Abstract
A descriptive cross-sectional study was conducted for adults (aged ≥ 50 y) with diabetes. Data was obtained from the 2009 European Health Interview Survey for Spain and the 2003 and 2006 Spanish National Health Surveys. To assess influenza vaccination status, we considered the response (yes or no) to the question “Have you received the influenza vaccine in the previous season?” Both dependent and independent variables were based on the survey questionnaires. The independent variables analyzed included socio-demographic characteristics, health-related variables and use of health care services.
The coverage among adults with diabetes in 2010 was 65.0% (95% CI: 62.1–67.7) compared with 41.2% (95% CI 40.0–42.4) for those without diabetes (p < 0.01) adjusted OR 1.67 (95% CI: 1.40–1.99). The positive predictors of vaccine uptake among diabetic adults were: higher age, being male, the presence of associated chronic conditions and physician visits in the last 2 wk.
The vaccine uptake among adults with diabetes was 61.4% (95% CI: 57.9–64.8) in 2003 and 63.8% (95% CI: 60.7–66.8) in 2006.The adjusted OR of having been vaccinated in 2010 with respect to 2003 was not significant 1.18 (95% CI: 0.97–1.44).
We conclude that the levels of influenza vaccination coverage are below desirable levels among adults with diabetes. Furthermore, trend analysis in influenza vaccination coverage indicates that influenza vaccination rates in adults with diabetes have not improved in recent years. Urgent strategies for increasing vaccination coverage among diabetes sufferers are necessary especially for those aged 50–59, women, those without chronic conditions and those who are not frequent users of health care services.
Introduction
Influenza infection is a preventable disease associated with high mortality, morbidity and a large number of hospitalizations each year, especially in individuals with underlying medical conditions such as diabetes. Thus, influenza immunization is a crucial component of preventive medicine and important for subjects with diabetes.Citation1
Recently, the Council of the European Union adopted a recommendation in which member states are encouraged to adopt and implement, where appropriate, plans or policies aimed at improving seasonal influenza vaccination coverage. The aim is to reach a vaccination coverage rate of 75% for older age groups and risk groups.Citation2
According to the American Diabetes Association, influenza vaccination is recommended for all individuals with diabetes, because it is safe, effective and mitigates influenza-related complications, hospitalizations and deaths in these patients.Citation3 Healthy People 2020 set a specific goal for seasonal influenza vaccination in high-risk adults (including diabetic patients) of 90%.Citation4
In Spain, influenza vaccination is recommended every year for persons of all ages with specific chronic conditions including diabetes. Influenza vaccination in Spain is fully funded to recommended groups.Citation5
Despite the broad consensus on recommending influenza vaccination in people with diabetes, most studies of influenza vaccination coverage in Spain have estimated low coverage figures of between 43–57%.Citation6,Citation7 According to published literature, some characteristics appear to be associated with higher adherence to influenza vaccination: older age and co-morbidity were independently associated with influenza vaccination.Citation6
Using data from the 2009 European Health Interview Survey for Spain (EHIS) and the 2003 and 2006 Spanish National Health Surveys (SNHS), this study sets out to describe influenza vaccination coverage among Spanish adults with diabetes. The data was analyzed by socio-demographic, health-related variables and use of health care services to explore if these factors are associated with the likelihood of adults with diabetes being vaccinated. Trends in influenza vaccination coverage from 2003–2009 were also analyzed.
Results
Using the 2009 EHIS database (n = 22,188), we analyzed the records of 11,089 subjects aged 50 y or over. Of them, 1,641 were identified as diabetes sufferers so the prevalence of diabetes was 14.8% (95% CI: 14.0–15.6). and show the distribution and vaccine coverage according to diabetes status and study variables.
