Use of the mobile phone multimedia messaging service for teledermatology

RESEARCH Original article... Q Use of the mobile phone multimedia messaging service for teledermatology Alexander Börve*, Anna Holst, Anette Gente-Lidholm, Raquel Molina-Martinez and John Paoli *Department of Orthopaedics, Sahlgrenska University Hospital, Institute of Clinical Sciences at the Sahlgrenska Academy, University of Gothenburg, Sweden; Department of Primary Health Care, Sahlgrenska School of Public Health, Institute of Medicine at the Sahlgrenska Academy, University of Gothenburg, Sweden; Department of Dermatology and Venereology, Sahlgrenska University Hospital, Institute of Clinical Sciences at the Sahlgrenska Academy, University of Gothenburg, Sweden Summary We examined the feasibility of using mobile phone Multimedia Messaging Service (MMS) to send teledermatology referrals from a general practitioner to a dermatologist. Digital photographs of skin conditions in 40 consecutive patients were sent together with relevant clinical information to dermatologists at a university hospital. Two dermatologists separately assessed the MMS referrals. The suspected diagnosis, triage and management decisions were compared to those given after separate face-to-face (FTF) visits, and again after agreeing on a final clinical and/or histopathological diagnosis. Thirty-two patients (80%) were diagnosed with skin tumours and 8 patients (20%) with other skin conditions. Both dermatologists were able to make a correct diagnosis in 31 patients (78%) based solely on the MMS referral. They also provided adequate management recommendations for 98% of the patients. Adequate triage decisions after assessment of the MMS referrals were made for 34 (85%) and 38 (95%) patients by the two dermatologists. There was an inter-observer concordance of 68% for the teledermatology diagnosis, compared to 88% concordance after the separate FTF visits. The diagnostic accuracy and adequacy of the triage and management decisions achieved using MMS referrals were similar to those obtained with other store-and-forward teledermatology methods. Introduction It is difficult for general practitioners (GPs) to recognize dermatological diseases and therefore a referral to a dermatologist is often needed. Dermatologists have nearly twice the diagnostic accuracy of non-dermatologists. 1,2 A recent systematic review of secondary teledermatology showed that digital photographs sent from a GP to a dermatologist via the Internet, had a diagnostic accuracy of 79% compared with histopathological diagnosis. 3 Digital cameras in mobile phones have also been used in teledermatology. In a pilot study we conducted in 2008, the inter-observer agreement was measured between 10 dermatologists on the diagnosis of patient queries sent by Multimedia Messaging Service (MMS). The MMS messages included digital photographs of the skin condition taken with the patients mobile phone camera and relevant clinical information written by the patients themselves. The study showed that there was an absolute agreement in 3 out Accepted 27 March 2012 Correspondence: Alexander Börve, Department of Orthopaedics, Sahlgrenska University Hospital, 413 45 Gothenburg, Sweden (Fax: þ46 31 342 8225; Email: alexander.borve@vgregion.se) Journal of Telemedicine and Telecare 2012; 18: 292 296 of 10 cases between the participating dermatologists and a high overall concordance (range 60 70%). 4 The aim of the present study was to examine if an MMS, containing digital photographs of dermatological conditions and text with relevant clinical information sent as a referral from a GP to a dermatologist, would allow for accurate diagnosis and proper patient triage. The primary objective was to measure the diagnostic accuracy of the method and the adequacy of prioritization, compared to the recommendations made in a face-to-face (FTF) consultation with a dermatologist. Methods The study was approved by the appropriate ethics committee and all patients gave written informed consent prior to inclusion. The study was carried out using a web-based application (Tele-Dermis, Gothenburg, Sweden) to which Swedish mobile phone users could send an MMS anonymously. The MMS comprised a single photograph and descriptive text. Three GPs from Backa Vårdcentral, a primary healthcare centre in Gothenburg, were invited to DOI: 10.1258/jtt.2012.120206

