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Evaluation of Stimulated Raman Scattering Microscopy for Identifying Squamous Cell Carcinoma in Human Skin

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Evaluation of Stimulated Raman Scattering Microscopy for Identifying Squamous Cell Carcinoma in Human Skin Lasers in Surgery and Medicine 45:496–502 (2013) Evaluation of Stimulated Raman Scattering Microscopy for Identifying Squamous Cell Carcinoma in Human Skin 1,2 1 1 1,3 4 Richa Mittal, MS, Mihaela Balu, PhD, Tatiana Krasieva, PhD, Eric O. Potma, PhD, Laila Elkeeb, MD, 4 1Ã Christopher B. Zachary, MBBS, FRCP, and Petra Wilder-Smith, DDS, PhD 1Beckman Laser Institute and Medical Clinic, University of California, Irvine, California 92612 2Department of Chemical Engineering and Materials Sciences, University of California, Irvine, California 92697 3Department of Chemistry, University of California, Irvine, California 92697 4Department of Dermatology, University of California, Irvine, California 92697 Background and Significance: There is a need to uncontrolled growth of epithelial keratinocytes. It is develop non-invasive diagnostic tools to achieve early and estimated that 700,000 cases of SCC are diagnosed accurate detection of skin cancer in a non-surgical manner. annually in the US, resulting in approximately 2,500 In this study, we evaluate the capability of stimulated deaths [2,3]. Although most of the non-melanoma skin Raman scattering (SRS) microscopy, a potentially non- cancer cases can be cured, rising incidence and local invasive optical imaging technique, for identifying the invasiveness constitute an important clinical challenge. pathological features of s squamous cell carcinoma (SCC) Today, non-melanoma skin cancer is diagnosed by visual tissue. inspection followed by invasive skin biopsy and histopath- Study design: We studied ex vivo SCC and healthy skin logical examination. Patients with SCC are at an increased tissues using SRS microscopy, and compared the SRS risk of future SCC tumor development, especially in the contrast with the contrast obtained in reflectance confocal same location or surrounding tissue. Primary cutaneous microscopy (RCM) and standard histology. SCCs can metastasize unless treated early by optimal Results and Conclusion: SRS images obtained at the surgical techniques, and thus early diagnosis is important. carbon-hydrogen stretching vibration at 2945 cmÀ1 exhibit While clinical diagnosis is generally quite accurate, these contrast related protein density that clearly delineates the suspicious lesions are currently diagnosed by an invasive cell nucleus from the cell cytoplasm. The morphological biopsy and sent for histopathological examination. Given features of SCC tumor seen in the SRS images show the advances in optical diagnostic devices, there exists a excellent correlation with the diagnostic features identi- need to develop non-invasive diagnostic tools to achieve fied by histological examination. Additionally, SRS exhib- early and accurate detection in a non-surgical manner, its enhanced cellular contrast in comparison to that seen in along with the ability to monitor these at-risk sites of field confocal microscopy. In conclusion, SRS represents an cancerization. attractive approach for generating protein density maps In the past decade, a number of non-invasive diagnostic with contrast that closely resembles histopathological methods have been studied for the skin including dermo- contrast of SCC in human skin. Lasers Surg. Med. scopy, high frequency ultrasound, optical coherence 45:496–502, 2013. ß 2013 Wiley Periodicals, Inc. tomography (OCT), reflectance confocal microscopy (RCM), and multiphoton microscopy. Dermoscopy is Key words: skin cancer; squamous cell carcinoma; routinely used in the clinical setting and its capability to stimulated Raman scattering; confocal reflectance micro- scopy; optical microscopy Conflict of Interest Disclosures: All authors have completed INTRODUCTION and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest and none were reported. Optical microscopy studies of skin cancer, the most Contract grant sponsor: American Society for Laser Medicine and Surgery ASLMS; Contract grant number: S12.12; Contract common form of cancer, have been facilitated by the grant sponsor: Air Force Office of Scientific Research AFOSR; manifestation of the disease in superficial tissue layers Contract grant number: FA9550-10-1-0538; Contract grant that are easily accessible for optical inspection. Due to the sponsor: NIH (LAMMP); Contract grant number: P41- EB015890; Contract grant sponsor: Chao Family Comprehensive optical accessibility of the epidermis, skin cancer is often Cancer Center and Cancer Center Support; Contract grant used as a model for evaluating novel diagnostic and number: P30 CA62203. Ã therapeutic approaches. While the majority of skin Correspondence to: Petra Wilder-Smith, DDS, PhD, Beckman Laser