Photoacoustic imaging for intraoperative micrographic control of the surgical margins of eyelid tumours

Basal cell carcinoma (BCC) is the most common form of eyelid skin cancer, and the standard technique for removal is excision with a predetermined marginal and postoperative histological analysis. Mohs surgery is an alternative technique that allows examination of the tumour margins by staged resection and simultaneous histopathological examination (Beaulieu et al. 2018). It is considered the most efficient method for the complete removal of high risk and complicated BCC. However, the procedure is time consuming and expensive, which limits its practice to specific cases. We here present a case where photoacoustic imaging (PA), an emerging non-invasive biomedical imaging modality, was used to detect that a pentagonal excision of an eyelid BCC was non-radical, which was later confirmed by histological examination. Photoacoustic imaging (PA) combines the advantages of optical spectroscopy and ultrasound and can provide high-resolution 3D images of the molecular composition of tissue. However, hitherto mainly animal studies have been performed, and only a few studies have been carried out on human skin tumours (Attia et al. 2017; Chuah et al. 2018), mostly melanomas. No study has yet described PA imaging of a BCC on the face or the eyelids, or used it to determine whether an excision is complete. An 87-year-old Caucasian male presented at the Department of Ophthalmology at Skåne University Hospital, Sweden, with a suspicious skin-coloured lesion on the left lower eyelid, of at least 6 months' duration. Clinically, a thin nodular BCC was suspected, and excision was planned. The lesion measured approximately 6 mm in diameter, and was located centrally, a few millimetres below the lash line. The tumour was surgically removed using a pentagonal excision procedure under local anesthesia, aiming at a surgical margin of 3–4 mm. The lesion was then placed in a plastic container filled with buffered saline solution, for ex vivo PA imaging using a Vevo LAZR-X imaging system (FUJIFILM VisualSonics Inc., Toronto, ON, Canada). Photoacoustic images were acquired using 59 wavelengths in the range 680–970 nm, and three-dimensional images were obtained by scanning the tumour using a linear stepping motor. Spectral unmixing was employed for the 3D scan to produce a coloured PA image, mapping the spatial distribution of tumour cells by means of their distinct optical absorption spectrum. After PA scanning, the lesion was examined histologically using standard haematoxylin and eosin staining. For methodological details see, Sheikh et al. (2018). The results of the PA examination showed a clear difference in the spectral signature from the BCC, defined as the middle of the visible tumour, and healthy tissue, defined as the tip of the pentagonal excision (Fig. 1A). Multiwavelength 3D scanning and spectral unmixing provided a map of the overall lesion architecture, and clearly revealed the tumour cell distribution (Fig. 1B). The tumour signal extended all the way out to the medial marginal, meaning that according to PA examination, the excision was non-radical. Subsequent histopathological examination revealed intermediate/infiltrating BCC, confirming that the excision was not complete in its medial portion (Fig. 1C). These results indicate that PA imaging could be used to delineate tumours in the periorbital region to achieve a more precise excision with better clearance, reducing the need for repeated excision. Further development is required to create a technique suitable for presurgical definition and delineation of the tumour borders. In the future, PA could also potentially be used for rapid examination of freshly excised unfixed tissue during surgery, to determine whether the excision is radical, or if further excision is necessary, saving time compared to conventional microscopic histology as in Mohs micrographic surgery.

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