Journal of Crohn's and Colitis Advance Access published May 7, 2015 Journal of Crohn's and Colitis, 2015, 1–6 doi:10.1093/ecco-jcc/jjv064 Original Article

Original Article

Vaccination in Inflammatory Bowel Disease Patients: Attitudes, Knowledge, and Uptake Gurtej Malhi,a,b,† Amir Rumman,b,† Reka Thanabalan,a Kenneth Croitoru,a,b Mark S Silverberg,a,b A Hillary Steinhart,a,b Geoffrey C Nguyena,b Mount Sinai Hospital Centre for Inflammatory Bowel Disease, Toronto, ON, Canada bDivision of Gastroenterology, Department of Medicine, University of Toronto, Toronto, ON, Canada

a

†Gurtej Malhi and Amir Rumman should be considered co-first authors. Corresponding author: Geoffrey C Nguyen, MD, PhD, FRCP[C], Mount Sinai Hospital, 600 University Avenue, Rm.437, Toronto, ON, M5G 1X5, Canada. Tel: +1-416-586-4800 ext 2819; fax: +1-416-586-5971; E-mail: [email protected]

Abstract Background:  Immunomodulators and biological agents, used to treat inflammatory bowel disease [IBD], are associated with an increased risk of infection, including vaccine-preventable infections. We assessed patient attitudes towards vaccination, knowledge of vaccine recommendations, and uptake of recommended vaccines. Methods:  Patients attending IBD clinics completed a self-administered, structured, paper-based questionnaire. We collected demographic data, medical and immunisation history, self-reported patient uptake, knowledge, and perceptions of childhood and adult vaccinations. Results:  The prevalence of treatment with biologicals, steroids, thiopurines, and methotrexate among the 300 respondents were 37.3%, 16.0%, 16.0%, and 5.7%, respectively. Self-reported vaccine completion was reported by 45.3% of patients. Vaccination uptake rates were 61.3% for influenza, 10.3% for pneumococcus, 61.0% for hepatitis B, 52.0% for hepatitis A, 26.0% for varicella, 20.7% for meningococcus, 5.3% for herpes zoster, and 11.0% for herpes papilloma virus [females only]. Significant predictors of vaccine completion were annual vaccination review by family physician (odds ratio [OR] = 1.82) or gastroenterologist [OR = 1.72], current steroid use [OR = 1.28], and current or prior treatment with biologicals [OR = 1.42]. The majority of patients reported that the primary responsibility to ensure vaccine completion lies with the patient [41.7%] and the family physician [32.3%]. Uncertainty about indications, fears of side effects, and concerns regarding vaccine safety were the most commonly reported reasons for non-uptake [22.0%, 20.7%, and 5.3%, respectively]. Conclusions:  Uptake of recommended vaccines among IBD patients is suboptimal. Annual vaccination reviews by both family physician and gastroenterologist may improve vaccine uptake. Interventions targeted at improving vaccination uptake in IBD patients are needed. Keywords: IBD; vaccination; vaccination uptake

1. Introduction Treatment of inflammatory bowel disease [IBD] is increasingly reliant on immunosuppressive agents. The use of immunosuppressive

therapy, which includes steroids and biological agents, is associated with a risk of infection, including vaccine-preventable infections.1 In general, adults with IBD should be advised to adhere to standard recommended immunisation schedules, but they should avoid

