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Training Primary Care Physicians in Dermoscopy for Skin Cancer Detection: a Scoping Review

Training Primary Care Physicians in Dermoscopy for Skin Cancer Detection: a Scoping Review In many countries, patients with concerning skin lesions will first consult a primary care physician (PCP). Dermoscopy has an evidence base supporting its use in primary care for skin cancer detection, but need for training has been cited as a key barrier to its use. How PCPs train to use dermoscopy is unclear. A scoping literature review was carried out to examine what is known from the published literature about PCP training in dermoscopy. The methodological steps taken in this review followed those described by Arksey and O’Malley, as revised by Levac et al. Four electronic databases were searched for evidence published up to June 2018. Sixteen articles were identified for analysis, all published since 2000. Ten training programs were identified all of which addressed dermoscopy of pigmented skin lesions, among other topics. Ten articles reported on a range of outcomes measured after training and showed generally positive results in terms of improved diagnostic performance, although no meta- analysis was conducted. However, it was unclear whether trained PCPs continued to use dermoscopy after training. Observational questionnaire data revealed that many PCPs use dermoscopy in practice without any formal training. The literature generally supports the use of dermoscopy by PCPs, but it is unclear whether current training leads to long-term change in PCPs’ use of dermoscopy in clinical practice. Understanding this problem, as well as exploring PCPs’ training needs, is essential to develop training programs that will facilitate the uptake and use of dermoscopy in primary care. . . . . . Keywords Dermoscopy Primary Health Care General Practice Melanoma Skin Cancer Continuing Medical Education Introduction cancers from PCPs to specialist services have risen dramati- cally inrecentyears [2]. Dermoscopy has been shown to be an Patients in many countries with new or changing skin lesions effective tool for the detection of melanoma and the triage of will first consult a primary care physician (PCP), commonly other pigmented skin lesions in primary care [3–5]. However, called a family physician or general practitioner. Skin disease these improvements in diagnosis are only achieved after train- makes up a significant proportion of PCP workload; for ex- ing [6], and lack of training has been cited by PCPs in obser- ample, it is estimated that up to 20% of PCP consultations in vational studies as a key barrier to the use of dermoscopy [7, 8]. the UK relate to the skin [1] and referrals of suspected skin Given the potential of dermoscopy to improve skin cancer de- tection in primary care, it is crucial to understand how to train PCPs in dermoscopy, and to highlight where the evidence base Electronic supplementary material The online version of this article is currently insufficient, in order to direct future research. (https://doi.org/10.1007/s13187-019-01647-7) contains supplementary material, which is available to authorized users. Scoping literature reviews have become an increasingly common approach used to summarize and report the existing * Jonathan A. Fee evidence in published literature [9]. Scoping reviews are sim- jfee03@qub.ac.uk ilar to systematic reviews in that they use rigorous and explicit methods that should allow reviews to be replicated. However, Centre for Medical Education, School of Medicine, Dentistry and they differ from systematic reviews in that they aim to map the Biomedical Sciences, Queen’s University Belfast, Whitla Medical main concepts, sources and types of evidence that exist in an Building, 97 Lisburn Road,, Belfast BT9 7BL, Northern Ireland area of research, rather than synthesizing the best available School of Clinical Medicine, The University of Queensland, evidence to answer a specific question [10]. A scoping review Brisbane, Australia presents, in narrative, tabular or diagrammatic form, an School of Medicine, Tehran University of Medical Sciences, account of results from studies with a wide range of study Tehran, Iran 644 J Canc Educ (2020) 35:643–650 designs. However, it does not formally appraise the qual- was sought to ensure that there was adequate coverage ity of the primary studies. It is therefore a useful method- of relevant databases for formal literature searches. ology where the aim is to understand and summarize the Formal literature searches were undertaken between June extent of research in a given area where the body of ev- and July 2018. Four electronic databases were searched: idence is heterogeneous in nature [9, 10]. Given the rela- Embase, MEDLINE, Scopus and Web of Science. Search tively unexplored area of dermoscopy training for PCPs, a terms were altered very slightly between databases to allow scoping review was undertaken with the aim of examining for differences in database subject headings (see current published evidence and to identify where evidence Supplementary Table 1 for Embase search strategy). may be currently insufficient. Relevant articles from previous work conducted by the re- search team were also screened. Methods Step 3: Study Selection Research Team Citations identified in database searches had their abstracts The research team consisted of a general practice special- screened by JAF. Where this was insufficient to make a deci- ty trainee (JAF), and three PCPs (FPM, CR and NDH) sion about selection, the whole article was read, but if there involved in clinical practice, teaching and medical educa- was uncertainty, the article was referred for full-text assess- tion research, all of whom have previous experience in ment for eligibility. As is standard in scoping review methods, scoping literature reviews. JAF, FPM and NDH contrib- articles available only in the form of conference abstracts were uted to the conception of the scoping review. JAF excluded at this stage. Articles written in languages other than screened articles, and JAF and NDH reviewed full texts English were also excluded. for study selection. All the authors contributed to the col- At this stage two reviewers, JAF and NDH met to discuss lation and reporting of the results. the articles. Both reviewers read the full-text articles and con- sidered them for inclusion according to pre-determined inclu- Research Ethics sion and exclusion criteria (Table 1). Any discrepancies in opinion between the reviewers were resolved by discussion Ethical approval was not required for this work, as a second- and agreement reached. ary analysis of published literature within the public domain. Irrespective of whether articles were included in the final review analysis, the reference lists of all articles reaching this Methodological Framework stage were searched, and additional new citations screened by JAF. Any additional articles that passed the screening stage Methodological frameworks for conducting scoping reviews also had their reference lists searched in an iterative process, have been published in the literature. Arksey and O’Malley until no further new citations were generated that reached the developed a framework which was subsequently refined by full-text assessment stage. Levac et al.