TY - JOUR AU - Halpern, Allan C. AB - Abstract Importance Photographs are invaluable dermatologic diagnostic, management, research, teaching, and documentation tools. Digital Imaging and Communications in Medicine (DICOM) standards exist for many types of digital medical images, but there are no DICOM standards for camera-acquired dermatologic images to date. Objective To identify and describe existing or proposed technology and technique standards for camera-acquired dermatologic images in the scientific literature. Evidence Review Systematic searches of the PubMed, EMBASE, and Cochrane databases were performed in January 2013 using photography and digital imaging, standardization, and medical specialty and medical illustration search terms and augmented by a gray literature search of 14 websites using Google. Two reviewers independently screened titles of 7371 unique publications, followed by 3 sequential full-text reviews, leading to the selection of 49 publications with the most recent (1985-2013) or detailed description of technology or technique standards related to the acquisition or use of images of skin disease (or related conditions). Findings No universally accepted existing technology or technique standards for camera-based digital images in dermatology were identified. Recommendations are summarized for technology imaging standards, including spatial resolution, color resolution, reproduction (magnification) ratios, postacquisition image processing, color calibration, compression, output, archiving and storage, and security during storage and transmission. Recommendations are also summarized for technique imaging standards, including environmental conditions (lighting, background, and camera position), patient pose and standard view sets, and patient consent, privacy, and confidentiality. Proposed standards for specific-use cases in total body photography, teledermatology, and dermoscopy are described. Conclusions and Relevance The literature is replete with descriptions of obtaining photographs of skin disease, but universal imaging standards have not been developed, validated, and adopted to date. Dermatologic imaging is evolving without defined standards for camera-acquired images, leading to variable image quality and limited exchangeability. The development and adoption of universal technology and technique standards may first emerge in scenarios when image use is most associated with a defined clinical benefit. Introduction Photographs are invaluable to dermatologic diagnosis, management, documentation, teaching, and research. Dermatologic digital image use has increased steadily, driven by universal Internet access, inexpensive digital cameras (including those embedded in mobile devices), and adoption of electronic health records. Digital Imaging and Communications in Medicine (DICOM) standards exist for many digital medical image types,1 but there are no DICOM standards for camera-acquired dermatologic images to date.2 Standards help ensure that digital images accurately represent skin diseases, have reproducible acquisition conditions to allow disease monitoring and comparison, and provide associated data for accurate identification and exchangeability. Standards are similarly essential to ensuring that image acquisition, archiving, and transmission do not compromise patient consent, privacy, or confidentiality. In the absence of universally accepted imaging standards for camera-acquired images in dermatology, we undertook a broad review of the scientific literature to identify existing standards. We summarize findings from the most compelling publications for each standard. The complexity of the standards’ development process is illustrated by the proposed standards in dermatologic oncology3,4 and teledermatology.5 Methods Systematic searches of peer-reviewed health care–related journals included in PubMed (1945-2013), EMBASE (1966-2013), and Cochrane (1898-2013) databases were performed in January 2013 using search terms from the following 3 categories: (1) photography (digital imaging), (2) standardization (guidelines and protocols), and (3) medical specialty (dermatology, ophthalmology, and plastic surgery) and medical illustration, without language, publication, or document type restrictions. A gray literature search of 14 websites was performed using Google searches of category 1 and category 2 terms. The complete search strategy is summarized in the eAppendix and eTable 1 in the Supplement. Two reviewers (E.A.Q. and B.A.T.) independently screened all publication titles, followed by 3 sequential full-text reviews. Table 1 lists inclusion and exclusion criteria. Descriptions of technology and technique standards were extracted, summarized, and tabulated during the first full-text review. Subsequent reviews identified guidelines or other publications, including the most recent or most detailed standards’ descriptions. Disagreements between reviewers were resolved by consensus or by a third