Acta Clinica Belgica International Journal of Clinical and Laboratory Medicine

ISSN: 1784-3286 (Print) 2295-3337 (Online) Journal homepage: http://www.tandfonline.com/loi/yacb20

Teledermatology in Belgium: a pilot study

Julie Kips, Jo Lambert, Katia Ongenae, An De Sutter & Evelien Verhaeghe

To cite this article: Julie Kips, Jo Lambert, Katia Ongenae, An De Sutter & Evelien Verhaeghe (2019): Teledermatology in Belgium: a pilot study, Acta Clinica Belgica, DOI: 10.1080/17843286.2018.1561812 To link to this article: https://doi.org/10.1080/17843286.2018.1561812

Published online: 08 Jan 2019.

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Teledermatology in Belgium: a pilot study Julie Kipsa, Jo Lambertb, Katia Ongenaeb, An De Sutter c and Evelien Verhaegheb aGeneral practitioner, Ghent University, Ghent, Belgium; bDepartment of , Ghent University, Ghent, Belgium; cDepartment of General practice and primary health care, Ghent University, Ghent, Belgium

ABSTRACT KEYWORDS Background: Teledermatology, the application of telemedicine in the field of dermatology, Telemedicine; can be a valuable tool to improve the efficiency of care in general practice. teledermatology; Objectives: In this pilot study, we implemented a teledermatology programme in Belgian dermatology; e-Health; context to assess the effect on referral rate and to evaluate the acceptability of teledermatol- organisation of health care ogy by clinicians and patients. Material and methods: A store-and-forward teledermatology service between 12 general practitioners (GPs) and 3 academic dermatologists was evaluated for a period of 3–6 months. Clinicians and patients were questioned about satisfaction, benefits and barriers. Results: In total, 54 teledermatologic consultations were performed. The referral rate was reduced. Thirty-one teleconsulations were performed instead of physical referral, of which nine patients were actually referred. In 23 cases, performed for a second opinion, two more patients were referred on the dermatologist’s advice. All clinicians want to continue working with teledermatology. GPs highlighted the educa- tional benefit, whereas dermatologists were interested in the triage effect and reduced referral rate. Patients indicated that teledermatology would encourage them to consult a GP sooner when experiencing dermatologic problems. Conclusion: Teledermatology proved to be a feasible and acceptable tool for both clinicians and patients. It also shows to be a valuable for triage and reducing unnecessary referrals. Considering the emergent pressure on health care in the next decades, teledermatology following GP selection could be useful for the Belgian health care system and deserves further elaboration in the search for effective tools to strengthen first line health care and streamline referral to secondary care.

Introduction comparable with conventional face-to-face consulta- tions [1,2,4–7]. In order for teledermatology to be Telemedicine is the use of communication technologies considered reliable, the diagnosis must be reproduci- in health care for the exchange of medical information ble by physicians using different modalities. over a distance. The visual character of dermatology Therefore, it is important to compare dermatologist makes it well-suited for telemedicine. Teledermatology in-person consultations and teledermatology for diag- has been the subject of research since 1995 and is one nostic agreement. Systematic reviews by Levin and of the most evolved telemedicine services [1]. Warshaw (2009) and Whited et al. (2015) reported Teledermatology has two established modalities: that good diagnostic agreement is the conclusion, store-and-forward teledermatology (SAFT) and live when comparing a teledermatology diagnosis and in- interaction teledermatology (LI). In the SAFT modality, person dermatologic diagnosis or histopathology with digital images and associated patient data are sent to traditional face-to-face consultations [1,7]. However, a distant site clinician who reviews the data hours or several factors may directly impact the reliability of days later. The LI modality involves real-time video teledermatology including proper imaging, compre- interaction between the consulting party and the hensive history, and skills of the teledermatologists teledermatologist. Store-and-forward modality is the and referring physicians. Therefore, it is imperative main technology of choice because of its technologi- to create good conditions and provide support and cal flexibility and lower cost of service delivery [2,3]. education to referring general practitioners (GPs) [4,7]. Teledermatology can be used either between another Currently, teledermatology is applied throughout all physician and a teledermatologist for triage/consulta- kinds of medical settings, e.g. in hospital and primary care, tion, or directly between patient and dermatologist nursing homes, home care settings. Although it was initi- (direct-to-consumer teledermatology) (Figure 1). ally developed for underserved and remote areas, the The diagnostic reliability of teledermatology for evidence for its cost-effectiveness in more densely popu- non-pigmented lesions has been shown to be lated settings is growing [2,6,8]. Teledermatology is

