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Perception of immunizations and vaccine recommendation sources for persons living with HIV compared with persons without HIV
SCIENCE AND PRACTICE Journal of the American Pharmacists Association 59 (2019) S39eS46
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RESEARCH
Perception of immunizations and vaccine recommendation sources for persons living with HIV compared with persons without HIV Alex R. Mills*, Stephanie J. Arnett, Mu Shan, Catherine Simmons, Monica L. Miller a r t i c l e i n f o
a b s t r a c t
Article history: Received 7 September 2018 Accepted 8 May 2019 Available online 24 June 2019
Objectives: To measure and compare the perception of immunizations, immunization status, and recommendation sources in persons living with HIV (PLWHs) and persons without HIV and determine a strategy for improving immunization rates by increasing awareness of pharmacy services. Design: A 19-item survey based on the Health Belief Model assessed patients’ perceptions and recommendation sources regarding immunization acceptance for specific vaccines: Tdap, pneumococcal, and hepatitis B (HepB). Survey items used a 5-point Likert-type scale assessing participants’ perceptions, with questions identifying participants’ most trusted sources of immunization information and patient demographics. Survey questions were designed to identify perceived susceptibility and severity of vaccine-preventable illness, barriers, benefits, and self-efficacy regarding immunization acceptance, and sources of patient-trusted immunization information. Setting and participants: Survey recruitment occurred in Indiana and included any patient 18 years of age or older picking up medications at a specialty pharmacy predominantly serving PLWHs or a traditional community chain pharmacy. Main outcome measures: Primary outcomes included perceived barriers to immunization acceptance obtained from Likert-type scale questions, patient-reported immunization rates of selected vaccines (Tdap, pneumococcal pneumonia, and HepB), and trusted immunization recommendation sources. Logistic regression was performed to model association between perceived barriers, HIV status, and immunization recommendation sources. Results: A total of 142 participants (68 PLWHs, 74 persons without HIV) completed the survey. PLWHs were more likely to have immunization barriers, but this was not statistically significant (odds ratio 2.537, 95% confidence interval 0.585e10.996). Both participant groups reported “family doctor” as the most trusted source, with only 5% selecting “pharmacist.” Significantly fewer PLWHs reported completing the HepB series (18% vs. 52%; P ¼ 0.0224). Conclusion: PLWHs possess barriers to immunization acceptance similar to persons without HIV yet report lower rates of HepB vaccine completion. Although pharmacists were less frequently selected as the most trusted source, additional studies on percptions of pharmacists’ role in immunizing PLWHs should be considered. © 2019 American Pharmacists Association®. Published by Elsevier Inc. All rights reserved.
As part of the Healthy People 2020 (HP2020) initiative to improve health outcomes for the U.S. population, one area of focus is increasing immunization rates and decreasing the incidence of vaccine-preventable diseases.1 For healthy adults, Disclosure: The authors declare no relevant conflicts of interest or financial relationships. Funding: This work was supported in part by an American Pharmacists Association Foundation Incentive Grant for Pharmacy Resident Research. The funder had no role in the design, data collection, interpretation, or report writing. Previous presentations: Midyear Clinical Meeting, American Society of Health-System Pharmacists, Orlando, FL, 2017; Annual Meeting, American
HP2020 set a goal of immunizing 80% to 90% of the population for 3 specific vaccines: pneumococcal, tetanusediphtheriaeacellular pertussis (Tdap), and hepatitis B (HepB).2 Recommendations and immunization schedules for Pharmacists Association, Nashville, TN, 2018; Great Lakes Pharmacy Resident Conference, West Lafayette, IN, 2018; and Virtual Poster Symposium, American College of Clinical Pharmacy, 2018. * Correspondence: Alex R. Mills, 873 West Carmel Drive, Carmel, IN 46032 E-mail address: [email protected] (A.R. Mills). ORCID Alex R. Mills: https://orcid.org/0000-0003-4236-2299.
https://doi.org/10.1016/j.japh.2019.05.008 1544-3191/© 2019 American Pharmacists Association®. Published by Elsevier Inc. All rights reserved.
SCIENCE AND PRACTICE A.R. Mills et al. / Journal of the American Pharmacists Association 59 (2019) S39eS46
Key Points Background: Healthy People 2020 has developed metrics to improve immunization rates for the U.S. population, and this includes persons living with HIV (PLWHs). Despite PLWHs being indicated to receive many of the same inactivated vaccines as the persons without HIV, immunization rates are considerably less than Healthy People 2020’s goal for Tdap, pneumococcal pneumonia, and hepatitis B (HepB), specifically for this population. PLWHs may possess barriers to immunization acceptance that differ from persons without HIV, yet such barriers have not been specifically identified in this special population. Findings: PLWHs possess the same barriers to immunization acceptance as persons without HIV, yet still report receiving fewer vaccines (HepB in particular). Although pharmacists are highly accessible to this population, few of the PLWHs viewed them as trusted immunization recommendation sources, suggesting opportunities to better market and expand pharmacist-driven immunization services. Further research is warranted to assess the perceived role of pharmacists in providing immunization services for this population, along with evaluation of the impact that pharmacists can have on improving PLWH immunization rates through the use of targeted marketing campaigns.
95% of PLWH were missing measurable titers for pertussis from another indicated vaccine, Tdap.8 Similar to HepB, pneumococcal and Tdap are recommended for this population and are safe regardless of a PLWH’s CD4 count.3 Barriers and perceptions to immunization acceptance, including misconceptions on vaccine efficacy and safety, perceived benefit of routine vaccination, and others, have been studied extensively in persons without HIV yet few studies have assessed or identified barriers in PLWHs. Observational studies have been conducted to evaluate predictors and barriers to influenza immunization in PLWHs, but none measured pneumococcal, Tdap, and HepB vaccination.9,10 Furthermore, those studies identified physicians as the primary source of immunization recommendation, but no studies have sought to identify what impact pharmacists may have on immunization acceptance in this population.10 Pharmacists are considered to be among the most trusted medical professionals in the United States, credited to their high level of accessibility to the public and consideration as medication experts.11 Regarding pharmacist-delivered immunizations, the literature supports their positive impact on immunization rates in other populations, yet no studies were identified that reviewed pharmacists administering or recommending immunizations to PLWHs.12,13 Objectives The objectives of this study were to (1) quantitatively measure and compare PLWHs’ perception of immunization needs with persons without HIV and (2) determine trusted immunization recommendation sources for PLWHs. In addition, investigators sought to obtain the current immunization status of PLWHs compared with those without HIV. Methods Theoretical framework
special populations have also been published by the Centers for Disease Control and Prevention and the Infectious Diseases Society of America in an effort to protect patients with specialty conditions, including human immunodeficiency virus (HIV) infection.2,3 Owing to the compromised immune system for persons living with HIV (PLWHs), this patient population is at an increased risk of 2 specific conditions: opportunistic infections and vaccine-preventable illnesses.2 Despite the widespread use of effective antiretroviral therapy and integration of pneumococcal, Tdap, and HepB vaccination recommendations into the national HIV treatment guidelines, PLWHs continue to be deficient in reaching the HP2020 goal.1,2 In PLWHs, immunization rates are significantly reduced for HepB and pneumococcal vaccines.4,5 For example, all individuals, including PLWHs, are indicated for a 3-dose series of the HepB virus vaccine regardless of immune status according to CD4 count.6 However, a review of studies observing PLWHs who completed the series found rates ranging from 42% to 76%, whereas persons without HIV have achieved the HP2020 goal with 90% completing the series.4,7 Furthermore, PLWH vaccination rates for pneumococcal in other developed countries, such as France and the United Kingdom, are well below those of persons without HIV, averaging a suboptimal rate of 65%.5 Data from a French multicenter study also identified that
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The Health Belief Model depicted in Figure 1 is a published psychosocial model frequently used to predict health behaviors. First developed in the 1950s and later adapted in 1988, its core assumptions are based on the understanding that a patient will perform a health-related behavior change after an internal assessment of 6 constructs: perceived susceptibility, severity, benefits, barriers, cues to action, and self-efficacy.14,15 Setting and participants Research was conducted at 2 community pharmacies from a large nationwide chain in Indianapolis, Indiana. One of the sites is designated as a specialty pharmacy that predominantly provides holistic care for PLWH and dispenses an average of 300 prescriptions per day. Unlike many specialty pharmacies, this one is open to the public, allowing for walk-in service as well as the shipment of HIV and non-HIV medications upon patient request. The pharmacy staff at this site received cultural competency and health literacyefocused training developed by the chain’s Clinical Programs and Training Department. The second is a traditional (nonspecialty) community pharmacy within the same chain that serves a larger volume of patients dispensing an average of 500 prescriptions per day. The traditional
SCIENCE AND PRACTICE Immunization perceptions in persons with HIV
Modifying Factors
Likelihood of Action
Age Sex Knowledge
Perceived Benefits Vs. Barriers to Change
Perceived Susceptibility of Disease
Perceived Threat of Disease
Likelihood of Behavioral Change
Perceived Self-Efficacy to Perform Action
Cues to Action: Education Symptoms Referral Sources
Patient Perceptions
Figure 1. Conceptual diagram of health belief model, adapted from Glanz et al.20
