# Seasonal influenza and pneumococcal vaccination coverage among immunocompromised adults in France: A need for improvement

Marine Cailleaux, Frederic Balusson, Fabienne Pelé, Gaelle Bury, Sophie Reissier, Marion Baldeyrou, Lilian Alix, Anastasia Saade, Elisabeth Polard, Pierre Tattevin

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Marine Cailleaux, Frederic Balusson, Fabienne Pelé, Gaelle Bury, Sophie Reissier, et al.. Seasonal influenza and pneumococcal vaccination coverage among immunocompromised adults in France: A need for improvement. Infectious Diseases Now, 2025, 56 (1), pp.105225. 10.1016/j.idnow.2025.105225. hal-05425456

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# Seasonal influenza and pneumococcal vaccination coverage among immunocompromised adults in France: A need for improvement

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Marine Cailleaux<sup>a</sup>, Frédéric Balusson<sup>b</sup>, Fabienne Pelé<sup>c</sup>, Gaëlle Bury<sup>a,d</sup>, Sophie Reissier<sup>e,f</sup>, Marion Baldeyrou<sup>a</sup>, Lilian Alix<sup>a,g</sup>, Anastasia Saade<sup>a,b,f</sup>, Elisabeth Polard<sup>g</sup>, Pierre Tattevin<sup>a,*</sup>

## ARTICLE INFO

### Keywords:

Immunocompromised

Vaccines

Streptococcus pneumoniae

Influenza

France

## ABSTRACT

**Objective:** To estimate influenza and pneumococcal vaccination coverage in immunocompromised adults in France.

**Methods:** We used the *Echantillon Généraliste des Bénéficiaires* database, a representative sample of 850,000 patients covered by health insurance, with prospective collection of data on health care. We included adult patients with at least one of the following conditions: people living with HIV (PLWH), solid organ transplant, cancer treated by chemotherapy, any patient under immunosuppressive/immunomodulating therapy.

**Results:** We enrolled 10,784 immunocompromised patients, with a median age of 49 years [35–63]. During 2011–2017, complete seasonal influenza vaccine coverage (i.e., one shot each year) was 14.3 % [13.6–15.0] and closely correlated with age: 1.2 %, 2.8 %, 10.9 %, and 38.7 %, in the age groups 18–34, 35–49, 50–65, and > 65 years, respectively (P < 0.01). Pneumococcal vaccine coverage was complete (13-valent conjugated vaccine followed by 23-valent polysaccharide vaccine) in 6.9 %, not correlated with age.

**Conclusions:** Influenza and pneumococcal vaccine coverage in France during the study period, was very low, complete in < 15 % of immunocompromised adults.

## 1. Introduction

Immunocompromised patients are disproportionately affected by influenza [1] and invasive pneumococcal diseases [2], with an increased risk of complications and death. However, the incidence and morbidity of these diseases may be reduced by influenza and pneumococcal vaccines [3,4]. We aimed to estimate influenza and pneumococcal vaccine coverage in a representative sample of immunocompromised adult patients in France, the objective being to identify subpopulations that would stand to benefit from additional efforts to improve vaccine coverage.

## 2. Methods

Included patients were drawn from the *Echantillon Généraliste des Bénéficiaires* (EGB) database, a representative sample of 805,000 patients corresponding to 1/97th of the total population covered by the main health insurance public system in France, the SNIIRAM (*Système National d'Information Inter-Régimes de l'Assurance-Maladie*) [5]. This database prospectively collects all medical expenses, including medical consultations, hospital admissions, and any medical treatment, including vaccines, immunosuppressive drugs, or chemotherapy. For each patient enrolled, socio-demographic data are available, as well as a list of the diseases fulfilling the criteria for the list of 30 long-term diseases (ALD, *Affection de Longue Durée*, https://www.service-public.fr/particuliers/vosdroits/F34068), and in case of hospital admission,

<footnote><sup>a</sup> Maladies Infectieuses et Emergentes (MIE), Pontchaillou University Hospital, Rennes, France</footnote>

<footnote><sup>b</sup> Institut de recherche en santé, environnement et travail (IRSET), Rennes University, Rennes, France</footnote>