CONTACT Julie Kips [email protected] General practitioner, Merelbeke, Belgium © 2019 Acta Clinica Belgica 2 J. KIPS ET AL.

Store-and- Live-interactive: Direct-to- Triage/ forward: Sending Consulting party consumer: The Consultative: stored digital and patient sends Another physician images and teledermatologist images or interacts sends images or associated patient interact via live live with the interacts live with a data to a distant site video. dermatologist. dermatologist for provider. either consultation or triage.

Figure 1. Modalities and uses of teledermatology. Adapted from teledermatology toolkit, American Academy of Dermatology [17]. integrated in the national health system of the melanoma were excluded by the GPs. The teledermatol- Netherlands, United Kingdom, Canada, Norway and ogy service was provided by KSYOS TeleMedical Centre, Saudi Arabia. In other countries like North America and a Dutch health care institution specialising in telemedi- Australia, it is supplied by large programmes [9–11]. cine. All GPs received on-site training in clinical photogra- Teledermatology can be of interest for different part- phy and the use of the teledermatology system before ners in the Belgian health care system. It can provide starting teledermatology. The GPs selected patients with atriagesystem,thatcouldbevaluableinacontextof skin conditions that were in their opinion suitable for emergent pressure on health care as our ageing popula- a teleconsult. The database of KSYOS TeleMedical tion will entail an increased demand for care, which will Centre used for this study held records on all teleconsults not be followed by an equal increase in health care work- performed from mid-July 2016 till the end of ers [12]. As teledermatology can reduce the number of January 2017. To create and close a teleconsult, GPs had face-to-face visits, it could lead to shorter waiting lists by to answer mandatory questions on outcome parameters. triage and better access to dermatologic advice. Therefore, teledermatology could provide a valuable The teledermatology consultation process tool to keep health care accessible and sustainable. In the field of telemedicine, however, Belgium is falling GPs sent teleconsults to the dermatologists with the use behind in comparison to other countries. Agoria, the of the SAF-based KSYOS Teledermatology Consultation Belgian federation of technology industry, stated in its System. A teleconsult consisted of two parts. The first part position paper on e-Health that the development of tele- contained basic patient data, clinical photographs, the medicine is slowed down by the lack of objective stimu- patient’shistoryandtheGP’s questions to the dermatol- lating measures, resulting from a lack of confidence, ogist. The second part was optional and contained more caused by insufficient knowledge of the evidence and detailed information on patient history and condition, the small scale of experimental projects in Belgium [12]. partly based on semistructured questions. If necessary, In this study, we aim to explore the benefits and a second teleconsultation round could be included, barriers of teledermatology in a Belgian pilot study, when the dermatologist needed more information which can provide a basis for larger scale projects. about the case or when the GP needed clarification of the dermatologist’s advice. After one or two rounds, the teleconsult was actively closed by the GPs. Clinicians were Materials and methods notified of new, answered or second-round teleconsults Setting by means of an anonymous notification e-mail in their regular e-mail inbox. Dermatologists were asked to The teledermatology service was implemented during answer a teleconsult within two working days. the period from mid-July 2016 until the end of GPs made pictures with the camera on their smart- January 2017. The setting for the study was phone or the Nikon Coolpix digital photo camera pro- a neighbourhood health centre in Ghent and a group vided by KSYOS (resolution of 16,1 Megapixels). There practice in Merelbeke. The teleconsults were answered was no cost for the patient, nor remuneration for the by three dermatologists of Ghent University Hospital. clinicians. The study was covered by the research liability insurance