[10, 11]. This was the framework followed in this review, as outlined in the following steps. Step 1: Identifying the Research Question Table 1 Inclusion and exclusion criteria for article selection Training is recognised as a significant barrier to dermoscopy Inclusion criteria: use in primary care, and the aim of this review was to broadly � Studies examining some aspect of dermoscopy training aimed at investigate dermoscopy training for PCPs. For this reason, an PCPs. open and inclusive question was formed: What can be known � Participants, if applicable, were mainly PCPs or specialty trainees (or from the literature about how PCPs train in dermoscopy? in countries where the term primary care is not in common use, physicians working in a generalist community setting to whom patients self-refer). Step 2: Identifying Relevant Studies Exclusion criteria: � General reviews of dermoscopy not focused on primary care. Initial informal literature searches were carried out to � Commentaries, editorials or letters discussing other articles. � PCPs working in a specialist or secondary care setting. identify the various terms used in the literature for � PCPs participating in screening programs. dermoscopy, PCPs and training. Previous work carried � Teledermoscopy studies in which dermatologists interpret the images. out by the research team had helped to refine some of � Dermoscopy interpreted by artificial intelligence. the search terms. The expertise of a medical librarian J Canc Educ (2020) 35:643–650 645 Step 4: Charting the Data interventional studies also included an observational, ques- tionnaire component [18]. The final two articles were narra- JAF created a data extraction spreadsheet using Microsoft® tive pieces [23, 24]. Excel (Microsoft, Redmond, USA) and populated it with de- tails of the included papers. Extracted data included authors, Origins of Research year of publication, origins of the research, study design, con- tent and mode of delivery of training interventions, outcome Of the articles selected for analysis, six (38%) originated from measures and key findings relating to the review question. The Australia; four (25%) from the USA; two each from Italy and corresponding author of one article was contacted to clarify the Netherlands and one each from Canada, France and Spain. some of their findings [12]. One study was carried out in two centres in different countries, so was counted towards each country’s total [4]. The first Step 5: Collating, Summarizing and Reporting article included in the review was published in 2000 [6], and the Results research in the area has been published steadily since 2005. Guidance published by members of the Joanna Briggs Dermoscopy Training Programs Institute and Joanna Briggs Collaborating Centres was used in reporting the results [13]. This included the classification Eleven articles reported on ten dermoscopy training programs of results under main conceptual categories such as ‘de- for PCPs. Ten articles reported on interventions that included livery format’ for dermoscopy training programs and ‘pre- participants and reported outcomes following the interven- vious dermoscopy training’. It also included use of a tions. The 11th article discussed the development of a skin flowchart to present the literature search and study selec- cancer training program for PCPs [23] but did not involve tion process, and Preferred Reporting Items for participants. The training programs varied widely in terms of Systematic Reviews and Meta-Analyses (PRISMA) guid- content, delivery format and outcome measures. These were ance was adopted for this purpose [14]. categorized, with categories adapted from those presented by Goulart et al. [16] in their systematic review. Definitions of the categories are presented in Supplementary Table 2. Results Curriculum content As shown in Fig. 1, 335 citations were identified from data- base searches, which were carried out sequentially. The fourth Eight curriculum elements were identified among the training database (Embase) produced only two new citations after the programs, and their inclusion in the different programs is exclusion of conference abstracts, neither of which passed the shown in Table 2. All training programs included instruction screening stage, and database searches were deemed to be on skin lesion diagnosis using dermoscopy, and 60% included sufficient. Reference lists identified a large number of addi- at least one dermatoscopic algorithm. Seventy per cent also tional records; however, very few were relevant to the scoping included training on the clinical diagnosis of skin lesions with- review, and only three articles identified in this way were out dermoscopy. All programs trained participants on the dif- included in the review analysis. ferentiation of benign and potentially malignant pigmented skin lesions, but only three included non-pigmented skin le- Study Design sions. Two studies included training on other diagnostic tools, such as dermatoscopic photography [5] and sequential digital Sixteen articles were included in the review analysis, compris- dermoscopy imaging [19]. All programs addressed at least ing a range of study designs. Three systematic reviews were three of the elements, and the largest number of elements identified, none of which conducted meta-analysis due to addressed in any one training program was seven, as detailed study heterogeneity [3, 15, 16]. Ten articles involved interven- in Table 2. tional studies, five of which reported on four randomised con- trolled trials (RCTs) [4–6, 12, 17]; the other five on uncon- Delivery Format trolled studies of various designs [18–22]. PCPs were the sole participants reported on in seven of the papers; a small number Training was delivered using at least one of four formats. Live of physician assistants or doctors in other medical specialties training and use of e-learning were the commonest formats participated in the studies reported in three articles, but these used, with six programs utilising each approach. Five pro- papers were included in the review as PCPs formed the ma- grams used literature to deliver content, and four used self- jority of participants [12, 17, 22]. One observational question- assessment. Seven programs used a combination of at least naire study was identified [7], and one of the uncontrolled two formats, and three programs employed three formats to 646 J Canc Educ (2020) 35:643–650 Fig. 1 PRISMA flowchart of 595 additional records study selection process [13] 335 records identified through identified through other sources database searching (e.g. reference lists) 394 duplicate records 930 records identified removed 536 unique records 510 records excluded screened for inclusion 10 full-text articles excluded: 26 full-text articles assessed for