send their referrals to the Department of Dermatology at Sahlgrenska University Hospital by using the MMS service instead of using the usual referral system, which is based on paper documents containing descriptive text sent through the ordinary postal service. Patients were only offered inclusion in the study if the GP considered that a referral to a dermatologist was necessary and if the skin condition or lesion could be photographed with a mobile phone camera. Patients with conditions associated with poor protocol compliance (e.g. dementia, drug or alcohol abuse) and under the age of 18 years were excluded. The GP obtained a digital photograph of the area of concern using a standardized mobile phone with a built-in digital camera (K800, Sony Ericsson) under controlled conditions (well-illuminated room, neutral background, no flash, autofocus and appropriate distance from patient to include the detail as well as the extent of the skin disease). A standardized MMS was sent with the digital photograph (compressed to a final size of 680 420 pixels) and text regarding the patient s sex and age, a description of the skin condition, its localization or distribution, its duration, the patient s symptoms, any significant medical history and/or any concomitant medication. The MMS message was sent to the web application, which generated an 8-digit identification code for that specific case. This identification code was automatically sent as a confirmation of receipt to the GP s mobile phone by Short Message Service (SMS). Simultaneously, two dermatologists also received an email message confirming that a new MMS referral had been sent to them. The dermatologists logged on to the web site within 48 hours to assess and triage the MMS referral. All images were viewed on standard 46-cm LCD computer screens. Regardless of the prioritization given, all patients were called for a single FTF visit with the two dermatologists. The dermatologists had 6-8 years of experience in dermatology including training in teledermatology. The MMS referral was assessed separately by the two dermatologists who decided on the following variables: (a) an initial diagnosis, (b) differential diagnoses, (c) a management suggestion and (d) the priority of the case. The prioritization concerned whether patients needed to visit a dermatologist in 0 2 weeks, 2 4 weeks, 4 12 weeks or did not require a FTF visit at all. The same two dermatologists then met all patients at a normal FTF visit within 0 4 weeks of the referral, regardless of the initial assessment. The clinical examination by the dermatologists during the FTF visit was carried out separately without providing the patient with diagnostic information. The dermatologists separately decided on the clinical diagnosis, the differential diagnoses, a management suggestion and the priority of the case after the FTF visit, as was done before when assessing the MMS referral. After this, the dermatologists finally met each other for an agreement on these variables before the patient was informed about the diagnosis and the suggested therapeutic approach. If there was diagnostic disagreement between the dermatologists or when considered necessary, a skin biopsy for histopathological examination was performed to obtain a definitive diagnosis. Finally, all included images were assessed by three dermatologists (including the two dermatologists who assessed the MMS referrals) image quality was rated as poor, sufficient, good or excellent. Results Forty consecutive patients (23 women and 17 men) with a mean age of 49 years (range 18 95) were included in the study. The mean waiting time for the FTF visit with the two dermatologists was 13 days (range 2 56). The final clinical diagnoses agreed upon by the two dermatologists after the FTF visit included 26 patients with benign tumours (14 with benign nevi, 9 with seborrhoeic keratoses, 2 with benign cysts and 1 with a papilloma), 6 patients with malignant lesions (3 with actinic keratoses, 2 with basal cell carcinomas and one with Bowen s disease), 6 patients (15%) with inflammatory skin diseases (4 with various dermatitides, one with psoriasis and one with urticaria) and 2 patients (5%) with other skin conditions (a keloid scar and a Borrelia infection). Thus, 32 patients (80%) were diagnosed with skin tumours. Diagnostic agreement was reached without the need for skin biopsies. Nevertheless, two biopsies were taken to confirm the clinical diagnosis, which had been agreed upon, showing a benign nevus in one patient and Bowen s disease in the other. Assessment and triage Only the single most likely diagnosis provided by the dermatologists after assessing each MMS referral was taken into account for data analysis (i.e. differential diagnoses were excluded). However, their triage decisions were obviously influenced by possible differential diagnoses. The diagnostic and triage decisions of both dermatologists made after assessing the MMS referrals and after the FTF visits are summarised in Table 1. Both dermatologists were able to make the correct diagnosis by MMS in 31 patients each, corresponding to 78% of the patients with a 95% confidence interval (CI) of 62 89%. Inter-observer concordance in the MMS diagnoses was achieved in 27 patients or 68% (95% CI, 51 81). This can be compared to the inter-observer concordance between the two dermatologists after their separate FTF visits seen in 88% of the patients (n ¼ 35; 95% CI, 73 96). Nevertheless, the two dermatologists had no difficulty in agreeing on a final clinical diagnosis after discussing the 5 remaining patients since the final diagnosis was among their differential diagnoses in these cases. Dermatologists 1 and 2 made adequate triage decisions after assessing the MMS referrals for 34 (85%) and 38 (95%) patients respectively. These patients were triaged to a FTF visit with an equal or higher priority than the one agreed upon by both dermatologists after the FTF visit. Dermatologist 1 gave higher priority than necessary in 3 Journal of Telemedicine and Telecare Volume 18 Number 5 2012 293