<footnote><sup>c</sup> Département de Médecine Générale (DMG), Rennes University, Rennes, France</footnote>

<footnote><sup>d</sup> Pédiatrie, Pontchaillou University Hospital, Rennes, France</footnote>

<footnote><sup>e</sup> Laboratoire de Bactériologie-Hygienne Hospitalière, Pontchaillou University Hospital, Rennes, France</footnote>

<footnote><sup>f</sup> Centre Régional de Pathologies Professionnelles et Environnementales, Pontchaillou University Hospital, Rennes, France</footnote>

<footnote><sup>g</sup> Pharmacologie, Pontchaillou University Hospital, Rennes, France</footnote>

<footnote>* Corresponding author.
E-mail address: pierre.tattevin@chu-rennes.fr (P. Tattevin).</footnote>
main diagnosis and comorbidities coded in the PMSI (Programme de Médicalisation des Systèmes d'Information), according to the International Classification of Diseases 10th revision (ICD-10).

We included all adult patients (age ≥ 18 years), with at least one of the following conditions: people living with HIV (PLWH), solid organ transplant (SOT), cancer treated by chemotherapy, inflammatory/auto-immune diseases treated with immunosuppressive agents, immunosuppressive treatment for unspecified reason. Patients on systemic corticosteroids were enrolled if they received > 10 mg equivalent prednisolone/day during at least two weeks, at least twice each year during the study period. Patients on immunosuppressive drugs were enrolled if they procured drugs from the following list at least twice a year during the study period: methotrexate, systemic corticosteroids, TNF alpha antagonists, anti-CD20, CTLA-4 agonists, anti-IL1, anti-IL6, leflunomide, azathioprine, cyclophosphamide and mycophenolate mofetil. Immunocompromised patients were identified via their long-term disease (ALD) and/or medical diagnoses documented during hospital admission and/or treatment. We included patients with at least one immunosuppressive condition documented between January 1st, 2011 and December 31st, 2012. Each patient was followed until December 31st, 2017. We collected data on influenza and pneumococcal vaccine uptake during the study period. For patients who died during follow-up, data collection was censored at the time of death.

Vaccine coverage was categorized as follows: i) for seasonal influenza vaccines, complete if the patient received one shot every year during the study period, incomplete if he received at least one influenza vaccine, but less than one per year, and absent when no influenza vaccine was received throughout the study period; ii) for pneumococcal vaccines, vaccine coverage was categorized as complete if the patient received at least one dose of 13-valent conjugated vaccine followed by at least one dose of polysaccharide 23-valent vaccine (the only pneumococcal vaccines available in France during the study period), incomplete for patients who received at least one pneumococcal vaccine but did not fulfill criteria for complete vaccination, and absent if no pneumococcal vaccine was received throughout the study period.

Continuous variables were presented as median values [interquartile range], categorical variables as numbers (%). Continuous variables were compared using the Student test, and categorical variables using the $\chi$-square or the Fisher exact test, as appropriate. Vaccine coverage was expressed as a percentage with a 95% confidence interval (95%CI). A P-value < 0.05 was considered significant.

The study protocol was approved by the Rennes University Hospital Ethics Committee (n°18.60). Informed consent was waived. Permanent access to the SNIIRAM is automatically granted to certain government agencies and public institutions such as university-affiliated hospitals. The scope of data access is defined by a Council of State decree, based on the opinion of the French data protection authority (CNIL).

## 3. Results

We enrolled 10,784 immunocompromised patients, with a median

<table><caption>**Table 1**

Characteristics of immunocompromised patients enrolled.</caption><thead><tr><th>Immunosuppression</th><th>numbers</th><th>Female-to-male ratio</th><th>Median age, years [interquartile range]</th></tr></thead><tbody><tr><td>Solid organ transplant</td><td>213</td><td>0.60</td><td>55 [43-63]</td></tr><tr><td>Immunosuppressive treatment for inflammatory/ autoimmune disease</td><td>1,410</td><td>1.64</td><td>55 [43-65]</td></tr><tr><td>People living with HIV</td><td>1,122</td><td>0.50</td><td>44 [34-51]</td></tr><tr><td>Cancer on chemotherapy</td><td>878</td><td>1.69</td><td>60 [50-69]</td></tr><tr><td>Immunosuppressive treatment for unspecified reasons</td><td>7,161</td><td>1.69</td><td>48 [31-63]</td></tr><tr><td>Total</td><td>10,784</td><td>1.45</td><td>49 [35-63]</td></tr></tbody></table>