eligibility 5 not dermoscopy training 3 not PCPs 1 commentary 1 not available 16 articles included in review deliver training, as shown in Table 2. Duration of training categories. Eight studies reported statistically significant varied from 1 h to 6 months and was not specified in one study improvements in at least one outcome measure. Of the [18]. Live training sessions lasted between 2 and 10 h, al- remaining studies, one reported on cost-effectiveness of though two studies specified that only 50–60% of this time dermoscopy in primary care and a cost-effectiveness ac- was dedicated to dermoscopy training [4, 5]. Longer training ceptability curve showed almost 100% chance of cost- periods were seen in self-directed learning programs, although effectiveness with €1000 investment [5]; the other did the study with the longest training period of 6 months did not not report any statistical tests [12]. report the length of time that participants actually spent en- Duration of follow-up when assessing outcomes after train- gaging with training materials [21]. In one study, the time ing interventions was reported in nine studies and ranged from taken to train and complete the post-training test were reported 2 days to 19 months, median 6 months. Shorter follow-up as a combined total [22]. periods were generally seen in studies in which participants were followed up to a post-intervention test. Studies with lon- Training Outcomes ger follow-up periods were generally trials involving data col- lection from participants’ clinical practice over a period of Ten of the 11 articles assessed participants following training, months. while one article was solely descriptive [23]. The outcome measures were heterogeneous, which precluded meta-analy- sis. Seven of the ten studies made a measure of diagnostic Previous Dermoscopy Training performance in the clinical setting, four measured knowledge or skills in a classroom setting using photographs, two Three studies explored the previous dermoscopy training un- assessed confidence or attitudes and one measured cost-effec- dertaken by PCPs. Two observational questionnaire studies tiveness, a system outcome [5]. One study adopted a pass found that approximately 16% of PCPs reported having had standard for participants, which was set at 85% [17]. Four some training in dermoscopy [7, 18]. Another article reported studies had outcome measures belonging to two different the provision of dermoscopy training for primary care trainees Included Eligibility Screening Identification J Canc Educ (2020) 35:643–650 647 Table 2 Characteristics of dermoscopy training programs for PCPs Article Training curriculum (listed by first author and year of publication Epidemiology Pigmented Non- Clinical Dermatoscopic Dermatoscopic Management Other and ordered by year of publication starting lesions pigmented diagnosis diagnosis algorithm diagnostic with the most recent) lesions tools Robinson, 2018 [17] X X XXX Robinson , 2018 [12] X X XXX Secker, 2017 [18]X X X X Koelink, 2014 [5]X X X X X X X Shaikh, 2012 [23]X X X X X X Grimaldi, 2009 [20]X X X Menzies, 2009 [19]X X X Youl, 2007 [21]X X X X X Argenziano, 2006 [4]X X X X X Dolianitis, 2005 [22]X X X Westerhoff, 2000 [6]X X X Article Delivery format Outcome measures (listed by first author and year of publication Live Literature E-learning Self-assessment Diagnostic performance Knowledge/skill Confidence/attitude System outcomes and ordered by year of publication starting with the most recent) c d d Robinson, 2018 [17] XX X X c a a Robinson , 2018 [12] XX X X Secker, 2017 [18]XX X X Koelink, 2014 [5]X X X Shaikh, 2012 [23] X X Not applicable Grimaldi, 2009 [20]X X X X d d Menzies, 2009 [19]XX X X X Youl, 2007 [21]X X Argenziano, 2006 [4]X X Dolianitis, 2005 [22]X X X X Westerhoff, 2000 [6]XX X No statistical test reported No statistical test reported, but reported almost 100% chance of cost-effectiveness with €1000 investment Twoarticlesreportedonthe same training program Statistically significant improvement reported in at least one measure in outcome category 648 J Canc Educ (2020) 35:643–650 by their training provider in the form of dermatoscopes and All training programs included the assessment of reference materials [24]. pigmented skin lesions, while a minority addressed non- One study looking at training among French PCPs [7] pigmented skin lesions. This fits with the findings of an ob- showed that over half of dermoscopy users had undertaken servational questionnaire study by Chappuis et al.[7]of no formal training, with the commonest type of formal train- French PCPs, which reported that dermoscopy was used more ing reported being from books (21%), individual instruction for the assessment of pigmented than for non-pigmented skin from a dermatologist (13%), attending a course (8%) or online lesions. However, it raises the concern that current training (5%). Of those in this study undertaking continued dermoscopy training may not equip PCPs well to identify training, the commonest forms were attending seminars (30%) non-pigmented skin cancers including amelanotic melano- and online training (30%), followed by books (13%), and a mas. The majority of training programs included instruction combination of forms (13%). The total time spent on on the clinical diagnosis of skin lesions, and several included dermoscopy training by most PCPs was short: less than other areas of background information such as risk factors for 1 day for 50% of respondents. Conversely respondents indi- skin cancer. This highlights that dermoscopy is an assessment cated that they felt 7 days was an acceptable length of training tool used as an adjunct rather than an alternative to PCPs’ to undertake. routine history and examination of skin lesions, and successful use of it will therefore be conditional on PCPs’ proficiency in these other fundamental clinical skills in skin cancer detection and lesion assessment. Discussion Diagnostic performance in the clinical setting was the most commonly reported outcome in trials, and dermoscopy signif- Principal Findings icantly improved performance in the majority. However only Assessing skin lesions and detecting skin cancer are impor- one trial addressed a systems outcome [5]. Trials all had rela- tant roles of PCPs, and training PCPs to use dermoscopy can tively short follow-up periods, so it is not possible to deter- help them in this task. This scoping review identified 16 arti- mine what effect, if any, dermoscopy training has had on cles that have addressed PCP training in dermoscopy. Three longer-term use of dermoscopy in clinical practice. Of note, articles were systematic reviews, and 11 articles reported on one study reported that none of the participants purchased a ten training programs for PCPs. Among these were ten inter- dermatoscope to continue to use it in clinical practice after the ventional studies; however, variability in study designs and conclusion of the study, despite the improved outcomes that outcome measures precluded any meta-analysis, in keeping dermoscopy training led to during