of UZ Ghent. Inclusion and exclusion Study design Inclusion criteria for patients were: ≥18 years, capable of giving informed consent. Naevi and/or brown pigmented The study primarily focused on two domains: effi- skin lesions that could be a naevus or dysplastic naevus or ciency and user satisfaction. Informed consent was ACTA CLINICA BELGICA 3 obtained from all individual clinicians and patients a second round was performed. The median time included in the study. The procedures performed in spent per teleconsultation by dermatologists was the study were in accordance with the ethical stan- less than 10 min. dards of the institutional research committee (UZ Ghent, EC 2016/0528). Diagnostic groups In this study, efficiency of teledermatology was mea- sured by the number of physical referrals prevented. In 47 teleconsults, a diagnosis could be made. These Areferralwasdefined as ‘prevented’ when the answer diagnoses can be categorised in seven main diagnostic to the standard question ‘Would you have referred this groups: eczema, infectious diseases, benign tumours, patient if teledermatology was not available?’ was ‘YES’ (pre)malignant tumours, erythematosquamous diseases and the answer to the second question, ‘Are you still and acneiform conditions (Figure 2). Most teleconsults referring this patient to the dermatologist?’,was‘NO’. were performed for advice on diagnosis or therapy. The first question was asked when a GP created a new teleconsult and the second question was asked when the ffi teleconsult was closed by the GP. User satisfaction of GPs E ciency and dermatologists was evaluated by a short question- In 31 cases (57%), GPs initiated a teleconsult instead of naire per teleconsult and a larger questionnaire before physically referring the patient. This means that the GP and after the project. Patient satisfaction was questioned would have referred the patient to the dermatologist if by the GP at the moment he or she informed the patient she did not dispose of teledermatology. After the tele- about the results. Excel was used for data analysis. dermatology process, only nine of these patients were actually referred. The referral rate was reduced with 71%. In addition, GPs initiated 23 teleconsults (43%) for Results a second opinion. In these cases, the GP would ’ Characteristics of use not have asked a dermatologist s advice if telederma- tology was not available. After the teledermatology During the period from mid-July 2016 until the end of consultation, two of these patients were yet referred January 2017, 12 GPs of two general practices partici- to the dermatologist on the dermatologist’s advice pated in the project, with a varying participation time of (Figure 3). 3–6.5 months. Two GPs opted not to participate in the The dermatologists gave the following reasons to study. One GP felt no need to receive dermatologic advise referral: need for clinical evaluation, need for advice, the second GP experienced smart phone pro- a technical act (, surgery) or need for dermato- blems. The average age of the GPs was 36 years (median scopic evaluation. In two cases, insufficient quality of 33, range 27–64 years), with a male female distribution of the pictures was a reason for the dermatologist to ask 5–7. The teleconsults were answered by three female for referral. academic dermatologists, with an average age of 47 years (range 43–50). In total, 54 teleconsults were performed, with Motivating factors and barriers a mean of 1.2 teleconsults per GP per month. All All clinicians wanted to continue working with tele- invited patients agreed and gave their informed con- dermatology in the future. They all believed that tele- sent. 41 patients (76%) completed the questionnaires. dermatology is a safe way to evaluate dermatologic The median response time of the dermatologist in the , with enough options in case of uncer- fi rst round of the teleconsult was 17 h. In seven cases, tainty (extra questions, advice to refer). They

Infectious diseases 12 Eczema 12 p

u Benign tumours 5 o r gsis (Pre)malignant lesions 5

o Erythematosquamous diseases 4 ng a

i Acneiform conditions 2 D Other 7 No diagnosis yet 7

02468101214 Number of teleconsults

Figure 2. Diagnostic groups made by teledermatology. 4 J. KIPS ET AL.