reviewer (A.C.H.). Three reviewers (E.A.Q., B.A.T., and A.C.H.) evaluated the publication selections after the first and third full-text reviews. Results Search Findings In total, 7371 unique publications were found in the literature and gray literature searches (Figure). The screening process identified 237 potentially relevant publications. The first full-text review revealed 162 publications that included descriptions of technology or technique standards, and these descriptions are summarized (categorized by standard) in eTables 2, 3, 4, 5, and 6 in the Supplement. Two subsequent reviews identified 49 guidelines or other publications with the most recent (1985-2013) or detailed description of technology and technique standards related to the acquisition or use of images of skin disease (or related conditions). The literature is replete with descriptions of obtaining images of skin disease, but few standards have been evaluated or validated in clinical studies6-8 or in other controlled settings.9-13 However, several standards have been set by consensus4,14-16 or with input from focus groups.3 Technology Imaging Standards Today, most skin disease images are acquired and processed by digital cameras, and camera output is then exported for additional processing, display, storage, and transmission by other digital equipment and associated process technology.2 Technology standards address the minimal functional capabilities required for equipment and process technology in the life cycle of skin disease images. Such standards have been described by international, regional, and national organizations,4,5,14-18 as well as by dermatologists and other physicians3,6-9,12,13,19-26 and by hospital-based medical photographers.10,27-30 The most recent standards are described. Image Spatial Resolution and Color Resolution The basic unit of a digital image is a pixel. In a digital camera–acquired image, each pixel represents photons collected at one photosite (well) on the camera sensor. Digital camera and image resolutions are often reported in total megapixels (eg, 3.1 megapixels) and pixel dimensions (eg, 2048 × 1536 pixels). Spatial resolution measures the capacity of a digital imaging system to produce or display an image in which 2 adjacent structures are perceived as distinct.14 The spatial resolution of a digital image, measured in pixels per inch (ppi), depends on the characteristics of the acquired image and the output device (monitor or printer).14 Color resolution for digital images is measured in bits. Most commercially available digital cameras have three 8-bit color channels (red, green, and blue), with each providing 256 color intensity levels. An array of color filters directs incoming light to the photosites, with each photosite acquiring only red, green, or blue light. The final image includes values for each color channel from each photosite (24-bit color and 16.8 million colors), but 2 color channel values at the photosite are interpolated by in-camera software.2 Many digital cameras can acquire images with color resolutions of 12 to 16 bits per channel (36-bit to 48-bit color).2,31 Digital image spatial and color resolutions are related to sensor photosite number and size. Photosite size has been steadily reduced,2 and current mobile device cameras have sensors with 8 to 14 million photosites.19 For a given photosite number, sensors with larger photosites generally have better signal-to-noise ratios and tonal gradations than sensors with smaller photosites.19 A 2012 digital camera buying guide for dermatologists recommended off-the-shelf 8-megapixel to 14-megapixel cameras,19 which can acquire images with spatial resolutions greatly exceeding those recommended in several teledermatology guidelines.5,14,17,18 The 2008 American Telemedicine Association (ATA) teledermatology guideline specified a minimal image spatial resolution of 75 ppi.14 A 2012 ATA guideline for store-and-forward (SF) images recommended a minimal image resolution of 800 × 600 pixels (preferred resolution, 1024 × 768 pixels).18 A 2013 SF teledermatology standards guideline from Primary Care Commissioning (PCC) in the United Kingdom recommended an image resolution of 2000 × 1500 pixels for images viewed on a computer display.5 The ATA teledermatology guideline recommended an image color resolution of 24 bits.14 The more recent PCC SF teledermatology guidelines recommended digital image acquisition using the same color space as that of the display on which the image would be viewed.5 No universally accepted standard currently exists for either spatial or color resolution of camera-acquired digital images of skin disease. However, a 1997 study6 in which dermatologists viewed digitalized images of skin diseases at several resolutions found that a 768 × 524–pixel image was sufficient for diagnosis in 7 of 8 cases and that higher resolution did not improve the results. Reproduction (Magnification) Ratios The magnification of an object in an image (relative