Vaccine 33 (2015) 182–186

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Seasonal influenza vaccination rates and reasons for non-vaccination in children with gastrointestinal disorders Noam Peleg a , Noam Zevit a,b , Raanan Shamir a,b , Gabriel Chodick a , Itzhak Levy a,c,∗ a b c

Sackler Faculty of Medicine, Tel.: Aviv University, Tel: Aviv, Petach Tikva, Israel Institute of Gastroenterology, Nutrition and Liver Diseases, Petach Tikva, Israel Unit of Pediatric Infectious Diseases, Schneider Children’s Medical Center of Israel, Petach Tikva, Israel

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Article history: Received 2 June 2014 Received in revised form 22 October 2014 Accepted 30 October 2014 Available online 11 November 2014 Keywords: Influenza Vaccine Immunization Gastroenterology

a b s t r a c t Objectives: Despite advances in the treatment and prevention of influenza, it is still considered an important cause of morbidity and mortality worldwide. Annual vaccination is the safest and most effective mean of prevention. Our study aims were to explore the uptake of influenza vaccination among children with gastrointestinal disorders, and to characterize non-adherent patients. Methods: The present cross-sectional study included parents of pediatric patients attending the Gastroenterology Institute at Schneider Children’s Medical Center of Israel between September and October 2011. Parents were asked to complete a questionnaire concerning demographic and clinical parameters, influenza vaccination of the child, and reasons for not vaccinating the child, when appropriate. Results: The study population included 273 patients (50% female), with a median age of 10 years (range, 2–18 years). Overall, the rate of seasonal influenza vaccination was 30.8%. Higher rates were found among immunosuppressed patients (46.1%), and in patients with inflammatory bowel disease (50%). There was no significant effect of patient age, gender, ethnic origin or parental level of education on the vaccination rate. Vaccination rates were significantly associated with parents’ information and knowledge of, as well as their personal beliefs regarding the vaccine (P < 0.001). Conclusions: Influenza vaccination rates are relatively low in the pediatric population attending gastroenterology clinics, in both high- and low-risk groups. The importance of parental knowledge in compliance with influenza vaccination of children should prompt general pediatricians and gastroenterologists to discuss and address the common misconceptions regarding the vaccine. © 2014 Elsevier Ltd. All rights reserved.

1. Introduction Influenza epidemics affect 10–20% of the general population every winter [1]. Seasonal influenza is associated with considerable morbidity and mortality and exerts a heavy economic burden on society [2]. Population groups primarily at risk for influenza complications are adults over age 65 years, patients with chronic diseases of the heart, lungs (e.g., asthma, chronic obstructive pulmonary disease), or kidneys, immunocompromised patients, pregnant women, morbidly obese patients and infants less than 2 years old [3]. According to the study of Thompson et al., about

∗ Corresponding author at: Pediatric Infectious Diseases Unit, Schneider Children’s Medical Center, 14 Kaplan Street, Petah Tikvah, Israel. Tel.: +972 507242381; fax: +972 39253487. E-mail address: [email protected] (I. Levy). http://dx.doi.org/10.1016/j.vaccine.2014.10.086 0264-410X/© 2014 Elsevier Ltd. All rights reserved.

50,000 people in the United States die every year of complications following influenza [3]. In addition, from October 2004 through September 2012, 830 pediatric influenza-associated deaths were reported in the United States, and 43% of them had no high-risk medical conditions [4]. The seasonal influenza vaccine has a variable efficacy against severe disease (70–80%) depending on the matching of circulating influenza A & B strains [5] and is considered the safest and most effective way to prevent infection [6]. Therefore, healthcare systems worldwide recommend either universal vaccination or vaccination of at-risk populations [7]. Nevertheless, during the 2010–2011 influenza seasons in the US, the rate of vaccination against influenza (one dose or more) in children aged 6 months to 18 years was only 49% [8]. Overall, in children at risk such as those with chronic diseases, the estimated yearly vaccination rate is 10% or lower [9], and in children with asthma, it does not exceed 25% [10]. Potential reasons for non-vaccination in general

