Perceptions and Attitudes of Pharmacogenomics Through the Lens of Community Pharmacists and Patients

With rising healthcare costs in the United States (US) and only 50–75% of medications producing an adequate therapeutic response, there is a need to diverge from the traditional one-size-fits-all approach to medicine to a personalized approach to disease management.^(1,2)

Pharmacogenomics (PGx), a central element of precision medicine, aims to customize medical treatment to an individual or a group of people by utilizing their individual genetic makeup to ensure the best and most personalized medical treatment.⁽³⁾ The purpose of PGx is to raise effectiveness and lower toxicity of medications for patients.⁽⁴⁾ The Food and Drug Administration (FDA) states that PGx information should be included in the manufacturer’s drug label when it is “useful to inform prescribers about the impact (or lack of impact) of genotype or phenotype.”⁽⁵⁾ As of 2020, there were upwards of 250 approved medications that had product labels referencing PGx in the FDA’s Table of Pharmacogenomic Biomarkers in Drug Labeling, all of which provide clinical guidance and information on drug dosing.⁽⁶⁾ Despite the advantages of utilizing PGx to prevent serious adverse drug reactions and optimize clinical efficacy, the integration of PGx into clinical practice has been challenging.⁽⁷⁾

Major barriers to PGx healthcare integration includes reimbursement/cost, timeliness of results, lack of patient and clinician knowledge, lack of standardization in clinical application, privacy concerns, legal/ethical concerns, and lack of provider competency/formal training.^(8–12) Despite these barriers, previous studies have consistently demonstrated patient interest in PGx testing.^(13–17) Gibson et al assessed patient knowledge, interest, and willingness to pay for PGx testing in a community pharmacy setting; 81% of patients were interested in getting PGx testing, however, the importance of further patient education around PGx was stressed.⁽¹⁵⁾ Comparisons of PGx knowledge and perceptions between attendees at a university-sponsored health fair and patients presenting to independent pharmacies showed both groups had positive reception to PGx; health fair attendees were more in favor of PGx, suggesting a need for greater outreach and education to the general public.⁽¹³⁾

Olander et al surveyed primary care clinicians’ attitudes and knowledge of PGx and determined that only 11% stated that they would contact a pharmacy for interpretation of PGx test results.⁽⁹⁾ Authors speculated that a lack of agreement among clinicians (including physicians, nurse practitioners, and physician assistants) could be attributed to clinicians’ incomplete understanding of the training and education background of their pharmacist colleagues. Studies have shown that some physicians do not have a clear understanding of pharmacist competency and their role in primary health care, and as such, may contribute to uncertainty on which healthcare clinician should be spearheading the interpretation of PGx results.⁽¹⁸⁾

Many pharmacists are already leading the movement of becoming the ‘go-to’ clinician to order, interpret, and apply PGx-related results, with their efforts supported by the American Pharmacists Association (APhA). APhA has issued a white paper discussing the incorporation and development of PGx into medication therapy management (MTM) services.⁽¹⁹⁾ By establishing pharmacists as the primary PGx clinician and eliminating the lack of agreement among clinicians, patient care will be optimized and patient needs will not go unmet.⁽²⁰⁾ Thus, this study aims to assess both the community pharmacists’ and patients’ perceptions and attitudes of PGx and provides a comparison between these groups, furthering the body of evidence related to PGx barriers and opportunities to enhance integration.

The primary objective of this study is to characterize perceptions and attitudes of pharmacists and patients towards PGx testing. A secondary aim of this study is to identify barriers to PGx implementation into clinical practice, such as a community pharmacy setting.

A cross-sectional survey study was designed to assess perceptions and attitudes using a Likert scale ranging from 1 (strongly disagree) to 5 (strongly agree). The survey was developed after conducting a literature search to determine common themes and questions that could further highlight perceptions and attitudes of both pharmacists and patients as well as barriers to PGx implementation.^(8–27) Characteristic variables discussed in the previous literature included income, personal health status, prior connection to genetic testing, and willingness to pay for a PGx service. Both pharmacist and patient surveys queried about perceptions and attitudes; ten questions identified as potential barriers in both surveys were developed for comparative analyses. Of these ten questions, three were related to perceptions, five were related to attitudes, and two were related to patient characteristics (personal health status and willingness to pay). The patient survey was prefaced with a brief statement describing PGx.