Table 1. Influenza vaccination coverage and distribution by sociodemographic variables among Spanish adults with and without diabetes. Data from the 2009 European Health Interview Survey (EHIS)
Table 2. Influenza vaccination coverage and distribution by health-related variables and health care service use among Spanish adults with and without diabetes. Data from the 2009 European Health Interview Survey (EHIS)
The coverage in 2010 was 65.0% (95% CI: 62.1–67.7) for diabetes sufferers and 41.2% (95%CI 40.0–42.4) for those without diabetes (p < 0.01). The multivariate analysis showed that diabetics had 1.67 (95% CI: 1.40–1.99) more probabilities of reporting vaccine uptake than non-diabetics.
In the bivarite analysis of coverage variables associated to a higher uptake among diabetes sufferers were: older age, with the highest figures for those aged 70 y or over (77.6%), fair, poor or very poor self-rated health (68.6%), those who also suffered other chronic diseases, non-smokers and those who practice no physical exercise.
Finally, physician visits in the last 2 wk, hospitalization in the last 12 mo and specialist visits in the last 2 wk were variables associated to higher coverage among diabetic subjects.
shows the predictors of influenza vaccination among Spanish adults with diabetes after logistic regression analysis. Diabetic subjects aged ≥ 70 y were 5.97 times more likely to have been vaccinated than those aged 50–59 y.
Table 3. Predictors of influenza vaccination among Spanish adults with diabetes. Data from the 2009 European Health Interview Survey (EHIS)
In , no significant difference is found in vaccination coverage by gender with figures of 64.2% (95% CI: 59.9–68.3) for men and 65.7% (95% CI: 61.9–69.3) for women (p > 0.05). However, after adjusting in the multivariate model, being male was associated to higher vaccination with an adjusted OR of 1.39 (95% CI: 1.02–1.90).
Likewise, the presence of an associated chronic condition and any physician visits in the last 2 wk increased likelihood of vaccination by 1.21 and 1.33, respectively.
Influenza coverage and trends from 2003–2009 are shown in . The proportion of adults with diabetes that reported having been vaccinated in 2003 was 61.4% (95% CI: 57.9–64.8) compared with 63.8% (95% CI: 60.7–66.8) in 2006 and 65% (95% CI: 62.1–67.7) in 2010. The adjusted OR of having been vaccinated in 2010 with respect to 2003 was not significant (1.18 95% CI: 0.97–1.44), showing no change over time in the coverage for the total population. When we stratified by age and sex we observed a significant improvement from 2003–2010 in the total age group 70 y or over (OR 1.40; 95% CI: 1.06–1.85) and among women with this age (OR 1.55; 95% CI: 1.09–2.20).
Table 4. Trends in influenza vaccination coverage among Spanish adults with diabetes using data from the 2003 National Health Survey, 2006 National Health Survey and 2009 European Health Interview Survey
Discussion
The most important result of this work is that 35% of Spaniards aged 50 y or over with diabetes did not receive the influenza vaccine in 2010.
Several studies have reported influenza vaccination rates among diabetics in the United States. Data from the 1997–2008 National Health Interview Surveys indicated that in adults with diabetes aged 50–64 y, the median vaccination coverage trends have increased from 43.2% to 53.7%, respectively.Citation8 Also in the United States and according to the BRFSS in 2003, the median influenza vaccination coverage rate among subjects with diabetes aged 50–64 y was 56.5% and 69.9% in people aged ≥ 65 y.Citation9
In our study, the likelihood of a diabetic subjects aged 60–69 y of being vaccinated was more than triple that of those aged 50–59 y, and around six times greater if the former were aged ≥ 70 y. Similar results have been found by other authors.Citation6,Citation7, Citation9-Citation13 In any case, we believe that the association of age with diabetes has little to do with diabetes status as previous studies in Spain have found that older people with or without high-risk conditions have higher compliance than younger ones.Citation14 In our opinion, the most probable explanation for this is that in Spain, influenza vaccination recommendation becomes universal for all persons aged 60/65 y or more (depending on the region) and that age-based strategies are more affective to increase vaccine uptake than high-risk strategies.Citation15,Citation16
Multivariate adjustment showed the male gender to be associated with a higher likelihood of being vaccinated among diabetics. In Europe, Dornet et al. found a significant higher influenza vaccination coverage in men with diabetes compared with women with diabetes (39.0% vs. 30.2%, respectively, p < 0.05).Citation17 In a Spanish study analyzing vaccine uptake in Spain between 1995–2006, a 12% greater probability of having received the vaccine was found in men aged 65 y and older with an associated chronic condition, compared with women with the same medical conditions.Citation14
Even if statistical and clinical significance are not the same, we think that the gender differences found in vaccine uptake among diabetic patients may be an important alarm signal pointing that women are not being treated or attended to as well as men. We consider as possible explanations for this that women have less social support, differences in the health status and provider bias.Citation14 This issue is relevant and requires further investigation.