N. Peleg et al. / Vaccine 33 (2015) 182–186

and against influenza in particular include insufficient information about the vaccine and its safety, low socioeconomic status, cost of the vaccine, fear of side effects, negative attitudes and prejudices towards immunizations, and low parental education [11–14]. In Israel, the current data on vaccination rates in the general population of children and in children with chronic illnesses or specific risk groups are limited. The current policy in Israel is to offer the vaccine for all adults and children older than 6 months. Although adult and pediatric patients in Israel can be vaccinated for free and can choose between live attenuated vaccine to inactivated one, Stein et al. have shown that vaccination rates in children in Israel were very low: only 4.1% of the children were vaccinated, and in high risk group patients only 6.5% were vaccinated [15]. The objectives of the present study were to determine these rates and to identify the main reasons for non-vaccination in children attending the Institute for Gastroenterology in a major tertiary pediatric medical center. This site was chosen because of the diversity of patients attending the clinic including both healthy children with functional abdominal pain as well as high risk groups such as immunocompromised patients.

2. Methods The study was conducted in the Institute of Gastroenterology, Nutrition, and Liver Diseases at Schneider Children’s Medical Center of Israel between September and October 2011. All visitors were invited to participate, regardless of medical condition or background features of any kind, including both patients visiting the clinic for an initial assessment and patients with long-term illness on a follow-up visit. All children were accompanied by at least one parent. The parents were asked to complete a questionnaire covering demographics, medical history, and influenza vaccination of the child. The questionnaire was written in Hebrew, and the wording was based on a similar study of compliance to vaccinations in children [16]. The demographic variables included patient age and gender, parents’ age, parents’ years of education, ethnic origin of the family, area of residence, and number of persons living in the home. Clinical variables included the child’s disease and its treatment, comorbidities, past surgery or invasive diagnostic procedures, receipt of regular medication, and immunization with the influenza vaccine of the child and other family members during the last flu season. In addition, to discern possible reasons for non-vaccination, the parents were asked to respond to questions regarding their knowledge about the influenza vaccine, their conceptions of its importance and risks, any recommendations or advice regarding the vaccine that they received from medical professionals, their trust in these professionals, and their confidence in the safety of vaccination in general and the flu vaccine in particular. The accessibility to the vaccine and its related costs were also investigated as a possible reason for non-vaccination. The influenza vaccination rate was calculated as the proportion of children vaccinated out of the total sample population. The 95% confidence interval was determined using the conventional formula for binomial distributions close to the normal distribution. The relationship of categorical variables with non-vaccination was analyzed with the chi-square test; t-test and analysis of variance (ANOVA) were used for continuous variables. The proposed reasons for non-vaccination and their frequency were determined. In addition, the demographic data were analyzed against the data on the parents’ personal beliefs and conceptions regarding vaccination. A 2 × 2 table was used for continuity correction, as accepted. Stepwise multivariable logistic regression analysis (P for inclusion 0.1) was performed to identify significant

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Table 1 Demographic characteristics of 273 children attending a gastroenterology clinic by influenza vaccination status. Total n (%)

Child vaccinated n (%)

136 (49.9%) 137 (50.1%)

45 (31.1%) 39 (28.7%)

91 (66.9%) 97 (71.3%)

0.5

42 (15.3%) 81 (30%) 85 (31.1%) 65 (23.6%)

8 (19%) 27 (33.3%) 30 (35.3%) 19 (29.2%)

34 (81%) 54 (66.7%) 55 (64.7%) 46 (70.8%)

0.25

231 (84.6%) 42 (16.4%)

68 (29.4%) 16 (38.1%)

163 (70.6%) 26 (61.9%)

0.28

Father’s education (years) 95 (34.8%) 8–12 13–15 133 (47.7%) 16–18 45 (16.5%)

27 (28.4%) 47 (35.3% 10 (22.2%)

68 (71.6%) 86 (64.7%) 35 (77.8%)

0.2

Mother’s education (years) 85 (31.1%) 8–12 145 (53.2%) 13–15 43 (15.7%) 16–18

26 (30.6%) 45 (31%) 13 (30.2%)

59 (69.4%) 100 (69%) 30 (69.8%)

0.9

No. of siblings 1–2 3–5 >6

35 (32.4%) 39 (27.1%) 10 (47.6%)

73 (67.6%) 105 (72.9%) 11 (52.4%)

0.15

Gender Male Female Age (years) ≤5 6–9 10–14 15–18 Origin Jewish Arab

108 (39.5%) 144 (52.8%) 21 (7.7%)