to its actual size) is determined by the digital camera sensor dimensions.29 To maintain an undistorted perspective, the camera lens focal length should be at least twice the sensor diagonal length; therefore, cameras with different sensor formats may need different lenses to achieve the same perspective.29 Consistent reproduction ratios for images acquired with a digital camera and lens pair may be obtained by calculating the correct lens setting29 or adopting a standard distance between the individual and the camera lens.15,29 The same reproduction ratios should be used in sequential images to ensure accurate interpretation. Reproduction ratios for sequential images have been included in United Kingdom imaging guidelines28 and the European Association for Cranio-Maxillo-Facial Surgery guidelines.15 Maintaining reproduction ratios may be necessary if sequential images are acquired with cameras with different sensor formats.19 Teledermatology guidelines have not included recommendations for reproduction ratios.5,14 Postacquisition Image Processing The postacquisition processing of a digital image is typically performed within the camera by proprietary software.2,21 Processing includes file format conversion from the native, camera-specific format (raw) to a format used for image viewing or printing. Data loss, including decreased tonal (dynamic) range, accompanies file conversion to the JPEG format.7 Some in-camera processing is performed even when the image is saved as a raw file, but minimizing data loss, such as tonal range, preserves options for subsequent processing steps.2 Digital images acquired and processed by hospital-based photographers are generally saved as raw files.11,31,32 Raw files are exported from camera to computer, the original images are saved and stored, an image copy is processed with image conversion software using a standard protocol, and minimal processing is recommended.11,31,32 The PCC SF teledermatology guidelines recommended that postacquisition image processing should be performed only as part of a planned image management work flow overseen by an imaging professional and after saving the original image.5 A European plastic surgery guideline also recommended minimal postacquisition image processing and discouraged postacquisition improvements in image appearance.16 Color Calibration Accurate color rendition of the skin is challenging because it absorbs and reflects light in a complex way.2 Color calibration procedures have been used experimentally to reduce variability in skin image color rendition acquired with different cameras.9,12,21 Color calibration procedures that transform the image acquisition color space to another color space have been described for clinical and dermoscopic images.9,12,13 The lighting used during image acquisition may affect digital camera color calibration.33 A recommended color calibration standard for clinical or dermoscopic images has not been reported to date. Compression Image compression is generally performed during file format conversion. In a study7 of 34 dermatologic images (clinical and videomicroscopic), image quality was evaluated after conversion to 5 image formats (JPEG, JPEG2000 [lossless and lossy], tagged image file format, and portable network graphics) at 2:1 to 20:1 compression. Visual assessment image quality scores were similar for both lossy and lossless formats at 5:1 compression, but lossy formats were inferior at greater compression ratios. Numerical assessment (color distance of each pixel from the original values) indicated that JPEG2000 (lossy) was superior to JPEG at all compression levels, and color distortion was similar in all 3 color channels.7 Dermoscopic slides converted to JPEG images at a 30:1 compression factor were equally informative for pigmented skin lesion diagnosis as the original slides.8 Image Output Digital images are generally displayed on a computer monitor or viewing device.2,5,14-16 The 2008 ATA teledermatology guideline recommended matching display monitor resolution to image resolution and calibrating computer monitors for luminance, gamma, and white point.14 The 2013 PCC SF teledermatology guideline recommended viewing images on a graphics monitor less than 5 years old, with an image resolution of 1280 × 1024 pixels, using a color space matching the camera color space, working at a gamma of 2.2, and calibrated for color, brightness, and contrast every 2 months.5 Acquiring a digital image at a resolution exceeding that of the intended display was not recommended.5 Digital images may be printed. The desired print size determines the image resolution requirement. An 8-megapixel image provides adequate pixel density (300 ppi) for a print that is 8.5 × 11 in (20 × 30 cm).19 Color management systems are useful in aligning the camera color profile with the color profiles of the output devices when images are acquired and output at the same institution.10,11 Color management systems may also reveal