Institute, 1002 Health Sciences Road East, University of carcinoma lesions are in the form of a basal cell carcinoma California, Irvine, CA 92612. E-mail: [email protected] (BCC), squamous cell carcinoma (SCC) is the second most Accepted 25 July 2013 Published online 31 August 2013 in Wiley Online Library common pathology, constituting 20% of all cutaneous (wileyonlinelibrary.com). malignancies [1]. SCC is a malignant tumor arising from DOI 10.1002/lsm.22168 ß 2013 Wiley Periodicals, Inc. EVALUATION OF SRS MICROSCOPY FOR SQUAMOUS CELL CARCINOMA 497 identify SCC in situ [4], pigmented BCCs and atypical melanocytic lesions has been demonstrated [5]. However, dermoscopy provides insufficient resolution to resolve important diagnostic and prognostic cellular details. OCT studies have identified features of BCC [6] and actinic keratosis (AK) [7] up to depths of 0.5–1.0 mm, however, due to the limited resolution capabilities of OCT, cellular, and subcellular features are not readily discern- ible in these images. Confocal microscopy on the other hand, has shown to be capable of resolving cellular and subcellular details, both with reflectance contrast in vivo [8–11] and with contrast agents ex vivo [11–16]. These Fig. 1. Diagram delineating the components of the stimulated high resolution optical microscopy techniques [17,18] have Raman scattering microscope set-up. AOM, acousto-optic modula- the greatest potential for clinical acceptance given their tor; DM, dichroic mirror; SL, scan lens; TL, tube lens; LIA, lock-in ability to visualize cellular structures and in reality amplifier; PD, photodiode. performing an in-vivo biopsy with all the advantages of immediacy, non-invasiveness, and patient acceptability. demonstration of meaningful diagnostic contrast for the Stimulated Raman scattering (SRS) is a non-linear case of SCC. In addition, a simple and robust imaging optical microscopy technique which probes the vibrational approach is required, which is compatible with real-time signature of a molecule [19,20]. Unlike fluorescence imaging applications in the clinic. In this work we use a imaging which probes exogenous or endogenous fluoro- rapid, simplified SRS approach for generating meaningful phores, the SRS imaging provides label-free contrast that contrast, based on the direct mapping of the protein-like can be used to visualize specific molecular compounds density of the methyl vibrational mode. This allows us to based on their vibrational spectroscopic properties. Among visualize the signal from proteins present in nuclei, cell the accessible vibrational modes, the carbon-hydrogen membrane, and most abundant proteins in extracellular (CH) vibrational stretching plays an important role in SRS matrix-collagen, keratin. The signal thus acquired is microscopy, because of the ubiquitous presence of CH compared with that seen in RCM. We conclude that SRS moieties and the relatively high Raman cross sections of microscopy provides more cellular details and a more the corresponding modes. A variety of CH stretching faithful representation of the tissue, which potentially modes, including CH3 (methyl), CH2 (methylene), and CH could lead to a better diagnostic evaluation of skin cancers. (methine) groups, produce strong vibrational band struc- tures in the 2,700 and 3,100 cmÀ1 spectrum region. The MATERIALS AND METHODS CH mode contributes to the vibrational signal of the 3 Tissue Samples proteins and lipids, while CH2 mode is dominant in aliphatic lipids and can be used to map out protein and Facial SCC and healthy skin tissue specimen were lipid densities in biological tissue. It has recently been obtained per UCI IRB # 2008–6307. After excision through Mohs surgery the tissues were fixed in 2% paraformalde- shown that SRS mapping of the CH2 and CH3 mode can provide contrast that is reminiscent of the contrast seen in hyde in phosphate buffered (PBS) saline. Tissues were hematoxylin and eosin (H&E) staining of excised tissue embedded in optimal cutting temperature (OCT) medium, m specimens [21]. These studies have opened doors toward snap frozen in liquid nitrogen and 20 m thick sections the generation of “histopathology-like” images of superfi- were cut using a Microtome Cryostat HM 505E (MICROM, cial tissues in vivo, avoiding the need for invasive biopsies Walldorf, Germany). Tissue sections were placed on a glass or the application of labeling agents. microscope slide, immersed in PBS, and covered with a No. One of the premier targets of the SRS technique is skin 1 borosilicate coverslip and sealed with epoxy glue. tissue. With penetration depths up to 0.5 mm, SRS Unstained sectioned tissue was used for SRS imaging microscopy holds promise as a diagnostic tool of skin while the alternate tissue sections were stained with H&E carcinomas, which are present in the optically accessible for comparison. Experiments were performed at room epidermis layer of
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