Teleconsult Teleconsult for second opinion Before teleconsult instead of referral 23 (43%) 31 (57%)

Not referred Not referred After teleconsult Referred 9 22 2 21

Extra referred on dermatologist's advice 01020304050

Figure 3. Effect of teledermatology on referral rate. perceived the programme as user friendly. The GPs Table 2. Personal motivators and potential barriers for were satisfied with the response time of the dermatologists. dermatologist. Personal motivators Potential barriers ffi When asked for personal motivating factors, GPs 1. Increased e ciency of care organisation, 1. Time investment triage especially withheld the learning effect. Secondly, they 2. Safe frame and reimbursement for 2. Lack of third appreciated the ability to deliver better care. Thirdly, existing telecommunication dimension (palpation) 3. Better cooperation with GP 3. No feedback about they valued an improved collaboration with the der- outcome matologists. When asked for potential barriers for future use, five GPs reported difficulties in taking good pictures. This corresponds with the dermatolo- necessity of a remuneration for the GP differed. For all gists’ report of poor picture quality in eight telecon- clinicians, integration of the data into the existing sults. GPs pointed out several reasons for this: (i) health record system would be a great advantage. insufficient resolution of the pictures taken with cam- era’s provided by KSYOS or with their smartphone Patient satisfaction camera, (ii) difficulty of focussing on skin lesions on hairy surfaces, (iii) poor technical skills (lighting, back- Forty-one patients filled out the questionnaire. Thirty- ground, focussing). Furthermore, four GPs named the eight patients did not prefer a physical referral over increased workload as a potential barrier (Table 1). a teleconsult. In 34 cases, patients felt they were The strongest motivating factor for dermatologists helped well. Thirty-five patients agreed that the avail- was the promise of an increased efficiency of care ability of teledermatology would stimulate them to go organisation and better triage. The second most impor- to the GP earlier with a dermatological problem. tant benefit was the availability of a safe frame for the fl already existing ow of telecommunication, and the Discussion possibility of remuneration for this work. Thirdly, they appreciated the better cooperation with GPs. Potential We aimed to assess the benefits and barriers of tele- barriers were time investment, the inability to use their dermatology in a Belgian general practice setting. hands to make the diagnosis, and the lack of feedback about the eventual outcome (Table 2). Efficiency A first important findinginthispilotstudyisthattele- Ideas for future implementation dermatology reduced the number of referrals to the der- All doctors believed that the GP should be liable for the matologist. The total reduction rate of 71% is comparable teledermatology service. Eight GPs thought that the to the results of previous studies in other countries liability should be shared with the dermatologist. All A recent study in the Netherlands with the same design, doctors agreed that there should be a remuneration for including 1820 GPs and 166 dermatologists showed the dermatologist, whereas the opinions on the a 74% reduction of the referral rate [8]. In other studies with different designs, the percentage of prevented face- to-face appointments varies between 13% and 81% [5,6]. Table 1. Personal motivators and potential barriers for GPs. A remarkable finding in our pilot study was that the Personal motivators Potential barriers distribution of indications for teleconsults was similar to 1. Learning effect 1. Difficulties to make good pictures larger scale international studies with a similar design [8]. 2. Better care for patient 2. Increased workload This suggests that our study can be considered as 3. Improved collaboration with a valuable sample, despite the small scale [8,9,11]. dermatologist Studies on a larger scale and with a longer follow-up will ACTA CLINICA BELGICA 5 be needed to support these findings. The reduction of the effective way of evaluating dermatologic pathologies. referral rate is an important outcome parameter in litera- The learning effect for the GP has earlier been described ture, and can correlate with a higher effective health care as a key motivating factor for implementation of teleder- system and shortening of waiting lists [5,6]. This study matology [11,16]. In addition, the dermatologist’s interest does not provide direct data on the time the dermatolo- inthetriageeffect also accords with earlier evidence. gist eventually could save, as compared to conventional Interestingly, dermatologists expressed the hope that care, One can even suppose that teledermatology may the already existing flow of questions by e-mail could in create more work, as there