Data were collected from February to April 2018. Pharmacists (n=234) surveyed were employed by one regional division of a large community pharmacy chain in Southern California. This community pharmacy chain was selected for survey inclusion as the primary investigator was affiliated with the company as a pharmacy resident. An email invitation to participate was sent with a link through an internal company pharmacist listserv to access the online survey hosted by Wufoo, a subscription-based platform. Paper surveys for patients and drop boxes with recruitment fliers (supplemental material) were placed across all ten pharmacies in the same regional pharmacy chain division in San Diego, California. This convenience sample surveyed participants at all pharmacies located within urban areas of San Diego County. The study protocol allowed for pharmacy staff to only inform patients, when asked, about basic survey completion; staff were not permitted to answer specific questions about the survey. Once patients completed their survey, they dropped the anonymous survey into a drop box located at the pharmacy, which was periodically collected. A power calculation was not estimated as this project involved a convenience sample.

STATA/IC 14.0 was used for descriptive and comparative analyses. Descriptive analyses included frequency counts and percentages. Comparative analyses were conducted using Mann Whitney U Test for the ten comparative questions that were asked of both pharmacists and patients. Multivariate linear regressions were used to analyze perception and attitude questions to determine if there was an association between these questions and characteristic variables of pharmacists and patients, as well as to assess for barriers. A priori level of significance was set at p< 0.05. The University of California San Diego Human Research Protections Program approved this study as exempt research.

Characteristics among pharmacists and patients are displayed in Table 1 with respect to gender, age, race, personal health rating, having had a history of using PGx or knowing someone who has, and willingness to pay out of pocket. There were no significant differences between the gender of the pharmacists and patients (p=0.57) or having previously participated or known someone that had participated in PGx testing (p=0.91). There was, however, a significant difference between pharmacists’ and patients’ race (p<0.001), personal health rating (p<0.001), and willingness to pay out of pocket, with patients indicating they would pay more than pharmacists (p<0.01). The response rate for pharmacist participants was 43%; the response rate for patient participants is unclear since the size of total sampling pool was unknown.

Table 2 contains frequencies of pharmacist responses to the perception and attitude questions. Many pharmacists agreed or strongly agreed to the following: understanding what PGx testing is (67%), being interested in educating their patients about PGx testing (71%), and the importance of identifying patients who could benefit from PGx services (81%). However, many did not feel that they had sufficient PGx training in pharmacy school (61%) and only 26% agreed or strongly agreed that they had time to incorporate PGx services into their daily workflow.

Most of the identified barrier questions did not show a statistically significant correlation (data not shown). However, two perception questions showed statistically significant and positive correlations between having PGx training in pharmacy school and feeling knowledgeable about the use of PGx in therapeutic decision-making (β=0.7; t=2.47; p<0.02) and understanding the clinical application of PGx in drug therapy management (β=0.63; t=2.08; p<0.05), while adjusting for other demographic factors. Additionally, two attitude questions revealed statistically significant and positive correlations between being Caucasian and believing patients’ PGx data should be easily accessible by community pharmacists (β=0.48; t=2.35; p<0.03) and that insurance companies should cover the cost of PGx testing (β=0.48; t=2.25; p<0.03), while adjusting for other demographic factors.

Table 3 contains frequencies of patient responses to the perception and attitude questions. Notable findings include that a majority of patients were not already aware about PGx but were interested in a PGx test. There was considerable concern among a majority of patients for how insurance companies may use their PGx information.

There were a number of important and statistically significant correlations, both positive and negative, between patient factors and their perceptions and attitudes (Table 4). Being Caucasian and having personally participated or known someone who had participated in PGx testing were patient factors that were positively correlated with several perception questions (see Table 4 for linear regression outputs). Among a few others, patients who self-reported poorer health status were negatively correlated with several of the perception questions.

With respect to the attitude questions, a patient factor that was positively correlated with an interest in a one-time PGx test was having a higher annual income (β=0.175; t=2.94; p<0.01) . All of these findings were in the context of adjusting for other demographic/patient factors.

