Vaccine 32 (2014) 5749–5754
Contents lists available at ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Factors associated with herpes zoster vaccination status and acceptance of vaccine recommendation in community pharmacies Benjamin S. Teeter a , Kimberly B. Garza a , T. Lynn Stevenson b , Margaret A. Williamson b , Megan L. Zeek c , Salisa C. Westrick a,∗ a
Health Outcomes Research and Policy, Harrison School of Pharmacy, Auburn University, 020 James E. Foy Hall, Auburn, AL 36849, United States Pharmacy Practice, Harrison School of Pharmacy, Auburn University, 1202 Walker Building, Auburn, AL 36849, United States c Harrison School of Pharmacy, Auburn University, 2316 Walker Building, Auburn, AL 36849, United States b
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Article history: Received 25 April 2014 Received in revised form 31 July 2014 Accepted 15 August 2014 Available online 27 August 2014 Keywords: Herpes zoster Zostavax® Education Shingles Pharmacy Vaccination
a b s t r a c t Objectives: 1. Identify patient characteristics, awareness and knowledge associated with herpes zoster (HZ) vaccination status. 2. Identify self-reported reasons for not receiving Zostavax® . 3. Assess the impact of a patient education program by measuring post-intervention interest in obtaining the Zostavax® vaccine across reasons for being unvaccinated. Methods: A cross-sectional design with patients aged 60 years or older in 51 community pharmacies in Alabama and Florida was utilized. During the Introductory Pharmacy Practice Experience in summer 2013, 137 immunization-certified student pharmacists provided patient education on HZ and Zostavax® to unvaccinated patients using the Shingles Vaccine Information Statement. An interviewer-administered questionnaire assessed patient awareness of HZ, receipt of recommendations to receive Zostavax® , and patient characteristics as well as vaccination status, reasons for being unvaccinated and interest in obtaining Zostavax® after the educational session. Results: A total of 681 patients participated in a conversation with a student pharmacist regarding their HZ vaccination status. The majority were female (57.6%), white (84.6%), and unvaccinated (73.6%). Results from logistic regression suggest that participants were more likely to be vaccinated if they received a recommendation from a healthcare provider (OR = 5.15), received the influenza vaccine during the previous year (OR = 3.56), or knew that Zostavax® was recommended for individuals over 60 years of age (OR = 3.55). The most frequently provided reasons for being unvaccinated were “haven’t gotten around to it/forgot” (27.2%) and “didn’t know it was needed” (27.1%). After the educational session, the majority (72.5%) of unvaccinated patients were interested in speaking with their pharmacist or physician about receiving Zostavax® . Analysis suggests that interest differed across initial reason for being unvaccinated (2 = 64.44; p < 0.01). Implications/conclusions: Recommendations from healthcare providers are valued by patients and can improve vaccination rates. The patient education program increased interest in receiving Zostavax® and this interest differed depending on the reason provided for being unvaccinated. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction Herpes zoster (HZ) results from the reactivation of the latent varicella zoster virus that affects the sensory nerve ganglion and the peripheral nerve and its branches. Patients with HZ infection
∗ Corresponding author. Tel.: +1 334 844 8314. E-mail addresses: [email protected] (B.S. Teeter), [email protected] (K.B. Garza), [email protected] (T.L. Stevenson), [email protected] (M.A. Williamson), [email protected] (M.L. Zeek), [email protected] (S.C. Westrick). http://dx.doi.org/10.1016/j.vaccine.2014.08.040 0264-410X/© 2014 Elsevier Ltd. All rights reserved.
typically present with a painful, pruritic skin condition on the affected dermatomes that usually develops into a vesicular rash. In the United States, an estimated 1.1 million cases of HZ occur annually, most commonly among older adults, with a 30% lifetime risk of developing HZ. Approximately 10–25% of patients with HZ will experience complications such as persistent pain for weeks to years post infection, known as postherpetic neuralgia (PHN), or ocular involvement, known as herpes zoster opthalmicus (HZO) [1,2]. In 2005, an estimated $566 million was spent on treatment of HZ and this healthcare burden can only be expected to increase as the population ages and thus incidence of HZ increases [2].
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The zoster vaccine, Zostavax® , was licensed in 2006 by the U.S. Food and Drug Administration for prevention of HZ, as well as prevention and treatment of PHN. Since 2008 the Advisory Committee on Immunization Practices (ACIP) has recommended a one-time single dose for all persons aged 60 years of age or older who have no contraindications [1]. Cost-effectiveness of Zostavax® varies depending on patients age and is most cost-effective for patients older than 70 years [3]. Despite the availability of HZ vaccine, a low vaccination rate for HZ is a public health concern. In 2011, only 15.8% of adults aged 60 or older reported having had HZ vaccination [4]. Several studies have explored factors and barriers associated with patients’ Zostavax® vaccination status. The most commonly found rationale for non-receipt of Zostavax® was lack of awareness of zoster vaccine existence and the most common rationale for receipt of the vaccine was recommendation of Zostavax® by a health-care provider [5–9]. Even though Zostavax® is likely to be recommended by physicians [10], it has the lowest rate of on-site administration of all adult vaccines provided by physicians due to referrals to pharmacies to handle Medicare Part D reimbursements [8,11]. Medicare Part D is the only portion of Medicare that provides coverage of Zostavax® but the reimbursement must be done by pharmacies [8]. While literature on pharmacy-based HZ vaccination services is still in an early stage of development, evidence suggests some success of pharmacy interventions to remove barriers to vaccination and increase Zostavax® vaccination rates [12–15]. Because of Part D reimbursement structure, convenience of pharmacy locations and hours, and pharmacists’ established roles as vaccination providers, pharmacists are in an optimal position to identify, educate, and vaccinate eligible patients against HZ [12]. In order to achieve the United States HZ vaccination goal of 30% [16], more research focusing on identifying effective interventions to increase HZ vaccination rate is imperative. Hence, this study implemented and evaluated a brief patient education program in community pharmacies. Specific study objectives were to: (1) identify factors associated with HZ vaccination status among pharmacy patients, (2) identify self-reported reasons for not receiving Zostavax® , and (3) assess post-intervention interests following the patient education program across different reasons for not receiving Zostavax® . 