Background

Seasonal influenza epidemics are a major public health problem worldwide, increasing annually the morbidity and mortality burden in vulnerable populations, particularly children younger than 2 years old and adults aged 65 years and older. Structures that concentrate vulnerable populations such as nursing homes for the elderly (NHs) or other long-term care facilities require special public health attention [1, 2]. Despite a high coverage of influenza vaccination (IV) among NH residents, influenza remains a major cause of death in this population [3].

Elderly people are poorly protected by vaccination due to immunosenescence [4]. Hence, prevention of influenza cases relies mainly on preventing infection among their direct contacts – an indirect protection strategy. In NHs, preventing influenza cases and deaths depends on preventing the virus from entering the community via the vaccination of healthcare workers (HCW) and other NH workers [5, 6]. Consequently, improving NH workers’ IV rate is a major public health target to alleviate the morbidity and mortality burden of influenza in the elderly population. In fact, 10% to 30% of HCW are infected with influenza each winter [7, 8], and most continue to work [9] which may lead to transmission of the virus to patients. Moreover, immunizing NH workers has been shown to decrease influenza transmission which increases the benefits of vaccination [5, 6].

IV of at least 75% of personnel is recommended by World Health Organization (WHO), CDC and the French Ministry of Health [10, 11]. In the US, various interventions performed in long-term facilities have contributed to an increase in HCW IV coverage from 36% in 2003 [12] to 86.4% in 2015 [13]. In France, HCW IV coverage, far from the WHO target, was 33.6% in 2008 and 25.6% in 2009 [3, 7, 8, 14,15,16,17,18].

In order to globally improve NH workers’ IV coverage, it is important to understand the determinants driving the vaccination status, particularly in settings with low coverage. The primary objective of the study is to estimate the IV coverage for the 2015–2016 winter season in NH workers in Ille-et-Vilaine, a department of the Brittany region, located in western France. Secondary objectives aim to assess the factors related to IV among NH workers.

Methods

Study design and population

A cross-sectional study was conducted among NH workers in French NHs in Ille-et-Vilaine (Fig. 1). The study took place on March 22nd 2016 and was performed as a collaboration between the French School of Public Health and Santé Publique France, in association with the regional health authority of Brittany. We performed a two-step randomized sampling, by randomly selecting NHs, then participants among the NHs. A sample size of 640 participants was computed based on an IV coverage estimation of 35%, an acceptance rate of 80%, an alpha risk of 5%, a study power of 80%, and a clustering effect. We randomly selected 40 NHs among the 137 NHs located in Ille-et-Vilaine and secondly, 16 NH workers were randomly chosen from each nursing home. Only permanent staff present at the time of the survey between 9 am and 7 pm were included, whereas temporary staff, interns, and liberal practitioners were excluded. No distinction between full time or part time workers was undertaken. In our study, NH workers included HCW such as physicians, nurses or pharmacists, administrative staff as well as facility and logistic staff. In order to reduce refusals, a letter introducing the survey was sent two weeks before the survey to the selected NHs.

Fig. 1
figure 1

Map of the 33 nursing homes surveyed in the Ille-et-Vilaine department

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Data collection

Data was collected through two standardized and pre-tested questionnaires given as Additional files: 1, 2, 3 and 4. Questionnaire were prepared in workgroups over a two-day period where outcomes, analysis plan and variables were defined. Questions to NH managers and NH workers were then drafted and both questionnaires were tested on a sample of 1 NH manager and 5 NH workers (3 physicians and 2 nurses). The first questionnaire was addressed to NH managers to obtain information about their establishment. We gathered NH status, size and information about vaccination (information or campaign) of the NH workers. The second questionnaire, targeting NH workers, was divided in three main parts: the first focused on socio-demographic items such as gender, age, occupation and experience in a NH; the second questioned NH workers on influenza risk factors and IV history; and finally, the third part gathered information concerning knowledge about vaccination as well as the perceived benefits and barriers of influenza vaccination. The total duration of the survey lasted no more than five minutes. Both questionnaires were administered in their original language (French). All questions were closed but interviewees were offered the possibility to give final comments or remarks. Questionnaires were administered face-to-face to NH workers in the participating NHs. All interviews were realized by 31 trained investigators as part of the IDEA international field epidemiology training course.