The comparative analyses between the ten questions related to potential barriers revealed that there were statistically significant differences between six of the questions: one related to perceptions, three related to attitudes, and two related to characteristics (Table 5). Pharmacists had significantly more awareness or understanding of PGx than patients, but both groups expressed concern for how insurers and employers may use their PGx information. A greater proportion of patients agreed that pharmacists should be the preferred PGx provider adjusting medications (p<0.01). Both groups favored insurance coverage for PGx services, though this was significantly greater in the patient group (p<0.001).

Our study findings suggest that pharmacists are aware of PGx but without PGx training in pharmacy school, pharmacists’ perceptions included not feeling knowledgeable about the use of PGx nor understanding the clinical application of PGx for therapeutic decision-making. These results are consistent with findings in previous studies.^(24,25) Despite the requirement from the Accreditation Council for Pharmacy Education and the American Association of Colleges of Pharmacy⁽²⁸⁾ necessitating pharmacy school curricula to incorporate PGx training, education must be in-depth and clinically relevant to what is seen in practice.⁽²²⁾ Utilizing varied educational approaches in addition to traditional didactic approaches to accommodate different learner types is crucial in keeping up with development of knowledge in PGx.⁽²⁶⁾ This creates an opportunity for pharmacists to have a greater impact, not only in MTM services utilizing PGx, but also as educators in pharmacy school curricula. Furthermore, other studies have highlighted pharmacist interest in continuing education on PGx training, however, with rapidly evolving knowledge in this distinctive field, it is important to create a standardized competency-based framework to educate students, faculty, and clinicians to provide education and training in PGx.^(12,17) As discussed in a practice brief, pharmacists need to incorporate the appropriate infrastructure in order to appropriately educate and position themselves as an integral and pivotal component of PGx practice.⁽¹¹⁾ Additionally, pharmacists are willing to educate their patients about PGx and see the value in PGx as a clinical service, but do not feel that they have ample time in their workflow as well as the resources to provide this service. Lastly, there is need for inter-professional education and collaboration among physicians and pharmacists. Given that only about 14.7% of physicians have received formal pharmacogenetic training during medical school and 23% reported PGx training in postgraduate medical training, this is another barrier that must be overcome.⁽⁹⁾ We determined that 70% of pharmacists believe in collaborating with physicians to offer PGx testing, and these types of inter-professional collaborations could also help physicians realize pharmacists’ important role in PGx implementation.

In addition to educational barriers, financial reimbursement is a fundamental limitation in the uptake of PGx. Previous studies have observed patient willingness to pay for PGx services as well as their perceptions around PGx in a community pharmacy setting; however, sample sizes in previous studies have been relatively small (n=27) with a completely homogenous racial population.⁽¹⁵⁾ Our study collected data from a larger sample size of patients as well as varying racial populations across multiple pharmacies. Our results suggest that patients are willing to pay varying amounts for an individualized PGx test. Some patients are willing to pay $300 or less (13%) for a PGx test, which is slightly higher than previously reported.⁽¹⁵⁾ However, 45% of patients would prefer to pay $50 or less and a majority (84%) agreed or strongly agreed that their insurance company should cover the cost of the PGx test. Despite some of these financial challenges, there have been studies aiming to validate reimbursement and the clinical utility of PGx through randomized control trials. A case-control longitudinal study published in 2017 concluded that PGx testing provided a promising strategy to reduce costs and utilization in those with mood and anxiety disorders.⁽²⁹⁾ Validating the cost-effectiveness is an important component of fully integrating PGx into routine clinical practice.

