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Potential of Contrast Agents to Enhance in Vivo Confocal Microscopy and Optical Coherence Tomography in Dermatology: a Review

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Potential of Contrast Agents to Enhance in Vivo Confocal Microscopy and Optical Coherence Tomography in Dermatology: a Review Received: 12 December 2018 Revised: 2 March 2019 Accepted: 7 March 2019 DOI: 10.1002/jbio.201800462 REVIEW ARTICLE Potential of contrast agents to enhance in vivo confocal microscopy and optical coherence tomography in dermatology: A review Hans C. Ring1* | Niels M. Israelsen2 | Ole Bang2 | Merete Haedersdal1 | Mette Mogensen1 1Department of Dermatology, Bispebjerg Hospital, Nielsine Nielsens Vej 9, 2400 København NV, Distinction between Faculty of Health and Medical Sciences, normal skin and University of Copenhagen, Copenhagen, Denmark pathology can be a 2 DTU Fotonik, Department of Photonics diagnostic challenge. Engineering, Technical University of Denmark, Kongens Lyngby, Denmark This systematic *Correspondence review summarizes Hans C. Ring, Department of Dermatology, how various contrast Bispebjerg Hospital, University of Copenhagen, agents, either topically delivered or injected into the skin, affect distinction between Bispebjerg Bakke 23, DK-2400 Copenhagen NV, Denmark. skin disease and normal skin when imaged by optical coherence tomography (OCT) Email: [email protected] and confocal microscopy (CM). A systematic review of in vivo OCT and CM studies Funding information using exogenous contrast agents on healthy human skin or skin disease was per- Innovationsfonden, Grant/Award Number: formed. In total, nine CM studies and one OCT study were eligible. Four contrast 4107-00011A agents aluminum chloride (AlCl) n = 2, indocyanine green (ICG) n = 3, sodium fluorescein n = 3 and acetic acid n = 1 applied to CM in variety of skin diseases. ICG, acetic acid and AlCl showed promise to increase contrast of tumor nests in keratinocyte carcinomas. Fluorescein and ICG enhanced contrast of keratinocytes and adnexal structures. In OCT of healthy skin gold nanoshells, increased contrast of natural skin openings. Contrast agents may improve delineation and diagnosis of skin cancers; ICG, acetic acid and AlCl have potential in CM and gold nanoshells facilitate visualization of adnexal skin structures in OCT. However, as utility of bed- side optical imaging increases, further studies with robust methodological quality are necessary to implement contrast agents into routine dermatological practice. KEYWORDS Au, contrast agent, contrast enhancer, fluorescence confocal microscopy, gold microparticles, medical skin imaging, optical coherence tomography, optical imaging, reflectance confocal microscopy 1 | INTRODUCTION diagnosis various skin diseases and to monitor treatment efficacy over time [1, 3–8]. Optical coherence tomography (OCT) and confocal micros- Distinction of normal skin architecture from skin pathol- copy (CM) are noninvasive medical imaging technologies ogy can be a diagnostic challenge in dermatological imag- capable of visualizing skin microarchitecture at the bedside. ing. Therefore, exogenous contrast agents that either These technologies are rapidly gaining clinical acceptance in highlight pathological changes in skin or enhance normal the field of dermatology and other medical specialties, for skin features are in demand. Medical imaging technologies example, ophthalmology [1, 2]. An array of clinical studies are increasingly applied in skin examinations, but contrast demonstrates a promising potential of CM and OCT to agents have yet to gain clinical acceptance. Our intention is J. Biophotonics. 2019;12:e201800462. www.biophotonics-journal.org © 2019 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 1of9 https://doi.org/10.1002/jbio.201800462 2of9 RING ET AL. to provide an overview of current exogenous contrast agents relevant OCT and CM studies applying contrast agents available for CM and OCT imaging of skin and skin disease in vivo to healthy human skin or skin disease. Assess- in vivo by performing a systematic review. ment of study quality was undertaken using the Oxford Contrast agents, in medical terms, a contrast agent is Centre for Evidence-based Medicine levels of evidence used to enhance contrast of anatomical structures, patholo- criteria. gies or fluids within the body for medical imaging purposes. The term contrast means the degree to which light and dark areas of an image differ in brightness. Exogenous contrast 2 | MATERIAL/METHODS agents are chemical or physical substances used to increase contrast and enhance the visibility of tissues or anatomical 2.1 | Search strategy structures. Contrast agents can be delivered to skin topically, A systematic search of Embase and Medline was performed subcutaneously or intravenously. Although utilization of (January 01, 1980 to February 2, 2019) with the following contrast agents for optical