A physician visit in the previous 2 wk is also a positive predictor of vaccine uptake among Spanish diabetes sufferers in our study. These findings coincide with results obtained in previous studies.Citation7,Citation12,Citation18 Obviously a greater number of physician visits increases the probability of receiving recommendations to be vaccinated from the health care workers (HCWs) and therefore to be vaccinated.Citation12 A study performed by Blank et al. in five European countries, in which the authors studied the principal factors that motivate subjects to get vaccinated, showed that the most important factor is a recommendation by a health care professional.Citation19
Lewis-Parmar et al. found that if vaccination is recommended by HCWs, the probability that a diabetes sufferer is vaccinated multiplies by 14-fold and that this was the unique source of information useful to increased vaccine uptake.Citation20
We believe that beside the fact that they have a specific recommendation for being diabetics, persons suffering with this disease tend to consider their own health status more, because of personal experience with the disease and frequent advice from health staff. Naturally, they would positively respond to influenza vaccination, as it affects their health status.
Another variable found to be independently associated with a greater likelihood of having been vaccinated is concomitantly suffering chronic conditions. This association has been observed, almost unfailingly, by different studies of subjects with diabetes.Citation6,Citation7,Citation12,Citation13
We analyzed the trend in influenza coverage among adults with diabetes from 2003–2010. Our results indicate that the adjusted OR of having been vaccinated in 2010 was 1.18 (95% CI: 0.97–1.44) when compared with 2003. This indicates that influenza vaccination rates in adults with diabetes are improving unsatisfactorily. Kroneman et al. found that a large number of people in high-risk groups believe their natural resistance provides sufficient protection against influenza and so do not get vaccinated (in Spain, 38%).Citation21 Further surveys also cite a low perception of risk by patients as a reason for them not being vaccinated.Citation22 Previously described factors that may influence non-vaccination in patients include vaccination program failures, information problems or personal characteristics, but we were unable to explore these in our study.Citation23,Citation24
Several strategies that have proved effective to increase influenza vaccination coverage, and should therefore be considered, include: (1) Make use of mass media to promote influenza vaccination; (2) provide information through educational interventions to health care workers and for persons suffering from diabetes and their families about risks and prevention strategies for influenza; (3) standing orders; (4) expanding access in health care settings; (5) use of computerized record reminders at the GP office, send personal invitation using letter, phone or the new technologies; (6) an organizational strategy that has demonstrated its effectiveness is giving financial incentive to physicians; (7) finally, previous studies conducted in Spain have shown that a simple age-based influenza vaccine recommendation has improved vaccine coverage levels for annual influenza vaccination for people with and without chronic conditions and, therefore, lowering the age for universal influenza vaccination should be considered.Citation15,Citation16,Citation20,Citation25-Citation28
Increasing influenza vaccination is expected to have an important effect and reduce the risk of morbidity, hospitalization, ICU admissions, costs and mortality among these subjects.Citation13,Citation29,Citation30 In the United States, Looijmans-Van den Akker et al. estimated that influenza vaccination of diabetic patients was associated with a 56% reduction in any complication, a 54% reduction in hospitalizations (26–71%) and a 58% reduction in deaths (13–80%).Citation13 In Taiwan, those diabetic subjects vaccinated had a hospitalization rate that was 11% less than the non-vaccine cohort. The vaccinated group was also less likely to be admitted to the intensive care unit (ICU) [adjusted HR 0.30 (95% CI: 0.19–0.47)] and less likely to die [3.13 vs. 7.96 per 100 person-year; adjusted HR 0.44 (95% CI: 0.36–0.54)].Citation30