age of 49 years [35–63], and a female-to-male ratio of 1.5 (6,397 females, 4,387 males, **Table 1**). The main groups of immunocompromised patients were those under immunosuppressive treatment for unspecified reason (n = 7,161, 66.4 %), immunosuppressive treatment for inflammatory/autoimmune disease (n = 1,410, 13.1 %), PLWH (n = 1,122, 10.4 %), patients with cancer undergoing chemotherapy (n = 878, 8.1 %), and SOT recipients (n = 213, 2.0 %).

Seasonal influenza vaccination coverage was complete in 1541 patients (14.3 % [13.6–15.0]), incomplete in 2551 (23.7 % [22.9–24.5]), and absent in 6692 (62.1 % [61.1–63.0]). The proportion of patients with complete vaccination coverage was moderately higher in SOT recipients (20.7 % [15.4–26.7]) and in patients receiving chemotherapy for cancer (17.3 % [14.9–20.0]), than in other categories of immunocompromised patients (13.9 % [13.2–14.6], *P* < 0.01). Age was strongly associated with seasonal influenza vaccination coverage, with complete vaccination coverage of 1.2 % [0.8–1.9], 2.8 % [2.2–3.4], 10.9 % [9.8–12.0], and 38.7 % [36.9–40.5], in the 18–34 years, 35–49 years, 50–65 years, and > 65 years, respectively (*P* < 0.01, **Table 2**) age groups.

Pneumococcal vaccination coverage was complete in 748 patients (6.9 % [6.5–7.4]), incomplete in 2897 (26.9 % [26.0–27.7]), and absent in 7139 (66.2 % [65.3–67.1]). The proportion of patients with complete pneumococcal vaccination coverage was moderately higher in PLWH (19.0 % [16.7–21.4]), patients receiving immunosuppressive agents for inflammatory/autoimmune diseases (15.0 % [13.2–17.0]) and SOT recipients (13.1 % [8.9–18.4]), than in other groups (5.5 % [5.1–6.0], *P* < 0.01). Age was not associated with pneumococcal vaccination coverage (**Table 3**).

Overall, 7484 patients (69.4 % [68.5–70.3]) received neither pneumococcal nor influenza vaccine during the study period, 2545 (23.6 % [22.8–24.4]) received at least one influenza vaccine, but no pneumococcal vaccine, 431 (4.0 % [3.6–4.4]) received at least one pneumococcal vaccine, but no influenza vaccine, and 324 (3.0 % [2.7–3.3]) received at least one influenza vaccine and one pneumococcal vaccine. Patients who received at least one influenza vaccine were 1.69 times (CI95%, 1.55–1.85) more likely to receive at least one pneumococcal vaccine, as compared to patients who received no influenza vaccine.

