Introduction

Melanoma is the fifth most common cancer among males and seventh among females in the USA, with evidence that incidence is increasing [23]. Melanoma comprises an estimated 75 % of skin cancer deaths even though detection and treatment at an early stage can be curative [1]. Skin examination by a skilled clinician improves the opportunity for early-stage detection of melanoma, which could contribute to a reduction of mortality [15].

The United States Surgeon General recommends that all providers remain vigilant about suspicious lesions [24]. While primary care visits provide an opportunity for observation of the skin during physical examinations, some primary care providers (PCPs) feel inadequately prepared for skin cancer detection or overburdened with addressing other health concerns [12, 9]. Research regarding barriers to implementing skin examinations in primary care practice indicates that most PCPs do not feel confident in their ability to detect skin cancers [16]. Interest in dermatology and courses related to skin cancer is increasing among PCPs [2, 10] as well as diagnostic aids for melanoma detection [14]. Evidence is growing that relevant specialty training completed by PCPs improves evaluation and diagnosis of melanoma [4, 13, 11].

The INFORMED (INternet curriculum FOR Melanoma Early Detection) Group, a collaboration of dermatology specialists and primary care, epidemiology, and behavioral science researchers, developed an interactive, online skill-based skin cancer curriculum that focuses on melanoma and skin cancer detection [7]. The curriculum was designed to inform practicing PCPs while improving confidence and skills for skin cancer detection. Given that skills and attitudes compose only one set of factors required to change provider practice, it became vital to explore potential implementation issues for a Web-based curriculum to aid efforts to increase melanoma screening in primary care. Feedback was solicited via focus groups among PCPs with the goal of refining and improving the curriculum and its content. Herein, we summarize the qualitative feedback obtained on the Web-based skin cancer detection curriculum and the feasibility of implementing skin cancer screening in primary care practices.

Methods

The INFORMED curriculum content emphasized identifying melanoma, basal and squamous cell cancer and common mimickers, and a short segment on how to do a complete skin examination.

Providers practicing at two health maintenance organizations of the nine integrated health systems that are members of the National Cancer Institute-supported Cancer Research Network (CRN), Henry Ford Health System and Kaiser Permanente Northern California, were recruited [25]. To encourage participation, participants were offered continuing medical education (CME) credits for completing the training, an honorarium for focus group participation, and a dermatoscope for each practice. Institutional review board’s approval was granted from all investigative sites.

After completing the training, clinicians participated in a 30-min feedback session led by an experienced focus group moderator and the site investigator. Discussions at each site were audio recorded, transcribed verbatim, and de-identified.

The feedback was collected using a semi-structured interview guide (a standardized set of open-ended questions that allows for flexibility of discussion based on the participants’ responses) that focused on four general domains: (1) overall impressions of the curriculum, (2) recommendations for improvement, (3) current skin examination practices of participants, and (4) suggestions for increasing skin screening by PCPs. After all of the sessions were completed, standard qualitative methods were utilized by two qualitative researchers using a priori themes [3]. Subthemes which emerged from these four broad categories were also examined. For discordant coding, the analysis team discussed those items and then came to consensus on appropriate coding. Overall, themes that emerged from the focus groups were similar between those conducted at Henry Ford Health System and at Kaiser Permanente Northern California; thus, no further distinction is made in the presentation or discussion of results.

Results

In total, 54 providers (53 physicians and 1 nurse practitioner) practicing internal medicine, geriatrics, or family medicine from nine practices participated; all providers who viewed the training participated in the focus groups. Providers’ years in practice ranged from 1 year to more than 30 years, with the majority practicing between 10 and 19 years. Fifty-four percent of the participants were women, and the participants were diverse in race/ethnicity. Complete demographics have been previously published [7]. The four domains from feedback sessions are presented below, and the representative quotations are presented in corresponding tables.

Domain 1: Overall Impressions of the Curriculum

Overall, feedback from practicing PCPs was positive and demonstrated an interest in learning more about skin cancer and benign lesions, not only melanoma. PCPs were open to improving their skills, especially if they had easy access to online medical education materials that were accessible for further reference, or reinforcement, once they had completed the training.

Subtheme 1.1: Differentiating Lesions

Specific features in the curriculum to reinforce learning were mentioned. The review and repetition of the A-B-C-D-E (asymmetry, border, color, diameter, and evolving) criteria for evaluating pigmented lesions like melanoma was considered valuable. The providers reported appreciation for the extra time devoted to melanoma; however, some noted that it is much more common to see basal cell carcinoma (BCC) and squamous cell carcinoma (SCC) in clinic and would have preferred more information on these. Favored aspects of the curriculum content included multiple photo examples of each cancerous lesion and comparison of benign mimickers to malignant skin cancers. While the curriculum helped to differentiate some of the cancers, some participants requested teaching/reference aids, such as a summary table or pocket references displaying all three skin cancers (melanoma, BCC, and SCC), and trademark clinical findings that they could easily access when providing clinical care.