Table 1 Correctly diagnosed and triaged MMS referrals in comparison with the final diagnoses and triage decisions agreed upon by both dermatologists after the FTF visit Correctly diagnosed MMS referrals Correctly triaged MMS referrals a Dermatologist 1 Dermatologist 2 Dermatologist 1 Dermatologist 2 All diagnoses (n ¼ 40) 31 (78%) 31 (78%) 34 (85%) 38 (95%) Benign tumour (n ¼ 26) 22 (85%) 21 (81%) 25 (96%) 26 (100%) Malignant tumour (n ¼ 6) 5 (83%) 4 (67%) 6 (100%) 6 (100%) Dermatitis not otherwise specified (n ¼ 6) 3 (50%) 5 (83%) 3 (50%) 4 (67%) Other (n ¼ 2) 1 (50%) 1 (50%) 0 (0%) 2 (100%) a Triage decision with an equal or higher priority given to the patient after assessment of the MMS referral in comparison to the final triage decision as agreed upon by both dermatologists after the face-to-face visit. cases and Dermatologist 2 did so in 9 cases. Twenty-six patients were given exactly the same priority by both dermatologists when assessing the MMS referrals, resulting in an inter-observer concordance of 65% (95% CI, 48 79). This concordance can be compared to the 73% inter-observer concordance in regards to the priority (n ¼ 29; 95% CI, 56 85%) given after the separate FTF visits. In the assessment of the MMS referrals, Dermatologist 1 considered that the skin conditions of 13 patients (33%) did not require a FTF visit: 7 benign tumours, 4 inflammatory skin diseases and 2 other skin conditions. In comparison, Dermatologist 2 assessed 8 patients (20%) as not requiring a FTF visit: 5 benign tumours and 3 inflammatory skin diseases. All malignant tumours were triaged for a FTF visit by both dermatologists, eventually leading to 8 skin tumours requiring treatment (curettage, excision, cryotherapy or biopsy). Both dermatologists recommended the use of dermatoscopy in order to exclude malignancy in 17 and 18 skin tumour cases respectively. After the FTF visit, 9 patients had diagnoses for which a FTF visit was not deemed necessary, including seborrhoeic keratoses, dermal nevi, a benign cyst, a papilloma, a patient with dermatitis and a patient with psoriasis. Missed diagnoses and incorrect triage The distribution of diagnostic and triage categories assigned to the patients by the two dermatologists after the MMS referral assessment is shown in Table 2. It also shows the separate FTF visits as compared to the final diagnoses and triage decisions that they agreed on after meeting to discuss the cases. Both dermatologists suggested a diagnosis within the same diagnostic category (benign tumour, malignant tumour, inflammatory skin disease and other skin condition) in 80% of the patients (n ¼ 32; 95% CI, 64 91) after assessing the MMS referral. The inter-observer concordance increased to 98% (n ¼ 39; 95% CI, 87 100) after the separate FTF visits. When assessing the MMS referrals, Dermatologist 1 misdiagnosed one patient with a malignant tumour (Bowen s disease) as an inflammatory disease ( psoriasis). However, Bowen s disease had been suggested as a differential diagnosis. For this reason, the patient was triaged for a FTF visit and the patient management was therefore adequate. Three patients were given an incorrect diagnosis and were not initially triaged to a FTF visit by Dermatologist 1 after assessing the MMS referrals. One of these patients was diagnosed with urticaria and dry skin and would theoretically have been recommended treatment via the GP with a topical steroid. Another patient would have been recommended a topical steroid for a dermatitis, which was assessed as a drug-induced rash. The last patient had a Borrelia infection. This was however one of the differential diagnoses provided by Dermatologist 1 who would have ordered serology testing for Borrelia via the GP. Thus, only one patient (3%) with urticaria would have received incorrect management by Dermatologist 1 with the MMS referral system. Two patients with a final diagnosis of a malignant tumour (basal cell carcinoma and Bowen s disease) were initially misdiagnosed by Dermatologist 2 as having an inflammatory skin disease (dermatitis) and another malignant tumour (basal cell carcinoma) based on the MMS referral. Nevertheless, this dermatologist suggested the correct diagnosis as a differential in both of these patients, so a FTF visit was recommended in both cases. Dermatologist 2 also misdiagnosed two patients without recommending a FTF visit. One of these patients had a benign nevus, which was thought to be a seborrhoeic keratosis. The other was the same patient with urticaria mentioned above who would have been managed in the same incorrect way as Dermatologist 1 had proposed. In summary, Dermatologist 2 would also have provided incorrect management to this single patient. Image quality The three dermatologists