are many consults initiated this way be poured into a safe format, with the possibility for second opinion. However, we recorded that the der- of remuneration for this work. matologist spent a short time spent per teleconsult (less Important facilitators for GPs and dermatologists were than 10 min) and eventual referrals were more specifically a user-friendly programme, an achievable time invest- oriented (specific consultation, surgery, . . .). In addition, ment, training and technical support and the substantial learning effect for the GP is highly likely to a remuneration for the dermatologist. This is in line with reduce the number of teleconsults on the long term. The earlier research [11,13,16]. Barriers for future implementa- study of Van der Heijden et al. (2011) described a decrease tion were the difficulty to take good pictures and the of the number of teleconsults per GP in the first year after impossibility to integrate teleconsultations into the exist- starting teledermatology, with a stabilisation of the num- ing . The acquisition of qualitative ber after the first year [8]. pictures also proved to be a challenge in earlier research. There is growing evidence that a teledermatology ser- The main problem is often not the resolution, but the vice can be cost-effective even in densely populated technique of taking pictures (lighting, background, cam- regions [2,5,6,8,13]. When evaluating teledermatology eraposition,...)[11]. Several countries, such as the United cost-effectiveness, it is important to consider societal States, have developed standards for good practice, costs in addition to health care system costs that are including technological requirements and practical associated with conventional care. By averting the need guidelines [17], but there are no international stan- for dermatological consultations, teledermatology not dards yet. only decreases appointment waiting times and the Difficulties in interfacing the teledermatology applica- amount of time needed for a consultation, but also tion with an existing electronic have been decreases travel costs and loss of productivity. A cost- described as a barrier in many countries [11]. In the future, evaluation in the Netherlands, with a fully implemented the development of practical guidelines and the design of teledermatology service, estimated teledermatology to anapplicationforteledermatologyontheeHealthplat- be cost-effective when the prevention of physical refer- form could encourage the broader application of rals is over 37% [8]. teledermatology. The impact of teledermatology on efficiency and We conclude that the participating physicians are costs, however, is context-dependent. In Belgium, the enthusiastic to work with teledermatology, provided waiting times for in-person dermatologic consulta- that there is a good infrastructural and organisational tions are high, but not as high as in the Netherlands. context. Benders and Rouppe van der Voort found a mean waiting time of 6 weeks for a general dermatologic consultation in 2008 [14]. According to Lambert and Patient satisfaction Deprez, the waiting time for a polyclinic consultation A final important outcome of this study is the high patient in UZ Ghent was 17 weeks in 2015 [15]. Furthermore, satisfaction. Teledermatology increased patient satisfac- it is foreseen that the demand will only increase, as tion by providing faster access to consultation as opposed the Belgian population is greying. The IMF predicts to in-person visits. Other studies present similar results that by 2050 the percentage of Belgian population [11,18]. Interestingly, almost all patients indicated that the over the age of 65 will increase from 16% to 25%. availability of teledermatology would stimulate them to In conclusion, teledermatology may provide better go to the GP with a dermatological problem. This out- access to dermatological advice in a more efficient and come can be very relevant for the Belgian context, as even cost-saving manner, but more research in Belgian patients with common dermatologic problems too context is necessary to support that hypothesis. often consult second- and third-line health care without visiting the general practitioner first. According to data Physician satisfaction, facilitators, barriers from the department of Dermatology at UZ Ghent (third- line), 73% of patients consult a dermatologist on their In this study, GPs and dermatologists all perceived tele- own initiative [19]. As teledermatology can leave manage- dermatology as a user-friendly technology with an added ment of common dermatologic care in the hands of the value for their practice, and want to continue working referring primary care provider, it can be a valuable tool to with teledermatology in the future. Importantly, the der- organise health care more efficiently. matologists perceive teledermatology as a safe and 6 J. KIPS ET AL.