Subtheme 1.2: Appreciation of Review

Many PCPs expressed that the curriculum was a good review of information they had previously learned but noted greater confidence in their knowledge post-review. Many participants said they would like to review all or part of the curriculum information again in the future (Table 1).

Table 1 Quotations representative of domain 1: overall impressions of the curriculum
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Domain 2: Improving the Curriculum

Providers generally felt more comfortable with deciding what lesions were appropriate to be referred to dermatology, reinforcing the quantitative findings of improved confidence and attitude towards skin cancer identification [7]. Many participants desired more time with the curriculum, and a few suggested having an expert-guided (dermatologist) curriculum so as to be able to ask questions and receive direct feedback. Some respondents also requested more comparisons between concerning and non-concerning lesions to better distinguish characteristics unique to lesions that should be referred.

Subtheme 2.1: Confidence Regarding Reassure vs Refer

Nearly every group commented on their discomfort with their role in making dermatology referrals and whether all of these referrals were clinically appropriate. Many said that this curriculum helped to increase their confidence in diagnosing possible skin cancer and making appropriate referrals. Some participants reported concerns of continuing to feel unprepared and not yet confident to make distinctions for complex lesions.

Subtheme 2.2: Learning Styles

Participants preferred the self-paced and self-evaluation aspect of the Web-based curriculum. The interactive and repetitive nature of the curriculum was also popular. As a demonstration of the variety of learning styles among our participants and perhaps reflecting the two-dimensional nature of online learning [5], some participants mentioned that viewing two-dimensional lesions in the curriculum was helpful but learning might be more effective with evaluating an actual lesion on a patient, especially with expert guidance. Several respondents indicated their preference to discuss content and consult with PCP colleagues during their clinical decision processes (Table 2).

Table 2 Quotations representative of domain 2: improving the curriculum
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Domain 3: Current Skin Practices

Generally, clinicians reported systematic and personal barriers to incorporating skin examinations in their daily practices. Time constraint was the most common barrier. Nearly all participants commented on the demands to attend to other health maintenance issues during increasingly shorter appointments. Most PCPs felt that they could complete an opportunistic examination during a physical examination (e.g., lung auscultation). Undressing of patients was a full skin examination barrier.

Several providers expressed the barrier of uncertainty about the extent of their role and responsibilities, including concern in pursuing lesions not previously identified by patients. Some respondents preferred to continue referrals to dermatologists when managing their patients (Table 3).

Table 3 Quotations representative of domain 3: current skin practices
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Domain 4: Intent and Increasing Frequency of Skin Screening in Primary Practice Setting

Generally, most PCPs felt that they had a grasp of the dermatology diagnostic process after the curriculum. Practically, several participants expressed that they intended to discuss warning signs, skin protection, and regular self-examinations with their patients. Many providers suggested that they could increase attention to skin irregularities during routine examinations and inquire about family history of skin cancers. Many PCPs agreed that they would ask their patients more frequently about skin changes.

Providers commented that support from the clinic administration and support staff of including skin checks would increase the likelihood of performing skin examinations. Some providers voiced concern that practice likely will not change after completing this educational program due to rigid time and workload constraints. Though their practices may not change, participants noted that the quality of their skin examinations would likely improve due to heightened awareness of distinguishing characteristics of skin cancer (Table 4).

Table 4 Quotations representative of domain 4: increasing frequency of skin screening in primary practice setting
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Discussion

Our focus group findings indicate that PCPs found the curriculum informative and increased their confidence in diagnosing and managing skin cancers. Participants recommended allocating time in the training session for questions, and some participants indicated that they would prefer to evaluate an actual lesion on a patient with expert guidance. Many providers commented that a lack of confidence in performing the screening and time constraints were the main barriers to incorporation of skin examinations during clinical visits. With improved confidence post-training, participants indicated that the quality of their skin examinations would improve but some noted that they did not feel confident in routinely performing or incorporating the exam into their practice. Despite improved confidence in diagnosing and managing skin cancers, participants indicated that time and institutional constraints remain to be barriers to implementation of skin examinations in clinical visits. PCPs also intend to increase discussion regarding skin protection and skin self-examinations with their patients. Focus group comments were incorporated into the final Web-based version (http://www.skinsight.com/info/for_professionals/skin-cancer-detection-informed/skin-cancer-education).