Besides immunological control of the disease in the individual using the influenza vaccine, there are other alternative strategies that might also help to improve protection or reduce the consequence of influenza among diabetes sufferers. People with diabetes and their household contacts should take everyday precautions for protecting against the flu, such as to avoid close contact with people who are sick, stay home when sick, washing hands often, avoid touching eyes, nose or mouth, to clean and disinfect frequently touched surfaces at home, work or school, especially when someone is ill and if possible, avoid crowded places when the influenza epidemic is active. Finally, the use of antiviral drugs such as prophylaxis or treatment by the diabetic person and their household contacts can also reduce the transmission or consequences of influenza.Citation27
Our study strength comes from the use of three large, national, representative surveys of the Spanish population and consistent use of the same questions and methodology. The Spanish Ministry of Health, in order to monitor the health of the nation, has been conducting the National Health Surveys every 2–5 y since 1987.Citation31-Citation34 In year 2009/10, the name of the survey was changed to European Health Interview Survey for Spain (2009).Citation34 These surveys have questions and methodology based in the US National Health Interview Survey. We think that the validity of these surveys to evaluate trends over time is unquestionable. Many Spanish researchers have used these surveys to investigate time trends in different health-related issues. Citation35–Citation38
However, there are a number of study limitations. First, the use of invalidated self-reported data on vaccination could lead to possible bias. However, several studies that have compared self-reported data against medical records observe that self-reporting on the influenza vaccination is highly sensitive and a high degree of agreement is seen. Citation39,Citation40
Second, to our knowledge, the validity of the questions used to classify subjects as diabetic or non-diabetic has not been evaluated. A study found 73.2% sensitivity and 99.3% specificity for self-reported diabetes when compared with medical records. Citation41 However, there is the possibility of misclassifying type 1 diabetes as type 2, but given the low prevalence of type 1 diabetes in the Spanish population, we believe it is unlikely. Spanish studies show that in Spain, over 95% of diabetic patients suffer from type 2 diabetes. Citation42
Third, the NHS and EHIS do not collect data on all conditions for which vaccination is indicated, an omission that could probably lead to underestimation of the percentage of subjects in whom vaccination would otherwise be indicated. Even so, we consider the relative importance of the missing conditions to be proportionally less than that of those included, so that any ensuing error may not be of great importance.
Fourthly, subjects interviewed (especially elderly) may have difficulties in being able to reliably recall which vaccine, seasonal or pandemic, they received, even if as commented in the methods section for those interviewed in the after November 2009, when the H1N1 pandemic influenza vaccine was available in Spain, interviewers were specifically trained to ask only about seasonal influenza. In any case, in our opinion, this limitation would not much affect the main conclusion of our investigation because another Spanish study, based on medical registries, found that the coverage for pandemic influenza was much lower than for the 2009 seasonal vaccine (14.6% vs. 41.8%). Furthermore, of those individuals vaccinated against pandemic H1N1 influenza, 84.6% had also previously received the 2009 seasonal influenza vaccine.Citation43 Therefore, the possible misclassification bias would be of small magnitude.