Child not vaccinated n (%)

P value

predictors of child’s uptake of seasonal influenza immunization. All the demographic and clinical variables studied as well as responses to questions on knowledge about the influenza vaccine, recommendations given, conceptions of its importance, risks accessibility and cost, were examined in addition to age and sex that were forced into the model. A backward selection procedure was then used to generate the final model. All statistical analyses were done with the SPSS version 15.0 (SPSS Inc., Chicago, IL). The study was approved by the institutional review board. All parents signed an informed consent form before inclusion in the study. 3. Results 3.1. Patient characteristics Three-hundred and ten patients were offered to participate in the study and 273 agreed (response rate of 88%). The study cohort consisted of 273 patients, 137 boys and 136 girls, with mean age 10.2 years (SD 4.75). Additional demographic data are presented in Table 1. According to the questionnaire responses, 84 children (30.8%) had influenza vaccinations during the previous influenza season and 189 (69.2%) had not. 3.2. Comorbidities and risk factors The distribution of the patients by underlying disease and vaccination status is shown in Table 2. There were 58 patients (21.2%) with inflammatory bowel disease (IBD), 42 (15.4%) with liver disease, and 173 (63.3%) with other diagnoses. Significant differences were observed in influenza vaccination rate among these patient groups ranging from 50% in IBD patients, 33.3% in participants with liver diseases to 23.7% in patients with other gastrointestinal diseases. Separate analysis of the 15 liver-transplant recipients showed that only 6 (33.3%) had been vaccinated. Overall, 89 patients (32.7%) had received immunosuppressive drugs (glucocorticosteroids, azathioprine or anti-TNF agents), of

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N. Peleg et al. / Vaccine 33 (2015) 182–186

Table 2 Distribution of underlying diseases in the study population by influenza vaccination status. Disease

Total (% of cohort)

Vaccinated

Not vaccinated

Inflammatory bowel disease Crohn’s disease Ulcerative colitis Liver disease Autoimmune hepatitis

58 (21.5%) 35 (13%) 23 (8.5%) 42 (15.4%) 15 (5.5%)

29 (50.0%) 18 (51.4%) 11 (47.8%) 14 (33.3%) 6 (40.0%)

29 (50.0%) 17 (48.6%) 12 (52.2%) 28 (66.7%) 9 (60.0%)

Liver transplant Chronic liver disease Wilson disease Acute liver disease Cirrhosis Congenital hepatic fibrosis

15 (15.5%) 7 (2.5%) 2 (0.7%) 1 (0.35%) 1 (0.35%) 1 (0.35%)

5 (33.3%) 3 (42.9%) 2 (100%) 0 (0%) 0 (0%) 0 (0%)

10 (66.7%) 4 (57.1%) 0 (0%) 1 (0.35%) 1 (100%) 1 (100%)

Other Celiac disease Abdominal pain Constipation Rectal bleeding Familial hypercholesterolemia Failure to thrive GERD Lactose intolerance Recurrent vomiting HP gastritis Peptic ulcer disease Cystic fibrosis Diarrhea Iron deficiency anemia Biliary atresia Choledochal cyst Eosinophilic esophagitis Esophageal atresia

173 (63.3%) 84 (30.7%) 27 (9.8%) 15 (5.5%) 6 (2.0%) 5 (2.0%) 5 (2.0%) 5 (2.0%) 5 (2.0%) 4 (1.2%) 4 (1.2%) 3 (1.0%) 2 (0.7%) 2 (0.7%) 2 (0.7%) 1 (0.35%) 1 (0.35%) 1 (0.35%) 1 (0.35%)

41 (23.7%) 15 (17.9%) 2 (7.4%) 8 (53.3%) 3 (50.0%) 2 (40.0%) 0 (0%) 2 (40.0%) 1 (20.0%) 1 (25.0%) 2 (25.0%) 0 (0%) 1 50.0%) 1 (50.0%) 1 (50.0%) 0 (0%) 0 (0%) 0 (0%) 1 (100%)

132 (76.3%) 69 (82.1%) 25 (92.6%) 7 (46.7%) 3 (50.0%) 3 (60.0%) 5 (100%) 3 (60.0%) 4 (80.0%) 3 (75.0%) 3 (75.0%) 3 (100%) 1 (50.0%) 1 (50.0%) 1 (50.0%) 1 (100%) 1 (100%) 1 (100%) 0 (0%)