community pharmacy provides the standard of care available at most community pharmacies and the staff also received the same cultural competency and health literacy training as the specialty pharmacy, which the investigators thought would potentially create a more welcoming environment for participant recruitment. All adult patients waiting in-store or picking up a prescription at either pharmacy were asked to voluntarily complete a questionnaire. Data collection and recruitment occurred from November 2017 to March 2018. All participants who started the questionnaire and completed 90% of survey items were included in analysis except those who were under the age of 18 years, did not report their age, or were not picking up a medication for their personal use. Study participation was voluntary and was granted exempt status by Purdue University’s Institutional Review Board. Design The questionnaire consisted of 19 items, which asked about demographics (age, sex, gender identity), health conditions (defined as taking at least 1 medication for any of the following conditions: hypertension, diabetes mellitus, dyslipidemia, HIV treatment, HIV prevention (preexposure prophylaxis), and chronic obstructive pulmonary disease or asthma), and perceived barriers to immunization acceptance. Questionnaire items were designed to identify (1) perceived susceptibility and severity to vaccine-preventable illness, (2) barriers, benefits, and self-efficacy related to immunization acceptance, and (3) trusted sources for immunization recommendations. The majority of questions used a 5-point Likert-type scale (from 1, strongly disagree, to 5, strongly agree) with multiplechoice questions for demographics, health conditions, self-reported doses of HepB vaccine, and trusted sources for immunization recommendations. The questions created for the questionnaire were adapted from a 2016 study completed by Harrison et al., in which a questionnaire was used to identify positive and negative predictors of immunization acceptance.10 The questions related to negative predictors were associated with common beliefs and misconceptions associated with influenza vaccination. Ultimately, it was interpreted that those beliefs were an indirect
barrier to immunization acceptance and aligned with the modifying variables of the Health Belief Model’s construct of “perceived barriers,” compelling us to create negatively worded statements to assess this construct. Specifically, participants were provided the statements “Vaccines will worsen my other health conditions” and “Vaccines are just a scam for the pharmaceutical companies to get more money.” These questions were designed to identify if participants possessed negative beliefs about vaccines that may act as an indirect barrier to receiving a vaccine. To assess “perceived benefits,” we constructed statements that assessed if participants believed the action of receiving an immunization would reduce the risk or severity of a vaccine-preventable illness. Specifically, the provided statements “Getting vaccinated is a good way to keep myself and others healthy” and “Vaccines prevent me from getting sick” were included in the questionnaire to identify positive beliefs about vaccines that serve as indirect markers aligning with the perceived benefit construct of the Health Belief Model. Finally, “perceived severity” was assessed by asking participants to agree or disagree with statements that inferred that participants possessed the belief immunizations can prevent hospitalizations or severe illness, an indirect measure of participants’ perception of potential consequences if not vaccinated. Statements that assessed participants’ “perceived severity” included “If I don’t keep up with my vaccinations, I could end up very sick/in the hospital” and a negatively worded statement, “Diseases that are covered by vaccines are not that serious.” Ultimately, it was hypothesized that participants who possessed these beliefs are likely to refuse or avoid immunizations because they would act as an indirect barrier to making a health behavior change (e.g., receiving an immunization). Accessibility and quality assurance Several steps were taken to improve questionnaire accessibility to account for differences in patients’ comfort level with technology, socioeconomic status, transportation barriers (e.g., unable to physically visit the pharmacy), educational level, health literacy, and preferred language. Questionnaires were available in 3 formats: (1) tablet computer application, S41
SCIENCE AND PRACTICE A.R. Mills et al. / Journal of the American Pharmacists Association 59 (2019) S39eS46
(2) paper questionnaire, (3) and telephone questionnaire. The questionnaire was available in both English and Spanish. To maintain privacy, participants completed the questionnaire independently and anonymously, with responses cleared from the device before research personnel reclaimed possession. Spanish questions were validated for consistency and understanding by a Spanish-speaking pharmacy technician. For participants unable to read or if health literacy was a concern, a student pharmacist read the questionnaire aloud to the participant in a consultation room to maintain privacy. Otherwise, trained recruitment personnel were instructed not to assist the participants with completing or answering the questionnaire. In addition, approximately 70% of patients at the specialty pharmacy have medications shipped to their place of residence. The pharmacy technician in charge of contacting these participants was trained on proper recruitment and delivery of the questionnaire over the telephone. Implementation and recruitment Study data were collected and managed with the use of Redcap (Research Electronic Data Capture) version 8.1.13, an electronic data capture tool hosted at Indiana University’s Clinical and Translational Sciences Institute. Redcap is a secure web-based application designed to support data capture for research studies, supporting cloud-based and offline data collection via tablet computers, as well as automated export procedures to common statistical packages.16 Research personnel and student pharmacists were trained on its use and scripting for recruitment based on approved institutional review board methods. To assess ease of use, wording, and elapsed time to complete the questionnaire, 6 pharmacy technicians and 3 student pharmacists working at both sites completed a pilot questionnaire before its implementation for study participants. After successful pilot testing and personnel training, recruitment occurred of all participants picking up prescriptions via completion of the questionnaire on tablet computer, paper, or telephone. In an effort to maintain consistency in the recruitment process across the various forms of the questionnaire, the offer to participate was provided at the conclusion of the in-person sale of their medications or after the shipment process has been completed. Outcome measures The primary outcome included perceived barriers to immunization acceptance obtained from Likert-type scale questions. Secondary outcomes included patient-reported immunization rates of selected vaccines (Tdap, pneumococcal [PCV13 and PPSV23], and HepB) and trusted immunization recommendation sources. Logistic regression was performed to model association between perceived barriers, HIV status, and immunization recommendation sources. Statistical analysis Before analysis, an estimated sample size calculation was performed in G-Power version 3.1 with the use of a 95% CI. We assumed a standard deviation of 2 in each sample’s response to Likert-type scale questions and mean difference of 1 for all Likert-type scale “perceived barriers” questions via an S42
independent 2-sample t test. To meet at least 80% power, the estimated sample size needed was at least 64 participants in each group (PLWHs vs. persons without HIV) Baseline participant characteristics and outcome measures were summarized as frequency and percentage for categoric variables and median and interquartile range (IQR) for nonnormal continuous variables. The difference between groups was compared by means of Wilcoxon-Mann-Whitney test for nonnormal continuous variables, t test for normal continuous variable, and chi-square test for categorical variables. The dependent variable “perceived barriers” was defined as “yes” if participants chose “agree” or “strongly agree” in any of the 3 barriers questions (“vaccines will worsen my other conditions,” “vaccines are just a scam for the pharmaceutical companies to make get more money,” and “Vaccines don’t work”); otherwise their response was considered to be “no.” Because the outcome was dichotomous in nature, a logistic regression model was used to measure the difference in perceived barriers between PLWHs and persons without HIV, adjusting for demographic and covariates (number of comorbidities, immunization recommendation sources). Descriptive statistics (mean ± SD) and an independent t test were analyzed for responses to “perceived barriers,” stratified into each individual survey item. In addition, the percentage of respondents selecting “agree” and “strongly agree” (defined as “yes” to perceived barriers) and any other response (defined as “no” to perceived barriers) were also reported for each related survey item. Immunization recommendation sources were regrouped as “family doctor,” “specialty doctor,” and “other” because of small samples in some of the categories. A 5% significance level was used for all tests. Analyses were performed with the use of SAS version 9.4 (SAS Institute, Cary, NC).
Results Demographics and comorbidities There were 142 participants who completed the questionnaire provided at both pharmacies: 68 classified as PLWHs and 74 classified as non-HIV for analysis purposes. The majority, 95% (134/142), of participants completed the questionnaire in person, whereas the remaining 5% (8/142) participated over the telephone. After implementing exclusion criteria (primarily due to participants not completing at least 90% of survey items) after data collection, 67 PLWHs and 64 persons without HIV remained for final analysis in the regression model, as depicted in Figure 2. All participants who completed the questionnaire over the telephone met inclusion criteria and were included in analysis. There were 11 participants excluded from the regression model due to missing values for their age range. Participant demographics are listed in Table 1. A majority (92.6%) of the PLWH cohort were male and the overall median age range was 45 to 54 years. Comparatively, the cohort without HIV was younger (median age range 35 to 44 years) and included slightly more men than women (58% and 42%, respectively). A Wilcoxon-Mann-Whitney scores analysis comparing PLWHs versus persons without HIV number of comorbidities was performed (Table 1), because the data were not normally distributed. Fisher exact test was performed for categorical values that contained a small sample size (n 5).
SCIENCE AND PRACTICE Immunization perceptions in persons with HIV
regarding perceived barriers, there was no significant difference between groups for perceived benefits (survey question, “These vaccines keep me healthy”) or perceived severity (survey question, “If I don’t keep up with my vaccinations, I could end up very sick and in the hospital”).
Parcipants compleng quesonnaire (n=142)
Classified as PLWH
Classified as non-HIV
(n=68)
(n=74)
Vaccine history
Met Exclusion Criteria
Met Exclusion Criteria
(n=1)
(n=10)
Met Inclusion Criteria
Met Inclusion Criteria
(n=67)
(n=64)
Missing age range data
Missing age range data
(n=8)
(n=3)
Included in Logisisc Regression
Included in Logisc Regression
(n=59)
(n=61)
Figure 2. Participant inclusion/exclusion criteria flowchart.
The PLWH cohort had a median of 1 comorbidity (IQR 0e2), which was defined as number of reported health conditions minus “HIV treatment,” and the cohort without HIV had a median of zero comorbidities (IQR 0e1.5). There was no significant difference between groups (P ¼ 0.33).
