katzenellenbogen R.A.
        Missed opportunities for adolescent vaccination, 2006-2011.
        J Adolesc Health. 2013; 53: 492-497
        • Mollema L.
        • Staal J.M.
        • van Steenbergen J.E.
        • Paulussen T.G.
        • de Melker H.E.
        An exploratory qualitative assessment of factors influencing childhood vaccine providers’ intention to recommend immunization in the Netherlands.
        BMC Public Health. 2012; 12: 128
        • Pulcini C.
        • Massin S.
        • Launay O.
        • Verger P.
        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
      5. SAGE working group dealing with vaccine hesitancy [Internet]. World Health Organization, 2014 ([cited 2016 August 12]. Available from:)
        • Katz-Sidlow R.J.
        • Sidlow R.
        A look at the pediatrician as parent: experiences with the introduction of varicella vaccine.
        Clin Pediatr (Philadelph). 2003; 42: 635-640
      6. Vaccine schedule [Internet]. European Center for Disease Prevention and Control, 2016 ([cited 2016 August 12]. Available from:)
        • Mullard A.
        Mediator scandal rocks French medical community.
        Lancet. 2011; 377: 890-892
        • Holman D.M.
        • Benard V.
        • Roland K.B.
        • Watson M.
        • Liddon N.
        • Stokley S.
        Barriers to human papillomavirus vaccination among US adolescents.
        JAMA Pediatr. 2014; 168: 76-82