the trial [12]. It may be that with previously published reviews [3, 15, 16]. current programs are not meeting the training needs of partic- ipants in order to facilitate on-going use of dermoscopy in The majority of programs used more than one format to deliver training, but the commonest formats were live delivery independent practice, and it is notable that only one study and e-learning. E-learning in a self-study format was consid- set a pass standard for participants [17]. However, it must also ered advantageous where participants had to reach a be acknowledged that training is not the only barrier to predetermined standard of competency, as the educational dermoscopy use, and others such as equipment costs must also time required to reach that standard varied between students be considered and addressed [7, 8]. [17]. E-learning formats were also considered helpful in over- coming distance barriers between learners and teachers, and in Limitations offering a degree of individualisation of learning to partici- pants [23]. However, while the risk of social isolation of Scoping reviews are exploratory, and despite using a rigorous learners using e-learning formats has been acknowledged and recognised methodology, other papers of relevance may [23], and attending in-person live teaching remains a popular have been overlooked. Furthermore, it is likely that choice for continuing professional development in dermoscopy training programs exist in unpublished forms, dermoscopy among PCPs [7], the influence on PCPs of direct for example for online or university dermoscopy courses. contact with dermoscopy experts or other learners in live for- However, while these could give further insights into mats was not explored in the studies identified in this review. dermoscopy training, it was decided not to search for these The duration of live teaching in training programs was gener- as part of this scoping review; these courses are open to ally short, similar to the short training that PCPs reported healthcare workers in many different specialties and roles, so undertaking in an observational questionnaire study [7]. may not have directly addressed the review question with its However, evidence that many PCPs are using dermoscopy focus on PCPs. in practice without any formal training raises questions about Given the high proportion of trials with significant results the accessibility of training, and the competence of these un- in this review, we must acknowledge the potential for publi- trained PCPs [7]. cation bias to influence our findings. By limiting our review to J Canc Educ (2020) 35:643–650 649 English language articles for practical reasons, published No qualitative work has been identified in the published work in other languages may have been overlooked. literature. Qualitative research could be useful in exploring The details of training programs were based on information translational problems, could be carried out at little cost and described in published articles, and there may have been ele- could contribute to a better understanding of PCPs’ percep- ments of programs that were not mentioned by authors and so tions of dermoscopy and dermoscopy training that may help to were not available to the reviewers. Categorising training pro- facilitate uptake of dermoscopy. grams will have obscured some of the nuanced differences between them but is acceptable in a scoping review where the aim is to describe the range and extent of published Conclusions evidence. Focusing on PCP training means that other forms of This scoping literature review has demonstrated that dermoscopy training in other areas of healthcare may have dermoscopy training for PCPs is currently highly varied, and gone unnoticed. Other specialties such as dermatology may published trials generally report positive outcomes of training have more established or better-tested forms of training. on clinical care in terms of improved diagnosis of skin lesions. However, unlike dermatologists, for PCPs, skin lesion assess- However, PCPs who attend short dermoscopy training pro- ment forms a minority, though significant part, of their clinical grams may not continue to use it longer-term in practice, while work, and dermoscopy use for PCPs will not be as regular as conversely, some PCPs are using dermoscopy with no formal for dermatologists. PCPs often work in more solitary clinical training. Given the valuable role of dermoscopy in the detec- environments, without close proximity to other dermoscopy tion of skin cancers, further work to better define these prob- users. The recognition of these differences, and an acknowl- lems and to seek timely solutions is essential. In particular, edgement that developing and retaining competencies in qualitative research could help to clarify PCPs’ training needs dermoscopy may require a distinct approach for PCPs, led to and to guide training program development to facilitate uptake a focus on PCP dermoscopy training in this review. of dermoscopy in primary care. Acknowledgements The authors would like to thank Richard Fallis, Research Gaps Medicine, Dentistry and Biomedical Sciences Librarian, Queen’s University Belfast, for his expertise in formulating the literature search strategy. This review has highlighted several important gaps in our JAF’s study fees and maintenance come from Health and Social Care current knowledge of dermoscopy training. Firstly, longer- Research and Development Division, Public Health Agency’sGP term follow-up is needed to determine whether current Academic Research Training Scheme and EAT/5336/17. dermoscopy training programs influence PCPs’ on-going practice. One study noted poor continuing use of dermoscopy Compliance with Ethical Standards among participants [12], and elucidating the factors that con- Conflicts of Interest The authors declare that they have no conflict of tribute to these translational difficulties more fully is essential interest. in supporting use of dermoscopy in primary care. The lack of long-term follow-up also means that there has Open Access This article is distributed under the terms of the Creative been limited study of the impact of PCP dermoscopy training Commons Attribution 4.0 International License (http:// creativecommons.org/licenses/by/4.0/), which permits unrestricted use, on wider healthcare systems such as dermatology or hospital distribution, and reproduction in any medium, provided you give skin cancer clinics. This is essential to determine whether appropriate credit to the original author(s) and the source, provide a link dermoscopy should remain the preserve of a small group of to the Creative Commons license, and indicate if changes were made. PCPs with specialist interest in dermatology and skin cancer, or whether it should be expanded to become a standard as- sessment tool across primary care, similar to a stethoscope or ophthalmoscope. 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Training Primary Care Physicians in Dermoscopy for Skin Cancer Detection: a Scoping Review

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Publisher