Limitations Agoria formulated different goals to further develop telemedicine in Belgium in the future: (i) The present study had some limitations. structural agreement between different authorities, First, the study has a small sample size, which limits (ii) more research on financial and economic impact the generalisability of the results. of telemedical solutions, (iii) more investment in net- A second shortcoming of this study is the absence work infrastructure and (iv) a legal and deontologic of any follow-up data on clinical and management frame [12]. outcome. However, large reviews showed no evi- Further studies should be conducted on a larger dence that clinical outcomes of teledermatology scale, with longer follow-up, and in different settings. were any different compared to conventional care Especially peripheral locations and nursing homes [1,4,7]. But future research in Belgium should also would be interesting locations to evaluate the pros include long-term follow-up data. and cons of teledermatology. Patients outside the GP Thirdly, the results can be biased by the specific practice can be interrogated about their health- setting of the study (neighbourhood health centre, seeking behaviour (e.g. in the waiting room for the academic hospital). As the use and reliability of tele- dermatologist). Patient outcomes should be studied dermatology is highly dependent on motivation and more extensively. The impact of teledermatology on skills of the teledermatologists and referring physi- the quality of life would be an interesting topic for cians, our results warrant a broader exploration of additional research. Furthermore, cost-effectiveness of the use of teledermatology in different settings. teledermatology in Belgium should be evaluated; Furthermore, naevi and/or brown pigmented skin a legal frame and good guidelines should be lesions that could be a naevus or dysplastic naevus developed. or melanoma were excluded by the GPs, as previous And finally, the field of application can be studies have demonstrated that SAF teledermatol- extended with teledermatoscopy, as used for the ogy cannot be reliably used to rule out melanoma screening and detection of [23]. [20–23]. In this study, the identification of ‘pigmen- ted lesions’ was based on the GP’s judgment. However, as a broad spectrum of pigmented lesions Conclusion and disorders exists, future studies should use more This study indicates that teledermatology can provide specified inclusion and exclusion criteria concerning patient access to dermatologic care in an efficient and pigmented skin lesions. In the future, the addition convenient manner in a Belgian a daily practice set- of dermoscopic images (teledermatoscopy) may ting. Important facilitators are a good infrastructural tackle this problem, as recent evidence reveals and organisational context. that addition of dermoscopic images to the tele- Teledermatology following GP selection could be consult can render sensitivity and specificity high an effective tool to strengthen first line health care enough (>90%) to assist the dermatologist in mak- and streamline referral to secondary care. This could ing referral decisions [23]. be very useful, considering the emergent pressure on And finally, we excluded patients not capable of health care in the next decades. However, further giving informed consent (e.g. demented people) and research is needed to evaluate the cost-effectiveness, children younger than 18. These patients account for to develop a legal frame, to investigate perceptions a reasonable part of the dermatologic pathologies and receptiveness of Belgian clinicians in different and are often restricted in mobility. They should be settings, and to explore the effect of teledermatology included in future studies, as teledermatology could on the health-seeking behaviour of Belgian patients be especially useful for these populations. more thoroughly. With the rapid advancements in technology, developing a practical and affordable Future perspectives platform for telemedical applications will be an essen- tial component for efficient and cost-effective care in In Belgium, telemedicine providers have not suc- the future. ceeded in continuing telemedical projects after the pilot phase yet, in spite of convincing outcomes. A major reason for that, is the absence of financial Disclosure statement support by the social security, which makes business No potential conflict of interest was reported by the models unequilibrated [12,24]. Although telederma- authors. tology has been proven to be cost-effective in many settings, remuneration remains the main obstacle for ORCID the implementation of telemedicine into the national health care system in many countries [18]. An De Sutter http://orcid.org/0000-0002-2540-8307 ACTA CLINICA BELGICA 7

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