Selcuk Mistik¹, Dilek Toprak², Abdullah Ozkiris³, Hasan Basri Ustunbas¹

1. Erciyes University Medical Faculty, Department of Family Medicine, Kayseri, Turkey
2. Afyon Kocatepe University Medical Faculty, Department of Family Medicine, Afyon, Turkey
3. Erciyes University Medical Faculty, Department of Ophthalmology, Kayseri, Turkey

Correspondence:
Dr. Selcuk Mistik
Erciyes University Medical Faculty
Department of Family Medicine
TR-38039, Kayseri, TURKEY
Tel: +90-352-437 49 37/ 23851
Fax: +90-352-437 52 85
E-mail: smistik@erciyes.edu.tr

INTRODUCTION

Influenza is a febrile disease, which is seen almost every winter and caused by influenza A and B viruses. Every year 5-20% of the population of the United States of America contracts influenza.
Two hundred thousand patients are hospitalized due to the complications of it, and 36,000 deaths occur due to influenza. In Germany, 600 patients die because of AIDS, 8,000 due to traffic accidents, whereas 16,000 deaths due to influenza have been reported^1-3.
Vaccination is necessary for the primary protection from influenza^4,5. World Health Organization has indicateddiabetes mellitus patients as a target group for influenza vaccination because of their increased risk.
The aim of this study was to evaluate the knowledge, attitude and behavior of diabetes mellitus patients who are a target group for influenza vaccination. In addition, it was also planned to compare the change in the vaccination status after training.

Patients
Diabetes mellitus patients who admitted to the Family Medicine and Ophthalmology Departments of Erciyes University Medical Faculty, and Family Medicine Department of Afyon Kocatepe University Medical Faculty between June-September 2005 were included in the study.
Patients selected were undergoing regular ophthalmologic examination for their diabetic retinopathy treatment and periodic health examination at Erciyes University Medical Hospital and were undergoing periodic health examination at Afyon Kocatepe University Medical Hospital.
Erciyes University Medical Faculty Ethical Committee has approved this study. Informed consent was obtained from the patients.

Questionnaire
A questionnaire comprised of 25 questions was administered to the patients. Thirty patients had training on influenza and influenza vaccination in September 2005. Influenza vaccination and having had influenza disease was asked at the end of the influenza season.
A comprehensive standardized questionnaire, which was designed to evaluate vaccination status of diabetes mellitus patients by Wahid et al., was used⁶. Our data collected by direct questioning included age, gender, marital status, occupation, level of education, occupation and level of education of the spouse, family's monthly income, type of diabetes, therapy, duration of diabetes and comorbid chronic diseases.
The questionnaire was validated for Turkish. A pilot study was performed before commencement of the study. The data was obtained from diabetes mellitus patients in a personal interview.
The questionnaire was performed between June 2005 and September 2006.

Patient training and vaccination results
The patients were invited to attend a training session on influenza and influenza vaccination following the cessation of the administration of the questionnaire. The invitation was made by phone calls, and patients who lived in the city center were preferred in order to achieve easier access to hospital. The patients were trained on influenza and influenza vaccination for an hour.
The vaccination status of all of the patients was questioned at the end of influenza season of 2005-2006, in June 2006, by telephone survey. In addition, epidemiological diagnosis criteria of World Health Organization for influenza (fever over 38ºC, cough, headache, and muscle pain) were asked of the patients for differential diagnosis.

Statistical analysis
Chi-squared test was used to define the significance of the data of the patients on getting vaccinated for influenza. Univariate logistic regression analysis was used to evaluate the effects of patient properties on vaccination status. These properties were age, gender, area, income level, type, duration and therapy of diabetes, occupation, education level, and comorbid conditions. P<0.05 was considered statistically significant.

Patient characteristics
Two hundred and three diabetes mellitus patients were enrolled in the study. Of the patients, 55% (112) were women and 45% (91) were men. The mean age of the diabetic patients was 57±10 (range 25-81) years. Duration of diabetes was 12±8 (0-40) years (mean±SD (range)). Fifty-two percent (n=105) of the patients were housewives, and 25% (n=52) were retired.
Eight (3.9%) of the 203 had Type 1 diabetes, 46.3% had hypertension, 17.7% suffered from coronary artery disease, 10.3% had chronic pulmonary disease, 5.9% had chronic renal disease, 3.4 had chronic liver disease, and 0.9% had had a stroke. There were no patients with a known immunodeficient state. Five patients had died during the study period. Deaths were not related to pneumonia.