who rated the image quality provided identical scores for 15 images. Two identical scores and one slightly superior or inferior (e.g. good, good and excellent ) were given for 21 images. In these cases, the two identical scores were considered to be the average score ( good, in the example above). Three different scores were provided for 4 images (e.g. poor, sufficient, good ). In such cases, the lowest and highest scores were eliminated to determine the average score ( sufficient, in the example above). On average, 9 cases were deemed as having excellent image quality, 19 were scored as having good quality, 9 were of sufficient quality and only 3 had poor quality. Nevertheless, all the MMS images could be assessed and a probable diagnosis and triage decision could be sent to the 294 Journal of Telemedicine and Telecare Volume 18 Number 5 2012

Table 2 Diagnostic categories and triage decisions made by both dermatologists at the different stages of the study MMS referral assessment Separate FTF visits Final decision Dermatologist 1 Dermatologist 2 Dermatologist 1 Dermatologist 2 Dermatologists 1 and 2 Diagnosis Benign tumour 23 (58%) 24 (60%) 26 (65%) 25 (63%) 26 (65%) Malignant tumour 8 (20%) 8 (20%) 6 (15%) 7 (18%) 6 (15%) Dermatitis not otherwise specified 6 (15%) 7 (18%) 7 (18%) 6 (15%) 6 (15%) Other 3 (8%) 1 (3%) 1 (3%) 2 (5%) 2 (5%) Triage Visit not necessary 13 (33%) 8 (20%) 9 (23%) 8 (20%) 9 (23%) 4 12 weeks 26 (65%) 25 (63%) 30 (75%) 30 (75%) 31 (78%) 2 4 weeks 0 (0%) 7 (18%) 0 (0%) 2 (5%) 0 (0%) 0 2 weeks 1 (3%) 0 (0%) 1 (3%) 0 (0%) 0 (0%) GP. The text containing the relevant clinical information in the MMS was helpful in the cases in which the image was of poor quality. Discussion In the present study, GPs referred 32 patients with suspicion of skin cancer and 8 patients with other dermatological conditions to a dermatologist using a teledermatology system based on an MMS message sent from a mobile phone. Both dermatologists assessing the MMS referrals were able to make a correct diagnosis in 78% of the patients. Although the number of patients in the study was limited, the diagnostic accuracy of the referrals sent via MMS was similar to other approaches involving ordinary digital photographs sent via email, or other store and forward systems. 5,6 Even though only one image of a low resolution (640 480 pixels) was sent in the MMS referrals, the picture quality was considered to be sufficient to excellent in 37 out of 40 cases. In the three cases in which the dermatologists scored the picture quality as poor, the clinical history which was provided compensated for the lack of image quality. The images provided via MMS together with the clinical patient history resulted in an inter-observer concordance of 68% for clinical diagnosis. This concordance increased to 88% after the separate FTF visits. It increased to 100% after the two dermatologists conferred and agreed on a final clinical diagnosis. In the majority of the 40 patients, the final clinical diagnosis was based on the opinion of two experienced dermatologists and not confirmed histopathologically. Nevertheless, these percentages were in accordance with the results of other teledermatology studies. 7 In addition, when studying the appropriateness of the management decisions, both dermatologists provided adequate management recommendations for 98% of the patients. All patients with malignant tumours received adequate management decisions. Nonetheless, caution should always be taken when carrying out teledermatology assessments of suspected skin cancer lesions. Most referrals in the study involved skin lesions suspected to be skin cancer. With the high incidence of skin cancer in Sweden, it is not uncommon that more referrals are sent from GPs to dermatologists with queries regarding suspected skin cancer rather than other dermatoses. In many of these cases, dermatologists opt to see the patient at a FTF visit in order to perform a dermatoscopic evaluation, even when the lesion looks apparently benign in the clinical image. Dermatologist 1 and dermatologist 2 recommended dermatoscopy in 17 and 18 cases respectively. Only 3 of these cases eventually needed treatment. The number of unnecessary FTF visits for many of these patients may have been reduced if the GP had had the option of sending a dermatoscopic image of the lesion in addition to the clinical photograph. In fact, there are indications that teledermatoscopy referrals from GPs to dermatologists may improve the diagnostic accuracy rates by up to 15%, especially for non-melanoma skin cancer lesions. 8 Other studies have shown that dermatoscopic images taken with digital cameras built into mobile telephones can be as good as FTF dermatoscopy. 9,10 It must, however, be acknowledged that teledermatology or teledermatoscopy can only answer specific dermatological queries and cannot substitute for a full body skin examination by a dermatologist. A recent study showed that dermatologists found incidental skin cancers that were not mentioned in the referral from a non-dermatologist in 15% of 400 male patients over the age of 65 years when performing full body skin examinations at the FTF visit. 