2. Methods The Zostavax® vaccine education intervention was implemented in 51 community pharmacies in Alabama and Florida in May–July 2013 as part of an introductory pharmacy practice experience (IPPE) for second year student pharmacists. To ensure consistency across students and pharmacy sites, students attended a 1-hour orientation, completed assigned readings, watched a demonstration video of patient–student interactions, and practiced patient interviews using the structured questionnaire and the HZ vaccine information statement (VIS) [17] prior to participating in the summer IPPE program. The protocol received an expedited review status from the authors’ Institutional Review Board. 2.1. Data collection A convenience sample of patients aged 60 or older were identified by 137 immunization-certified student pharmacists when picking up their medications from their pharmacy. This group of patients was selected because it is recommended by ACIP that all individuals aged 60 or older with no contraindications receive Zostavax® . Using a structured interviewer-administered questionnaire, students assessed patients’ HZ vaccination status, HZ awareness, and whether they ever received a Zostavax® vaccine
recommendation. Patients who stated that they had not received the vaccine were asked to specify in their own words their reason for not being vaccinated. Students transcribed each patient’s reason verbatim. After transcribing their response, the students proceeded with the Zostavax® vaccine education intervention for unvaccinated patients. The vaccine education intervention consisted of 2 steps. First, the student pharmacist utilized the HZ VIS to inform the patients about the severity of HZ, Zostavax® vaccine effectiveness and contraindications. The HZ VIS is a two-page document provided by the Centers for Disease Control and Prevention. VISs provide information about the risks and benefits of the vaccines, contraindications, what to do if there is an adverse reaction, and where to find additional information about the disease or vaccine. Second, after providing the education intervention, students assessed the patients’ post-intervention interest in discussing getting vaccinated with their pharmacist or physician. Lastly, the supervising pharmacist talked with the patients who were interested in obtaining the Zostavax® vaccine; this last step was not documented, however. Each student was instructed to interview at least 5 patients and their supervising pharmacist preceptor signed off after the interviews. 2.2. Measures and data analyses To identify factors associated with HZ vaccination status (Objective 1), this study measured patient characteristics, pharmacy characteristics and patients’ HZ knowledge and awareness. Chisquare analyses were used to explore relationships between these factors and vaccination status. Next, factors that had statistically significant relationships with the dependent variable were then entered into a logistic regression model with vaccination status as the dependent variable. For the second objective, which was to report patients’ reason for not being vaccinated, an open-ended question was asked and students recorded verbatim patients’ reason for not receiving the vaccine. The research team then classified the responses into different unique reasons and reported the frequency for each reason. For the third objective, after the vaccine education intervention was completed, students assessed patient post-intervention interests in speaking with their physician or pharmacist about getting the Zostavax® vaccine. Chi-square analysis was conducted to examine differences in the effect of the education intervention on the post-intervention interests among patients across reasons for not vaccinating. An a priori alpha of 75
188 (27.6) 199 (29.2) 142 (20.9) 152 (22.3)
160 (85.1) 134 (67.3) 96 (67.6) 111 (73.0)
28 (14.9) 65 (32.7) 46 (32.4) 41 (27.0)
White Non-white
576 (84.6) 105 (15.4)
411 (71.3) 90 (85.7)
165 (28.7) 15 (14.3)
Yes No
659 (96.8) 22 (3.2)
481 (73.0) 20 (90.9)
178 (27.0) 2 (9.1)
Yes No
360 (52.9) 321 (47.1)
250 (69.4) 251 (78.2)
110 (30.6) 70 (21.8)
0–1 2–3 4–9 >10
79 (11.6) 99 (14.5) 224 (32.9) 279 (41.0)
64 (81.0) 64 (64.6) 168 (75.0) 205 (73.5)
15 (19.0) 35 (35.4) 56 (25.0) 74 (26.5)
Grocery/mass merchandiser Independent Specialized clinic Standalone chain
145 (21.3) 192 (28.2) 80 (11.7) 264 (38.8)
103 (71.1) 146 (76.0) 56 (70.0) 196 (74.2)
42 (28.9) 46 (24.0) 24 (30.0) 68 (25.8)
Metropolitan area core Metropolitan area high commuting Micropolitan area Small town/rural area
498 (73.1) 56 (8.5) 105 (15.4) 20 (3.0)
360 (72.3) 43 (76.8) 82 (76.6) 16 (80.0)
138 (27.7) 13 (23.2) 25 (23.4) 4 (20.0)
Yes No
509 (74.7) 172 (25.3)
344 (67.6) 157 (91.3)
165 (32.4) 15 (8.7)
Yes No
641 (94.1) 35 (5.9)
465 (72.5) 32 (91.4)
176 (27.5) 3 (8.6)
Yes No
552 (81.1) 113 (16.9)
393 (71.2) 95 (84.1)
159 (28.8) 18 (15.9)
Yes No
464 (68.1) 217 (31.9)
301 (64.9) 200 (92.2)
163 (35.1) 17 (7.8)
Yes No
263 (38.6) 418 (61.4)
134 (51.0) 367 (87.8)
129 (49.0) 51 (12.2)
Demographic characteristics
Sex
0.777
Age
>0.001
0.002
Race
Has a regular physician
0.061
Has Medicare prescription drug benefits
0.010
Number of pharmacy visits during the past 6 months
0.088
Type of pharmacy
0.644
Rurality of pharmacy frequented
0.646
Received influenza vaccine last year
>0.001
Knowledge and awarenessa Heard of shingles
0.014
Known anyone with shingles
0.005
Aware that vaccine is recommended over 60
>0.001
Recommended to receive vaccine by health care provider
a
2 (p-Value)
>0.001
Few participants who responded “not sure” to knowledge/awareness questions were omitted from any analyses.