For the 3 selected vaccines (Tdap, pneumococcal, and HepB), there was no significant difference between PLWHs and persons without HIV in receiving Tdap or at least 1 dose of HepB, but PLWHs reported receiving pneumococcal vaccination more than the non-HIV cohort (Table 1). Further analysis demonstrated significantly more persons without HIV completed the HepB series than PLWHs (52.9% vs. 18.2%; P ¼ 0.022). Vaccination administration and recommendation sources Several of the categories (i.e., “pharmacist,” “website,” “nurse,” “other health professional”) for trusted recommendation sources had very low responses. To run an analysis to identify significant differences between groups, these categories were regrouped into a single category labeled “other.” After regrouping (Table 3), the most commonly selected recommendation source was “family doctor,” with 62% of PLWHs selecting this option versus 70% of persons without HIV (P ¼ 0.0006). Of note, “pharmacist” only accounted for 5% (n ¼ 6) of overall responses, with 3% of PLWHs selecting this option versus 6% of persons without HIV (n ¼ 2 and 4, respectively). Discussion
Perceived barriers Descriptive statistics and t test results for the individual “perceived barriers” items are presented in Table 2. No significant differences between PLWHs and persons without HIV who completed this survey were identified. Descriptive statistics of perceived barrier survey items and percentage of participants defined as having or not having perceived barriers to immunization acceptance are reported in Table 2, with no significant difference between groups. Incorporating survey responses into the logistic analysis (Table 3) revealed that the perceived barriers PLWHs may hold were not statistically significantly different from those of persons without HIV (odds ratio [OR] 2.537, 95% CI 0.585e10.996). Covariates of immunization recommendation sources and number of comorbidities also did not meet statistical significance in the logistic regression model for perceived barriers. Of note, participants aged 18 to 34 years had statistically significantly less perceived barriers than those 55 years of age and older, whereas those aged 35e54 years had statistically significantly more perceived barriers (ORs 0.382 and 8.406, respectively). Perceived benefits and severity The difference in perceived benefits and severity between groups were also analyzed with the use of an independent t test (Table 2). Similar to the logistic regression model
This study demonstrated overall that PLWHs do not have significantly more or different barriers to immunizations compared with persons without HIV. Although previous studies demonstrated PLWHs are less likely to accept routine and indicated immunizations, this study is, to our knowledge, the first seeking to quantitatively identify patients’ specific barriers between PLWHs and persons without HIV in the same geographic location.9,10 This study also addresses the gap in literature related to whom PLWHs trust for an immunization recommendation, expanding beyond the physician or HIV specialist and including the pharmacist, who has an everincreasing role in the HIV continuum of care.17 Because this study’s data demonstrated that both groups possess the same barriers to receiving immunizations, current educational programs and materials could be used to promote immunization acceptance in the PLWH population. A notable barrier for immunizations in the persons without HIV concerns misconceptions regarding their safety, efficacy, and value of vaccinations.18 Addressing these misconceptions by providing evidence-based recommendations and “debunking” myths regarding vaccines should be provided by health professionals, especially those who care for PLWHs. A multicenter study by Handy et al. identified that a significant barrier to vaccine acceptance was lack of accurate information regarding currently licensed vaccines.19 Participants in their focus groups reported an increased likelihood of accepting a vaccine recommendation when given reliable information from their S43
SCIENCE AND PRACTICE A.R. Mills et al. / Journal of the American Pharmacists Association 59 (2019) S39eS46
Table 1 Participant demographics, vaccine history, and trusted recommendation sources, n (%) Variable Age range, y 18e34 35e54 55 Sex Male Female Gender identity Male Female Transgender Do not identify as any listed Insurance status Employer-provided Medicaid Medicare HIP/HIP 2.0 Insurance through family’s plan No insurance Comorbidities Hypertension Diabetes Dyslipidemia COPD/Asthma None of these Number of comorbidities, median (IQR) Patient-reported vaccine history, n (%) Tdap Pneumococcala Hepatitis B Hepatitis B series completionb Vaccine recommendation sourcec Family doctor Specialty doctor Othersd
PLWH (n ¼ 67)
Non-HIV (n ¼ 64)
5 (9) 30 (53) 22 (39)
26 (49) 17 (42) 10 (19)
63 (92.6) 5 (7.4)
38 (57.6) 28 (42.4)
62 (92.5) 5 (7.5) e e
38 (57.6) 28 (42.4) e e
10 4 37 16 0 1
(14.7) (5.9) (54.4) (23.5)
33 7 11 3 10 1
(50.8) (10.8) (16.9) (4.6) (15.4) (1.5)
21 10 23 8 0 1
(30.9) (14.7) (33.8) (11.8) (0e2)
19 12 13 3 35 0
(29.9) (18.5) (20.0) (4.6) (53.8) (0e1.5)
0.852 0.643 0.018 0.208 < 0.001 0.33
31 51 22 4
(45.6) (75.0) (32.4) (18.2)
34 20 17 9
(54.0) (31.7) (27.0) (52.9)
0.486 < 0.001 0.451 0.022
P value < 0.001
< 0.001
< 0.001
0.006
(1.5)
41 (62) 18 (27) 7 (11)
45 (70) 2 (3) 17 (27)
< 0.001
Abbreviations: COPD, chronic obstructive pulmonary disease; HIP, Healthy Indiana Plan; HIV, human immunodeficiency virus; IQR, interquartile range; PLWH, persons living with HIV; Tdap, tetanusediphtheriaeacellular pertussis. a Listed in questionnaire as “Pneumonia (Prevnar, Pneumovax).” b Defined as reporting 3 doses; total sample: PLWH ¼ 22, non-HIV ¼ 17. c Listed in questionnaire as “Which is your primary source for information on vaccines that you trust?” d Others include pharmacist, news, social media, nurse, other health professional, TV or movie celebrity, friends/family, website.
health care provider.19 We hypothesize that transferring this information to PLWH providers with more frequent vaccine education can potentially increase vaccine acceptance in this patient population. We used the Health Belief Model in designing our survey with the objective of adequately identifying and comparing health behaviors between PLWHs and persons without HIV, yet our results showed no statistically significant difference.20 Despite these results, our study supports previous literature and data related to immunizations in PLWHs in several ways. Survey participants’ self-reported immunization rates closely match national and global data depicting PLWHs as significantly underimmunized, particularly concerning HepB and Tdap.1,8 Of note, a majority of PLWH participants reported receiving at least 1 pneumococcal immunization. This may be attributed to the increased integration of immunization histories into the Electronic Medical Record or increased awareness of PLWHs being indicated for immunization. Conversely, significantly more persons without HIV completed the HepB 3-dose series compared with PLWHs, supporting the national evidence of PLWHs being underimmunized for this disease.
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These findings are also similar to results from Harrison et al., identifying physicians as the primary source for trusted immunization recommendations in PLWHs, although this was not statistically significant compared with persons without HIV.10 Unlike the study by Harrison et al., we assessed patients’ perception of the role pharmacists may play in providing PLWHs these recommended immunizations, yet few participants in either group selected the pharmacist as the trusted immunization recommendation source. This finding identifies an opportunity for improved marketing of pharmacist immunization services. Pharmacists are uniquely positioned to positively affect immunization rates, including the immunocompromised and PLWHs.11-13 Their high level of accessibility, level of expertise, and overall reputation make them a valuable resource for achieving the HP2020 goals.1 This study identified that PLWHs share similar barriers to immunizations compared with persons without HIV; combining this information with current vaccination programs and more frequent, regular immunization assessments could warrant expansion of pharmacist-driven immunization services for PLWHs. Pharmacists in most states have access to vaccine registries, and
SCIENCE AND PRACTICE Immunization perceptions in persons with HIV
Table 2 Comparison of PLWH and non-HIV survey responses to perceived barriers, benefits, and severity related to immunization acceptancea PLWH n ¼ 67
Survey item
Mean Perceived barriers “Vaccines don’t work.” “Vaccines are just a scam for the pharmaceutical company to make more money.” “Vaccines will worsen my other health conditions.” Perceived benefits “Vaccines keep me healthy.” “Getting vaccinated is a good way to keep myself and others healthy.” Perceived severity “If I don’t keep up with my vaccinations, I could end up very sick or in the hospital.”
P valued
Non-HIV n ¼ 64 Yesb
Noc
Mean
Yesb
Noc
1.71 ± 1.23 1.78 ± 1.24
9.7% 9.0%
90.3% 91.0%
1.70 ± 1.20 1.56 ± 1.07
12.1% 12.1%
87.9% 87.9%
0.976 0.294
1.71 ± 1.16
13.4%
86.6%
1.63 ± 1.08
6.2%
93.8%
0.697
4.51 ± 0.88 4.48 ± 1.01
89.6% 87.5%
10.4% 12.5%
4.3 ± 1.11 4.38 ± 1.06
87.5% 83.3%
12.5% 16.7%
0.249 0.567
3.96 ± 1.5
70.1%
29.9%
4.08 ± 1.17
68.9%
31.1%
0.604
Abbreviations as in Table 1. a Survey responses completed on 5-point Likert-type scale from 1 ¼ strongly disagree to 5 ¼ strongly agree. b Defined as selecting “strongly agree” or “agree” on survey items. c Defined as selecting any Likert-type scale option besides “strongly agree” or “agree” on survey items. d P values based on difference of 2 means from Likert-type scale questions according to independent t test.
using this tool in pharmacies or pharmacist-driven clinics caring for PLWHs could further address gaps in immunization history.21 Increasing the use of immunization registries and being aware that PLWHs share similar barriers to vaccination acceptance may allow the pharmacist to successfully tailor recommendations to overcome a patient’s barriers and increase vaccination rates. Limitations This study does have limitations. First, we did not achieve power for the regression analysis; 11 participants were excluded before running the regression analysis because of missing age data. Additional research in this area on a large scale may be beneficial in identifying significant differences in perceptions of immunization needs between these groups. In addition, other theoretical frameworks have been used to identify and address barriers to immunizations in persons without HIV, but they are more qualitative in nature.22 We used the Health Belief Model to design our questionnaire to identify participant beliefs regarding vaccinations, which could be argued is an indirect barrier and may affect the internal validity of these results.
