Evaluation of pharmacy students' knowledge and perceptions of pharmacogenetics before and after a simulation activity

Evaluation of pharmacy students' knowledge and perceptions of pharmacogenetics before and after a simulation activity

Currents in Pharmacy Teaching and Learning xxx (xxxx) xxx–xxx Contents lists available at ScienceDirect Currents in Pharmacy Teaching and Learning j...

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Currents in Pharmacy Teaching and Learning xxx (xxxx) xxx–xxx

Contents lists available at ScienceDirect

Currents in Pharmacy Teaching and Learning journal homepage: www.elsevier.com/locate/cptl

Experiences in Teaching and Learning

Evaluation of pharmacy students' knowledge and perceptions of pharmacogenetics before and after a simulation activity ⁎

Radha V. Patel , Melissa Chudow, Teresa T. Vo, Erini S. Serag-Bolos Department of Pharmacotherapeutics and Clinical Research, University of South Florida, College of Pharmacy, 12901 Bruce B. Downs Blvd, MDC 30, Tampa, FL 33612, USA

AR TI CLE I NF O

AB S T R A CT

Keywords: Simulation Pharmacogenetics Standardized patient Counseling Curriculum

Background and purpose: The purpose of this study was to evaluate students’ knowledge and perceptions of the clinical application of pharmacogenetics through a simulation activity and to assess communication of pharmacogenetic-guided treatment recommendations utilizing standardized patients. Educational activity and setting: Third-year students in the four-year doctor of pharmacy (PharmD) program at University of South Florida College of Pharmacy completed a pharmacogenetics simulation involving a patient case review, interpretation of pharmacogenetic test results, completion of a situation, background, assessment, recommendation (SBAR) note with drug therapy recommendations, and patient counseling. Voluntary assessments were completed before and after the simulation, which included demographics, knowledge, and perceptions of students’ ability to interpret and communicate pharmacogenetic results. Findings: Response rates for the pre- and post-simulation assessments were 109 (98%) and 104 (94%), respectively. Correct responses in application-type questions improved after the simulation (74%) compared to before the simulation (44%, p < 0.01). Responses to perception questions shifted towards “strongly agree” or “agree” after the simulation (p < 0.01). Discussion and summary: The simulation gave students an opportunity to apply pharmacogenetics knowledge and allowed them to gain an appreciation of pharmacists’ roles within the pharmacogenetics field.

Background and purpose Pharmacogenetics information is present in the Food and Drug Administration (FDA) approved product labeling of over 150 medications. This labeling outlines the impact of genetic variations on pharmacokinetics, pharmacodynamics, and/or clinical outcomes, but provides little guidance on how that information should be implemented.1 The Clinical Pharmacogenetics Implementation Consortium (CPIC) has developed guidelines for select drug-gene pairs to empower clinicians with an understanding of how to use labeled pharmacogenetics information in a clinically meaningful way.2 With ongoing research and initiatives aimed at personalizing patient care by integration of pharmacogenetic information into the clinical decision-making process as well as growing public interest, pharmacists, as pharmacotherapy experts, are expected to have a working knowledge-base of pharmacogenetics to address questions from the lay and medical communities.3–6 As a way to address this growing need, pharmacogenetics is a required element of the didactic doctor of pharmacy (PharmD) curriculum as indicated by the



Corresponding author. E-mail addresses: [email protected] (R.V. Patel), [email protected] (M. Chudow), [email protected] (T.T. Vo), [email protected] (E.S. Serag-Bolos). http://dx.doi.org/10.1016/j.cptl.2017.09.012

1877-1297/ © 2017 Published by Elsevier Inc.

Please cite this article as: Patel, R.V., Currents in Pharmacy Teaching and Learning (2017), http://dx.doi.org/10.1016/j.cptl.2017.09.012