prescription drug benefits (52.9%). About 40% of the participants reported visiting a pharmacy greater than 10 times during the previous 6 months, of which the greatest percentage were standalone chain pharmacies (38.8%). The majority (74.7%) reported having received the influenza vaccination the previous year. As for their knowledge and awareness, the majority of participants had heard of HZ (94.1%), had known someone with HZ (81.1%), and knew that the Zostavax® vaccine was recommended for people over the age
of 60 (68.1%) but had not received a recommendation from a health care provider to receive the vaccination (61.4%). Of 681 participants, 501 (73.6%) had not been vaccinated. The second and third columns of Table 1 show the number (%) of unvaccinated and vaccinated patients by their demographic characteristics and HZ knowledge and awareness. Results of chi square analyses suggest that HZ vaccination status differed across age groups, races, whether patients have Medicare prescription drug
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Table 2 Participant characteristics, knowledge, and awareness associated with vaccination status (unadjusted versus adjusted logistic regression). Variable
Unadjusted OR (95% CI)
p-Value
Adjusted OR (95% CI)
p-Value
60–64 65–69 70–74 >75
1.00 2.77 (1.68–4.57) 2.74 (1.61–4.67) 2.11 (1.23–3.62)
>0.001 >0.001 0.007
1.00 1.82 (1.01–3.29) 1.65 (0.88–3.14) 1.30 (0.67–2.51)
0.048 0.127 0.438
Non-white White
1.00 2.41 (1.35–4.28)
0.003
1.00 1.51 (0.75–3.01)
0.246
No Yes
1.00 1.58 (1.12–2.23)
0.010
1.00 1.45 (0.94–2.23)
0.097
No Yes
1.00 5.02 (2.86–8.80)
>0.001
1.00 3.56 (1.93–6.57)
>0.001
No Yes
1.00 4.04 (1.22–13.35)
0.022
1.00 1.46 (0.37–5.73)
0.585
No Yes
1.00 2.14 (1.25–3.65)
0.006
1.00 1.34 (0.68–2.63)
0.395
No Yes
1.00 6.37 (3.75–10.83)
>0.001
1.00 3.55 (1.98–6.37)
>0.001
No Yes
1.00 6.93 (4.74–10.13)
>0.001
5.15 (3.42–7.75)
>0.001
Age
Race
Has Medicare prescription drug benefits
Received influenza vaccine last year
Heard of shingles
Known anyone with shingles
Aware that vaccine is recommended over 60
Recommended to receive vaccine by health care provider
OR: odds ratio; CI: confidence interval.
benefits, and last year’s influenza vaccination status. Analyses of participant knowledge and awareness variables also suggested that those who had heard of HZ, had known anyone with HZ, were aware of the recommendation, and had received a recommendation were more likely to be vaccinated against HZ. Table 2 shows further analysis into the participant characteristics and knowledge and awareness variables that were identified as having a relationship with participant vaccination status. Results from logistic regression suggest that a participant who received a recommendation from a health care provider was more likely to have received the Zostavax® vaccine than someone who had not received a recommendation (OR = 5.15). Additionally, it was significantly more likely that a participant would have received the Zostavax® vaccine if they had received the influenza vaccination last year (OR = 3.56) or knew that the vaccine was recommended for individuals 60 years of age or older (OR = 3.55).
3.3. Objective 3: Post-intervention interest in speaking with a healthcare provider Table 3 (2nd and 3rd columns) shows participant’s postintervention interest in speaking with a pharmacist or physician by previously stated reason for being unvaccinated. Of the 129 participants who reported not getting around to it or forgetting, 118 (91.5%) said they were interested in speaking with their pharmacist or physician about receiving the vaccine. Furthermore, a vast majority (79.4%) of those who reported not having received a physician’s recommendation and 75.8% of those who did not know it was Table 3 Patients’ self-reported reasons for being unvaccinated and post-intervention interest in speaking with their physician or pharmacist about receiving zoster vaccine (N = 473)a . Initial reason for being unvaccinated
Number (%)
Post-intervention interest in speaking with the pharmacist about receiving vaccine Number (% of those reporting this reason)
Didn’t get around to it/forgot Didn’t know it was needed Financial reasons Just don’t want it Doctor didn’t recommend Don’t like shots/needles Not at risk of getting shingles Could cause side effects Doctor recommended against
129 (27.2)
118 (91.5)
128 (27.1) 47 (9.9) 40 (8.5) 34 (7.2) 26 (5.5) 25 (5.3)
97 (75.8) 34 (72.3) 19 (47.5) 27 (79.4) 13 (50.0) 10 (40.0)
23 (4.9) 21 (4.4)
14 (60.9) 11 (52.4)
3.2. Objective 2: Self-reported reasons for being unvaccinated A total of 473 unvaccinated participants provided a reason why they were unvaccinated (Table 3, 1st column). Almost all participants provided one reason that was the main influence in their decision not to be vaccinated. For few participants who provided multiple reasons, researchers trained in qualitative analysis classified the responses into one of the groups used for analysis based on the wording of the responses. The largest percentage of the unvaccinated population stated that they just hadn’t gotten around to it or had forgotten (27.2%) with the second largest group reporting that they did not know it was needed (27.1%).
a
2 = 64.44; p < 0.01.
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needed were interested in speaking with their pharmacist or physician after the education. Additionally, more than half of those who reported financial reasons (72.3%) or potential side effects (60.9%) were interested in speaking with their pharmacist or physician after the education intervention. Chi-square analysis suggests that post-intervention interests differed across initial reasons for being unvaccinated.