Table 3 Association of perceived barriers in PLWH vs. noneHIV-infected population (n ¼ 120a) Factor Non-HIV vs. PLWH (overall) Age, y 18e34 vs. 55 35e54 vs. 55 Sex Female vs. male Vaccine recommendation source Family doctor vs. specialty doctor Othersb vs. specialty doctor Comorbidities
OR
95% CI
2.537
0.585
10.996
0.214
P value
0.382 8.406
0.019 0.985
7.826 71.729
0.005
0.567
0.081
3.994
0.569
1.068 1.846 0.632
0.177 0.233 0.320
6.432 14.638 1.249
0.744 0.187
Abbreviations: OR, odds ratio; others as in Table 1. a Eleven observations were deleted because of missing values for the response or explanatory variables. b Others include pharmacist, news, social media, nurse, other health professional, TV or movie celebrity, friends/family, website.
Second, no response rate was calculated when recruiting participants to complete the questionnaire, including a participant refusal rate. Both pharmacies were open to the public and created an opportunity for any patient to participate in this survey, resulting in our design using a convenience sampling approach. Although this may decrease the internal validity of the study and potentially mask nonresponse bias held by the participants, we think it allowed for the greatest sample size possible in this setting. In an effort to include as many participants as possible, we offered the questionnaire to patients both in-store and over the telephone. Despite this, only 5% of participants (8/142) consented and completed the questionnaire over the telephone. Individuals surveyed about immunization acceptance over the telephone may have differing perceptions to immunizations compared with those visiting a pharmacy in person, yet we were unable to confidently identify if there was in fact a difference between these groups. Soon after recruitment and data collection began, it was noted that several PLWHs use patient assistance programs to gain affordable access to their antiretroviral therapy, but this option was not available for these patients to select in the demographics section of the questionnaire. This may have led to misrepresentation of the payer/insurance status for these participants, but we do not think that these payers negatively affect patients’ access to nor their perceptions of immunizations. A survey of PLWHs in 1 geographic location (Indianapolis, IN) may not be generalizable to the rest of the United States because there are numerous grant-funded HIV clinics in the area that may be more attuned to identifying this patient population’s needs, suggesting the need to expand the recruitment area in future research.23 Regarding demographics, race was not considered or recorded, which also may affect the generalizability of this population. In addition, because the demographics of both groups were significantly different, more studies with similar patient characteristics are needed to definitively compare differences in perceived barriers between persons without HIV and PLWHs. Finally, all data collected from participants were self-reported, increasing the risk of response bias and decreasing the internal validity of the study. S45
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Future directions Further studies are warranted with larger populations or different theoretical frameworks to identify potential differences in perceptions of immunization needs between PLWHs and persons without HIV. The authors expect to use the data related to immunization rates and recommendation sources to create a more targeted intervention, specifically assessing the direct impact pharmacists may have on immunization rates in PLWHs. In addition, surveying PLWHs regarding what role they consider pharmacists play in their care beyond medication distribution and counseling may be beneficial in identifying opportunities to better market pharmacy services. A focus on identifying potential differences in immunization acceptance and education between individuals who visit a pharmacy in person versus conducting business over the telephone also should be considered. Finally, completing a cost analysis evaluating potential cost savings missed when a recommendation to administer or receive an immunization in a PLWH is refused may be considered; this could potentially justify expansion of pharmacist-driven clinical services. Conclusion In this study, PLWHs did not perceive immunizations significantly less favorably compared with the non-HIV population yet were less likely to complete the HepB vaccine series, creating the need for more targeted educational materials and service models to address these barriers. Because this study population demonstrated no significant difference in barriers to immunization acceptance in PLWHs versus the non-HIV population, using currently available education materials to address these barriers in PLWH may be an initial step to improve immunizations in this population. Ultimately, pharmacists should continue to portray themselves as trusted immunization resources for PLWHs to address this gap in care. Acknowledgments The investigators acknowledge the advisors, preceptors, and fellow residents of the Purdue Research Project Development Program for their insight, feedback, and support of this project. In addition, the investigators thank all the pharmacy staff for their passionate support and recruitment efforts. Finally, the authors thank the American Pharmacists Association Foundation for the receipt of a 2018 Incentive Grant for Pharmacy Resident Research. References 1. Office of Disease Prevention and Health Promotion. Healthy People 2020: immunization and infectious diseases. Available at: https://www. healthypeople.gov/2020/topics-objectives/topic/immunization-and-infec tious-diseases. Accessed February 13, 2018. 2. Centers for Disease Control and Prevention; National Institutes of Health; HIV Medicines Association of t Infectious Diseases Society of America. Guidelines for the prevention and treatment of opportunistic infections in HIV-infected adults. Atlanta, GA: CDC; 2017. Available at: http:// aidsinfo.nih.gov/guidelines. Accessed February 13, 2018.
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3. Rubin LG, Levin MJ, Ljungman P, et al. 2013 IDSA clinical practice guideline for vaccination of the immunocompromised host. Clin Infect Dis. 2014;58:309e318. 4. Mena G, García-Basteiro AL, Bayas JM. HepB and A vaccination in HIVinfected adults: a review. Hum Vaccin Immunother. 2015;11(11): 2582e2598. 5. Valour F, Cotte L, Voirin N, et al. Vaccination coverage against hepatitis A and B viruses, Streptococcus pneumoniae, seasonal flu, and A(H1N1)2009 pandemic influenza in HIV-infected patients. Vaccine. 2014;32(35): 4558e4564. sard A, Gagneux-Brunon A, Lucht F, Botelho-Nevers E, Launay O. Im6. Fre munization of HIV-infected adult patientsdFrench recommendations. Hum Vaccin Immunother. 2016;12(11):2729e2741. 7. Price H, Bansi L, Sabin CA, Bhagani S, Burroughs A, Chadwick D, et al. HepB virus infection in HIV-positive individuals in the UK Collaborative HIV Cohort (UK CHIC) study. PLoS One. 2012;7:e49314. 8. Grabmeier-Pfistershammer K, Herkner H, Touzeau-Roemer V, Rieger A, Burgmann H, Poeppl W. Low tetanus, diphtheria and acellular pertussis (Tdap) vaccination coverage among HIV infected individuals in Austria. Vaccine. 2015;33(32):3929e3932. 9. Gallagher KM, Juhasz M, Harris NS, Teshale EH. Predictors of influenza vaccination in HIV-infected patients in the United States, 1990e2002. J Infect Dis. 2007;196(3):339e346. 10. Harrison N, Poeppl W, Herkner H, et al. Predictors for and coverage of influenza vaccination among HIV-positive patients: a cross-sectional Questionnaire. HIV Medicine (2016). 2016:1e7. 11. Gallup. Social issues. Americans rate providers high on honesty, ethics. Available at: http://news.gallup.com/topic/category_social_issues.aspx. Accessed December 3, 2017. 12. van Amburgh JA, Waite NM, Hobson EH, Migden H. Improved influenza vaccination rates in a rural population as a result of a pharmacistmanaged immunization campaign. Pharmacotherapy. 2001;21(9): 1115e1122. 13. Baroy J, Chung D, Frisch R, Apgar D, Slack MK. The impact of pharmacist immunization programs on adult immunization rates: a systematic review and meta-analysis. J Am Pharm Assoc. 2016;56(4): 418e426. 14. Rosenstock I. Historical Origins of the Health Belief Model. Vol. 2, No. 4. Ann Arbor, MI: University of Michigan: Health Education Monographs; 1974. 15. Champion VL. Instrument development for health belief model constructs. Adv Nurs Sci. 1984;6:73e85. 16. Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research Electronic Data Capture (Redcap)da metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42(2):377e381. 17. Foisy MM, Tseng A, Blaikie N. Pharmacists’ provision of continuity of care to patients with human immunodeficiency virus infection. Am J Health Syst Pharm. 1996;53(9):1013e1017. 18. College of Physicians of Philadelphia. Misconceptions about vaccines. Available at: https://www.historyofvaccines.org/content/articles/misc onceptions-about-vaccines. Accessed June 2, 2018. 19. Handy LK, Maroudi S, Powell M, et al. The impact of access to immunization information on vaccine acceptance in three countries. PLoS One. 2017;12(8):e0180759. 20. Glanz K, Rimer BK, Lewis FM. Health Behavior and Health Education. Theory, Research and Practice. Hoboken, NJ: Wiley & Sons; 2002. 21. Centers for Disease Control and Prevention. Immunization information systems. Available at: https://www.cdc.gov/vaccines/programs/iis. Accessed June 2, 2018. 22. Green L, Kreuter M. Health Program Planning: An Educational and Ecological Approach. 4th ed. New York: McGraw-Hill Humanities/Social Science/Languages; 2004. 23. Health Resources and Services Administration. Ryan White HIV/AIDS program data reports and slide decks. Available at: http://www.hab.hrsa. gov. Accessed April 20, 2018. Alex R. Mills, PharmD, AAHIVP, Walgreen Co./Purdue University College of Pharmacy, Indianapolis, IN Stephanie J. Arnett, PharmD, CDE, BCACP, Walgreen Co., Indianapolis, IN Mu Shan, MS, Department of Epidemiology and Biostatistics, Indiana University, Indianapolis, IN Catherine Simmons, RPh, Walgreen Co., Indianapolis, IN Monica L. Miller, PharmD, MS, Department of Pharmacy Practice, Purdue University College of Pharmacy, West Lafayette, IN
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RESEARCH
Perception of immunizations and vaccine recommendation sources for persons living with HIV compared with persons without HIV Alex R. Mills*, Stephanie J. Arnett, Mu Shan, Catherine Simmons, Monica L. Miller a r t i c l e i n f o
a b s t r a c t
Article history: Received 7 September 2018 Accepted 8 May 2019 Available online 24 June 2019
Objectives: To measure and compare the perception of immunizations, immunization status, and recommendation sources in persons living with HIV (PLWHs) and persons without HIV and determine a strategy for improving immunization rates by increasing awareness of pharmacy services. Design: A 19-item survey based on the Health Belief Model assessed patients’ perceptions and recommendation sources regarding immunization acceptance for specific vaccines: Tdap, pneumococcal, and hepatitis B (HepB). Survey items used a 5-point Likert-type scale assessing participants’ perceptions, with questions identifying participants’ most trusted sources of immunization information and patient demographics. Survey questions were designed to identify perceived susceptibility and severity of vaccine-preventable illness, barriers, benefits, and self-efficacy regarding immunization acceptance, and sources of patient-trusted immunization information. Setting and participants: Survey recruitment occurred in Indiana and included any patient 18 years of age or older picking up medications at a specialty pharmacy predominantly serving PLWHs or a traditional community chain pharmacy. Main outcome measures: Primary outcomes included perceived barriers to immunization acceptance obtained from Likert-type scale questions, patient-reported immunization rates of selected vaccines (Tdap, pneumococcal pneumonia, and HepB), and trusted immunization recommendation sources. Logistic regression was performed to model association between perceived barriers, HIV status, and immunization recommendation sources. Results: A total of 142 participants (68 PLWHs, 74 persons without HIV) completed the survey. PLWHs were more likely to have immunization barriers, but this was not statistically significant (odds ratio 2.537, 95% confidence interval 0.585e10.996). Both participant groups reported “family doctor” as the most trusted source, with only 5% selecting “pharmacist.” Significantly fewer PLWHs reported completing the HepB series (18% vs. 52%; P ¼ 0.0224). Conclusion: PLWHs possess barriers to immunization acceptance similar to persons without HIV yet report lower rates of HepB vaccine completion. Although pharmacists were less frequently selected as the most trusted source, additional studies on percptions of pharmacists’ role in immunizing PLWHs should be considered. © 2019 American Pharmacists Association®. Published by Elsevier Inc. All rights reserved.