Data analysis

Vaccine coverage was estimated from data obtained from the interviews with the personnel. IV coverage was defined as the proportion of vaccinated NH workers for the 2015–2016 winter season. We first conducted a univariate analysis using Chi2 and Fisher exact tests to determine which determinants were significantly associated with vaccine coverage. All factors with p values lower than 0.2 were integrated in a multivariate Poisson model with and without random effects. Prevalence ratios (PR) and their 95% confidence intervals (CI) were used as measures of association. A p value lower than 0.05 was considered to be statistically significant. Data were centralized with WEPI software (Epiconcept) and analyses were performed using Stata 13® (StataCorp, Texas, USA).

Results

Participation

Of the 40 NHs randomized among the 137 in the administrative district, 33 (85%) participated in this survey. Two refused and 5 could not be visited for logistic reasons. Of the 485 personnel surveyed, 480 answered and 5 refused principally due to lack of time (response rate 99%) (Fig. 2). We excluded three responders who did not match inclusion criteria to finally include a total of 477 NH workers in our study.

Fig. 2
figure 2

Study sample flow chart. *Late arrival or acute gastro enterities epidemic in NH. **We excluded three responders who were not matching inclusion cirteria

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Characteristics of nursing homes and workers

Among NHs, 52.5% were public versus 47.5% with a private status, with a median number of 71 beds (min 28; max 270) (Table 1). The median number of permanent personnel was 43 (min 23; max 111) and the median ratio employee/resident was 0.73 (min 0.42; max 1.33).

Table 1 Population according to the nursing home characteristics
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Concerning the IV campaign, 81.8% of NH managers declared they had given information and offered the possibility of vaccination to the NH workers. Of the total study sample, 87.0% of NH workers were female. The mean age was 41 years (min 20; max 66), and they worked in a NHs for an average of 11.5 years (min 0.6; max 38). Most of them were HCW (42.9%) or facilities and logistics staff (35.7%). Administrative positions were held by 11% of workers. Overall, 84.1% of NH workers declared to be in contact with residents more than once per day.

Influenza vaccination coverage among workers

Of all NH workers, 20.0% [95% CI 15.3%–26.4%] declared having received the IV during the 2015/16 season, among which 80% have been vaccinated within the establishment. 21.3% [95% CI 16.6%–27.3%] of them reported being regularly vaccinated, as defined by at least two vaccinations during the last three years.

Median IV coverage for all sampled establishments for the season 2015–2016 was estimated at 18.2% ranging from 0% to a maximum of 69.2% (Fig. 3).

Fig. 3
figure 3

Distribution of the nursing homes according to their rate of seasonal influenza vaccination

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Predictors of influenza vaccine uptake

Socio-demographic, influenza risk factors, and vaccine history predictors

Vaccinated NH workers were older than the non-vaccinated (Table 2). Statistical analysis showed that personnel aged above 30 years were more vaccinated than personnel between 20 and 29 years (p < 0.01). A lower vaccine coverage was observed among the facilities and logistic staff members relative to the HCW (p < 0.004). Furthermore, having experienced a “severe” influenza infection (defined as “you had to be bedridden”) was positively associated with a higher vaccination rate (p < 0.045) (Table 2).

Table 2 Characteristics of the NH personnel and their seasonal IV coverage
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Knowledge about influenza

About NH workers’ knowledges of influenza and IV, 75.0% of them spontaneously mentioned hand washing as a prevention tool to avoid influenza transmission (Table 3). Wearing a mask and gloves was listed by 49.5% of NH workers, preventing contacts by 27.6% and vaccination by 24.4%. Knowledge of recommended prevention tools against transmission of influenza viruses was significantly associated with IV coverage. Spontaneous citation of one or more prevention tools was positively associated with a higher rate of vaccination (p < 0.001). An increasing association between the number of tools spontaneously cited and IV coverage was observed (p < 0.001). Moreover, 9.2% of NH workers reported homeopathy and 26.4% pointed out other tools not recommended by the national health authorities.

Table 3 NH personnel knowledge and perception on influenza and the seasonal IV coverage
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Finally, 73.9% of employees knew that IV needs to be administrated every year. And, knowledge of the frequency of the vaccination, known by a large part of the employees, was positively associated with a higher vaccination rate (p < 0.001). (Table 3).