The feedback demonstrates that the curriculum was appreciated among participating PCPs, but it is also effective in improving their subjective confidence in when to refer patients to dermatology. Adoption of the Web-based curriculum in primary care practices at Henry Ford Health Systems and Kaiser Permanente Northern California has also shown quantitative improvement in the diagnosis and management of skin lesions [7]. Participants completed pretest, immediate posttest, and a 6-month posttest and demonstrated significant improvement in scores for correctly reassuring patients regarding suspicious lesions [7]. Participants’ confidence in performing a skilled complete skin examination improved from pretest score 3.6 (1.1) to immediate posttest score 4.3 (0.7) and sustained confidence at the 6-month posttest with 4.2 (1.0) [7]. This is important as previous reports have cited PCPs’ lack of confidence as the main barrier to implementing skin cancer screening [16]. However, despite improving confidence through the INFORMED curriculum qualitatively and quantitatively in diagnosing and managing skin cancers, participants remained hesitant to incorporate skin cancer screening in their daily practice.

Some barriers to successful implementation defined by this study include time, workload, and institutional barriers. Providers expressed concerns about competing demands for their time and with integrating the skin examination into established clinic flow. Participating PCPs felt that they may not be able to increase skin cancer screenings, because both administration and support staff may not have similar expectations. Feedback from PCPs in this study suggests that even in large integrated health system environments dedicated to health maintenance and promotion, institutional barriers exist; this may be even more challenging in other settings. It is established that common barriers preventing implementation of an evidence-based intervention include lack of participant enthusiasm, an organization’s culture, high cost of implementation, intensive time demands, and interaction among these factors [6, 8, 18, 21, 22]. While our focus groups were targeted at helping us to improve the Web-based curriculum, participant feedback underscored the importance of addressing PCP concerns as demands and the interaction of practice and institutional obstacles to ensure success of integrating skin screening into practice. If effectively addressed, integration of more routine skin examination by PCPs has the potential to make an impact on the earlier diagnosis of melanoma. Empowerment, managing expectations, and confidence building will be a key to successfully weaving skin cancer screening into primary care.

While barriers to skin cancer screening implementation have not been well examined, the literature exploring barriers to colorectal cancer, cervical cancer, and breast cancer screening demonstrates that physicians noted managing work overload, addressing comorbid medical illness, and treating competing priorities as barriers to screening [17, 19]. Thus, addressing the organizational issues of work overload and time limitations may help improve not only skin cancer screening but also cancer screening, in general, in the primary care setting.

Both quantitative and qualitative feedback of the curriculum is vital for the successful implementation of a skin screening program internally and for future dissemination [7]. The CRN facilitates cancer research in integrated health-care settings and may be an ideal beginning for implementation of the curriculum in multiple integrated health-care settings before disseminating more broadly among PCPs. The qualitative feedback presented in this study is important for directing changes that may be needed for the possible dissemination and implementation of a Web-based skin cancer curriculum in other primary care practices both at the clinic and institutional level. Committed institution-level support and planning to identify and address both practice and institutional barriers to implementation is imperative for implementation and dissemination of the INFORMED skin cancer curriculum. This ability to scale up an effective intervention is a key issue for dissemination and implementation science [20].

Study Limitations

These study’s findings should be interpreted within the context of its limitations. First, all providers self-selected to complete the curriculum and may have been more interested to incorporate skin cancer screening in their daily practice than general PCPs. Additionally, participants completed the curriculum and subsequent focus groups after long clinic days. Because of the time needed for administrative and study details, participants’ pace through the course at those sessions was accelerated and both of these factors may influence their perceptions of the curriculum. While this evening session may have found providers tired, this may also demonstrate a realistic perspective on how the skin examination and this curriculum fit into providers’ busy schedules and viewpoints. Although this study was open to nurse practitioners and physician assistants, there were a limited number in this study and those present were outnumbered by physicians; hence, interpretation in this group is limited. Participants were employed by two large health maintenance organizations that tend to emphasize preventive efforts more so than some other health systems; thus, further exploration with similar health maintenance organizations is warranted as this curriculum is well aligned with health maintenance organization missions.

Conclusion

Participants were able to absorb new training and improve their skin screening skills, improving confidence in when to refer and when to reassure patients about concerning lesions. Despite improving PCP’s confidence in their ability to detect malignant lesions, participants still noted additional barriers to incorporating skin cancer screening in their practice. The popularity of low-cost, Web-based delivery supports the possibility for widespread dissemination. Future efforts should focus on reducing institutional barriers to implementation of skin cancer screening. Given the rising incidence of melanoma [23], the number of dermatologists available to screen patients will not meet needs. We hope our finding will help inform institutions, who may be considering implementation of INFORMED or similar skin cancer programs, to better prepare and plan for the incorporation of skin cancer screening into practice. Our findings support that provider confidence and skills improvement are insufficient alone; planning and preparation at the institutional level are imperative for successful implementation into practice. Convenient, economical, and accessible online educational curriculum hold potential for improving skin cancer prevention and detection by PCPs.