Springer Journals
Copyright
Copyright © The Author(s) 2019
Subject
Biomedicine; Cancer Research; Pharmacology/Toxicology
ISSN
0885-8195
eISSN
1543-0154
DOI
10.1007/s13187-019-01647-7
Publisher site
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Abstract

In many countries, patients with concerning skin lesions will first consult a primary care physician (PCP). Dermoscopy has an evidence base supporting its use in primary care for skin cancer detection, but need for training has been cited as a key barrier to its use. How PCPs train to use dermoscopy is unclear. A scoping literature review was carried out to examine what is known from the published literature about PCP training in dermoscopy. The methodological steps taken in this review followed those described by Arksey and O’Malley, as revised by Levac et al. Four electronic databases were searched for evidence published up to June 2018. Sixteen articles were identified for analysis, all published since 2000. Ten training programs were identified all of which addressed dermoscopy of pigmented skin lesions, among other topics. Ten articles reported on a range of outcomes measured after training and showed generally positive results in terms of improved diagnostic performance, although no meta- analysis was conducted. However, it was unclear whether trained PCPs continued to use dermoscopy after training. Observational questionnaire data revealed that many PCPs use dermoscopy in practice without any formal training. The literature generally supports the use of dermoscopy by PCPs, but it is unclear whether current training leads to long-term change in PCPs’ use of dermoscopy in clinical practice. Understanding this problem, as well as exploring PCPs’ training needs, is essential to develop training programs that will facilitate the uptake and use of dermoscopy in primary care. . . . . . Keywords Dermoscopy Primary Health Care General Practice Melanoma Skin Cancer Continuing Medical Education Introduction cancers from PCPs to specialist services have risen dramati- cally inrecentyears [2]. Dermoscopy has been shown to be an Patients in many countries with new or changing skin lesions effective tool for the detection of melanoma and the triage of will first consult a primary care physician (PCP), commonly other pigmented skin lesions in primary care [3–5]. However, called a family physician or general practitioner. Skin disease these improvements in diagnosis are only achieved after train- makes up a significant proportion of PCP workload; for ex- ing [6], and lack of training has been cited by PCPs in obser- ample, it is estimated that up to 20% of PCP consultations in vational studies as a key barrier to the use of dermoscopy [7, 8]. the UK relate to the skin [1] and referrals of suspected skin Given the potential of dermoscopy to improve skin cancer de- tection in primary care, it is crucial to understand how to train PCPs in dermoscopy, and to highlight where the evidence base Electronic supplementary material The online version of this article is currently insufficient, in order to direct future research. (https://doi.org/10.1007/s13187-019-01647-7) contains supplementary material, which is available to authorized users. Scoping literature reviews have become an increasingly common approach used to summarize and report the existing * Jonathan A. Fee evidence in published literature [9]. Scoping reviews are sim- jfee03@qub.ac.uk ilar to systematic reviews in that they use rigorous and explicit methods that should allow reviews to be replicated. However, Centre for Medical Education, School of Medicine, Dentistry and they differ from systematic reviews in that they aim to map the Biomedical Sciences, Queen’s University Belfast, Whitla Medical main concepts, sources and types of evidence that exist in an Building, 97 Lisburn Road,, Belfast BT9 7BL, Northern Ireland area of research, rather than synthesizing the best available School of Clinical Medicine, The University of Queensland, evidence to answer a specific question [10]. A scoping review Brisbane, Australia presents, in narrative, tabular or diagrammatic form, an School of Medicine, Tehran University of Medical Sciences, account of results from studies with a wide range of study Tehran, Iran 644 J Canc Educ (2020) 35:643–650 designs. However, it does not formally appraise the qual- was sought to ensure that there was adequate coverage ity of the primary studies. It is therefore a useful method- of relevant databases for formal literature searches. ology where the aim is to understand and summarize the Formal literature searches were undertaken between June extent of research in a given area where the body of ev- and July 2018. Four electronic databases were searched: idence is heterogeneous in nature [9, 10]. Given the rela- Embase, MEDLINE, Scopus and Web of Science. Search tively unexplored area of dermoscopy training for PCPs, a terms were altered very slightly between databases to allow scoping review was undertaken with the aim of examining for differences in database subject headings (see current published evidence and to identify where evidence Supplementary Table 1 for Embase search strategy). may be currently insufficient. Relevant articles from previous work conducted by the re- search team were also screened. Methods Step 3: Study Selection Research Team Citations identified in database searches had their abstracts The research team consisted of a general practice special- screened by JAF. Where this was insufficient to make a deci- ty trainee (JAF), and three PCPs (FPM, CR and NDH) sion about selection, the whole article was read, but if there involved in clinical practice, teaching and medical educa- was uncertainty, the article was referred for full-text assess- tion research, all of whom have previous experience in ment for eligibility. As is standard in scoping review methods, scoping literature reviews. JAF, FPM and NDH contrib- articles available only in the form of conference abstracts were uted to the conception of the scoping review. JAF excluded at this stage. Articles written in languages other than screened articles, and JAF and NDH reviewed full texts English were also excluded. for study selection. All the authors contributed to the col- At this stage two reviewers, JAF and NDH met to discuss lation and reporting of the results. the articles. Both reviewers read the full-text articles and con- sidered them for inclusion according to pre-determined inclu- Research Ethics sion and exclusion criteria (Table 1). Any discrepancies in opinion between the reviewers were resolved by discussion Ethical approval was not required for this work, as a second- and agreement reached. ary analysis of published literature within the public domain. Irrespective of whether articles were included in the final review analysis, the reference lists of all articles reaching this Methodological Framework stage were searched, and additional new citations screened by JAF. Any additional articles that passed the screening stage Methodological frameworks for conducting scoping reviews also had their reference lists searched in an iterative process, have been published in the literature. Arksey and O’Malley until no further new citations were generated that reached the developed a framework which was subsequently refined by full-text assessment stage. Levac et al.