4. Discussion This study identified factors associated with HZ vaccination status, determined self-reported reasons for not receiving the Zostavax® vaccine, and assessed post-intervention interests after receiving brief patient education. This study determined the impact of an education intervention on interest in receiving the vaccine across self-reported reasons for being unvaccinated. Even though this study did not assess patients’ decisions to be vaccinated against HZ, it is a good first step to assess their intention. Consistent with previous research, this study found that patients were more likely to have received the vaccination if it had been recommended by a health care provider [5,6,18]. This reiterates the point that recommendations from health care providers are valued by patients and therefore, encouraging our health care providers to recommend the Zostavax® vaccination may help to increase vaccination rates. Additionally, similar to previous research, patients who were aware the vaccine was recommended for individuals aged 60 years or older were also significantly more likely to have received the vaccination [6,19]. Increasing the amount of publicity highlighting this recommendation may help to increase vaccination rates as well. Overall, the educational intervention was beneficial, with 72.5% of the individuals who provided a reason for being unvaccinated stating that they were interested in speaking with a pharmacist or physician about receiving the vaccination after the education intervention. This finding suggests that a brief education intervention provided by a student pharmacist in a community pharmacy setting is not only appreciated and seen as a learning experience for patients but can also be effective in increasing interest in the vaccine. It is possible that patients saw value in the education provided and realized the importance of talking with a healthcare provider about receiving the vaccine. In real-world community pharmacy settings, a brief interaction between a patient and pharmacist may encourage the patient to receive the vaccination or at least motivate them to speak with their primary care physician about the vaccine. Additionally, for those pharmacies that supervise student interns, this type of brief education intervention would be a great opportunity for vaccination-certified student pharmacists to reach out to patients. Interestingly, the level of interest sparked by the intervention varied according to initial reason given for not having previously been vaccinated. The three reasons for not having been vaccinated that were associated with the greatest amount of interest in speaking with a healthcare provider about receiving the vaccine included “didn’t get around to it/forgot,” “didn’t know it was needed” and “doctor didn’t recommend.” For those who had not received the vaccination because they had not gotten around to it or had forgotten about it, the educational intervention served as a cue to action [20]. A vast majority of individuals with this reason (91.5%) were interested in speaking with a pharmacist or physician about getting vaccinated after receiving the reminder. Providing this reminder in a pharmacy where an individual can actually receive the vaccine may have led these individuals to be vaccinated immediately following the education session. In addition, given the delayed benefit of receiving the vaccine (prevents future disease) and more immediate costs (money, time, pain of injection, etc.), patients may opt to
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forgo vaccination because the benefits do not seem to outweigh the costs. Emphasizing the benefits by stressing the risk and severity of HZ may be the nudge these individuals need in order to take action. For those who didn’t know the vaccine was needed, the intervention provided necessary knowledge of the recommendations for vaccination. For those patients whose reason for not previously being vaccinated was not having received a recommendation from their physician, the educational intervention may have acted as an endorsement from a health care provider regarding the importance of receiving the vaccine. Other reasons for not having been vaccinated were associated with much less interest post-intervention. These include fear of shots/needles, perception of low risk for getting shingles, and “just don’t want it.” Patients with these reasons may not benefit from this type of intervention. Other methods for overcoming these barriers and negative perceptions may be necessary to increase rate of vaccination among this subgroup. Finally, providing an education intervention in a pharmacy where a pharmacist can provide the vaccination may have led some of the 343 patients to receive the vaccination during that same pharmacy visit. Although data was not collected on this aspect, the fact that so many participants wanted to speak with their pharmacist or physician suggests that there was a great interest in receiving the vaccination after the education intervention. Research utilizing the Theory of Reasoned Action and the Theory of Planned Behavior has established that behavioral intentions are a good predictor of future behavior [21–23] and therefore, the interest of the participants and intention to speak with their pharmacist that day about the vaccine may have very well led to actual receipt of the vaccine. This study is not without limitations. The use of a convenience sample of individuals who were willing to participate may have resulted in self-selection bias and may have resulted in a sample that was not representative of the population. For example, the vaccination rate among this sample was higher than the national average. Additionally, social desirability may have biased their responses to questions. This may have been especially true when asked if they were interested in speaking with the pharmacist or a physician about receiving the vaccine since there was no action required on the part of the patient and no data was collected on whether they actually spoke with any vaccination provider. Another potential limitation of this study is the use of student pharmacists for the intervention. This may have affected the consistency of the education intervention that was delivered. Attempts were made to reduce this by requiring students to go through training and practice to ensure intervention fidelity. Finally, other factors, such as education level, may have contributed to vaccination status and were not explored.
5. Conclusion About 1 in 4 study participants (26.4%) were vaccinated against HZ. Participants were more likely to be vaccinated if they had received a recommendation from a health care provider, knew of the recommendation that all individuals 60 years of age or older should receive the vaccine, and received the influenza vaccine during the previous year. Among unvaccinated participants, the majority reported that they did not know the vaccine was recommended for them or that they had simply not gotten around to receiving the vaccine. After a brief education intervention with a student pharmacist in a community pharmacy, the majority of patients were interested in speaking with a healthcare provider about receiving the vaccine; but the post-intervention interests in speaking to someone about receiving the vaccine differed across reasons given for not having been previously vaccinated. Community pharmacies are in an excellent position to increase awareness
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of Zostavax® vaccine recommendations among the elderly population. This increased awareness may lead to improvement in the HZ vaccination rate in the US. Conflict of interest statement All authors have reviewed the final draft of this manuscript and have declared that they have no conflicts of interest. References [1] Harpaz R, Ortega-Sanchez IR, Seward JF. Prevention of herpes zoster: recommendations of the advisory committee on immunization practices (acip). MMWR Recomm Rep 2008;57(RR–5):1–30. [2] Soni A, Hill SC. Average health care use and expenses for Shingles among the U.S. Civilian noninstitutionalized population. In: Statistical brief #194. Rockville, MD: Agency for Healthcare Research and Quality; 2003–2005. [3] Rothberg MB, Virapongse A, Smith KJ. Cost-effectiveness of a vaccine to prevent herpes zoster and postherpetic neuralgia in older adults. Clin Infect Dis 2007;44(10):1280–8. [4] Centers for Disease Control and Prevention. Noninfluenza vaccination coverage among adults—United States, 2011. MMWR morbidity and mortality weekly report, vol. 62. Washington, DC: Centers for Disease Control and Prevention; 2013. p. 66–72. [5] Lu P, Euler G, Jumaan A, Harpaz R. Herpes zoster vaccination among adults aged 60 years or older in the united states, 2007: uptake of the first new vaccine to target seniors. Vaccine 2009;27(6):882–7. [6] Joon Lee T, Hayes S, Cummings DM, Cao Q, Carpenter K, Heim L, Edwards H. Herpes zoster knowledge, prevalence, and vaccination rate by race. J Am Board Fam Med 2013;26(1):45–51. [7] Lu PJ, Euler GL, Harpaz R. Herpes zoster vaccination among adults aged 60 years and older, in the U.S., 2008. Am J Prev Med 2011;40(2):e1–6. [8] Hurley LP, Lindley MC, Harpaz R, Stokley S, Daley MF, Crane LA, et al. Barriers to the use of herpes zoster vaccine. Ann Intern Med 2010;152(9):555–60. [9] Jung JJ, Elkin ZP, Li X, Goldberg JD, Edell AR, Cohen MN, et al. Increasing use of the vaccine against zoster through recommendation and administration by ophthalmologists at a city hospital. Am J Ophthalmol 2013;155(5):787–95.