<table><caption>**Table 2**

Influenza vaccination coverage,ª according to age and immunosuppression group.</caption><thead><tr><th></th><th>Complete, n (%)</th><th>Incomplete, n (%)</th><th>Absent, n (%)</th></tr></thead><tbody><tr><td>Immunosuppression group (<strong>P</strong> <strong style="text-decoration: overline;">0.01</strong>) Solid organ transplant</td><td>44 (20.7 %)</td><td>82 (38.5 %)</td><td>87 (40.8 %)</td></tr><tr><td>Immunosuppressive treatment for inflammatory/autoimmune disease</td><td>186 (13.2 %)</td><td>365 (25.9 %)</td><td>859 (60.9 %)</td></tr><tr><td>People living with HIV</td><td>126 (11.2 %)</td><td>346 (30.8 %)</td><td>650 (57.9 %)</td></tr><tr><td>Cancer on chemotherapy</td><td>152 (17.3 %)</td><td>235 (26.8 %)</td><td>491 (55.9 %)</td></tr><tr><td>Immunosuppressive treatment for unspecified reasons</td><td>1033 (14.4 %)</td><td>1523 (21.3 %)</td><td>4605 (64.3 %)</td></tr><tr><td>Age group (<strong>P</strong> <strong style="text-decoration: overline;">0.01</strong>) 18–34 years</td><td>20 (1.2 %)</td><td>172 (10.7 %)</td><td>1422 (88.1 %)</td></tr><tr><td>35–49 years</td><td>87 (2.8 %)</td><td>458 (14.6 %)</td><td>2587 (82.6 %)</td></tr><tr><td>50–65 years</td><td>353 (10.9 %)</td><td>931 (28.7 %)</td><td>1960 (60.4 %)</td></tr><tr><td>> 65 years</td><td>1081 (38.7 %)</td><td>990 (35.4 %)</td><td>723 (25.9 %)</td></tr><tr><td>TOTAL</td><td>1541 (14.3 %)</td><td>2551 (23.7 %)</td><td>6692 (62.0 %)</td></tr></tbody></table>

<footnote>ª Seasonal influenza vaccine coverage was categorized as follows: complete if the patient received one shot every year during the study period; incomplete if he received at least one shot of influenza vaccine, but less than one shot per year; and absent if no influenza shot was received throughout the study period.</footnote>
<table><caption>**Table 3**
Pneumococcal vaccination coverage,ª according to age and immunosuppression group.</caption><thead><tr><th></th><th>Complete, n<br>(%)</th><th>Incomplete, n<br>(%)</th><th>Absent, n<br>(%)</th></tr></thead><tbody><tr><td>Immunosuppression group (P &lt; 0.01) Solid organ transplant</td><td>28 (13.2 %)</td><td>87 (40.8 %)</td><td>98 (46.0 %)</td></tr><tr><td>Immunosuppressive treatment for inflammatory/autoimmune disease</td><td>212 (15.0 %)</td><td>696 (49.4 %)</td><td>502 (35.6 %)</td></tr><tr><td>People living with HIV</td><td>213 (19.0 %)</td><td>570 (50.8 %)</td><td>339 (30.2 %)</td></tr><tr><td>Cancer on chemotherapy</td><td>38 (4.3 %)</td><td>159 (18.1 %)</td><td>681 (77.6 %)</td></tr><tr><td>Immunosuppressive treatment for unspecified reasons</td><td>257 (3.6 %)</td><td>1385 (19.3 %)</td><td>5519 (77.1 %)</td></tr><tr><td>Age group (P=NS) 18–34 years</td><td>80 (5.0 %)</td><td>NA</td><td>NA</td></tr><tr><td>35–49 years</td><td>222 (7.1 %)</td><td>NA</td><td>NA</td></tr><tr><td>50–65 years</td><td>286 (8.8 %)</td><td>NA</td><td>NA</td></tr><tr><td>&gt; 65 years</td><td>160 (5.7 %)</td><td>NA</td><td>NA</td></tr><tr><td>TOTAL</td><td>748 (6.9 %)</td><td>NA</td><td>NA</td></tr></tbody></table>

NA, not available; NS, not significant.

ª Pneumococcal vaccines coverage was categorized as follows: complete if the patient ever received at least one shot of 13-valent conjugated vaccine, followed by at least one dose of polysaccharide 23-valent vaccine (the only pneumococcal vaccines available in France during the study period); incomplete if only one shot of pneumococcal vaccine was received; and absent if no uptake of pneumococcal vaccine was documented in the patient file.

## 4. Discussion

The main findings of this prospective national study, based on a representative sample of 10,784 immunocompromised adult patients eligible for influenza and pneumococcal vaccination are the following: i) pneumococcal and seasonal influenza vaccine coverages in this population during the study period (2011–2017) were very low, as < 15 % of patients had complete vaccine coverage; ii) seasonal influenza vaccine coverage was closely associated with age, complete in < 5 % of immunocompromised patients younger than 50 years, vs. 38 % of those older than 65 years; iii) pneumococcal vaccine coverage remained low in all age groups, though slightly higher in PLWH, SOT recipients, and patients receiving immunosuppressive agents for inflammatory/autoimmune diseases; iv) vaccine coverage against both pathogens was correlated, with > 70 % patients classified in the same category for both vaccines (i.e., 69.4 % patients received none of these vaccines, and 3.0 % had complete coverage for both).