[10, 11]. This was the framework followed in this review, as outlined in the following steps. Step 1: Identifying the Research Question Table 1 Inclusion and exclusion criteria for article selection Training is recognised as a significant barrier to dermoscopy Inclusion criteria: use in primary care, and the aim of this review was to broadly � Studies examining some aspect of dermoscopy training aimed at investigate dermoscopy training for PCPs. For this reason, an PCPs. open and inclusive question was formed: What can be known � Participants, if applicable, were mainly PCPs or specialty trainees (or from the literature about how PCPs train in dermoscopy? in countries where the term primary care is not in common use, physicians working in a generalist community setting to whom patients self-refer). Step 2: Identifying Relevant Studies Exclusion criteria: � General reviews of dermoscopy not focused on primary care. Initial informal literature searches were carried out to � Commentaries, editorials or letters discussing other articles. � PCPs working in a specialist or secondary care setting. identify the various terms used in the literature for � PCPs participating in screening programs. dermoscopy, PCPs and training. Previous work carried � Teledermoscopy studies in which dermatologists interpret the images. out by the research team had helped to refine some of � Dermoscopy interpreted by artificial intelligence. the search terms. The expertise of a medical librarian J Canc Educ (2020) 35:643–650 645 Step 4: Charting the Data interventional studies also included an observational, ques- tionnaire component [18]. The final two articles were narra- JAF created a data extraction spreadsheet using Microsoft® tive pieces [23, 24]. Excel (Microsoft, Redmond, USA) and populated it with de- tails of the included papers. Extracted data included authors, Origins of Research year of publication, origins of the research, study design, con- tent and mode of delivery of training interventions, outcome Of the articles selected for analysis, six (38%) originated from measures and key findings relating to the review question. The Australia; four (25%) from the USA; two each from Italy and corresponding author of one article was contacted to clarify the Netherlands and one each from Canada, France and Spain. some of their findings [12]. One study was carried out in two centres in different countries, so was counted towards each country’s total [4]. The first Step 5: Collating, Summarizing and Reporting article included in the review was published in 2000 [6], and the Results research in the area has been published steadily since 2005. Guidance published by members of the Joanna Briggs Dermoscopy Training Programs Institute and Joanna Briggs Collaborating Centres was used in reporting the results [13]. This included the classification Eleven articles reported on ten dermoscopy training programs of results under main conceptual categories such as ‘de- for PCPs. Ten articles reported on interventions that included livery format’ for dermoscopy training programs and ‘pre- participants and reported outcomes following the interven- vious dermoscopy training’. It also included use of a tions. The 11th article discussed the development of a skin flowchart to present the literature search and study selec- cancer training program for PCPs [23] but did not involve tion process, and Preferred Reporting Items for participants. The training programs varied widely in terms of Systematic Reviews and Meta-Analyses (PRISMA) guid- content, delivery format and outcome measures. These were ance was adopted for this purpose [14]. categorized, with categories adapted from those presented by Goulart et al. [16] in their systematic review. Definitions of the categories are presented in Supplementary Table 2. Results Curriculum content As shown in Fig. 1, 335 citations were identified from data- base searches, which were carried out sequentially. The fourth Eight curriculum elements were identified among the training database (Embase) produced only two new citations after the programs, and their inclusion in the different programs is exclusion of conference abstracts, neither of which passed the shown in Table 2. All training programs included instruction screening stage, and database searches were deemed to be on skin lesion diagnosis using dermoscopy, and 60% included sufficient. Reference lists identified a large number of addi- at least one dermatoscopic algorithm. Seventy per cent also tional records; however, very few were relevant to the scoping included training on the clinical diagnosis of skin lesions with- review, and only three articles identified in this way were out dermoscopy. All programs trained participants on the dif- included in the review analysis. ferentiation of benign and potentially malignant pigmented skin lesions, but only three included non-pigmented skin le- Study Design sions. Two studies included training on other diagnostic tools, such as dermatoscopic photography [5] and sequential digital Sixteen articles were included in the review analysis, compris- dermoscopy imaging [19]. All programs addressed at least ing a range of study designs. Three systematic reviews were three of the elements, and the largest number of elements identified, none of which conducted meta-analysis due to addressed in any one training program was seven, as detailed study heterogeneity [3, 15, 16]. Ten articles involved interven- in Table 2. tional studies, five of which reported on four randomised con- trolled trials (RCTs) [4–6, 12, 17]; the other five on uncon- Delivery Format trolled studies of various designs [18–22]. PCPs were the sole participants reported on in seven of the papers; a small number Training was delivered using at least one of four formats. Live of physician assistants or doctors in other medical specialties training and use of e-learning were the commonest formats participated in the studies reported in three articles, but these used, with six programs utilising each approach. Five pro- papers were included in the review as PCPs formed the ma- grams used literature to deliver content, and four used self- jority of participants [12, 17, 22]. One observational question- assessment. Seven programs used a combination of at least naire study was identified [7], and one of the uncontrolled two formats, and three programs employed three formats to 646 J Canc Educ (2020) 35:643–650 Fig. 1 PRISMA flowchart of 595 additional records study selection process [13] 335 records identified through identified through other sources database searching (e.g. reference lists) 394 duplicate records 930 records identified removed 536 unique records 510 records excluded screened for inclusion 10 full-text