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Contents lists available at ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Factors associated with herpes zoster vaccination status and acceptance of vaccine recommendation in community pharmacies Benjamin S. Teeter a , Kimberly B. Garza a , T. Lynn Stevenson b , Margaret A. Williamson b , Megan L. Zeek c , Salisa C. Westrick a,∗ a
Health Outcomes Research and Policy, Harrison School of Pharmacy, Auburn University, 020 James E. Foy Hall, Auburn, AL 36849, United States Pharmacy Practice, Harrison School of Pharmacy, Auburn University, 1202 Walker Building, Auburn, AL 36849, United States c Harrison School of Pharmacy, Auburn University, 2316 Walker Building, Auburn, AL 36849, United States b
a r t i c l e
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Article history: Received 25 April 2014 Received in revised form 31 July 2014 Accepted 15 August 2014 Available online 27 August 2014 Keywords: Herpes zoster Zostavax® Education Shingles Pharmacy Vaccination
a b s t r a c t Objectives: 1. Identify patient characteristics, awareness and knowledge associated with herpes zoster (HZ) vaccination status. 2. Identify self-reported reasons for not receiving Zostavax® . 3. Assess the impact of a patient education program by measuring post-intervention interest in obtaining the Zostavax® vaccine across reasons for being unvaccinated. Methods: A cross-sectional design with patients aged 60 years or older in 51 community pharmacies in Alabama and Florida was utilized. During the Introductory Pharmacy Practice Experience in summer 2013, 137 immunization-certified student pharmacists provided patient education on HZ and Zostavax® to unvaccinated patients using the Shingles Vaccine Information Statement. An interviewer-administered questionnaire assessed patient awareness of HZ, receipt of recommendations to receive Zostavax® , and patient characteristics as well as vaccination status, reasons for being unvaccinated and interest in obtaining Zostavax® after the educational session. Results: A total of 681 patients participated in a conversation with a student pharmacist regarding their HZ vaccination status. The majority were female (57.6%), white (84.6%), and unvaccinated (73.6%). Results from logistic regression suggest that participants were more likely to be vaccinated if they received a recommendation from a healthcare provider (OR = 5.15), received the influenza vaccine during the previous year (OR = 3.56), or knew that Zostavax® was recommended for individuals over 60 years of age (OR = 3.55). The most frequently provided reasons for being unvaccinated were “haven’t gotten around to it/forgot” (27.2%) and “didn’t know it was needed” (27.1%). After the educational session, the majority (72.5%) of unvaccinated patients were interested in speaking with their pharmacist or physician about receiving Zostavax® . Analysis suggests that interest differed across initial reason for being unvaccinated (2 = 64.44; p < 0.01). Implications/conclusions: Recommendations from healthcare providers are valued by patients and can improve vaccination rates. The patient education program increased interest in receiving Zostavax® and this interest differed depending on the reason provided for being unvaccinated. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction Herpes zoster (HZ) results from the reactivation of the latent varicella zoster virus that affects the sensory nerve ganglion and the peripheral nerve and its branches. Patients with HZ infection
∗ Corresponding author. Tel.: +1 334 844 8314. E-mail addresses: [email protected] (B.S. Teeter), [email protected] (K.B. Garza), [email protected] (T.L. Stevenson), [email protected] (M.A. Williamson), [email protected] (M.L. Zeek), [email protected] (S.C. Westrick). http://dx.doi.org/10.1016/j.vaccine.2014.08.040 0264-410X/© 2014 Elsevier Ltd. All rights reserved.
typically present with a painful, pruritic skin condition on the affected dermatomes that usually develops into a vesicular rash. In the United States, an estimated 1.1 million cases of HZ occur annually, most commonly among older adults, with a 30% lifetime risk of developing HZ. Approximately 10–25% of patients with HZ will experience complications such as persistent pain for weeks to years post infection, known as postherpetic neuralgia (PHN), or ocular involvement, known as herpes zoster opthalmicus (HZO) [1,2]. In 2005, an estimated $566 million was spent on treatment of HZ and this healthcare burden can only be expected to increase as the population ages and thus incidence of HZ increases [2].
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The zoster vaccine, Zostavax® , was licensed in 2006 by the U.S. Food and Drug Administration for prevention of HZ, as well as prevention and treatment of PHN. Since 2008 the Advisory Committee on Immunization Practices (ACIP) has recommended a one-time single dose for all persons aged 60 years of age or older who have no contraindications [1]. Cost-effectiveness of Zostavax® varies depending on patients age and is most cost-effective for patients older than 70 years [3]. Despite the availability of HZ vaccine, a low vaccination rate for HZ is a public health concern. In 2011, only 15.8% of adults aged 60 or older reported having had HZ vaccination [4]. Several studies have explored factors and barriers associated with patients’ Zostavax® vaccination status. The most commonly found rationale for non-receipt of Zostavax® was lack of awareness of zoster vaccine existence and the most common rationale for receipt of the vaccine was recommendation of Zostavax® by a health-care provider [5–9]. Even though Zostavax® is likely to be recommended by physicians [10], it has the lowest rate of on-site administration of all adult vaccines provided by physicians due to referrals to pharmacies to handle Medicare Part D reimbursements [8,11]. Medicare Part D is the only portion of Medicare that provides coverage of Zostavax® but the reimbursement must be done by pharmacies [8]. While literature on pharmacy-based HZ vaccination services is still in an early stage of development, evidence suggests some success of pharmacy interventions to remove barriers to vaccination and increase Zostavax® vaccination rates [12–15]. Because of Part D reimbursement structure, convenience of pharmacy locations and hours, and pharmacists’ established roles as vaccination providers, pharmacists are in an optimal position to identify, educate, and vaccinate eligible patients against HZ [12]. In order to achieve the United States HZ vaccination goal of 30% [16], more research focusing on identifying effective interventions to increase HZ vaccination rate is imperative. Hence, this study implemented and evaluated a brief patient education program in community pharmacies. Specific study objectives were to: (1) identify factors associated with HZ vaccination status among pharmacy patients, (2) identify self-reported reasons for not receiving Zostavax® , and (3) assess post-intervention interests following the patient education program across different reasons for not receiving Zostavax® . 