11 The present study is the first to use the Tele-Dermis system for referrals from a GP to a dermatologist in a standardized manner. The application was designed to receive digital mobile phone images with text from anonymous users, and was first tested in 2008. 4 Other teledermatology studies using mobile phone cameras to photograph skin conditions have not been sent via MMS through a standardized system. Instead, they have taken a picture with a digital camera in a mobile phone, downloaded it to a computer or sent it as an email attachment for further assessment. In the UK, it is estimated that 10 15% of all patients seeking help at primary healthcare centres have skin problems, leading to numerous referrals from GPs to dermatologists. 12 The information in conventional referral letters to dermatologists varies greatly in quality, making it difficult to triage them adequately. Thus, there is an obvious risk of incorrect prioritization in which patients Journal of Telemedicine and Telecare Volume 18 Number 5 2012 295

with serious skin tumours may be incorrectly triaged to wait 4 12 weeks. Meanwhile, patients with insignificant skin conditions and completely benign lesions may be called within 0 2 weeks for a FTF visit. Thus, a teledermatology approach to referrals from GPs to dermatologists such as the one described in the present study may have several benefits in comparison with the conventional referral system. First of all, the assessment of the referrals should be better since a photograph provides important additional information. Second, a digital referral would be delivered immediately to the dermatologist instead of incurring the usual delay of several days when sent by post. Subsequently, triage could be carried out within 24 48 hours and the GP and patient could be given a preliminary assessment straightaway. Furthermore, unnecessary visits to a dermatologist could be avoided and where appropriate, treatment could be initiated through the GP. Suspicious skin lesions could be prioritized for a more urgent visit to a dermatologist and preparations could be made to perform surgery directly during the patient s first visit. In conclusion, the present study suggests that MMS could be a useful alternative to conventional paper referrals sent by post, which is the standard method used in the Swedish National Health Service. Acknowledgements: We thank the staff at the Primary Healthcare Centre Backa Vårdcentral and the GPs Mats Olsson, Marie Skarström and Praxitelis Korthellos who helped to include patients in the study. We also thank the Signe och Olof Wallenius Stiftelse and the Göteborg Medical Society for their generous grants. Alexander Börve is the owner of the Tele-Dermis and idoc24 software; the other authors have no conflicts of interest. References 1 Ramsay DL, Fox AB. The ability of primary care physicians to recognize the common dermatoses. Arch Dermatol 1981;117:620 2 2 Tran H, Chen K, Lim AC, Jabbour J, Shumack S. Assessing diagnostic skill in dermatology: a comparison between general practitioners and dermatologists. Australas J Dermatol 2005;46:230 4 3 van der Heijden JP, de Keizer NF, Bos JD, Spuls PI, Witkamp L. Teledermatology applied following patient selection by general practitioners in daily practice improves efficiency and quality of care at lower cost. Br J Dermatol 2011;165:1058 65 4 Börve A, Molina-Martinez R. A pilot study of a medical information service using mobile phones in Sweden. J Telemed Telecare 2009;15:421 2 5 Morton CA, Downie F, Auld S, et al. Community photo-triage for skin cancer referrals: an aid to service delivery. Clin Exp Dermatol 2011;36:248 54 6 Moreno-Ramirez D, Ferrandiz L, Nieto-Garcia A, et al. Store-and-forward teledermatology in skin cancer triage: experience and evaluation of 2009 teleconsultations. Arch Dermatol 2007;143:479 84 7 Warshaw EM, Hillman YJ, Greer NL, et al. Teledermatology for diagnosis and management of skin conditions: a systematic review. J Am Acad Dermatol 2011;64:759 72 8 Warshaw EM, Gravely AA, Nelson DB. Accuracy of teledermatology/ teledermoscopy and clinic-based dermatology for specific categories of skin neoplasms. J Am Acad Dermatol 2010;63:348 52 9 Kroemer S, Frühauf J, Campbell TM, et al. Mobile teledermatology for skin tumour screening: diagnostic accuracy of clinical and dermoscopic image tele-evaluation using cellular phones. Br J Dermatol 2011;164:973 9 10 Massone C, Brunasso AM, Campbell TM, Soyer HP. Mobile teledermoscopy melanoma diagnosis by one click? Semin Cutan Med Surg 2009;28:203 5 11 Viola KV, Tolpinrud WL, Gross CP, Kirsner RS, Imaeda S, Federman DG. Outcomes of referral to dermatology for suspicious lesions: implications for teledermatology. Arch Dermatol 2011;147:556 60 12 Primary Care Dermatology Society. See http://www.pcds.org.uk/ about-us/the-primary-care-dermatology-society (last checked 28 February 2012) 296 Journal of Telemedicine and Telecare Volume 18 Number 5 2012