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Accreditation Council for Pharmacy Education (ACPE) “Standards 2016”.7 However, pharmacogenetic instruction varies from less than 10–60 hours content exposure, delivered through various methods, including didactic lectures, laboratory exercises, and patient care skills courses.8–10 The guidance document published by the American Association of Colleges of Pharmacy (AACP) pharmacogenomics special interest group provides examples of pharmacogenetics content and assessment methods throughout PharmD curricula and how they align with the Center for the Advancement of Pharmacy Education (CAPE) Educational Outcomes 2013. The document concludes with a call to action for incorporation of pharmacogenetics into the clinical pharmacy core curricula.10,11 Previously published studies have demonstrated that an active learning exercise involving personal genetic testing enhanced knowledge of pharmacogenetics concepts among medical and pharmacy students.12–14 Moreover, a clinical pharmacogenetics rotation experience for pharmacy students, residents, and fellows provided opportunities to interpret and apply genotype-guided therapy for the management of warfarin.15 Knoell et al.9 described a pharmacogenetic exercise that consisted of a counseling session where students obtained consent to perform a deoxyribonucleic acid (DNA) swab, interpreted the results, and created a plan. While the use of simulation-based activities has been shown to increase knowledge, confidence, clinical performance, and critical thinking skills, the application and communication of pharmacogenetics in a simulated clinical environment with standardized patients (SPs) is limited in the literature.9,16 The goal of our simulation was to mimic a clinical scenario a student may encounter during advanced pharmacy practice experiences (APPEs) while continuing to strengthen both written and verbal communication skills. Specific objectives of the simulation included: interpretation of pharmacogenetic results utilizing the CPIC guidelines, completion of a written situation, background, assessment, recommendation (SBAR) note detailing therapeutic recommendations, and patient counseling on the purpose of the pharmacogenetic test, results, and treatment plan. The objective of the research component of this activity was to evaluate students’ knowledge and perceptions of the clinical application of pharmacogenetics through the simulation activity and to assess written and verbal communication of pharmacogenetic-guided treatment recommendations utilizing SPs. We hypothesized that students’ ability to utilize course content would increase critical thinking skills through a patient case and students’ understanding of pharmacists’ roles in pharmacogenetics would be enhanced. Educational activity and setting This was an online non-randomized, voluntary, unpaired pre- and post-assessment study assessing students’ knowledge and perceptions of pharmacogenetics before and after a pharmacogenetic simulation activity. During the fall 2015 semester, 113 student pharmacists in their third professional year (P3) were concurrently enrolled in two 16-week three-credit required courses, translational pharmacogenomics and the pharmaceutical skills V course at the University of South Florida College of Pharmacy (USF COP) in Tampa, Florida. Pharmaceutical skills V is part of a longitudinal patient-care laboratory course comprised primarily of simulations with the use of SPs and interprofessional activities during the P3 year. Specific pharmacogenetics content for the simulation was developed by the coordinator of the translational pharmacogenomics course, who is also a post graduate year 2 (PGY-2) trained pharmacogenetics clinical pharmacist. The simulation was focused on cytochrome P450 2C19 (CYP2C19) genotype-guided antiplatelet therapy given the availability of CPIC guidelines.2 Student were lectured on this topic during week 8 and tested on this material during week 11 of the semester. In order to reinforce application, the simulation was conducted during week 13 of the semester. By the time of the simulation, the students had lectures on the pharmacogenomic applications of all major therapeutic areas with CPIC guidelines, including a primer in basic genetics. Genetics is also a required prerequisite for the college. Students had previously participated in similar simulations not related to pharmacogenetics earlier in the semester. Hence, the students were very familiar with the format and expectations of the simulation. One week prior to the simulation, students were notified via an announcement in the Pharmaceutical Skills V course's learning management system to review the cardiology-related pharmacogenetics materials prior to the activity and were also provided with an electronic slide presentation regarding appropriate techniques for counseling patients on pharmacogenetics test results. Students were also notified the activity would be completed within their pre-assigned academic team (five to six students per team) and to bring their laptops/tablets. The pharmacogenetics simulation was conducted in October 2015, during week 13 of the semester, at the Center for Advanced Clinical Learning (CACL) within the USF COP. The CACL is a state of the art simulation center with 12 clinical examination rooms equipped with digital video monitoring and a closed circuit computerized evaluation system, on the USF Health campus. Computers are located both inside and outside the room for student use, and all rooms are linked to master video monitoring within the simulation center control room. Each exam room also has a double-sided mirror that allows evaluators to view and hear the live encounter outside of the room. The CACL also oversees the SP program for university. The program recruits lay people through the Office of Curriculum and Medical Education at the USF Morsani College of Medicine. The SPs are trained using a pre-developed curriculum focused on role-playing and providing written and verbal feedback to students focusing on communication and interpersonal skills. Scripts are provided for specific activities in order to allow the SP to role play clinical encounters with the goal of training student learners. This well-established program provides approximately 60,000 SP encounters each year at USF Health. The simulation only required two faculty members to orient and guide the students to their assigned rooms. On the day of the activity, each team arrived at the simulation center during their assigned time. The simulation was divided into three rounds of 40 min in order to accommodate all 20 academic teams during the three-hour class period. Prior to beginning the simulation, students received a 15-min orientation and were invited to individually complete a non-randomized, voluntary, anonymous pre-simulation assessment. The assessment was built in Qualtrics® (Provo, UT) and consisted of eight multiple-choice questions and four Likert scale questions (1 – “strongly disagree” to 5 – “strongly agree”). Three of the multiple-choice questions collected demographic information 2