inconsistencies in acquired images related to lighting or camera.10,11 For images acquired and viewed at different institutions, the ATA teledermatology guideline provides recommendations.14 The guideline suggests attaching a color calibration label (eg, GretagMacbeth ColorChecker; Robin Myers Imaging) to an image to improve color calibration of the display monitor. Image Archiving and Storage Archiving and storage systems for digital image systems generally use a standardized naming convention to generate unique image names.22,31 Additional indexing terms (metadata) may be added as defined keywords, and the use of standardized metadata fields, such as those developed by the International Press Telecommunications Council, has been recommended.22,31 Technical data (camera exchangeable image file format) captured during image acquisition should be imported with the image.22 Clinical and dermoscopic images have been stored in a picture archiving and communication system, which requires conversion to a DICOM medical image format (a header with standardized metadata fields plus a compressed image).25 Clinical and dermoscopic images may also be stored in databases created with image management software, and these databases may be linked to electronic medical records.25 Concerns over unauthorized access to patient images may drive the choice of a storage system.15,16,25 Daily and archive backups with encryption are recommended for digital image storage.5,14,15,31 Images used in SF teledermatology consultations become part of the patient’s electronic medical record and must be stored in compliance with regulations on medical record retention.5,14 Image Security During Storage and Transmission Storage and transmission of images for SD teledermatology consultations require network and software security protocols to protect patient privacy and confidentiality.5,14 No publications on standards for cloud computing security were identified. Technique Imaging Standards Technique standards include those related to environmental conditions for image acquisition (eg, lighting) and other activities (eg, positioning, consent) affecting image quality, consistency, or use. Technique standards have been described by international, regional, and national organizations,4,5,14-16,18,34-36 as well as by dermatologists and other physicians3,15,24 and by hospital-based medical photographers.10,27,28,32,37 The most recent standards are described. Environmental Conditions Important environmental conditions include lighting, background, and camera position.5,14,15,24,27,28,32,36-38 Recommendations vary by location (photographic studio, clinic examining room, or hospital emergency department) and the intended use of the image. Lighting Lighting is the most important environmental condition affecting image quality and consistency.14,24,31 In formal photographic studios, ambient light is replaced by 2 studio floodlights (diffused by umbrellas or soft boxes) positioned on either camera side at 45° angles to the patient, and lights are positioned 1 to 1.5 m in front of the patient.15,24 Backlighting may be used to eliminate shadows.21 Aging and voltage fluctuations may affect studio light output, requiring exposure and color balance adjustments.30,31 The marked variations in natural light intensity and color temperature make it unsuitable for images used in disease monitoring.24 Artificial lighting varies greatly in intensity and color temperature.24 A handheld flashgun or camera flash may provide more consistent lighting.24,28 A flashsock may be used to avoid overexposure in close-up images.24 The PCC 2013 teledermatology guideline recommended an electronic flash, with 2 images acquired from different angles to compensate for detail obscured by skin light reflectance.5 The ATA teledermatology guideline recommended a light intensity of 150 foot-candles (at the patient) using daylight fluorescent light tubes but noted that lighting and background may affect the skin color.14 The 3-dimensional architecture of nail pathologies is shown most clearly in images acquired with skim or oblique lighting.39 Digital cameras with automatic white balance adjustment are useful in compensating for variations in light intensity.5,14,24 Manual white balance adjustment is useful to control exposure, thus compensating for variations in lighting intensity or color temperature.14,30,31 Background Background color and surface properties may affect image appearance. The background material should extend beyond the focal plane.14 Nonreflective surfaces are preferred.14,24,32,37 Blue, gray, or neutral colors are frequently recommended.5,14,15,18,24,36 White or black may also be used.28,32,37 White is associated with harsh shadows, and black is associated with less contrast and the need for backlighting.15,36 A bedsheet or towel may be used in less formal settings.28,37 Camera Position Fixing the distance between patient and camera ensures standard reproduction ratios when images are used