Information

The main channels of information about seasonal IV received by the NH workers were primarily communication within the establishment and secondly communication by the media (Table 3). We also observed that 53.7% of the administrative employees were sensitive to posters as a medium. There were 51.9% of the HCW and 55.1% of the facilities and logistics staff that stated being more receptive to meetings and trainings (Table 4).

Table 4 NH personnel information type preference
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Perceived benefits of influenza vaccination

Perceived benefits and barriers to seasonal IV are shown in Table 5. Among the employees, 73.7% agreed that being vaccinated protects the NH residents. This proportion is also high for the non-vaccinated NH workers (74.1%). Otherwise, 52.9% NH workers agreed with the fact that being vaccinated prevents oneself from getting influenza.

Table 5 NH personnel perceived benefits and barriers of seasonal influenza vaccination 2015–2016
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Perceived barriers to influenza vaccination

Table 5 shows that 33.4% of NH workers thought that the influenza vaccine is ineffective and 24.1% of NH workers believed that the promotion of the vaccine was only linked to financial interests. Finally, 26.9% NH workers were convinced that seasonal IV causes serious side effects and 17.1% cited financial costs as a barrier.

Discussion

The French Ministry of Health has set a 75% target for seasonal IV coverage among NH workers; however, our study estimates the 2015–2016 seasonal IV coverage in Ille-et-Vilaine, in this population, to be 20.0% [15.3%–26.4%]. Vaux et al. [19] reported a 33.6% IV coverage in French NH workers for the 2007–2008 season. Contrary to our study, their study was also showing that private NHs had higher coverage rates than public ones (45.2% versus 29.8%, p < 0.001). However, Vaux et al. [19] used data declared by NH management and not direct NH workers interviews, which may introduce bias and prevent the identification of factors linked to individual perception and knowledge.

Social influence may explain the high IV coverage heterogeneity observed in our NH sample, from 0% to 69%, which is consistent with previous studies showing that social influence plays a major role in the decision of vaccination. Studies have found that having a relationship (being a colleague or relative) with people who receive or recommend influenza vaccination is a factor associated to being vaccinated against influenza (p < 0.012). Having a NH director or/and NH physician highly invested in the promotion of IV, has also a strong positive impact on NH workers vaccination (p < 0,001) [14, 20, 21].

Regarding occupational determinants, we show a significantly higher coverage in administrative staff compared to HCW. This may be explained by the fact that different staff may be sensitive to different kinds of information. We observe strong variations by occupation concerning the preferred communication medium: posters for most of the administrative staff (53.7%) and meetings for most HCW (51.9%). Presently, IV campaigns in French NHs seem to be inefficient; indeed, knowing that a campaign occurred is not significantly link to IV. Looking at individual score of knowledge and perception, our study illustrates a major paradox: firstly, we show that knowledge about means of preventing influenza transmission is highly associated with seasonal IV. Most personnel knew that influenza infection could be avoided by washing their hands, wearing masks and gloves, or avoiding contact with infected people. Of note, “homeopathic vaccine” was also cited by close to 10% of personnel and was proposed by some facilities as an alternative to the real vaccine. In addition, 52.9% of the participants knew that being vaccinated could prevent them from being sick (half of the non-vaccinated), and 73.7% stated that their own vaccination could protect NH residents (two thirds of the non-vaccinated employees). These figures showed that improved education of personnel may play a role in promoting vaccination.

Communication that counters inaccurate beliefs may also need to be specifically implemented. In our study, a third of NH workers interviewed believed that influenza vaccine was ineffective and 26.9% said that it should be avoided due to its side effects. Recent influenza related epidemic events, such as the scare in 2004 of an avian A/H5N1 influenza pandemic, or more recently, the 2009–2010 A/H1N1 pandemic, may have led to influenza communication fatigue or desensitization [20]]. In the Looijmans study, media attention to avian influenza appeared as a positive factor for vaccination (OR 2.24, 95% CI 1.12–4.50), contrary to the 2009–2010 pandemic that did not show any effect [22, 23]. Mass media coverage and health authorities’ communication may have been unable to counter polemics and rumors spread via other channels. For example, the influence of social networks in propagating ideas concerning vaccination has recently been shown [24], which can be considered as a potential issue for health authorities. Receiving information about the effectiveness of the vaccine through an informational meeting and from a nursing home physician has been shown to have a positive impact in different countries [15, 19, 20]. Nevertheless, despite a low IV coverage, NH workers felt they were sufficiently informed, 76.3% by the NHs and 67.5% by the media. Others means of communication have also proven their efficacy like personal reminders [25], newsletters [12], electronic mails, or dedicated websites [26]. However, being vaccinated was associated with having previously experienced a “severe” influenza episode in the past (PR 1.48, 95% CI 1.01–2.17) which shows the differential impact between theoretical and practical knowledge of influenza infection consequences.