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(age, gender, preferred learning styles), and five of the multiple-choice questions were knowledge-based and corresponded with material previously taught in the translational pharmacogenomics course and directly related to the content of the simulation. The Likert scale questions aimed to assess students’ perceptions of their individual and team's ability to interpret and provide drug therapy recommendations based on pharmacogenetics results. The first page of the assessment included a waiver of informed consent. Students who were absent on the day of the simulation and those who did not complete the assessment were excluded from the study. Participation in this study did not impact the student's grade for the activity or the courses. After the pre-simulation assessment, each academic team was given 40 min to complete the simulation experience involving a patient with acute coronary syndrome who had undergone a percutaneous coronary intervention with stent placement. During the first 25–30 min of the simulation, each academic team was given a patient case (available to the reader upon request) along with the pharmacogenetic test results. The team was asked to interpret the results and provide their written recommendation to the attending physician regarding antiplatelet therapy in the form of a SBAR. Teams were permitted to utilize guidelines and other drug information resources to complete the SBAR. Once completed, one note per team was submitted electronically through the course's learning management system. The second part of the simulation consisted of one to two students from each team taking the lead on counseling the SP to explain why the pharmacogenetics test was ordered, what the test result meant, and how the test result would impact the selection of antiplatelet therapy. Rubrics (available to the reader upon request) were used to evaluate the written SBAR (14 points) and patient counseling sessions (50 points). In order to minimize variability in the grading of the simulation, one study investigator evaluated all of the written SBAR notes and one study investigator evaluated all the recorded patient counseling sessions. At the end of the simulation, students were invited to complete the post-simulation assessment that contained the same questions as the pre-simulation assessment. After the students completed the assessment, an informal 10-min post-simulation debrief session was held to gather verbal feedback from the students. Data were analyzed using IBM SPSSv18. Nominal data, such as gender, preferred learning style, and responses to multiple-choice questions on the pre- and post-simulation assessments, were analyzed using the chi-square test. Ordinal data, including responses to the perception questions using the Likert scale, were analyzed using the Wilcoxon-Mann-Whitney test. All p-values were two-sided with an alpha level set at 0.05 for statistical significance. Assessment data and team scores from the written SBAR and patient counseling rubrics were analyzed using descriptive statistics. This study was approved under expedited review by the USF Institutional Review Board. Findings Of the 111 students that completed the simulation activity, 109 (98%) and 104 (94%) students completed the pre- and postsimulation assessments, respectively. Differences in gender in the pre-simulation assessment, female (46%) and male (54%), compared to the post-simulation assessment, 45% (female) and 55% (male), were not statistically significant, p = 0.93. The majority of students completing the pre- and post-simulations assessments were less than 30 years of age (95% and 97%, respectively). A large portion of students indicated their preference towards a combination of learning styles (52% versus 56%) followed by visual learning (28% versus 27%), kinesthetic learning (16% versus 13%) and auditory learning (4% versus 5%). Although a majority of students favored a combination of learning styles, this was not statistically significant, p = 0.88. Results from the knowledge questions are summarized in Table 1. More students answered the knowledge-based questions correctly after the simulation. There was no statistically significant difference seen in recall type questions, such as basic drug interaction questions. On the other hand, a statistically significant difference was seen in responses for questions that focused on guidelines and application of knowledge when presented as a patient case. Additionally, changes in student perceptions regarding their comfort level in formulating a patient-specific plan based on pharmacogenetic results, the team's ability to document recommendations, and the role of the pharmacist in clinical practice as related to pharmacogenetics were statistically significant Table 1 Pre/post-assessment knowledge question responses. Answered Correctly