Vaccination status
Overall, 18 (8.8%) (95% confidence interval (CI)) = (5.34-13.65) participants reported that they had influenza vaccine during the previous influenza season. Pneumococcal vaccination was reported by none of the participants.
The rate of patients who would like to get an influenza vaccine the next season was 26.6% (n=54). In total, 44 (21.6%) patients were influenced to get their influenza vaccine. Physicians were those who most commonly suggested vaccination to these patients (46.2%, n=25). The commonest reason cited for not having had an influenza vaccine was 'not being aware of the need' (47% n=96). In addition, 12.8% (n=26) stated that an influenza vaccine had never been offered. Of the patients who got influenza vaccine (n=18), all were given this suggestion by doctors. Nine got one vaccine during the past five years, 5 got it twice, and 4 got it three or more times.
The intention of getting pneumococcal vaccine the next season was 11.8% (n=24). Twenty-three (11.3%) patients were recommended to get their pneumococcal vaccine. Physicians most commonly suggested pneumococcal vaccination to these patients (5.9%, n=12). Fifty-seven percent of pneumococcal nonvaccinees (n=116) stated 'not being aware of the need' as the most common reason for being a nonvaccinee. Forty-seven (23.2%) stated that pneumococcal vaccine had never been offered to them.
Age, gender, marital status, geographical area, education level, occupation, type, duration and therapy of diabetes mellitus, and comorbid chronic diseases did not have a statistically significant effect on vaccination uptake (p>0.05) (Table 1).
Univariate logistic regression analysis only revealed the effect of education level on vaccination status (odds ratio (OR) (95% CI) = 0.341 (0.123-0.946) (Table1). The possibility of being a nonvaccinee was increased 2.93 times for the patients with education level of primary school or less.

Telephone survey after influenza season
At the end of the influenza season in 2006, the patients were telephoned and some questions regarding influenza and influenza vaccine were asked. A patient was called on three different days when not reached. Forty-five patients could not be reached overall. Five of those who had training (Table 2).
World Health Organization's epidemiological diagnosis criteria for influenza used to differentiate between influenza and the common cold (Table 2). There was no statistically significant difference for being vaccinated between the group who had training and the rest of the study group (p=0.511). However, there was an increase in the rates when compared with the previous season (15.1% vs. 8.8%), but this increase was not statistically significant (p=0.07). The rate of having influenza did not have a statistically significant difference between the groups who had training and those who did not (p=0.576).

The influenza vaccination rate of 8.8% and no pneumococcal vaccination in our study, is very low when compared with the previous studies regarding these two vaccines in diabetes mellitus patients.
There were only nine studies on influenza and pneumococcal vaccination in diabetic patients from 1993 to 2005 (Table3). Of these, five are from the USA and UK, and the remaining studies are from Belgium, Israel, Greece and Spain. Only four of these studies report both influenza and pneumococcal vaccination rates in diabetic patients. This study is the first study reporting vaccination rates of these two vaccines for diabetic patients in Turkey and the fifth study reporting the vaccination rates of two vaccines in the literature.
The limitation of this study was not being able to reach some patients by telephone survey. In addition, epidemiological criteria for the diagnosis of influenza were not giving the correct diagnosis in many cases. However, it was better to ask these questions rather then directly accepting patients' declaration, to differentiate between influenza and common cold.
The reported rates of influenza vaccination in diabetes mellitus patients vary from 44% to 62.1%^6-13, and 2% to 35% for pneumococal vaccination^6,8,9,13.
The Healthy People 2010 public health goals are to administer the influenza vaccine to 90% of diabetic adults >65 years and 60% of diabetic adults <65 by the year 2010¹⁴. It has been reported that there are no UK recommendations as to the minimum vaccination rate that is desirable in diabetic patients. Although the influenza and pneumococcal vaccines were provided free of charge, a concerted media campaign had never been conducted and no incentive was provided for primary care health professionals to achieve a high vaccination uptake⁶. There is no consensus on the minimum vaccination rates of diabetes patients in Turkey as well. In addition, a total of 2.5 million doses of vaccines were available on the market for the 2006-2007 influenza season, which will probably not be enough for the vaccination of 60% of diabetic patients. The vaccines are provided free of charge for diabetic patients, however the patients are not aware of the necessity of vaccination. The level of being unaware of the need for vaccination was 47% in our study was high and similar to the findings of 69% by Wahid et al and 68% by Sotiropoulos et al^6-13.
Sotiropoulos et al have stated the importance of primary care physicians in order to achieve optimal vaccination rates, and several repeated physician visits have been recommended¹³. In our study, we did not observe an increasing effect of group training, which support this suggestion.
The existence of comorbid conditions such as IHD, COPD and hypertension has been reported as significant predictors of receiving influenza vaccine^6,13. Our study did not demonstrate such a relationship probably due to low vaccination rate.
In order to achieve these desired levels of immunization, identification of patients, creation of registers, effective recall and reminder systems have been recommended¹⁵. The major challenge seems to be the lack of consensus on the necessity of diabetes mellitus patients' vaccination, of the health authorities. In addition, although American Diabetes Association suggests influenza and pneumococal vaccination of diabetes patients, a study from Israel stated that there was no extra benefit for the vaccination of diabetes patients^12,15. Furthermore, definitive proof of the efficacy of influenza vaccination specifically in people with diabetes is still lacking¹⁵.

This study demonstrated that diabetes mellitus patients in our study group have been vaccinated at a very low percent, with influenza vaccine and there was no one who had pneumococcal vaccine. Our assessment is that high vaccination levels may be achieved after the national health statement of the country, with the collaborative work of primary care and hospital physicians, including diabetes, ophthalmology and nephrology polyclinics. Training programs should be done face to face with each patient in order to increase the vaccination rates. Furthermore, required levels of vaccine should be supplied.
In summary, in order to prevent influenza which causes considerable morbidity and mortality in diabetes mellitus patients, it is important to get the patients vaccinated or at least suggest they get their influenza vaccine at repeated patient visits. Primary care physicians may play a better role in achieving higher rates of vaccination.

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