Recently, Corace et al. concluded that the Health Belief Model was a promising tool to measure the impact of behavioral changes on the increase of IV coverage among HCW [14]. Perceived benefits and barriers are modifying variables used in the Health Belief Model; however, other variables of this model were not taken into consideration in our study as we did not aim to investigate this concept more deeply. Thus, further studies need to be conducted to explore the outlooks regarding to perceived threats, self-efficacy, as well as cues to actions in order to increase IV uptake.

While being the first study in France to directly interview such a sample of NH workers regarding knowledge and opinions about IV, our study was subject to some limitations. NH participation rate was high (2 refusals out of 40 NHs), and NH workers refusal rate was limited to 1%, but data collection was constrained by the fact that questionnaires had to be administered face-to-face during a single day. In addition, due to logistical issues, our study was performed in a single French department of Brittany (Ille-et-Vilaine). However, potential socio-demographic disparities within Brittany are unlikely to dramatically bias our results. Representativeness of Brittany with regards to France concerning NH workers vaccination is unknown, but to our knowledge, no known characteristics of the Region would impair our estimates at the national level. Although face-to-face interviews are an added value to our study, interviewers could have involuntarily influenced answers of NH workers, a bias minimized by interviewers’ training. Finally, as the subject of this study may have been sensitive to some or all, approaching personal beliefs on vaccination might have made the personnel answer differently from their true opinions.

Despite these limitations, we show that access to vaccination is not likely to be a determinant of low IV coverage, since only 0.4% of the responders declared being vaccinated as time consuming and considering that 80% of the vaccinations occurred inside the facilities. In addition, although 17.1% of the respondents cited IV financial cost as a barrier, the vaccine is available for free (or reimbursed) for the recommended population. Hence, we may “only” face a vaccination “hesitancy” issue, a concern defined by WHO as a “delay in acceptance or refusal of vaccines despite the availability of vaccine services” [27, 28]. Addressing vaccine “hesitancy” is complex and requires targeting multiple potential determinants.

Since most of the personnel vaccination was performed inside NHs like most of the vaccine communication, improvements may have to be targeted at the work place. Indeed, better results are found with IV campaign using staff of mobile units [26], flexible day and time (OR 1.45 95% CI 1.12–1.96) [12], and additional time slots during the day and night, 68.8% versus 41.4% [1].

The next step after influenza vaccine facilitation may be making it mandatory. Compulsory reassignment, wearing a mask or unpaid leave from work in case of refusal to get vaccinated are also different policies associated with a higher IV coverage (p < 0.002) [29]. In Norway, public opinion is in favor of freedom of choice (69% among vaccinated, 92.4% among non-vaccinated) [30], so is the Dutch population (77.6% and 96.5% respectively) [20]], but in the US, several hospitals have already made seasonal IV mandatory for HCWs with direct patient contact [15, 31]. Pre-post studies indicate that mandatory vaccination is successful in achieving near-universal vaccination rates of 95% to 98.5% [32], an idea defended by public health specialists for ethical and financial benefits reasons [33,34,35]. Since NHs have a moral responsibility to protect their residents, NH workers mandatory IV may have to be considered in the future if IV coverage remains low due to inefficiency of voluntary incitation measures.

Conclusions

Our study showed that NH workers IV maybe largely insufficient in western France and possibly throughout the country. High variations in IV coverage among NHs shows the key role of NH management and the working environment. Vaccine “hesitancy” may also be the main reason explaining this public health issue. Specific communication tools focusing on false beliefs should be developed and adapted to the various professional population, as well as the new modes of communication (social media). Failing to do so may pave the way to more debatable strategies such as compulsory IV.