Assessment Questions What is the CYP2C19 phenotype of a patient carrying two loss of function alleles? Clinical Pharmacogenomics Implementation Consortium developed guidelines for using CYP2C19-genotype guided antiplatelet therapy for which of the following indications? A past medical history of stroke is a contraindication for the use of which of the following antiplatelet medications? Which of the following proton pump inhibitors should be used with caution or avoided in patients prescribed clopidogrel? Which of the following medications may be influenced by a patient's CYP2C19 genotype? CYP, Cytochrome P450. a Chi Square test, p < 0.05 significant.

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Pre (N = 109) n(%)

Post (N = 104) n(%)

p value

103 (95) 51 (47)

103 (99) 63 (61)

0.06 0.04a

48 (44)

76 (73)

< 0.01a

98 (90)

97 (93)

0.38

50 (46)

60 (58)

0.07

4 46 (44) 48 (46) 43 (41)

23 (21) 24 (22)

38 (37)

28 (26)

7 (6)

69 (63)

71 (65)

65 (60)

45 (41)

Pre n (%)

Pre n (%) Post n (%)

Agree

Strongly Agree

CYP, Cytochrome P450. a Wilcoxon-Mann-Whitney test, p < 0.05 significant, shift towards strongly agree/agree in the post-assessment.

Assessment Questions I feel comfortable formulating a patient-specific treatment plan based on a patient's CYP2C19 genotype. I believe my team will be able to make a group decision regarding drug therapy recommendations based on pharmacogenetic results. I believe my team will be able to provide written communication to the healthcare provider regarding drug therapy recommendations based on pharmacogenetic results. I understand the role of pharmacogenomics testing and associated pharmacist's roles in clinical practice.

Table 2 Pre/post-assessment perception question responses.

53 (51)

48 (46)

48 (46)

55 (53)

Post n (%)

11 (10)

11 (10)

14 (13)

44 (40)

Pre n (%)

Neutral

5 (5)

6 (6)

8 (8)

8 (8)

Post n (%)

2 (2)

1 (1)

1 (1)

9 (8)

Pre n (%)

Disagree

1 (1)

1 (1)

1 (1)

1 (1)

Post n (%)

3 (3)

2 (2)

1 (1)

4 (4)

Pre n (%)

2 (2)

1 (1)

1 (1)

2 (2)

Post n (%)