As part of the Healthy People 2020 (HP2020) initiative to improve health outcomes for the U.S. population, one area of focus is increasing immunization rates and decreasing the incidence of vaccine-preventable diseases.1 For healthy adults, Disclosure: The authors declare no relevant conflicts of interest or financial relationships. Funding: This work was supported in part by an American Pharmacists Association Foundation Incentive Grant for Pharmacy Resident Research. The funder had no role in the design, data collection, interpretation, or report writing. Previous presentations: Midyear Clinical Meeting, American Society of Health-System Pharmacists, Orlando, FL, 2017; Annual Meeting, American
HP2020 set a goal of immunizing 80% to 90% of the population for 3 specific vaccines: pneumococcal, tetanusediphtheriaeacellular pertussis (Tdap), and hepatitis B (HepB).2 Recommendations and immunization schedules for Pharmacists Association, Nashville, TN, 2018; Great Lakes Pharmacy Resident Conference, West Lafayette, IN, 2018; and Virtual Poster Symposium, American College of Clinical Pharmacy, 2018. * Correspondence: Alex R. Mills, 873 West Carmel Drive, Carmel, IN 46032 E-mail address: [email protected] (A.R. Mills). ORCID Alex R. Mills: https://orcid.org/0000-0003-4236-2299.
https://doi.org/10.1016/j.japh.2019.05.008 1544-3191/© 2019 American Pharmacists Association®. Published by Elsevier Inc. All rights reserved.
SCIENCE AND PRACTICE A.R. Mills et al. / Journal of the American Pharmacists Association 59 (2019) S39eS46
Key Points Background: Healthy People 2020 has developed metrics to improve immunization rates for the U.S. population, and this includes persons living with HIV (PLWHs). Despite PLWHs being indicated to receive many of the same inactivated vaccines as the persons without HIV, immunization rates are considerably less than Healthy People 2020’s goal for Tdap, pneumococcal pneumonia, and hepatitis B (HepB), specifically for this population. PLWHs may possess barriers to immunization acceptance that differ from persons without HIV, yet such barriers have not been specifically identified in this special population. Findings: PLWHs possess the same barriers to immunization acceptance as persons without HIV, yet still report receiving fewer vaccines (HepB in particular). Although pharmacists are highly accessible to this population, few of the PLWHs viewed them as trusted immunization recommendation sources, suggesting opportunities to better market and expand pharmacist-driven immunization services. Further research is warranted to assess the perceived role of pharmacists in providing immunization services for this population, along with evaluation of the impact that pharmacists can have on improving PLWH immunization rates through the use of targeted marketing campaigns.
95% of PLWH were missing measurable titers for pertussis from another indicated vaccine, Tdap.8 Similar to HepB, pneumococcal and Tdap are recommended for this population and are safe regardless of a PLWH’s CD4 count.3 Barriers and perceptions to immunization acceptance, including misconceptions on vaccine efficacy and safety, perceived benefit of routine vaccination, and others, have been studied extensively in persons without HIV yet few studies have assessed or identified barriers in PLWHs. Observational studies have been conducted to evaluate predictors and barriers to influenza immunization in PLWHs, but none measured pneumococcal, Tdap, and HepB vaccination.9,10 Furthermore, those studies identified physicians as the primary source of immunization recommendation, but no studies have sought to identify what impact pharmacists may have on immunization acceptance in this population.10 Pharmacists are considered to be among the most trusted medical professionals in the United States, credited to their high level of accessibility to the public and consideration as medication experts.11 Regarding pharmacist-delivered immunizations, the literature supports their positive impact on immunization rates in other populations, yet no studies were identified that reviewed pharmacists administering or recommending immunizations to PLWHs.12,13 Objectives The objectives of this study were to (1) quantitatively measure and compare PLWHs’ perception of immunization needs with persons without HIV and (2) determine trusted immunization recommendation sources for PLWHs. In addition, investigators sought to obtain the current immunization status of PLWHs compared with those without HIV. Methods Theoretical framework
special populations have also been published by the Centers for Disease Control and Prevention and the Infectious Diseases Society of America in an effort to protect patients with specialty conditions, including human immunodeficiency virus (HIV) infection.2,3 Owing to the compromised immune system for persons living with HIV (PLWHs), this patient population is at an increased risk of 2 specific conditions: opportunistic infections and vaccine-preventable illnesses.2 Despite the widespread use of effective antiretroviral therapy and integration of pneumococcal, Tdap, and HepB vaccination recommendations into the national HIV treatment guidelines, PLWHs continue to be deficient in reaching the HP2020 goal.1,2 In PLWHs, immunization rates are significantly reduced for HepB and pneumococcal vaccines.4,5 For example, all individuals, including PLWHs, are indicated for a 3-dose series of the HepB virus vaccine regardless of immune status according to CD4 count.6 However, a review of studies observing PLWHs who completed the series found rates ranging from 42% to 76%, whereas persons without HIV have achieved the HP2020 goal with 90% completing the series.4,7 Furthermore, PLWH vaccination rates for pneumococcal in other developed countries, such as France and the United Kingdom, are well below those of persons without HIV, averaging a suboptimal rate of 65%.5 Data from a French multicenter study also identified that
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The Health Belief Model depicted in Figure 1 is a published psychosocial model frequently used to predict health behaviors. First developed in the 1950s and later adapted in 1988, its core assumptions are based on the understanding that a patient will perform a health-related behavior change after an internal assessment of 6 constructs: perceived susceptibility, severity, benefits, barriers, cues to action, and self-efficacy.14,15 Setting and participants Research was conducted at 2 community pharmacies from a large nationwide chain in Indianapolis, Indiana. One of the sites is designated as a specialty pharmacy that predominantly provides holistic care for PLWH and dispenses an average of 300 prescriptions per day. Unlike many specialty pharmacies, this one is open to the public, allowing for walk-in service as well as the shipment of HIV and non-HIV medications upon patient request. The pharmacy staff at this site received cultural competency and health literacyefocused training developed by the chain’s Clinical Programs and Training Department. The second is a traditional (nonspecialty) community pharmacy within the same chain that serves a larger volume of patients dispensing an average of 500 prescriptions per day. The traditional
SCIENCE AND PRACTICE Immunization perceptions in persons with HIV
Modifying Factors
Likelihood of Action
Age Sex Knowledge
Perceived Benefits Vs. Barriers to Change
Perceived Susceptibility of Disease
Perceived Threat of Disease
Likelihood of Behavioral Change
Perceived Self-Efficacy to Perform Action
Cues to Action: Education Symptoms Referral Sources
Patient Perceptions
Figure 1. Conceptual diagram of health belief model, adapted from Glanz et al.20
community pharmacy provides the standard of care available at most community pharmacies and the staff also received the same cultural competency and health literacy training as the specialty pharmacy, which the investigators thought would potentially create a more welcoming environment for participant recruitment. All adult patients waiting in-store or picking up a prescription at either pharmacy were asked to voluntarily complete a questionnaire. Data collection and recruitment occurred from November 2017 to March 2018. All participants who started the questionnaire and completed 90% of survey items were included in analysis except those who were under the age of 18 years, did not report their age, or were not picking up a medication for their personal use. Study participation was voluntary and was granted exempt status by Purdue University’s Institutional Review Board. Design The questionnaire consisted of 19 items, which asked about demographics (age, sex, gender identity), health conditions (defined as taking at least 1 medication for any of the following conditions: hypertension, diabetes mellitus, dyslipidemia, HIV treatment, HIV prevention (preexposure prophylaxis), and chronic obstructive pulmonary disease or asthma), and perceived barriers to immunization acceptance. Questionnaire items were designed to identify (1) perceived susceptibility and severity to vaccine-preventable illness, (2) barriers, benefits, and self-efficacy related to immunization acceptance, and (3) trusted sources for immunization recommendations. The majority of questions used a 5-point Likert-type scale (from 1, strongly disagree, to 5, strongly agree) with multiplechoice questions for demographics, health conditions, self-reported doses of HepB vaccine, and trusted sources for immunization recommendations. The questions created for the questionnaire were adapted from a 2016 study completed by Harrison et al., in which a questionnaire was used to identify positive and negative predictors of immunization acceptance.10 The questions related to negative predictors were associated with common beliefs and misconceptions associated with influenza vaccination. Ultimately, it was interpreted that those beliefs were an indirect