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2 live-attenuated vaccines while on immunosuppressive therapy.2,3 Current practice recommendations for routine vaccinations in IBD patients are shown in Box 1.4 Despite guideline recommendations for vaccination in IBD patients receiving immunosuppressive therapy,2,5 deficiencies in vaccination have been documented in both adult6,7,8 and paediatric populations.9,10 In a recent study, only 47.7% of IBD patients reported receiving the hepatitis B vaccine, 42.6% the pneumococcal vaccine, and 34.1% the hepatitis A vaccine.8 Suboptimal uptake of vaccinations in IBD patients has been attributed to a host of patient and physician factors. Patient factors include lack of knowledge and counselling about vaccines, concerns about vaccine safety, and lack of appropriate counselling about vaccination safety and efficacy.6,8,11,12 Physician factors include lack of knowledge about vaccination recommendations and uncertainty about the safety of vaccinations in patients on immunosuppressive therapy.13,14,15 Although the deficiencies in vaccination uptake in IBD patients are well documented, there is a paucity of information about patient attitudes towards vaccination, knowledge of vaccination recommendations, and preferences around the provision of vaccination care. Furthermore, predictors of vaccination uptake are not well characterised. As immunosuppressive therapies for IBD continue to evolve, evidence is needed to direct patient education and counselling initiatives and to direct physicians’ attention to areas of patients’ concerns. The aims of this survey study were to identify predictors of vaccination uptake in IBD patients, assess the knowledge and attitudes of IBD patients towards vaccination, and identify patient preferences in the provision of vaccinations.

2. Methods

entries were excluded from the study. The study was approved by the Mount Sinai Hospital Research Ethics Board.

2.2. Survey To assess uptake of vaccinations and knowledge of current vaccination recommendations among IBD patients, we developed and administered a paper-based survey instrument, the Survey on Awareness and Attitudes towards Vaccination in Inflammatory Bowel Disease [SAAV-IBD]. The SAAV-IBD consisted of 46 structured, close-ended questions. It was self-administered, but a research facilitator was available to provide assistance if needed. The survey collected demographic variables, self-reported clinical variables, self-reported vaccination completion, and an assessment of knowledge of current vaccination recommendations. Demographic variables included age, age at IBD diagnosis, employment status, and highest educational attainment. Clinical variables included IBD type [Crohn’s disease, ulcerative colitis, or indeterminate colitis] and current and previous IBD therapy, including use of steroids and biologicals. We also assessed frequency of annual follow-up with a family physician or gastroenterologist. In addition to assessing self-reported uptake of all routine childhood and adult vaccinations, we collected data about knowledge of these vaccinations. This included awareness of the participant’s vaccination status, whether the participant thought the vaccine was live-attenuated, and whether the participant thought the vaccination was indicated for them. We also assessed common misconceptions about vaccinations and vaccine-associated complications. To assess the participant’s attitude towards vaccination, we assessed reasons for non-compliance with vaccination and expectations for vaccination care provision [family physician vs gastroenterologist].

2.1.  Study population

2.3. Outcomes

We surveyed patients presenting for care to the IBD Clinic or Endoscopy Suite at Mount Sinai Hospital’s Centre for Inflammatory Bowel Disease, a specialised, multidisciplinary tertiary care centre in Toronto, Ontario. Patients were recruited between September 1, 2013 and January 31, 2014. The inclusion criteria were informed consent, age over 18 years, and a known diagnosis of Crohn’s disease, ulcerative colitis or indeterminate colitis. Patients with incomplete

The primary outcome was patient-reported completion of all recommended vaccinations. We aimed to identify demographic, clinical, and behavioural predictors of vaccination completion. Secondary outcomes were: uptake of specific adult recommended vaccines, which included hepatitis A  and B, influenza [within past year], varicella, pneumococcal vaccine, meningococcal vaccine, human papilloma virus [only females], and herpes zoster]; knowledge of