articles excluded: 26 full-text articles assessed for eligibility 5 not dermoscopy training 3 not PCPs 1 commentary 1 not available 16 articles included in review deliver training, as shown in Table 2. Duration of training categories. Eight studies reported statistically significant varied from 1 h to 6 months and was not specified in one study improvements in at least one outcome measure. Of the [18]. Live training sessions lasted between 2 and 10 h, al- remaining studies, one reported on cost-effectiveness of though two studies specified that only 50–60% of this time dermoscopy in primary care and a cost-effectiveness ac- was dedicated to dermoscopy training [4, 5]. Longer training ceptability curve showed almost 100% chance of cost- periods were seen in self-directed learning programs, although effectiveness with €1000 investment [5]; the other did the study with the longest training period of 6 months did not not report any statistical tests [12]. report the length of time that participants actually spent en- Duration of follow-up when assessing outcomes after train- gaging with training materials [21]. In one study, the time ing interventions was reported in nine studies and ranged from taken to train and complete the post-training test were reported 2 days to 19 months, median 6 months. Shorter follow-up as a combined total [22]. periods were generally seen in studies in which participants were followed up to a post-intervention test. Studies with lon- Training Outcomes ger follow-up periods were generally trials involving data col- lection from participants’ clinical practice over a period of Ten of the 11 articles assessed participants following training, months. while one article was solely descriptive [23]. The outcome measures were heterogeneous, which precluded meta-analy- sis. Seven of the ten studies made a measure of diagnostic Previous Dermoscopy Training performance in the clinical setting, four measured knowledge or skills in a classroom setting using photographs, two Three studies explored the previous dermoscopy training un- assessed confidence or attitudes and one measured cost-effec- dertaken by PCPs. Two observational questionnaire studies tiveness, a system outcome [5]. One study adopted a pass found that approximately 16% of PCPs reported having had standard for participants, which was set at 85% [17]. Four some training in dermoscopy [7, 18]. Another article reported studies had outcome measures belonging to two different the provision of dermoscopy training for primary care trainees Included Eligibility Screening Identification J Canc Educ (2020) 35:643–650 647 Table 2 Characteristics of dermoscopy training programs for PCPs Article Training curriculum (listed by first author and year of publication Epidemiology Pigmented Non- Clinical Dermatoscopic Dermatoscopic Management Other and ordered by year of publication starting lesions pigmented diagnosis diagnosis algorithm diagnostic with the most recent) lesions tools Robinson, 2018 [17] X X XXX Robinson , 2018 [12] X X XXX Secker, 2017 [18]X X X X Koelink, 2014 [5]X X X X X X X Shaikh, 2012 [23]X X X X X X Grimaldi, 2009 [20]X X X Menzies, 2009 [19]X X X Youl, 2007 [21]X X X X X Argenziano, 2006 [4]X X X X X Dolianitis, 2005 [22]X X X Westerhoff, 2000 [6]X X X Article Delivery format Outcome measures (listed by first author and year of publication Live Literature E-learning Self-assessment Diagnostic performance Knowledge/skill Confidence/attitude System outcomes and ordered by year of publication starting with the most recent) c d d Robinson, 2018 [17] XX X X c a a Robinson , 2018 [12] XX X X Secker, 2017 [18]XX X X Koelink, 2014 [5]X X X Shaikh, 2012 [23] X X Not applicable Grimaldi, 2009 [20]X X X X d d Menzies, 2009 [19]XX X X X Youl, 2007 [21]X X Argenziano, 2006 [4]X X Dolianitis, 2005 [22]X X X X Westerhoff, 2000 [6]XX X No statistical test reported No statistical test reported, but reported almost 100% chance of cost-effectiveness with €1000 investment Twoarticlesreportedonthe same training program Statistically significant improvement reported in at least one measure in outcome category 648 J Canc Educ (2020) 35:643–650 by their training provider in the form of dermatoscopes and All training programs included the assessment of reference materials [24]. pigmented skin lesions, while a minority addressed non- One study looking at training among French PCPs [7] pigmented skin lesions. This fits with the findings of an ob- showed that over half of dermoscopy users had undertaken servational questionnaire study by Chappuis et al.[7]of no formal training, with the commonest type of formal train- French PCPs, which reported that dermoscopy was used more ing reported being from books (21%), individual instruction for the assessment of pigmented than for non-pigmented skin from a dermatologist (13%), attending a course (8%) or online lesions. However, it raises the concern that current training (5%). Of those in this study undertaking continued dermoscopy training may not equip PCPs well to identify training, the commonest forms were attending seminars (30%) non-pigmented skin cancers including amelanotic melano- and online training (30%), followed by books (13%), and a mas. The majority of training programs included instruction combination of forms (13%). The total time spent on on the clinical diagnosis of skin lesions, and several included dermoscopy training by most PCPs was short: less than other areas of background information such as risk factors for 1 day for 50% of respondents. Conversely respondents indi- skin cancer. This highlights that dermoscopy is an assessment cated that they felt 7 days was an acceptable length of training tool used as an adjunct rather than an alternative to PCPs’ to undertake. routine history and examination of skin lesions, and successful use of it will therefore be conditional on PCPs’ proficiency in these other fundamental clinical skills in skin cancer detection and lesion assessment. Discussion Diagnostic performance in the clinical setting was the most commonly reported outcome in trials, and dermoscopy signif- Principal Findings icantly improved performance in the majority. However only Assessing skin lesions and detecting skin cancer are impor- one trial addressed a systems outcome [5]. Trials all had rela- tant roles of PCPs, and training PCPs to use dermoscopy can tively short follow-up periods, so it is not possible to deter- help them in this task. This scoping review identified 16 arti- mine what effect, if any, dermoscopy training has had on cles that have addressed PCP training in dermoscopy. Three longer-term use of dermoscopy in clinical practice. Of note, articles were systematic reviews, and 11 articles reported on one study reported that none of the participants purchased a ten training programs for PCPs. Among these were ten inter- dermatoscope to continue to use it in clinical practice after the ventional studies; however, variability in study designs and conclusion of the study, despite the improved outcomes that outcome measures precluded any meta-analysis, in