barrier to immunization acceptance and aligned with the modifying variables of the Health Belief Model’s construct of “perceived barriers,” compelling us to create negatively worded statements to assess this construct. Specifically, participants were provided the statements “Vaccines will worsen my other health conditions” and “Vaccines are just a scam for the pharmaceutical companies to get more money.” These questions were designed to identify if participants possessed negative beliefs about vaccines that may act as an indirect barrier to receiving a vaccine. To assess “perceived benefits,” we constructed statements that assessed if participants believed the action of receiving an immunization would reduce the risk or severity of a vaccine-preventable illness. Specifically, the provided statements “Getting vaccinated is a good way to keep myself and others healthy” and “Vaccines prevent me from getting sick” were included in the questionnaire to identify positive beliefs about vaccines that serve as indirect markers aligning with the perceived benefit construct of the Health Belief Model. Finally, “perceived severity” was assessed by asking participants to agree or disagree with statements that inferred that participants possessed the belief immunizations can prevent hospitalizations or severe illness, an indirect measure of participants’ perception of potential consequences if not vaccinated. Statements that assessed participants’ “perceived severity” included “If I don’t keep up with my vaccinations, I could end up very sick/in the hospital” and a negatively worded statement, “Diseases that are covered by vaccines are not that serious.” Ultimately, it was hypothesized that participants who possessed these beliefs are likely to refuse or avoid immunizations because they would act as an indirect barrier to making a health behavior change (e.g., receiving an immunization). Accessibility and quality assurance Several steps were taken to improve questionnaire accessibility to account for differences in patients’ comfort level with technology, socioeconomic status, transportation barriers (e.g., unable to physically visit the pharmacy), educational level, health literacy, and preferred language. Questionnaires were available in 3 formats: (1) tablet computer application, S41
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(2) paper questionnaire, (3) and telephone questionnaire. The questionnaire was available in both English and Spanish. To maintain privacy, participants completed the questionnaire independently and anonymously, with responses cleared from the device before research personnel reclaimed possession. Spanish questions were validated for consistency and understanding by a Spanish-speaking pharmacy technician. For participants unable to read or if health literacy was a concern, a student pharmacist read the questionnaire aloud to the participant in a consultation room to maintain privacy. Otherwise, trained recruitment personnel were instructed not to assist the participants with completing or answering the questionnaire. In addition, approximately 70% of patients at the specialty pharmacy have medications shipped to their place of residence. The pharmacy technician in charge of contacting these participants was trained on proper recruitment and delivery of the questionnaire over the telephone. Implementation and recruitment Study data were collected and managed with the use of Redcap (Research Electronic Data Capture) version 8.1.13, an electronic data capture tool hosted at Indiana University’s Clinical and Translational Sciences Institute. Redcap is a secure web-based application designed to support data capture for research studies, supporting cloud-based and offline data collection via tablet computers, as well as automated export procedures to common statistical packages.16 Research personnel and student pharmacists were trained on its use and scripting for recruitment based on approved institutional review board methods. To assess ease of use, wording, and elapsed time to complete the questionnaire, 6 pharmacy technicians and 3 student pharmacists working at both sites completed a pilot questionnaire before its implementation for study participants. After successful pilot testing and personnel training, recruitment occurred of all participants picking up prescriptions via completion of the questionnaire on tablet computer, paper, or telephone. In an effort to maintain consistency in the recruitment process across the various forms of the questionnaire, the offer to participate was provided at the conclusion of the in-person sale of their medications or after the shipment process has been completed. Outcome measures The primary outcome included perceived barriers to immunization acceptance obtained from Likert-type scale questions. Secondary outcomes included patient-reported immunization rates of selected vaccines (Tdap, pneumococcal [PCV13 and PPSV23], and HepB) and trusted immunization recommendation sources. Logistic regression was performed to model association between perceived barriers, HIV status, and immunization recommendation sources. Statistical analysis Before analysis, an estimated sample size calculation was performed in G-Power version 3.1 with the use of a 95% CI. We assumed a standard deviation of 2 in each sample’s response to Likert-type scale questions and mean difference of 1 for all Likert-type scale “perceived barriers” questions via an S42
independent 2-sample t test. To meet at least 80% power, the estimated sample size needed was at least 64 participants in each group (PLWHs vs. persons without HIV) Baseline participant characteristics and outcome measures were summarized as frequency and percentage for categoric variables and median and interquartile range (IQR) for nonnormal continuous variables. The difference between groups was compared by means of Wilcoxon-Mann-Whitney test for nonnormal continuous variables, t test for normal continuous variable, and chi-square test for categorical variables. The dependent variable “perceived barriers” was defined as “yes” if participants chose “agree” or “strongly agree” in any of the 3 barriers questions (“vaccines will worsen my other conditions,” “vaccines are just a scam for the pharmaceutical companies to make get more money,” and “Vaccines don’t work”); otherwise their response was considered to be “no.” Because the outcome was dichotomous in nature, a logistic regression model was used to measure the difference in perceived barriers between PLWHs and persons without HIV, adjusting for demographic and covariates (number of comorbidities, immunization recommendation sources). Descriptive statistics (mean ± SD) and an independent t test were analyzed for responses to “perceived barriers,” stratified into each individual survey item. In addition, the percentage of respondents selecting “agree” and “strongly agree” (defined as “yes” to perceived barriers) and any other response (defined as “no” to perceived barriers) were also reported for each related survey item. Immunization recommendation sources were regrouped as “family doctor,” “specialty doctor,” and “other” because of small samples in some of the categories. A 5% significance level was used for all tests. Analyses were performed with the use of SAS version 9.4 (SAS Institute, Cary, NC).
Results Demographics and comorbidities There were 142 participants who completed the questionnaire provided at both pharmacies: 68 classified as PLWHs and 74 classified as non-HIV for analysis purposes. The majority, 95% (134/142), of participants completed the questionnaire in person, whereas the remaining 5% (8/142) participated over the telephone. After implementing exclusion criteria (primarily due to participants not completing at least 90% of survey items) after data collection, 67 PLWHs and 64 persons without HIV remained for final analysis in the regression model, as depicted in Figure 2. All participants who completed the questionnaire over the telephone met inclusion criteria and were included in analysis. There were 11 participants excluded from the regression model due to missing values for their age range. Participant demographics are listed in Table 1. A majority (92.6%) of the PLWH cohort were male and the overall median age range was 45 to 54 years. Comparatively, the cohort without HIV was younger (median age range 35 to 44 years) and included slightly more men than women (58% and 42%, respectively). A Wilcoxon-Mann-Whitney scores analysis comparing PLWHs versus persons without HIV number of comorbidities was performed (Table 1), because the data were not normally distributed. Fisher exact test was performed for categorical values that contained a small sample size (n 5).
SCIENCE AND PRACTICE Immunization perceptions in persons with HIV
regarding perceived barriers, there was no significant difference between groups for perceived benefits (survey question, “These vaccines keep me healthy”) or perceived severity (survey question, “If I don’t keep up with my vaccinations, I could end up very sick and in the hospital”).
Parcipants compleng quesonnaire (n=142)
Classified as PLWH
Classified as non-HIV
(n=68)
(n=74)
Vaccine history
Met Exclusion Criteria
Met Exclusion Criteria
(n=1)
(n=10)
Met Inclusion Criteria
Met Inclusion Criteria
(n=67)
(n=64)
Missing age range data
Missing age range data
(n=8)
(n=3)
Included in Logisisc Regression
Included in Logisc Regression
(n=59)
(n=61)
Figure 2. Participant inclusion/exclusion criteria flowchart.
The PLWH cohort had a median of 1 comorbidity (IQR 0e2), which was defined as number of reported health conditions minus “HIV treatment,” and the cohort without HIV had a median of zero comorbidities (IQR 0e1.5). There was no significant difference between groups (P ¼ 0.33).