for monitoring skin conditions or treatment outcomes.15,29,32 Marked patient and camera positions are used in photographic studios.15,32,36,37 In SF teledermatology, camera-to-patient distance has not been standardized because it is often impacted by resolution requirements, lens type, and so forth (Table 2).5,14 Patient Pose and Standard View Sets Patient pose sets for specific skin diseases or plastic surgery have been developed. The European Association for Cranio-Maxillo-Facial Surgery developed patient pose sets for presurgical and postsurgical images for oral or facial surgery.15,16,28 A United Kingdom pose set for patients undergoing cleft repair, developed by the Institute of Medical Illustrators, has been used for presurgical evaluation (before age 1 year) and postsurgical follow-ups to age 20 years.28 Other patient pose sets have been developed to monitor the evolution of dysplastic nevi in patients at high risk for melanoma using total body photography.3,27 Store-and-forward teledermatology guidelines have recommended standard view sets for SF images while noting that some skin diseases may be difficult to image adequately.5,14 Store-and-forward view sets should include a regional image for each anatomic location involved and at least 1 close-up (macro) image showing detailed views of the lesion (with ruler for size approximation).5,14 All images should be taken perpendicular to the plane of the lesion.14 Alternate views may be helpful.5,14 Patient Consent, Privacy, and Confidentiality Standards for patient consent, privacy, and confidentiality of identifiable data depend on unharmonized global, regional, national, and local laws and regulations.35,40-42 A 2009 survey by the British Association of Dermatologists indicated that existing regulations are not always being followed: only 42% of dermatologists using digital cameras obtained written consent for image use, and 74% kept identifiable patient images on portable digital devices.43 Increased use of electronic medical records and mobile devices for skin disease image acquisition, viewing, and transmission44,45 has raised concerns about risks associated with uncontrolled image use.35,40-42 This risk may result in new regulations and may impact other imaging standards.3,5,14,15 Proposed Standards for Specific Dermatology Use Cases Several proposed standards for specific-use cases were identified in the literature. These cases illustrate the links between clinical issues and technology and technique standards. Total Body Photography: Pose Standard In developing a proposed pose standard for patients at high risk for melanoma who required monitoring with total body photography, Halpern et al3 first identified clinical, technical, and practical considerations in focus sessions. The minimal image resolution (technology) was determined by a clinical criterion: “[it] should permit the recognition of skin markings and assessment of the borders and color variegation of small (2-4 mm) pigmented lesions.”3(p594) The pose set was limited to 30 images to maximize acceptability by clinicians and patients. These decisions drove the basic camera specification to either low ISO 35-mm film photography or digital single-lens reflex cameras capturing images with a minimum of 3 megapixels. Privacy considerations led to the separation of facial images from others.3 This pose set was evaluated at the authors’ medical center3 and in a clinical study46 at another institution. Teledermatology: Photography Training Standard The 2013 PCC guideline incorporated a photography training standard for staff acquiring SF images.5 The training standard stated: The person taking the images should have access to good-quality photographic equipment and be trained in capturing high-quality images. The photographer should be identifiable from within the record of the dermatology event and their competence should be measured by the quality of the images. Where there is a need for dermoscopic images, training in the effective use of a dermatoscope is required.5(p22) Pak47 notes the importance of photography training in SF teledermatology. Certification of total body photographers is available but is not widely required or obtained (http://www.bca.org/certification/total_body.html). In a 2010 study48 of patient-acquired SF skin disease images, 15% of patients could not acquire diagnostic-quality images, suggesting the need for photography training. Dermoscopy: Evaluation of Skin Lesions A 2007 proposal4 for standardizing reports of dermoscopic evaluations of skin tumors included the following recommendations: (1) use standardized terms to describe skin tumor structures; (2) include information related to the imaging equipment (brand name, manufacturer, type of illumination, and spectral band) and magnifications; and (3) provide both clinical (body section and close-up) and dermoscopic images of the tumor. Clinical and dermoscopic images obtained during the dermoscopic evaluation of a skin tumor