keeping dermoscopy training led to during the trial [12]. It may be that with previously published reviews [3, 15, 16]. current programs are not meeting the training needs of partic- ipants in order to facilitate on-going use of dermoscopy in The majority of programs used more than one format to deliver training, but the commonest formats were live delivery independent practice, and it is notable that only one study and e-learning. E-learning in a self-study format was consid- set a pass standard for participants [17]. However, it must also ered advantageous where participants had to reach a be acknowledged that training is not the only barrier to predetermined standard of competency, as the educational dermoscopy use, and others such as equipment costs must also time required to reach that standard varied between students be considered and addressed [7, 8]. [17]. E-learning formats were also considered helpful in over- coming distance barriers between learners and teachers, and in Limitations offering a degree of individualisation of learning to partici- pants [23]. However, while the risk of social isolation of Scoping reviews are exploratory, and despite using a rigorous learners using e-learning formats has been acknowledged and recognised methodology, other papers of relevance may [23], and attending in-person live teaching remains a popular have been overlooked. Furthermore, it is likely that choice for continuing professional development in dermoscopy training programs exist in unpublished forms, dermoscopy among PCPs [7], the influence on PCPs of direct for example for online or university dermoscopy courses. contact with dermoscopy experts or other learners in live for- However, while these could give further insights into mats was not explored in the studies identified in this review. dermoscopy training, it was decided not to search for these The duration of live teaching in training programs was gener- as part of this scoping review; these courses are open to ally short, similar to the short training that PCPs reported healthcare workers in many different specialties and roles, so undertaking in an observational questionnaire study [7]. may not have directly addressed the review question with its However, evidence that many PCPs are using dermoscopy focus on PCPs. in practice without any formal training raises questions about Given the high proportion of trials with significant results the accessibility of training, and the competence of these un- in this review, we must acknowledge the potential for publi- trained PCPs [7]. cation bias to influence our findings. By limiting our review to J Canc Educ (2020) 35:643–650 649 English language articles for practical reasons, published No qualitative work has been identified in the published work in other languages may have been overlooked. literature. Qualitative research could be useful in exploring The details of training programs were based on information translational problems, could be carried out at little cost and described in published articles, and there may have been ele- could contribute to a better understanding of PCPs’ percep- ments of programs that were not mentioned by authors and so tions of dermoscopy and dermoscopy training that may help to were not available to the reviewers. Categorising training pro- facilitate uptake of dermoscopy. grams will have obscured some of the nuanced differences between them but is acceptable in a scoping review where the aim is to describe the range and extent of published Conclusions evidence. Focusing on PCP training means that other forms of This scoping literature review has demonstrated that dermoscopy training in other areas of healthcare may have dermoscopy training for PCPs is currently highly varied, and gone unnoticed. Other specialties such as dermatology may published trials generally report positive outcomes of training have more established or better-tested forms of training. on clinical care in terms of improved diagnosis of skin lesions. However, unlike dermatologists, for PCPs, skin lesion assess- However, PCPs who attend short dermoscopy training pro- ment forms a minority, though significant part, of their clinical grams may not continue to use it longer-term in practice, while work, and dermoscopy use for PCPs will not be as regular as conversely, some PCPs are using dermoscopy with no formal for dermatologists. PCPs often work in more solitary clinical training. Given the valuable role of dermoscopy in the detec- environments, without close proximity to other dermoscopy tion of skin cancers, further work to better define these prob- users. The recognition of these differences, and an acknowl- lems and to seek timely solutions is essential. In particular, edgement that developing and retaining competencies in qualitative research could help to clarify PCPs’ training needs dermoscopy may require a distinct approach for PCPs, led to and to guide training program development to facilitate uptake a focus on PCP dermoscopy training in this review. of dermoscopy in primary care. Acknowledgements The authors would like to thank Richard Fallis, Research Gaps Medicine, Dentistry and Biomedical Sciences Librarian, Queen’s University Belfast, for his expertise in formulating the literature search strategy. This review has highlighted several important gaps in our JAF’s study fees and maintenance come from Health and Social Care current knowledge of dermoscopy training. Firstly, longer- Research and Development Division, Public Health Agency’sGP term follow-up is needed to determine whether current Academic Research Training Scheme and EAT/5336/17. dermoscopy training programs influence PCPs’ on-going practice. One study noted poor continuing use of dermoscopy Compliance with Ethical Standards among participants [12], and elucidating the factors that con- Conflicts of Interest The authors declare that they have no conflict of tribute to these translational difficulties more fully is essential interest. in supporting use of dermoscopy in primary care. The lack of long-term follow-up also means that there has Open Access This article is distributed under the terms of the Creative been limited study of the impact of PCP dermoscopy training Commons Attribution 4.0 International License (http:// creativecommons.org/licenses/by/4.0/), which permits unrestricted use, on wider healthcare systems such as dermatology or hospital distribution, and reproduction in any medium, provided you give skin cancer clinics. This is essential to determine whether appropriate credit to the original author(s) and the source, provide a link dermoscopy should remain the preserve of a small group of to the Creative Commons license, and indicate if changes were made. PCPs with specialist interest in dermatology and skin cancer, or whether it should be expanded to become a standard as- sessment tool across primary care, similar to a stethoscope or ophthalmoscope. 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Published: Aug 2, 2020

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