For the 3 selected vaccines (Tdap, pneumococcal, and HepB), there was no significant difference between PLWHs and persons without HIV in receiving Tdap or at least 1 dose of HepB, but PLWHs reported receiving pneumococcal vaccination more than the non-HIV cohort (Table 1). Further analysis demonstrated significantly more persons without HIV completed the HepB series than PLWHs (52.9% vs. 18.2%; P ¼ 0.022). Vaccination administration and recommendation sources Several of the categories (i.e., “pharmacist,” “website,” “nurse,” “other health professional”) for trusted recommendation sources had very low responses. To run an analysis to identify significant differences between groups, these categories were regrouped into a single category labeled “other.” After regrouping (Table 3), the most commonly selected recommendation source was “family doctor,” with 62% of PLWHs selecting this option versus 70% of persons without HIV (P ¼ 0.0006). Of note, “pharmacist” only accounted for 5% (n ¼ 6) of overall responses, with 3% of PLWHs selecting this option versus 6% of persons without HIV (n ¼ 2 and 4, respectively). Discussion
Perceived barriers Descriptive statistics and t test results for the individual “perceived barriers” items are presented in Table 2. No significant differences between PLWHs and persons without HIV who completed this survey were identified. Descriptive statistics of perceived barrier survey items and percentage of participants defined as having or not having perceived barriers to immunization acceptance are reported in Table 2, with no significant difference between groups. Incorporating survey responses into the logistic analysis (Table 3) revealed that the perceived barriers PLWHs may hold were not statistically significantly different from those of persons without HIV (odds ratio [OR] 2.537, 95% CI 0.585e10.996). Covariates of immunization recommendation sources and number of comorbidities also did not meet statistical significance in the logistic regression model for perceived barriers. Of note, participants aged 18 to 34 years had statistically significantly less perceived barriers than those 55 years of age and older, whereas those aged 35e54 years had statistically significantly more perceived barriers (ORs 0.382 and 8.406, respectively). Perceived benefits and severity The difference in perceived benefits and severity between groups were also analyzed with the use of an independent t test (Table 2). Similar to the logistic regression model
This study demonstrated overall that PLWHs do not have significantly more or different barriers to immunizations compared with persons without HIV. Although previous studies demonstrated PLWHs are less likely to accept routine and indicated immunizations, this study is, to our knowledge, the first seeking to quantitatively identify patients’ specific barriers between PLWHs and persons without HIV in the same geographic location.9,10 This study also addresses the gap in literature related to whom PLWHs trust for an immunization recommendation, expanding beyond the physician or HIV specialist and including the pharmacist, who has an everincreasing role in the HIV continuum of care.17 Because this study’s data demonstrated that both groups possess the same barriers to receiving immunizations, current educational programs and materials could be used to promote immunization acceptance in the PLWH population. A notable barrier for immunizations in the persons without HIV concerns misconceptions regarding their safety, efficacy, and value of vaccinations.18 Addressing these misconceptions by providing evidence-based recommendations and “debunking” myths regarding vaccines should be provided by health professionals, especially those who care for PLWHs. A multicenter study by Handy et al. identified that a significant barrier to vaccine acceptance was lack of accurate information regarding currently licensed vaccines.19 Participants in their focus groups reported an increased likelihood of accepting a vaccine recommendation when given reliable information from their S43
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Table 1 Participant demographics, vaccine history, and trusted recommendation sources, n (%) Variable Age range, y 18e34 35e54 55 Sex Male Female Gender identity Male Female Transgender Do not identify as any listed Insurance status Employer-provided Medicaid Medicare HIP/HIP 2.0 Insurance through family’s plan No insurance Comorbidities Hypertension Diabetes Dyslipidemia COPD/Asthma None of these Number of comorbidities, median (IQR) Patient-reported vaccine history, n (%) Tdap Pneumococcala Hepatitis B Hepatitis B series completionb Vaccine recommendation sourcec Family doctor Specialty doctor Othersd
PLWH (n ¼ 67)
Non-HIV (n ¼ 64)
5 (9) 30 (53) 22 (39)
26 (49) 17 (42) 10 (19)
63 (92.6) 5 (7.4)
38 (57.6) 28 (42.4)
62 (92.5) 5 (7.5) e e
38 (57.6) 28 (42.4) e e
10 4 37 16 0 1
(14.7) (5.9) (54.4) (23.5)
33 7 11 3 10 1
(50.8) (10.8) (16.9) (4.6) (15.4) (1.5)
21 10 23 8 0 1
(30.9) (14.7) (33.8) (11.8) (0e2)
19 12 13 3 35 0
(29.9) (18.5) (20.0) (4.6) (53.8) (0e1.5)
0.852 0.643 0.018 0.208 < 0.001 0.33
31 51 22 4
(45.6) (75.0) (32.4) (18.2)
34 20 17 9
(54.0) (31.7) (27.0) (52.9)
0.486 < 0.001 0.451 0.022
P value < 0.001
< 0.001
< 0.001
0.006
(1.5)
41 (62) 18 (27) 7 (11)
45 (70) 2 (3) 17 (27)
< 0.001
Abbreviations: COPD, chronic obstructive pulmonary disease; HIP, Healthy Indiana Plan; HIV, human immunodeficiency virus; IQR, interquartile range; PLWH, persons living with HIV; Tdap, tetanusediphtheriaeacellular pertussis. a Listed in questionnaire as “Pneumonia (Prevnar, Pneumovax).” b Defined as reporting 3 doses; total sample: PLWH ¼ 22, non-HIV ¼ 17. c Listed in questionnaire as “Which is your primary source for information on vaccines that you trust?” d Others include pharmacist, news, social media, nurse, other health professional, TV or movie celebrity, friends/family, website.
health care provider.19 We hypothesize that transferring this information to PLWH providers with more frequent vaccine education can potentially increase vaccine acceptance in this patient population. We used the Health Belief Model in designing our survey with the objective of adequately identifying and comparing health behaviors between PLWHs and persons without HIV, yet our results showed no statistically significant difference.20 Despite these results, our study supports previous literature and data related to immunizations in PLWHs in several ways. Survey participants’ self-reported immunization rates closely match national and global data depicting PLWHs as significantly underimmunized, particularly concerning HepB and Tdap.1,8 Of note, a majority of PLWH participants reported receiving at least 1 pneumococcal immunization. This may be attributed to the increased integration of immunization histories into the Electronic Medical Record or increased awareness of PLWHs being indicated for immunization. Conversely, significantly more persons without HIV completed the HepB 3-dose series compared with PLWHs, supporting the national evidence of PLWHs being underimmunized for this disease.
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These findings are also similar to results from Harrison et al., identifying physicians as the primary source for trusted immunization recommendations in PLWHs, although this was not statistically significant compared with persons without HIV.10 Unlike the study by Harrison et al., we assessed patients’ perception of the role pharmacists may play in providing PLWHs these recommended immunizations, yet few participants in either group selected the pharmacist as the trusted immunization recommendation source. This finding identifies an opportunity for improved marketing of pharmacist immunization services. Pharmacists are uniquely positioned to positively affect immunization rates, including the immunocompromised and PLWHs.11-13 Their high level of accessibility, level of expertise, and overall reputation make them a valuable resource for achieving the HP2020 goals.1 This study identified that PLWHs share similar barriers to immunizations compared with persons without HIV; combining this information with current vaccination programs and more frequent, regular immunization assessments could warrant expansion of pharmacist-driven immunization services for PLWHs. Pharmacists in most states have access to vaccine registries, and
SCIENCE AND PRACTICE Immunization perceptions in persons with HIV
Table 2 Comparison of PLWH and non-HIV survey responses to perceived barriers, benefits, and severity related to immunization acceptancea PLWH n ¼ 67
Survey item
Mean Perceived barriers “Vaccines don’t work.” “Vaccines are just a scam for the pharmaceutical company to make more money.” “Vaccines will worsen my other health conditions.” Perceived benefits “Vaccines keep me healthy.” “Getting vaccinated is a good way to keep myself and others healthy.” Perceived severity “If I don’t keep up with my vaccinations, I could end up very sick or in the hospital.”
P valued
Non-HIV n ¼ 64 Yesb
Noc
Mean
Yesb
Noc
1.71 ± 1.23 1.78 ± 1.24
9.7% 9.0%
90.3% 91.0%
1.70 ± 1.20 1.56 ± 1.07
12.1% 12.1%
87.9% 87.9%
0.976 0.294
1.71 ± 1.16
13.4%
86.6%
1.63 ± 1.08
6.2%
93.8%
0.697
4.51 ± 0.88 4.48 ± 1.01
89.6% 87.5%
10.4% 12.5%
4.3 ± 1.11 4.38 ± 1.06
87.5% 83.3%
12.5% 16.7%
0.249 0.567
3.96 ± 1.5
70.1%
29.9%
4.08 ± 1.17
68.9%
31.1%
0.604
Abbreviations as in Table 1. a Survey responses completed on 5-point Likert-type scale from 1 ¼ strongly disagree to 5 ¼ strongly agree. b Defined as selecting “strongly agree” or “agree” on survey items. c Defined as selecting any Likert-type scale option besides “strongly agree” or “agree” on survey items. d P values based on difference of 2 means from Likert-type scale questions according to independent t test.
using this tool in pharmacies or pharmacist-driven clinics caring for PLWHs could further address gaps in immunization history.21 Increasing the use of immunization registries and being aware that PLWHs share similar barriers to vaccination acceptance may allow the pharmacist to successfully tailor recommendations to overcome a patient’s barriers and increase vaccination rates. Limitations This study does have limitations. First, we did not achieve power for the regression analysis; 11 participants were excluded before running the regression analysis because of missing age data. Additional research in this area on a large scale may be beneficial in identifying significant differences in perceptions of immunization needs between these groups. In addition, other theoretical frameworks have been used to identify and address barriers to immunizations in persons without HIV, but they are more qualitative in nature.22 We used the Health Belief Model to design our questionnaire to identify participant beliefs regarding vaccinations, which could be argued is an indirect barrier and may affect the internal validity of these results.