imaging is an evolving field in two search queries: “contrast agent AND skin AND CM” dermatology, the method has not yet gained substantial clini- and “contrast agent AND skin AND OCT and “contrast cal impact. Indeed, application of contrast agents prior to agent AND skin AND fluorescence”. Furthermore, the refer- optical imaging, such as gold nanoparticles or fluorescent ence lists from the included articles were manually searched dyes such as indocyanine green (ICG) appear to have poten- for additional relevant studies. Two authors H.C.R. and tial for generating strong contrast signals in skin, thus poten- M.M. performed data extraction and quality assessment tially enhancing diagnostic accuracy of optical imaging independently. The overall search strategy is available in devices at the bedside [9–11]. Supporting Information Figure S1. OCT is a laser-based imaging technology that provides fast image acquisition, enabling real time, high-resolution, 2.2 | Inclusion criteria noninvasive, cross-sectional and en face representation and analysis of skin structures [3, 12, 13]. The imaging The target intervention was the use of a contrast agent in depthinskinis1to2mm,andresolution3to10μm OCT or CM imaging, and no restriction was placed on the depending on the OCT system and properties of the skin. type of OCT system or CM system. The target conditions OCT images are derived from measuring the signal of a were skin disease and normal skin. All human studies reference laser beam mixed with light scattered from were included with no restrictions on age, sex, ethnicity within the skin and is based on interferometry. OCT does or type of study. Case reports and case series were not detect fluorescence. Most commercially available sys- included. Only papers in English were included. More- tems have handheld probes with sizes such as modern over, only studies investigating gold nanoparticles with diameters above 80 nm were included. Particle size ultrasound systems and use an infrared laser centered at appears to constitute an important parameter defining the approximately 1300 nm. biological action of gold nanoparticles. This minimum Reflectance and fluorescence CM is a laser-based imag- particle size was selected based on the findings that ing technology, offering real-time microscopy to a depth of nanoparticles larger than 80 nm do not penetrate through 200 to 300 μm and resolution 0.5 to 1.25 μm. The laser light epidermis into dermis and cannot cause harm by passing focuses on a small skin area of interest and is reflected and the blood–brain barrier [14–16]. Exclusion criteria were scattered due to variations in refractive index of skin struc- other reviews, in vitro, ex vivo or phantom model studies. tures. The light travels back through the objective lens and Studies applying intravenous contrast agents were not reaches the selective aperture (pinhole) that prevents the pas- included, as we searched for contrast agents applied or sage of out-of-focus light. The confocality of the microscope injected directly to the skin. arises mainly from the diameter of the selective pinhole, which determines the resolution. The commercial CM sys- tem has a 0.5 × 0.5 mm field of view and image blocks can 2.3 | Methodological quality be captured to provide larger 8 × 8 mm image mosaics. Assessment of the quality of eligible studies was undertaken Whereas, contrast in reflectance CM (RCM) images is pro- using the Oxford Centre for Evidence-based Medicine vided by, for example, keratin and melanin that serve as (OCEBM) Levels of Evidence Working Group criteria (The endogenous chromophores, in fluorescence CM (FCM) con- Oxford 2011 Levels of Evidence). To rate the scientific qual- trast is derived from exogenous fluorescent dyes applied to ity of each study, all studies were graded according to or injected into the skin. Commercial systems usually consist OCEBM criteria using the question: “Is this diagnostic or of a flexible probe that can be applied to the skin area of monitoring test accurate?” and scored on a level from 1 to interest. 5. Oxford grades of recommendations ranges from A-D We systematically reviewed the literature using [17], which was also designated to each eligible study. See Embase and Medline databases to provide an overview of Tables S1. RING ET AL. 3of9 3 | RESULTS contrast to normal skin was increased compared with RCM images. The initial search yielded a total of 90 references, of which Fluorescein sodium: The normal skin architecture and 9 CM studies with 179 patients and 1 OCT study with psoriatic skin lesions have been investigated using fluores- 11 patients were eligible. All eligible studies were published cein sodium. In 22 patients, Swindel LD et al [20] demon- between 2003 and 2018. strated enhanced superficial skin architecture and clear The nine CM studies investigated four contrast agents: transition in keratinocyte size, shape and morphology aluminum
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