2. Methods The Zostavax® vaccine education intervention was implemented in 51 community pharmacies in Alabama and Florida in May–July 2013 as part of an introductory pharmacy practice experience (IPPE) for second year student pharmacists. To ensure consistency across students and pharmacy sites, students attended a 1-hour orientation, completed assigned readings, watched a demonstration video of patient–student interactions, and practiced patient interviews using the structured questionnaire and the HZ vaccine information statement (VIS) [17] prior to participating in the summer IPPE program. The protocol received an expedited review status from the authors’ Institutional Review Board. 2.1. Data collection A convenience sample of patients aged 60 or older were identified by 137 immunization-certified student pharmacists when picking up their medications from their pharmacy. This group of patients was selected because it is recommended by ACIP that all individuals aged 60 or older with no contraindications receive Zostavax® . Using a structured interviewer-administered questionnaire, students assessed patients’ HZ vaccination status, HZ awareness, and whether they ever received a Zostavax® vaccine
recommendation. Patients who stated that they had not received the vaccine were asked to specify in their own words their reason for not being vaccinated. Students transcribed each patient’s reason verbatim. After transcribing their response, the students proceeded with the Zostavax® vaccine education intervention for unvaccinated patients. The vaccine education intervention consisted of 2 steps. First, the student pharmacist utilized the HZ VIS to inform the patients about the severity of HZ, Zostavax® vaccine effectiveness and contraindications. The HZ VIS is a two-page document provided by the Centers for Disease Control and Prevention. VISs provide information about the risks and benefits of the vaccines, contraindications, what to do if there is an adverse reaction, and where to find additional information about the disease or vaccine. Second, after providing the education intervention, students assessed the patients’ post-intervention interest in discussing getting vaccinated with their pharmacist or physician. Lastly, the supervising pharmacist talked with the patients who were interested in obtaining the Zostavax® vaccine; this last step was not documented, however. Each student was instructed to interview at least 5 patients and their supervising pharmacist preceptor signed off after the interviews. 2.2. Measures and data analyses To identify factors associated with HZ vaccination status (Objective 1), this study measured patient characteristics, pharmacy characteristics and patients’ HZ knowledge and awareness. Chisquare analyses were used to explore relationships between these factors and vaccination status. Next, factors that had statistically significant relationships with the dependent variable were then entered into a logistic regression model with vaccination status as the dependent variable. For the second objective, which was to report patients’ reason for not being vaccinated, an open-ended question was asked and students recorded verbatim patients’ reason for not receiving the vaccine. The research team then classified the responses into different unique reasons and reported the frequency for each reason. For the third objective, after the vaccine education intervention was completed, students assessed patient post-intervention interests in speaking with their physician or pharmacist about getting the Zostavax® vaccine. Chi-square analysis was conducted to examine differences in the effect of the education intervention on the post-intervention interests among patients across reasons for not vaccinating. An a priori alpha of 75
188 (27.6) 199 (29.2) 142 (20.9) 152 (22.3)
160 (85.1) 134 (67.3) 96 (67.6) 111 (73.0)
28 (14.9) 65 (32.7) 46 (32.4) 41 (27.0)
White Non-white
576 (84.6) 105 (15.4)
411 (71.3) 90 (85.7)
165 (28.7) 15 (14.3)
Yes No
659 (96.8) 22 (3.2)
481 (73.0) 20 (90.9)
178 (27.0) 2 (9.1)
Yes No
360 (52.9) 321 (47.1)
250 (69.4) 251 (78.2)
110 (30.6) 70 (21.8)
0–1 2–3 4–9 >10
79 (11.6) 99 (14.5) 224 (32.9) 279 (41.0)
64 (81.0) 64 (64.6) 168 (75.0) 205 (73.5)
15 (19.0) 35 (35.4) 56 (25.0) 74 (26.5)
Grocery/mass merchandiser Independent Specialized clinic Standalone chain
145 (21.3) 192 (28.2) 80 (11.7) 264 (38.8)
103 (71.1) 146 (76.0) 56 (70.0) 196 (74.2)
42 (28.9) 46 (24.0) 24 (30.0) 68 (25.8)
Metropolitan area core Metropolitan area high commuting Micropolitan area Small town/rural area
498 (73.1) 56 (8.5) 105 (15.4) 20 (3.0)
360 (72.3) 43 (76.8) 82 (76.6) 16 (80.0)
138 (27.7) 13 (23.2) 25 (23.4) 4 (20.0)
Yes No
509 (74.7) 172 (25.3)
344 (67.6) 157 (91.3)
165 (32.4) 15 (8.7)
Yes No
641 (94.1) 35 (5.9)
465 (72.5) 32 (91.4)
176 (27.5) 3 (8.6)
Yes No
552 (81.1) 113 (16.9)
393 (71.2) 95 (84.1)
159 (28.8) 18 (15.9)
Yes No
464 (68.1) 217 (31.9)
301 (64.9) 200 (92.2)
163 (35.1) 17 (7.8)
Yes No
263 (38.6) 418 (61.4)
134 (51.0) 367 (87.8)
129 (49.0) 51 (12.2)
Demographic characteristics
Sex
0.777
Age
>0.001
0.002
Race
Has a regular physician
0.061
Has Medicare prescription drug benefits
0.010
Number of pharmacy visits during the past 6 months
0.088
Type of pharmacy
0.644
Rurality of pharmacy frequented
0.646
Received influenza vaccine last year
>0.001
Knowledge and awarenessa Heard of shingles
0.014
Known anyone with shingles
0.005
Aware that vaccine is recommended over 60
>0.001
Recommended to receive vaccine by health care provider
a
2 (p-Value)
>0.001
Few participants who responded “not sure” to knowledge/awareness questions were omitted from any analyses.