Our findings are in line with several large-scale studies reporting low vaccine coverage rates in at-risk population despite national and international recommendations [3,4]: 28 %-59 % for influenza, and 9 %-49 % for pneumococci [6–10]. Vaccine coverage was particularly low in France during the study period for most recommended vaccines, at a time when vaccine hesitancy was on the rise. Indeed, a 67-country survey performed in 2016 reported that the highest level of disagreement with the statement ‘vaccines are safe’ was observed in France, reaching 41 % [11]. Of note, the health care system in France provides free and easy access to most vaccines in eligible population, including the immunocompromised patients enrolled in our study. Hence, low vaccine coverage cannot be explained by cost issues. The main documented barriers to improved vaccine coverage in immunocompromised patients are classically: i) limited awareness of healthcare workers on the particularly high importance of vaccines in immunocompromised patients; ii) sub-optimal health care system organization; iii) lack of clarification regarding responsibility for vaccine prescription (i.e., specialist, or general practitioner); iv) sub-optimal recording of previous immunization in medical charts; and v) vaccine hesitancy. A recent cross-translational multicentric survey suggested that health care providers in France are well-informed on the official guidelines for vaccines in immunocompromised patients, but with sub-optimal organization,

marked by limited access to specific consultations for infection prevention in this population [12]. Innovative interventions are currently being tested, including structured medico-pharmaceutical collaborative management to improve vaccination coverage [13]. More complete information on at-risk patients, who are increasingly involved in medical decision-making regarding their own care, may prove beneficial [10], as would reinforced commitment from general practitioners [14].

Our study has limitations. First, as a single-country study covering a limited time period, its findings may not be generalizable to other settings. Second, as the data we collected data on vaccine procurement were limited to France’s national health care system, we may have underestimated vaccine coverage for patients who had received vaccines through other systems (e.g., during hospital admission), and we may have overestimated vaccine coverage when patients collected their vaccines at the pharmacy, but administration was not performed. Third, during the last year of the study, there was an international stock-out of the 23-valent polysaccharide pneumococcal vaccine, which may be factored into the low rate of pneumococcal vaccine coverage. However, our study also has strengths, including a large sample size, with a representative sample comprising more than 10,000 immunocompromised patients, and follow-up of 6 years, with comprehensive collection of data from the national health care system.

In conclusion, we found a very low rate of pneumococcal and influenza vaccine coverage during 2011–2017 in a representative sample of > 10,000 immunocompromised adults in France. Given the high burden of influenza and invasive pneumococcal diseases in this population, targeted interventions to boost vaccine coverage is a public health priority. Of note, vaccine schedules in immunocompromised adults have changed since the study was completed, especially for pneumococcal vaccines: Currently, a single dose of the 20- or 21-valent conjugated vaccine is recommended, which may improve vaccine coverage.

Funding.

This study was funded by a grant from the ‘Groupe Vaccination-Prévention’, French Society of Infectious Diseases.

### CRediT authorship contribution statement

**Marine Cailleaux:** Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Writing – original draft. **Frédéric Balusson:** Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Validation, Writing – review & editing. **Fabienne Pelé:** Conceptualization, Formal analysis, Methodology, Validation, Writing – review & editing. **Gaëlle Bury:** Methodology, Validation, Writing – review & editing. **Sophie Reissier:** Methodology, Validation, Writing – review & editing. **Marion Baldeyrout:** Methodology, Validation, Writing – review & editing. **Lilian Alix:** Methodology, Data curation, Formal analysis, Writing – review & editing. **Anastasia Saade:** Methodology, Validation, Writing – review & editing. **Elisabeth Polard:** Conceptualization, Formal analysis, Methodology, Validation, Writing – review & editing. **Pierre Tattevin:** Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Writing – original draft.

### Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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