Strongly Disagree

< 0.01a

< 0.01a

< 0.01a

< 0.01a

p value

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(p < 0.01) favoring “agree” or “strongly agree” in the post-simulation assessment compared to the pre-simulation assessment. Table 2 outlines the results of student responses to the perception questions. The average written SBAR and patient counseling grade among the 20 academic teams was 13.5 out of 14 (range 12–14) and 48.6 out of 50 (range 45–50), respectively. Additional verbal feedback gathered from the post-simulation debriefs and course evaluations suggests that the majority of students enjoyed the hands-on approach of the activity and the opportunity to work within their academic teams to collectively reach a recommendation. Few students expressed the desire to complete such simulations individually to ensure adequate competence. Students also provided positive feedback that they gained a deeper appreciation for the pharmacist's role in the therapeutic decision-making process based on a patient's genetic profile. Discussion Pharmacogenetics is deemed by ACPE as an element of the didactic pharmacy curriculum, and is one of the four pillars at the USF COP.7 This emerging aspect of pharmacy practice allows for personalization of therapeutic modalities based on a patient's genetics to maximize effectiveness and reduce adverse effects of medications as well as enhances overall safety. This simulation allowed for integration of other essential pharmacist skills such as critical thinking and verbal and written communication skills. The simulation can be mapped to several CAPE outcomes such as 2.1 (patient-centered care), 3.1 (problemsolving), and 3.6 (communication). In addition, the simulation incorporated several components of the communication domain, such as written (SBAR) and verbal communication (team work and patient counseling).11 Students reported favoring visual and kinesthetic learning styles over auditory, which is consistent with the literature regarding adult learning theory.17 Moreover, students’ reported preference for a combination of learning styles correlates to findings on the knowledge-based assessment questions. Transformative learning changes the way learners consider their environment and involves a shift in awareness.17 This is supported by the statistically significant increase in knowledge on the application type questions on the post-simulation assessment. Based on the post-assessment, students demonstrated they may be able to retain concepts that involve knowledge of guidelines or case-based questions when it is directly related to a simulation activity. However, long-term retention was not assessed as part of our study. Overall, students performed well on the written SBAR and verbal patient counseling sessions. This may be attributed to the purposeful reiteration of these communication skills throughout the curriculum and especially in the P3 year, where students encounter multiple cases that align with content from other courses. Students were familiar with the rubrics used in this simulation, which were only modified with regards to point values for each section. Strengths of this simulation include enhanced application of knowledge acquired through the didactic curriculum as demonstrated by the knowledge assessment results. Curricular alignment is a key focus at the USF COP to enhance content delivery in a coordinated manner and provide an appropriate stepwise approach for mastery of skills. The use of trained SPs also allows for a more real life application of patient interaction and counseling instead of using faculty members or other students as patients. The pharmacogenetics simulation serves to prepare students for other scenarios, such as during APPEs, that may require patient-specific treatment recommendations based on pharmacogenetic results. Tasking the students with reviewing a case, completing an SBAR, and counseling the SP within a 40-min time period also provided the students the ability to utilize their time wisely and expose them to what they may experience on APPEs or during clinical practice. Feedback from students was overall positive with specific mention of the hands-on approach and the ability to work and learn as a team. Such feedback suggests that students recognize the value of teambased learning. In development, faculty intentionally avoided certain challenges by allowing students to work in teams in order to reduce costs associated with hiring SPs that also minimized time needed for grading and providing feedback. Furthermore, the ability to video record the counseling sessions eliminated issues with inter-rater reliability since one faculty member graded all of the assignments by watching the patient counseling sessions and reviewing the written SBAR notes at a later time. The study is not without limitations. The pre- and post-simulation assessments were not paired, which limits the ability to assess individual students’ change in knowledge and perceptions. Even though the majority of students preferred completing the simulation within their academic teams, this limits the ability to assess each member's contribution to the team. One way to overcome this limitation could be through the use of self and peer evaluations and incorporating this as a component of the overall simulation grade. The authors do not anticipate barriers to acceptance of a similar pharmacogenetics simulation at other institutions. Content of didactic lectures would need to be aligned in order to adequately prepare students for the activity. It is appreciated that many colleges and schools of pharmacy may not have the resources or funds to support the use of a simulation center and/or SPs. This activity could be replicated with the use of small break out rooms and patients could be role-played by faculty members or APPE students. Counseling sessions could be recorded through the use of personal recording devices. The approach of using personal recording devices should be carefully considered in order to ensure it is in compliance with the Family Educational Rights and Privacy Act (FERPA) and program policies.18 Another alternative would be to conduct live grading, which may require more evaluators during the activity. Based on the positive student feedback, future directions involve development of a pharmacogenetics elective course as well as enhanced internship and research opportunities in this area. Future modifications for this simulation activity under consideration include incorporation of a practice component where students perform obtaining the sample through a buccal swab as well as utilizing self and peer evaluations. Furthermore, the simulation may be modified to allow an interprofessional component with medical and nursing students. This would further raise awareness and enhance the team-based approach when it comes to application 5