prescription drug benefits (52.9%). About 40% of the participants reported visiting a pharmacy greater than 10 times during the previous 6 months, of which the greatest percentage were standalone chain pharmacies (38.8%). The majority (74.7%) reported having received the influenza vaccination the previous year. As for their knowledge and awareness, the majority of participants had heard of HZ (94.1%), had known someone with HZ (81.1%), and knew that the Zostavax® vaccine was recommended for people over the age
of 60 (68.1%) but had not received a recommendation from a health care provider to receive the vaccination (61.4%). Of 681 participants, 501 (73.6%) had not been vaccinated. The second and third columns of Table 1 show the number (%) of unvaccinated and vaccinated patients by their demographic characteristics and HZ knowledge and awareness. Results of chi square analyses suggest that HZ vaccination status differed across age groups, races, whether patients have Medicare prescription drug
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Table 2 Participant characteristics, knowledge, and awareness associated with vaccination status (unadjusted versus adjusted logistic regression). Variable
Unadjusted OR (95% CI)
p-Value
Adjusted OR (95% CI)
p-Value
60–64 65–69 70–74 >75
1.00 2.77 (1.68–4.57) 2.74 (1.61–4.67) 2.11 (1.23–3.62)
>0.001 >0.001 0.007
1.00 1.82 (1.01–3.29) 1.65 (0.88–3.14) 1.30 (0.67–2.51)
0.048 0.127 0.438
Non-white White
1.00 2.41 (1.35–4.28)
0.003
1.00 1.51 (0.75–3.01)
0.246
No Yes
1.00 1.58 (1.12–2.23)
0.010
1.00 1.45 (0.94–2.23)
0.097
No Yes
1.00 5.02 (2.86–8.80)
>0.001
1.00 3.56 (1.93–6.57)
>0.001
No Yes
1.00 4.04 (1.22–13.35)
0.022
1.00 1.46 (0.37–5.73)
0.585
No Yes
1.00 2.14 (1.25–3.65)
0.006
1.00 1.34 (0.68–2.63)
0.395
No Yes
1.00 6.37 (3.75–10.83)
>0.001
1.00 3.55 (1.98–6.37)
>0.001
No Yes
1.00 6.93 (4.74–10.13)
>0.001
5.15 (3.42–7.75)
>0.001
Age
Race
Has Medicare prescription drug benefits
Received influenza vaccine last year
Heard of shingles
Known anyone with shingles
Aware that vaccine is recommended over 60
Recommended to receive vaccine by health care provider
OR: odds ratio; CI: confidence interval.
benefits, and last year’s influenza vaccination status. Analyses of participant knowledge and awareness variables also suggested that those who had heard of HZ, had known anyone with HZ, were aware of the recommendation, and had received a recommendation were more likely to be vaccinated against HZ. Table 2 shows further analysis into the participant characteristics and knowledge and awareness variables that were identified as having a relationship with participant vaccination status. Results from logistic regression suggest that a participant who received a recommendation from a health care provider was more likely to have received the Zostavax® vaccine than someone who had not received a recommendation (OR = 5.15). Additionally, it was significantly more likely that a participant would have received the Zostavax® vaccine if they had received the influenza vaccination last year (OR = 3.56) or knew that the vaccine was recommended for individuals 60 years of age or older (OR = 3.55).
3.3. Objective 3: Post-intervention interest in speaking with a healthcare provider Table 3 (2nd and 3rd columns) shows participant’s postintervention interest in speaking with a pharmacist or physician by previously stated reason for being unvaccinated. Of the 129 participants who reported not getting around to it or forgetting, 118 (91.5%) said they were interested in speaking with their pharmacist or physician about receiving the vaccine. Furthermore, a vast majority (79.4%) of those who reported not having received a physician’s recommendation and 75.8% of those who did not know it was Table 3 Patients’ self-reported reasons for being unvaccinated and post-intervention interest in speaking with their physician or pharmacist about receiving zoster vaccine (N = 473)a . Initial reason for being unvaccinated
Number (%)
Post-intervention interest in speaking with the pharmacist about receiving vaccine Number (% of those reporting this reason)
Didn’t get around to it/forgot Didn’t know it was needed Financial reasons Just don’t want it Doctor didn’t recommend Don’t like shots/needles Not at risk of getting shingles Could cause side effects Doctor recommended against
129 (27.2)
118 (91.5)
128 (27.1) 47 (9.9) 40 (8.5) 34 (7.2) 26 (5.5) 25 (5.3)
97 (75.8) 34 (72.3) 19 (47.5) 27 (79.4) 13 (50.0) 10 (40.0)
23 (4.9) 21 (4.4)
14 (60.9) 11 (52.4)
3.2. Objective 2: Self-reported reasons for being unvaccinated A total of 473 unvaccinated participants provided a reason why they were unvaccinated (Table 3, 1st column). Almost all participants provided one reason that was the main influence in their decision not to be vaccinated. For few participants who provided multiple reasons, researchers trained in qualitative analysis classified the responses into one of the groups used for analysis based on the wording of the responses. The largest percentage of the unvaccinated population stated that they just hadn’t gotten around to it or had forgotten (27.2%) with the second largest group reporting that they did not know it was needed (27.1%).
a
2 = 64.44; p < 0.01.
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needed were interested in speaking with their pharmacist or physician after the education. Additionally, more than half of those who reported financial reasons (72.3%) or potential side effects (60.9%) were interested in speaking with their pharmacist or physician after the education intervention. Chi-square analysis suggests that post-intervention interests differed across initial reasons for being unvaccinated.