Our study also shows patients were interested in utilizing PGx as a one-time service. Based on a 2017 survey of PGx in a community pharmacy, 74% of patients reported either being somewhat or not very familiar with the term.⁽¹⁵⁾ This is important as familiarity is correlated with knowledge of a term and thus the likelihood of patients being aware of PGx.⁽¹⁵⁾ As the number of direct-to-consumer genetic companies grow, more patients will inherently become accustomed with the term of PGx. Many patients (87%) understood the use of PGx testing would provide useful and beneficial information about their medications and 70% of patients understood some of their medications may have to be changed or adjusted based on PGx results; these results could be explained by the relatively high educational level of patients (85% with a bachelor’s degree or higher) from the urban setting in our survey. We also collected annual income in our demographic questions to explore some possible relationships between patient’s demographics and barriers to PGx implementation. It was not surprising to observe that annual income was statistically significant and positively correlated with patient interest in obtaining PGx tests. Having more disposable income potentially translates to a higher likelihood of spending additional health-related expenses. The several positive correlations observed between being Caucasian and having an interest in PGx testing and a greater understanding of the usefulness of PGx could be explained by the fact that a majority (~71%) of the patient respondents were Caucasian, with 59% of these patients having an income over $75,000. Additionally, research supports the correlation between ethnicity and health disparities across income, ethnic background, education, etc.⁽²⁷⁾ Some of these disparities are further highlighted in our study by the negative correlation between patients who reported a poorer personal health rating and understanding of their medications (and side effects), and the risks and benefits associated with PGx testing. Also, these patients who self-reported a poorer health status were negatively correlated with preferring their physicians to adjust their medications based on PGx results. This could be explained by the previous knowledge that patients with lower socioeconomic and educational backgrounds tend to report poorer general health, and thus may not have access to traditional primary care providers.⁽³⁰⁾Table 4 includes all correlations from our regression analysis, with some warranting future investigation.

Our comparative analyses demonstrated that there was a statistically significant difference between pharmacists and patients regarding awareness of PGx, desire for insurance to cover the cost of the PGx test, personal health rating, preferred provider for PGx services, and willingness to pay cash. It was not surprising that pharmacists had more awareness of PGx testing, given their extensive training in pharmaceutical sciences and mandatory pharmacy school curricula. Despite these differences in awareness of PGx, an almost equal majority of both groups (84% for pharmacists and 85% for patients) did not know someone who had personally undergone PGx testing, a suggestion of the minimal presence of PGx in routine clinical practice. When it came to the cost of PGx testing, it was noteworthy that there was a statistically significant difference in perspectives between pharmacists and patients related to insurance coverage of the PGx test. Patients are more likely to want their insurance company to cover the full cost of the PGx test compared to pharmacists, who by training inherently are more likely to have a better understanding of the healthcare system and the various components that make up formulary decisions and healthcare spending. Given the income gap between pharmacists and patients, we did expect to see a difference in willingness to pay. Personal health rating was also different among pharmacists and patients; we were not surprised by this result as the health status of patients coming to a pharmacy for prescriptions, in general, may not be as good as working pharmacists. An important observation in the comparative analyses was the positive value that patients placed on their pharmacists as a preferred provider to manage their medications based on PGx results, more so than pharmacists placed on themselves. This discrepancy speaks to the attitudes pharmacists currently have towards implementing PGx compared to the confidence patients have in their pharmacists, further emphasizing the need to train and educate our current and future pharmacists to fill this gap.

Several limitations in our study must be discussed. Our pharmacist population was homogeneous from one organization. Although this homogeneity can be useful in terms of implementing a clinical service in this one regional division of a large community pharmacy chain, it is not representative of the broader pharmacist population. Pharmacist response rate was 43%, although this is greater than in previously reported studies (3.7%).⁽¹⁵⁾ Given the fact that our survey used a Likert scale for the perception and attitude questions, there was an inherent survey response bias present with our results. Additionally, selection or a sampling bias is present as the patients and pharmacists were only surveyed from one regional division of a large community pharmacy chain. The discrepancy between patients’ preference for pharmacists as their preferred PGx provider compared to pharmacists’ responses could be explained by selection bias. Additionally, patients’ interest in a one-time PGx could also be attributed to this bias. Lastly, we were only able to collect data for approximately two months; otherwise, our sample size may have been larger, producing more robust results.

Understanding the perceptions and attitudes of pharmacists and patients in the implementation of PGx in community pharmacies is essential. Pharmacists are well positioned healthcare providers that can bridge gaps in PGx implementation; however, they lack optimal perceptions and attitudes in utilizing PGx information for therapeutic decision-making. This extent of PGx education must be standardized across pharmacists’ training. Patients expressed interest in personal PGx testing, are willing to pay for such services and prefer pharmacists to adjust medications based on PGx results. Potential identified barriers have emphasized the need to train and educate our current and future pharmacists to meet patients’ expectations while fulfilling their interest to educate their patients on PGx.