Lastly, it is important to note that any information obtained within an interview context may be subject to recall and non-response bias, and the tendency of interviewees to give socially acceptable responses. In the three surveys studied, initial response rates were around 65%. Citation32–Citation34
Based on self-reported influenza vaccination data from the 2003 NHS, 2006 NHS and 2009 EHIS, we conclude that the levels of influenza vaccination coverage are below desirable levels among adults with diabetes aged 50 y or older and still far from the European Union recommendations.Citation2 Furthermore, trend analysis in influenza vaccination coverage indicates that influenza vaccination rates in adults with diabetes have not improved in recent years. Urgent strategies for increasing vaccination coverage among diabetes sufferers are necessary and must target those aged 50–59, women, those without chronic conditions and those who are not frequent users of health care services, as these are the groups who least follow vaccination recommendations.
Patients and Methods
Data for our investigation was obtained from the EHIS in 2009. This research was proposed by the European Commission to the European Union (EU) Member States and conducted by the Spanish National Statistics Institute. The EHIS is a home-based, personal interview examining a nationwide, representative sample of the civilian, non-institutionalized population aged 16 y or over, residing in main family dwellings (households) in Spain. Citation34 The data collection period ran from April 2009–March 2010 and a sample of 22,188 subjects was selected.
To analyze trends in influenza vaccination coverage in 2003 and 2006, we used data from the SNHS, which included 21,650 and 29,478 interviews, respectively. The methods of the SNHS are the same as those used in the EHIS. More details on the methodologies of both surveys are described elsewhere.Citation32,Citation33 The variables used in our study were collected identically in all the surveys used. Both dependent and independent variables were based on the survey questionnaires. We analyzed the vaccination coverage and predictors for vaccine uptake among all subjects with diabetes. To identify those with type 2 diabetes in our study, we included all subjects aged 50 or over if they answered yes to one or two of the following questions: “Has your doctor told you that you are currently suffering from diabetes?” and /or “Have you taken any medication to treat diabetes in the last 2 wk?” To assess influenza vaccination status, we considered the response (yes or no) to the question, “Have you received the influenza vaccine in the previous season?” The vaccination status was not verified using documentary evidence.
Vaccination information from surveys only referred to seasonal influenza vaccination. This is especially relevant for those interviewed after November 2009 (when the H1N1 pandemic influenza vaccine was available in Spain) where interviewers were trained to explicitly explain to the subject during the interview that the question was only about seasonal influenza vaccination and not the pandemic vaccine. The independent variables analyzed are (1) age, gender, marital status, educational level and size of town or city; (2) health-related variables, namely, (a) self-rated health, (b) self-reported presence of concomitant chronic illness, (c) obesity (BMI ≥ 30), (d) tobacco use, (e) alcohol consumption and (f) physical exercise and (3) use of health care services, namely (a) any visit to the physician in the last 2 wk besides the reason (including scheduled health care visits and acute health issues), (b) hospital admission in the last year and (c) visits to a specialist physician in the last 2 wk.
The number of chronic conditions (0, 1 and 2 or more) was identified in those who self-reported an affirmative answer to the presence of any of the following physician-diagnosed diseases: respiratory disease (asthma and chronic bronchitis), heart diseases, depression and/or anxiety or cancer.
Statistical analysis
We estimated the proportions of vaccinated subjects (coverage) according to study variables among those with and without diabetes and compared these coverages using the χ2 test.
Multivariate logistic regression models were conducted to identify those variables independently associated with vaccine uptake among diabetes sufferers (predictors) and to assess the time trend in vaccination from 2003–2010. Before including variables in the model, we checked the statistical relationship (correlation analysis) between those that could measure similar characteristics (e.g., “associated chronic diseases” and “use of health-care services”). For bivariate and multivariate statistical analysis we used the “svy” commands of STATA software. Statistical significance was set at α < 0.005 (two-tailed).
According to Spanish legislation, ethics committee approval was not required, as this analysis was conducted on de-identified, public-use data sets.
| Abbreviations: | ||
| EHIS | = | European Health Interview Survey for Spain |
| SNHS | = | Spanish National Health Surveys |
Acknowledgments
This study forms part of a research project funded by “Carlos III Institute FIS” grant PS09/01609.
Disclosure of Potential Conflicts of Interest
No potential conflicts of interest were disclosed.
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