4. Discussion This study identified factors associated with HZ vaccination status, determined self-reported reasons for not receiving the Zostavax® vaccine, and assessed post-intervention interests after receiving brief patient education. This study determined the impact of an education intervention on interest in receiving the vaccine across self-reported reasons for being unvaccinated. Even though this study did not assess patients’ decisions to be vaccinated against HZ, it is a good first step to assess their intention. Consistent with previous research, this study found that patients were more likely to have received the vaccination if it had been recommended by a health care provider [5,6,18]. This reiterates the point that recommendations from health care providers are valued by patients and therefore, encouraging our health care providers to recommend the Zostavax® vaccination may help to increase vaccination rates. Additionally, similar to previous research, patients who were aware the vaccine was recommended for individuals aged 60 years or older were also significantly more likely to have received the vaccination [6,19]. Increasing the amount of publicity highlighting this recommendation may help to increase vaccination rates as well. Overall, the educational intervention was beneficial, with 72.5% of the individuals who provided a reason for being unvaccinated stating that they were interested in speaking with a pharmacist or physician about receiving the vaccination after the education intervention. This finding suggests that a brief education intervention provided by a student pharmacist in a community pharmacy setting is not only appreciated and seen as a learning experience for patients but can also be effective in increasing interest in the vaccine. It is possible that patients saw value in the education provided and realized the importance of talking with a healthcare provider about receiving the vaccine. In real-world community pharmacy settings, a brief interaction between a patient and pharmacist may encourage the patient to receive the vaccination or at least motivate them to speak with their primary care physician about the vaccine. Additionally, for those pharmacies that supervise student interns, this type of brief education intervention would be a great opportunity for vaccination-certified student pharmacists to reach out to patients. Interestingly, the level of interest sparked by the intervention varied according to initial reason given for not having previously been vaccinated. The three reasons for not having been vaccinated that were associated with the greatest amount of interest in speaking with a healthcare provider about receiving the vaccine included “didn’t get around to it/forgot,” “didn’t know it was needed” and “doctor didn’t recommend.” For those who had not received the vaccination because they had not gotten around to it or had forgotten about it, the educational intervention served as a cue to action [20]. A vast majority of individuals with this reason (91.5%) were interested in speaking with a pharmacist or physician about getting vaccinated after receiving the reminder. Providing this reminder in a pharmacy where an individual can actually receive the vaccine may have led these individuals to be vaccinated immediately following the education session. In addition, given the delayed benefit of receiving the vaccine (prevents future disease) and more immediate costs (money, time, pain of injection, etc.), patients may opt to
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forgo vaccination because the benefits do not seem to outweigh the costs. Emphasizing the benefits by stressing the risk and severity of HZ may be the nudge these individuals need in order to take action. For those who didn’t know the vaccine was needed, the intervention provided necessary knowledge of the recommendations for vaccination. For those patients whose reason for not previously being vaccinated was not having received a recommendation from their physician, the educational intervention may have acted as an endorsement from a health care provider regarding the importance of receiving the vaccine. Other reasons for not having been vaccinated were associated with much less interest post-intervention. These include fear of shots/needles, perception of low risk for getting shingles, and “just don’t want it.” Patients with these reasons may not benefit from this type of intervention. Other methods for overcoming these barriers and negative perceptions may be necessary to increase rate of vaccination among this subgroup. Finally, providing an education intervention in a pharmacy where a pharmacist can provide the vaccination may have led some of the 343 patients to receive the vaccination during that same pharmacy visit. Although data was not collected on this aspect, the fact that so many participants wanted to speak with their pharmacist or physician suggests that there was a great interest in receiving the vaccination after the education intervention. Research utilizing the Theory of Reasoned Action and the Theory of Planned Behavior has established that behavioral intentions are a good predictor of future behavior [21–23] and therefore, the interest of the participants and intention to speak with their pharmacist that day about the vaccine may have very well led to actual receipt of the vaccine. This study is not without limitations. The use of a convenience sample of individuals who were willing to participate may have resulted in self-selection bias and may have resulted in a sample that was not representative of the population. For example, the vaccination rate among this sample was higher than the national average. Additionally, social desirability may have biased their responses to questions. This may have been especially true when asked if they were interested in speaking with the pharmacist or a physician about receiving the vaccine since there was no action required on the part of the patient and no data was collected on whether they actually spoke with any vaccination provider. Another potential limitation of this study is the use of student pharmacists for the intervention. This may have affected the consistency of the education intervention that was delivered. Attempts were made to reduce this by requiring students to go through training and practice to ensure intervention fidelity. Finally, other factors, such as education level, may have contributed to vaccination status and were not explored.
5. Conclusion About 1 in 4 study participants (26.4%) were vaccinated against HZ. Participants were more likely to be vaccinated if they had received a recommendation from a health care provider, knew of the recommendation that all individuals 60 years of age or older should receive the vaccine, and received the influenza vaccine during the previous year. Among unvaccinated participants, the majority reported that they did not know the vaccine was recommended for them or that they had simply not gotten around to receiving the vaccine. After a brief education intervention with a student pharmacist in a community pharmacy, the majority of patients were interested in speaking with a healthcare provider about receiving the vaccine; but the post-intervention interests in speaking to someone about receiving the vaccine differed across reasons given for not having been previously vaccinated. Community pharmacies are in an excellent position to increase awareness
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of Zostavax® vaccine recommendations among the elderly population. This increased awareness may lead to improvement in the HZ vaccination rate in the US. Conflict of interest statement All authors have reviewed the final draft of this manuscript and have declared that they have no conflicts of interest. References [1] Harpaz R, Ortega-Sanchez IR, Seward JF. Prevention of herpes zoster: recommendations of the advisory committee on immunization practices (acip). MMWR Recomm Rep 2008;57(RR–5):1–30. [2] Soni A, Hill SC. Average health care use and expenses for Shingles among the U.S. Civilian noninstitutionalized population. In: Statistical brief #194. Rockville, MD: Agency for Healthcare Research and Quality; 2003–2005. [3] Rothberg MB, Virapongse A, Smith KJ. Cost-effectiveness of a vaccine to prevent herpes zoster and postherpetic neuralgia in older adults. Clin Infect Dis 2007;44(10):1280–8. [4] Centers for Disease Control and Prevention. Noninfluenza vaccination coverage among adults—United States, 2011. MMWR morbidity and mortality weekly report, vol. 62. Washington, DC: Centers for Disease Control and Prevention; 2013. p. 66–72. [5] Lu P, Euler G, Jumaan A, Harpaz R. Herpes zoster vaccination among adults aged 60 years or older in the united states, 2007: uptake of the first new vaccine to target seniors. Vaccine 2009;27(6):882–7. [6] Joon Lee T, Hayes S, Cummings DM, Cao Q, Carpenter K, Heim L, Edwards H. Herpes zoster knowledge, prevalence, and vaccination rate by race. J Am Board Fam Med 2013;26(1):45–51. [7] Lu PJ, Euler GL, Harpaz R. Herpes zoster vaccination among adults aged 60 years and older, in the U.S., 2008. Am J Prev Med 2011;40(2):e1–6. [8] Hurley LP, Lindley MC, Harpaz R, Stokley S, Daley MF, Crane LA, et al. Barriers to the use of herpes zoster vaccine. Ann Intern Med 2010;152(9):555–60. [9] Jung JJ, Elkin ZP, Li X, Goldberg JD, Edell AR, Cohen MN, et al. Increasing use of the vaccine against zoster through recommendation and administration by ophthalmologists at a city hospital. Am J Ophthalmol 2013;155(5):787–95.
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