Box 1.  Summary of current practice recommendations for routine vaccinations in IBD patients. Vaccines recommended per routine guidelines Tetanus [as part of Td, Tdap, or DTaP] HPV [quadrivalent vaccine against types 6, 11, 16, and 18]a Hepatitis A [single-antigen vaccine or as part of hepatitis A and B combination vaccine] Hepatitis B vaccine Poliomyelitis Pertussis [as part of Tdap or DTaP] Inactivated influenza [trivalent inactivated vaccine, annually] Vaccines recommended prior to initiation of immune-modulator therapy Varicella vaccineb Pneumococcus vaccine [PCV13, PPSV23]c Td, tetanus, diphtheria; Tdap, tetanus, diphtheria, and acellular pertussis; DTaP, paediatric combination vaccine against tetanus, diphtheria, and acellular pertussis; HPV, human papillomavirus; PCV1, 13-valent pneumococcal conjugate vaccine; PPSV23, 23-valent pneumococcal polysaccharide vaccine; CDC-ACIP, Centers for Disease Control and Prevention – Advisory Committee on Immunization Practices. a Both males and females, according to national guidelines. The current Canadian guidelines recommend the HPV vaccine to both males and females between 9 and 26 years of age. b In those without a clear history of chickenpox, shingles, or receipt of two doses of varicella vaccine and seronegative for varicella zoster virus antibody [VZV] IgG. c The specific sequence of administration for these two vaccines varies with patient characteristics and history of prior vaccination, with either as outlined in the CDC-ACIP vaccination schedule [http://www.cdc.gov/vaccines/schedules/downloads/adult/adult-schedule.pdf].

Vaccination In IBD Patients

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vaccinations among IBD patients; and reasons for non-uptake of recommended vaccinations.

2.4.  Statistical analyses Statistical analyses were conducted using SPSS [v 17.0, SPSS Inc., Chicago, IL]. The frequency and distribution of the study population was first determined using descriptive analyses. The appropriate statistical test was then selected: the two sample t-test or the MannWhitney rank sum test was used to compare the distributions of continuous variables between groups, depending on whether the data were normally distributed or not. The chi-square test was used

for categorical variables. ANOVA [analysis of variance] was used for comparisons involving more than two groups. A p-value of < 0.05 was considered significant. Significant variables were identified and used to construct a multivariate nominal logistical regression model for predictors of self-reported vaccine completion.

3. Results A total of 305 patients completed the SAAV-IBD; five patients were excluded from the final analyses due to incomplete data. Table  1 characterises the study population. The mean age at study inclusion

Table 1.  Characteristics of the study population, stratified by self-reported completion of recommended vaccinations. Characteristic

Age at study inclusion, mean [SD] Age at IBD diagnosis, mean [SD] Male Crohn’s disease Ulcerative colitis Indeterminate colitis Employment status  Employed  Retired  Unemployed  Student  Disabled  Homemaker Highest educational attainment   Incomplete high school   Completed high school   Completed college/university   Completed postgraduate studies Current IBD therapy  Steroids  Thiopurine  MTX  Biologicals Previous IBD therapy  Steroids  Thiopurine  MTX  Biologicals Annual family physician visits   Less than once/year   1–3 times per year   4–6 times per year   Over 6 times per year Annual gastroenterologist visits   Less than once/year   1–3 times per year   4–6 times per year   Over 6 times per year Annual vaccine status updates   By family physician   By gastroenterologist Vaccination responsibility   Shared responsibility   Primarily patient   Primarily GP   Primarily GI

Total [n = 300]

Vaccinations Complete

p-value

Yes [n = 136]

No [n = 164]

35.9 [14.3] 23.0 [11.3] 66 [48.5] 83 [61] 49 [36] 4 [2.9]

35.0 [12.3] 23.7 [10.0] 80 [48.8] 90 [54.9] 71 [43.3] 3 [1.8]

NS NS NS NS NS NS

201 [67] 10 [3.3] 9 [3] 54 [18] 15 [5] 8 [2.7]

89 [65.4] 6 [4.4] 4 [2.9] 27 [19.9] 6 [4.4] 4 [2.9]

115 [70.1] 4 [2.4] 5 [3] 27 [16.5] 9 [5.5] 4 [2.4]

NS

6 [2] 68 [22.7] 163 [54.3] 63 [21]

3 [2.2] 34 [25] 68 [50] 31 [22.8]

3 [1.8] 34 [20.7] 95 [57.9] 32 [19.5]

NS

48 [16] 48 [16] 17 [5.7] 112 [37.3]

26 [19.1] 20 [14.7] 7 [5.1] 56 [41.2]

22 [13.4] 28 [17.1] 10 [6.1] 56 [34.1]