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of pharmacogenetics in clinical practice. The evolving field of pharmacogenetics poses a unique opportunity for the academy and pharmacy curricula to develop new and innovative ways to integrate pharmacogenetics within the PharmD curriculum. This study could be used as an example of an innovative teaching approach to enhance pharmacogenetic application within the pharmacy curricula that could be replicated by other institutions. In addition, to our knowledge, this is the first pharmacogenetic simulation activity to utilize SPs. Summary The pharmacogenetics simulation provided students a unique opportunity to apply pharmacogenetics knowledge to a patient case in a simulated clinical environment. Curricular alignment and strategic integration of key pharmacogenetics concepts with an emphasis on written and verbal communication allowed for deeper understanding and application of materials. There was an improvement in correct responses for the application-based questions in the post-simulation assessment compared to before the simulation. The results of the post-simulation assessment suggest a favorable shift in perceptions regarding the role of the pharmacist as it relates to pharmacogenetics. Acknowledgements The authors would like to thank the CACL staff involved with facilitating the simulation. Conflicts of interest None. Financial disclosures None. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. References 1. US Food and Drug Administration. Table of pharmacogenomic biomarkers in drug labeling; Updated July 12, 2017. Available at: 〈http://www.fda.gov/drugs/ scienceresearch/researchareas/pharmacogenetics/ucm083378.htm〉. Accessed 19 September 2017. 2. Clinical Pharmacogenetics Implementation Consortium. Guidelines. Available at: 〈https://cpicpgx.org/guidelines〉. Accessed 19 September 2017. 3. Weitzel KW, Elsey AR, Langaee TY, et al. Clinical pharmacogenetics implementation: approaches, successes, and challenges. Am J Med Genet C Semin Med Genet. 2014;166C(1):56–67. 4. O’Donnell PH, Danahey K, Jacobs M, et al. Adoption of a clinical pharmacogenomics implementation program during outpatient care–initial results of the University of Chicago “1,200 Patients Project”. Am J Med Genet C Semin Med Genet. 2014;166C(1):68–75. 5. Reiss SM. American Pharmacists Association. Integrating pharmacogenomics into pharmacy practice via medication therapy management. J Am Pharm Assoc (2003). 2011;51(6):e64–e74. 6. McCullough KB, Formea CM, Berg KD, et al. Assessment of the pharmacogenomics educational needs of pharmacists. Am J Pharm Educ. 2011;75(3) [Article 51]. 7. Accreditation Council for Pharmacy Education. Accreditation standards and key elements for the professional program in pharmacy leading to the doctor of pharmacy degree (“Standards 2016”); Published February 2015. Available at: 〈https://www.acpe-accredit.org/pdf/Standards2016FINAL.pdf〉. Accessed 19 September 2017. 8. Murphy JE, Green JS, Adams L, Squire RB, Kuo GM, KcKay A. Pharmacogenomics in the curricula of colleges and schools of pharmacy in the United States. Am J Pharm Educ. 2010;74(1) [Article 7]. 9. Knoell DL, Johnston JS, Bao S, Kelley KA. A genotyping exercise for pharmacogenetics in pharmacy practice. Am J Pharm Educ. 2009;73(3) [Article 43]. 10. Kisor DF, Smith HE, Grace E, Johnson SG, Weitzel KW, Farrell CL. The DNA of pharmacy education: CAPE outcomes and pharmacogenomics. Available at: 〈http:// www.aacp.org/resources/education/cape/Documents/The_DNA_of_Pharmacy_Education-CAPE_Outcomes_and_Pharmacogenomics_2015.pdf〉. Accessed 19 September 2017. 11. Medina MS, Plaza CM, Stowe CD, et al. Center for the advancement of pharmacy education 2013 educational outcomes. Am J Pharm Educ. 2013;77(8) [Article 162]. 12. Salari K, Karczewski KJ, Hudgins L, Ormond KE. Evidence that personal genome testing enhances student learning in a course on genomics and personalized medicine. PLoS One. 2013;8(7):e68853. 13. Adams SM, Anderson KB, Coons JC, et al. Advancing pharmacogenomics education in the core PharmD curriculum through student personal genomic testing. Am J Pharm Educ. 2016;80(1) [Article 3]. 14. Frick A, Benton CS, Scolaro KL, et al. Transitioning pharmacogenomics into the clinical setting: training future pharmacists. Front Pharmacol. 2016;7(241) [Article 241]. 15. Drozda K, Labinov Y, Jiang R, et al. A pharmacogenetics service experience for pharmacy students, residents, and fellows. Am J Pharm Educ. 2013;77(8) [Article 175]. 16. Seybert AL. Patient simulation in pharmacy education. Am J Pharm Educ. 2011;75(9) [Article 187]. 17. Literacy Information and Communication System. TEAL center fact sheet no. 11: adult learning theories. Available at: 〈https://lincs.ed.gov/programs/teal/guide/ adultlearning〉. Accessed 19 September 2017. 18. US Department of Education. Family Educational Rights and Privacy Act (FERPA); Updated June 26, 2015. Available at: 〈http://www2.ed.gov/policy/gen/guid/ fpco/ferpa/index.html〉. Accessed 19 September 2017.

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