contributed value to the evaluation report. However, image metadata and using standardized terms for image features provided more value. In a 2002 study49 evaluating pigmented skin lesions, contact images (fixed magnification ×10, Dermaphot; Heine) obtained without oil application improved melanoma diagnostic specificity vs distant photographs. The contact method was cited as the reference standard for pigmented skin lesions less than 14 mm.49 Distant imaging was recommended for larger or nodular lesions.49 Discussion National or regional guidelines incorporating standards have been developed in teledermatology5,14,18 and plastic surgery,15,16 and limited standards are available for dermatologic oncology.3,4 However, there is no universally accepted standard to date. Standards developed for specific uses have been described3-5 and share the following 2 characteristics: (1) a well-defined clinical benefit was associated with diagnostic use of images and (2) the standard was easy to apply.3-5 Imaging standards were often developed as a package because technology and technique standards overlap and interact (Table 2).3-5,14-16 Digital photographs are commonly being incorporated into electronic medical records and are increasingly used for documentation and as visual skin assessment tools. Photographic standards are necessary to ensure exchangeable, comparable, and diagnostic-quality images. The risks associated with nonstandardized dermatologic imaging vary with utilization (eg, diagnostic imaging vs documentation). Nonstandardized photographs can hinder diagnosis, misrepresent clinical findings, and prevent accurate comparison over time and across clinical settings. A lack of standards also has efficiency, privacy, and medicolegal implications for the exchange of images among health care providers and health care systems. A standardized approach to dermatologic imaging has the potential to improve clinical care. For example, photographic biopsy-site documentation decreases the risk of wrong-site surgery,50 yet the acquisition of such images (let alone the technology and technique standards for obtaining, storing, and viewing such images) has not been standardized in dermatologic practice to date. The optimal use of images for education, diagnosis, monitoring, documentation, and coordination of care would benefit from the development and adoption of technology and technique standards for camera-acquired skin disease images by ensuring quality and exchangeability.2-5,9,12,14-17,21,28,40,47,49 Standardized image quality may require balancing intended image use against pragmatic considerations, such as cost and clinical practicality.3-5 Utilization of off-the-shelf hardware is inherently difficult to standardize. However, using basic acquisition, processing, compression, output, metadata, storage, and secure transmission recommendations could help ensure uniformity. Conclusions While technology is rapidly evolving, adherence to minimal quality metrics and consistent use of basic metadata will help ensure the usefulness and exchangeability of camera-acquired digital dermatologic images for the foreseeable future. The International Society for Digital Imaging of the Skin is working toward the development of digital imaging standards. Back to top Article Information Accepted for Publication: February 27, 2015. Corresponding Author: Allan C. Halpern, MD, Dermatology Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, 16 E 60th St, New York, NY 10022 (halperna@mskcc.org). Published Online: May 13, 2015. doi:10.1001/jamadermatol.2015.33. Author Contributions: Drs Quigley and Halpern had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Quigley, Halpern. Acquisition, analysis, or interpretation of data: All authors. Drafting of the manuscript: Quigley, Tokay, Jewell, Marchetti. Critical revision of the manuscript for important intellectual content: All authors. Administrative, technical, or material support: Halpern. Study supervision: Halpern. Conflict of Interest Disclosures: Dr Quigley reported receiving royalties from UpToDate, Inc. Ms Tokay reported receiving monetary compensation for her contributions to this article. Dr Marchetti reported receiving honoraria from Next Meeting Generation for lecturing. Dr Halpern reported serving as a consultant to Caliber Imaging and Diagnostics, Inc, Canfield Scientific, Inc, DermTech, and SciBase AB and reported serving on the data safety and monitoring board of Quintiles and Janssen Research and Development, LLC. No other disclosures were reported. References 1. Digital Imaging and Communications in Medicine. DICOM part 3: information object definitions.http://medical.nema.org/standard.html. Accessed June 24, 2014. 2. Madden BC. A proposal for working group 19: dermatologic standards: DICOM whitepaper.2011. http://theskinappearancelaboratory.org/. Accessed November 24, 2013. 3. Halpern AC, Marghoob AA, Bialoglow TW, Witmer W, Slue W. 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