Total

273 (100%)

84 (30.8%)

189 (69.2%)

3.4. Parental knowledge and information (Table 3) Most of the study population (91.2%) were aware of the availability of an influenza vaccine, including all parents of children vaccinated and 87.3% of not vaccinated children Recommendations to vaccinate the child were made by the general pediatrician and by the specialist in 85.7% and 77.4% of vaccinated cases, respectively. Much lower respective rates (27.5% and 19.0%) were calculated among parents to not-vaccinated children. Similar differences between parents to vaccinated and not vaccinated children were found in proportion of parents that were informed by their general practitioners of gastroenterologist. Table 3. 3.5. Perceptions and beliefs (Table 4) Further analysis of the questionnaire responses showed that 73.2% of the parents believed that the influenza vaccine is effective in preventing the flu, with a significant (P < 0.001) difference between parents of vaccinated children (92.9%) and non-vaccinated children (64.6%). A lower, though still high, percentage of parents believed that the vaccine is safe (63.3%), substantially higher (84.5% vs. 54.0%) among parents of vaccinated children compared to parents to non-vaccinated children. Parents to non-vaccinated children were significantly (P < 0.001) more likely to consider influenza as a mild diseases or to believe their child in not at risk to develop the disease, compared to parents with a vaccinated child. Proportion of parents who believed that influenza immunization can result in developing influenza was comparable among both groups, exceeding 70%. Table 4. Multivariable logistic regression analysis showed that vaccination of a sibling, recommendation by a physician and yearly vaccination were all significantly associated with influenza vaccination (Table 5).

GERD—gastroesophageal reflux disease, HP—Helicobacter pylori

whom 41 (46%) were vaccinated and 48 (53.9%) were not (P < 0.001). Among the 184 patients (67.3%) who had not received immunosuppressive therapy, 43 (23.4%) were vaccinated and 141 (76.6%) were not (P < 0.001).

3.3. Family vaccination data Sixty-seven parents (24.5%) reported that their children regularly received the annual vaccine against influenza. During the previous flu season, 64 of these children (95.5%) were vaccinated compared to a vaccination rate of only 9.7% among children who were not regularly vaccinated (20/206) (P < 0.001). The vaccination rate for all the participants’ parents was 19%, and 18.6% for all the siblings of the study patients. Yet, only 67.3% of the children (n = 52) whose parents were vaccinated received the vaccine themselves compared to 22.2% of 221 participants whose parents were not vaccinated (P < 0.001).

4. Discussion In this study only 84 (30.8%) of 273 patients had been vaccinated against the influenza virus during the preceding flu season. Vaccination rates were higher in subgroups at high risk for influenza complications, though still not as high as expected: 50% in patients with IBD and 46.1% in immune-compromised patients. These results are higher than those of Melmed et al. [17,18], who reported vaccination rates as low as 28% in patients with IBD. However, their study was conducted in a primarily adult cohort, whereas in children, parental concerns regarding influenza illness might be expected to raise vaccination rate. In immune-compromised patients, influenza infection poses a danger, and seasonal vaccine is recommended by professional organizations worldwide. In the present study, vaccination rates for the immunocompromised group relative to the whole cohort clearly did not comply with these recommendations [5]. In addition, the study cohort

Table 3 Proportion of parent answering affirmatively on questionnaire items on knowledge and information on influenza vaccination by the children’s vaccination status. Parental questionnaire items I am aware of the vaccine availability I was informed about the vaccine by the general physician I was informed about the vaccine by the gastroenterologist I was advised about vaccinating my child by the general physician I was advised about vaccinating my child by the gastroenterologist Vaccination is my first priority I trust the GP and the specialist

Vaccinated (n = 84)

Not vaccinated (n = 189)

n

% of total

n

% of total

84 72 65 72 64 72 78

100.0 85.7 77.4 85.7 76.2 85.7 92.9

165 61 40 52 36 47 173

87.3 32.3 21.2 27.5 19.0 24.9 91.5

P value

Seasonal influenza vaccination rates and reasons for non-vaccination in children with gastrointestinal disorders.

Despite advances in the treatment and prevention of influenza, it is still considered an important cause of morbidity and mortality worldwide. Annual ...
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