Table 3 Association of perceived barriers in PLWH vs. noneHIV-infected population (n ¼ 120a) Factor Non-HIV vs. PLWH (overall) Age, y 18e34 vs. 55 35e54 vs. 55 Sex Female vs. male Vaccine recommendation source Family doctor vs. specialty doctor Othersb vs. specialty doctor Comorbidities
OR
95% CI
2.537
0.585
10.996
0.214
P value
0.382 8.406
0.019 0.985
7.826 71.729
0.005
0.567
0.081
3.994
0.569
1.068 1.846 0.632
0.177 0.233 0.320
6.432 14.638 1.249
0.744 0.187
Abbreviations: OR, odds ratio; others as in Table 1. a Eleven observations were deleted because of missing values for the response or explanatory variables. b Others include pharmacist, news, social media, nurse, other health professional, TV or movie celebrity, friends/family, website.
Second, no response rate was calculated when recruiting participants to complete the questionnaire, including a participant refusal rate. Both pharmacies were open to the public and created an opportunity for any patient to participate in this survey, resulting in our design using a convenience sampling approach. Although this may decrease the internal validity of the study and potentially mask nonresponse bias held by the participants, we think it allowed for the greatest sample size possible in this setting. In an effort to include as many participants as possible, we offered the questionnaire to patients both in-store and over the telephone. Despite this, only 5% of participants (8/142) consented and completed the questionnaire over the telephone. Individuals surveyed about immunization acceptance over the telephone may have differing perceptions to immunizations compared with those visiting a pharmacy in person, yet we were unable to confidently identify if there was in fact a difference between these groups. Soon after recruitment and data collection began, it was noted that several PLWHs use patient assistance programs to gain affordable access to their antiretroviral therapy, but this option was not available for these patients to select in the demographics section of the questionnaire. This may have led to misrepresentation of the payer/insurance status for these participants, but we do not think that these payers negatively affect patients’ access to nor their perceptions of immunizations. A survey of PLWHs in 1 geographic location (Indianapolis, IN) may not be generalizable to the rest of the United States because there are numerous grant-funded HIV clinics in the area that may be more attuned to identifying this patient population’s needs, suggesting the need to expand the recruitment area in future research.23 Regarding demographics, race was not considered or recorded, which also may affect the generalizability of this population. In addition, because the demographics of both groups were significantly different, more studies with similar patient characteristics are needed to definitively compare differences in perceived barriers between persons without HIV and PLWHs. Finally, all data collected from participants were self-reported, increasing the risk of response bias and decreasing the internal validity of the study. S45
SCIENCE AND PRACTICE A.R. Mills et al. / Journal of the American Pharmacists Association 59 (2019) S39eS46
Future directions Further studies are warranted with larger populations or different theoretical frameworks to identify potential differences in perceptions of immunization needs between PLWHs and persons without HIV. The authors expect to use the data related to immunization rates and recommendation sources to create a more targeted intervention, specifically assessing the direct impact pharmacists may have on immunization rates in PLWHs. In addition, surveying PLWHs regarding what role they consider pharmacists play in their care beyond medication distribution and counseling may be beneficial in identifying opportunities to better market pharmacy services. A focus on identifying potential differences in immunization acceptance and education between individuals who visit a pharmacy in person versus conducting business over the telephone also should be considered. Finally, completing a cost analysis evaluating potential cost savings missed when a recommendation to administer or receive an immunization in a PLWH is refused may be considered; this could potentially justify expansion of pharmacist-driven clinical services. Conclusion In this study, PLWHs did not perceive immunizations significantly less favorably compared with the non-HIV population yet were less likely to complete the HepB vaccine series, creating the need for more targeted educational materials and service models to address these barriers. Because this study population demonstrated no significant difference in barriers to immunization acceptance in PLWHs versus the non-HIV population, using currently available education materials to address these barriers in PLWH may be an initial step to improve immunizations in this population. Ultimately, pharmacists should continue to portray themselves as trusted immunization resources for PLWHs to address this gap in care. Acknowledgments The investigators acknowledge the advisors, preceptors, and fellow residents of the Purdue Research Project Development Program for their insight, feedback, and support of this project. In addition, the investigators thank all the pharmacy staff for their passionate support and recruitment efforts. Finally, the authors thank the American Pharmacists Association Foundation for the receipt of a 2018 Incentive Grant for Pharmacy Resident Research. References 1. Office of Disease Prevention and Health Promotion. Healthy People 2020: immunization and infectious diseases. Available at: https://www. healthypeople.gov/2020/topics-objectives/topic/immunization-and-infec tious-diseases. Accessed February 13, 2018. 2. Centers for Disease Control and Prevention; National Institutes of Health; HIV Medicines Association of t Infectious Diseases Society of America. Guidelines for the prevention and treatment of opportunistic infections in HIV-infected adults. Atlanta, GA: CDC; 2017. Available at: http:// aidsinfo.nih.gov/guidelines. Accessed February 13, 2018.
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3. Rubin LG, Levin MJ, Ljungman P, et al. 2013 IDSA clinical practice guideline for vaccination of the immunocompromised host. Clin Infect Dis. 2014;58:309e318. 4. Mena G, García-Basteiro AL, Bayas JM. HepB and A vaccination in HIVinfected adults: a review. Hum Vaccin Immunother. 2015;11(11): 2582e2598. 5. Valour F, Cotte L, Voirin N, et al. Vaccination coverage against hepatitis A and B viruses, Streptococcus pneumoniae, seasonal flu, and A(H1N1)2009 pandemic influenza in HIV-infected patients. Vaccine. 2014;32(35): 4558e4564. sard A, Gagneux-Brunon A, Lucht F, Botelho-Nevers E, Launay O. Im6. Fre munization of HIV-infected adult patientsdFrench recommendations. Hum Vaccin Immunother. 2016;12(11):2729e2741. 7. Price H, Bansi L, Sabin CA, Bhagani S, Burroughs A, Chadwick D, et al. HepB virus infection in HIV-positive individuals in the UK Collaborative HIV Cohort (UK CHIC) study. PLoS One. 2012;7:e49314. 8. Grabmeier-Pfistershammer K, Herkner H, Touzeau-Roemer V, Rieger A, Burgmann H, Poeppl W. Low tetanus, diphtheria and acellular pertussis (Tdap) vaccination coverage among HIV infected individuals in Austria. Vaccine. 2015;33(32):3929e3932. 9. Gallagher KM, Juhasz M, Harris NS, Teshale EH. Predictors of influenza vaccination in HIV-infected patients in the United States, 1990e2002. J Infect Dis. 2007;196(3):339e346. 10. Harrison N, Poeppl W, Herkner H, et al. Predictors for and coverage of influenza vaccination among HIV-positive patients: a cross-sectional Questionnaire. HIV Medicine (2016). 2016:1e7. 11. Gallup. Social issues. Americans rate providers high on honesty, ethics. Available at: http://news.gallup.com/topic/category_social_issues.aspx. Accessed December 3, 2017. 12. van Amburgh JA, Waite NM, Hobson EH, Migden H. Improved influenza vaccination rates in a rural population as a result of a pharmacistmanaged immunization campaign. Pharmacotherapy. 2001;21(9): 1115e1122. 13. Baroy J, Chung D, Frisch R, Apgar D, Slack MK. The impact of pharmacist immunization programs on adult immunization rates: a systematic review and meta-analysis. J Am Pharm Assoc. 2016;56(4): 418e426. 14. Rosenstock I. Historical Origins of the Health Belief Model. Vol. 2, No. 4. Ann Arbor, MI: University of Michigan: Health Education Monographs; 1974. 15. Champion VL. Instrument development for health belief model constructs. Adv Nurs Sci. 1984;6:73e85. 16. Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research Electronic Data Capture (Redcap)da metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42(2):377e381. 17. Foisy MM, Tseng A, Blaikie N. Pharmacists’ provision of continuity of care to patients with human immunodeficiency virus infection. Am J Health Syst Pharm. 1996;53(9):1013e1017. 18. College of Physicians of Philadelphia. Misconceptions about vaccines. Available at: https://www.historyofvaccines.org/content/articles/misc onceptions-about-vaccines. Accessed June 2, 2018. 19. Handy LK, Maroudi S, Powell M, et al. The impact of access to immunization information on vaccine acceptance in three countries. PLoS One. 2017;12(8):e0180759. 20. Glanz K, Rimer BK, Lewis FM. Health Behavior and Health Education. Theory, Research and Practice. Hoboken, NJ: Wiley & Sons; 2002. 21. Centers for Disease Control and Prevention. Immunization information systems. Available at: https://www.cdc.gov/vaccines/programs/iis. Accessed June 2, 2018. 22. Green L, Kreuter M. Health Program Planning: An Educational and Ecological Approach. 4th ed. New York: McGraw-Hill Humanities/Social Science/Languages; 2004. 23. Health Resources and Services Administration. Ryan White HIV/AIDS program data reports and slide decks. Available at: http://www.hab.hrsa. gov. Accessed April 20, 2018. Alex R. Mills, PharmD, AAHIVP, Walgreen Co./Purdue University College of Pharmacy, Indianapolis, IN Stephanie J. Arnett, PharmD, CDE, BCACP, Walgreen Co., Indianapolis, IN Mu Shan, MS, Department of Epidemiology and Biostatistics, Indiana University, Indianapolis, IN Catherine Simmons, RPh, Walgreen Co., Indianapolis, IN Monica L. Miller, PharmD, MS, Department of Pharmacy Practice, Purdue University College of Pharmacy, West Lafayette, IN