Ir J Med Sci DOI 10.1007/s11845-015-1296-3
Mohs micrographic surgery for periocular skin tumours in Ireland M. P. Treacy1 • N. C. Wynne1 • J. L. Gale1 • E. Duignan1 • B. Moran1 • A. M. Flynn1,2 • P. Ormond1,2 • R. Barry1,2 • R. Khan1 • P. Moriarty1 • L. Cassidy1
Received: 1 November 2014 / Accepted: 6 April 2015 Ó Royal Academy of Medicine in Ireland 2015
Abstract Objective To describe the shared care and outcomes of patients with periocular skin tumours who underwent Mohs micrographic surgery (MMS) performed by dermatologists, followed by oculoplastic reconstruction undertaken by ophthalmologists at two teaching and one private hospital in Ireland. Research design and methods This was a retrospective chart review at the Royal Victoria Eye and Ear Hospital, St James Hospital and the Hermitage Clinic. Results One hundred and twenty seven patients had periocular Mohs surgery between November 2006 and January 2013 mainly indicated for basal cell carcinoma. The mean follow-up time was 2 years and to date there have been no local recurrences. Conclusions MMS is available in Ireland and should be considered for patients with facial tumours in the ocular region. Keywords Mohs micrographic surgery Periocular tumours Periocular reconstruction Periocular BCCs
Introduction Mohs micrographic surgery (MMS) is a tissue-sparing excisional technique for non-melanomatous skin tumours where it is theoretically possible to achieve complete control of the & N. C. Wynne [email protected]
Royal Victoria Eye and Ear Hospital, Adelaide Road, Dublin 2, Ireland, Ireland
St James Hospital, James Street, Dublin 8, Ireland
tumour margin. Frederick Mohs , who was an American general surgeon, developed the technique in the 1930s. Thin saucer-shaped layers of tissue are sequentially excised and microscopically examined by the surgeon, who is typically a dermatologist with fellowship training in the technique . The layers are anatomically mapped and tissue is removed until the margins are free from malignant cells. The margin is examined in a horizontal fashion allowing inspection in its entirety . This differs from the traditional methods of histopathological examination where only a portion of the margin is examined using vertical slices, known as the bread-loaf technique . Mohs surgery enables complete excision of the lesion, whilst maximising retention of healthy tissue. The size of the subsequent wound is minimised, making reconstruction easier . Five to ten per cent of skin cancers are located in the periocular region where the skin and soft tissue are important for functional and cosmetic reasons . This region, known as the H-Zone, is considered to be a high-risk area for the local recurrence of tumours because of the anatomical architecture of the embryological fusion planes  (Fig. 1). Furthermore, the periocular skin and soft tissue are important for functional and cosmetic reasons, and due to the paucity of redundant tissue in these areas the temptation exists to minimise margins when conducting traditional surgery, thereby risking inadequate excision [6, 3]. MMS therefore offers particular advantages in the treatment of periocular tumours . The reconstruction of defects in this anatomical region can be complicated and usually requires specialist skills and close patient follow-up. For this reason the care of patients with periocular skin tumours is often shared between Mohs surgeons and ophthalmologists . The Royal Victoria Eye and Ear Hospital (RVEEH) regularly collaborates with St. James Hospital (SJH) to share the care of patients with periocular skin tumours from
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Fig. 1 The ‘‘H-Zone’’ indicating the embryological fusion planes where recurrence of cutaneous lesions is more likely
November 2009. The MMS is conducted in SJH by one of two dermatologists. Oculoplastic reconstruction typically occurs in the RVEEH on the following morning, by an oculoplastic ophthalmic surgeon. In addition to this routine arrangement there are some further patients who underwent MMS in SJH and who had oculoplastic reconstruction at the Hermitage Clinic. Also prior to November 2009, as early as 2006, there were a small number of cases that had MMS in SJH and reconstruction at the RVEEH and these cases are included in this study. This paper describes our experience treating patients with non-melanomatous periocular skin tumours using MMS and oculoplastic reconstruction in Ireland. The aim of this retrospective case series was to review the outcomes of these patients.
Methods The electronic hospital inpatient enquiry (HIPE) system in the RVEEH was interrogated to find patients who had reconstructive surgery following periocular MMS in SJH and this revealed 88 cases. The MMS surgery records were then examined in SJH and a further 39 cases were identified who had surgery at the Hermitage Clinic. The charts of all patients were examined and the following clinical details were recorded: age at time of surgery; sex of the patient; whether the lesion was a primary or recurring tumour; tumour location and histological subtype; number of MMS stages required; defect size; closure technique; complications; whether recurrence occurred during followup; time to recurrence; and length of follow-up.
Results In total there were 127 Mohs Micrographic surgeries performed between November 2006 and January 2013. One was carried out in 2006, one in 2007, seven in 2009, thirty-
two in 2010, fifty-two in 2011, thirty-two in 2012 and two during January 2013. There were 63 women and 64 men who had an average age of 68 years (youngest 28 oldest 91, SD 13 years). All of the MMS operations were performed in SJH by either Dr. Patrick Ormond or Dr. Rupert Barry. Reconstruction was carried out in RVEEH by Professor Lorraine Cassidy (79 cases) and Mr. Paul Moriarty (9 cases) and in the Hermitage Medical Clinic by Ms. Riswana Khan (39 cases). One hundred and seven primary basal cell carcinomas (BCCs) were excised of various subtypes; there were 68 nodular, 26 infiltrating, eight nodulocystic, five adenoid, three multifocal and two superficial BCCs. In addition to the primary BCCs there were five recurring BCCs, three of which were nodular and two were sclerosing subtypes. There were six squamous cell carcinomas (SCCs) and one sebaceous gland carcinoma excised. It transpired that nine patients (7 %) had non-malignant lesions removed. Sixty-one per cent of the lesions were cleared in the first MMS stage, 32 % were cleared in the second stage, five per cent in third stage and two per cent required a fourth stage to clear the margins. One patient could not tolerate the procedure under local anaesthetic and was transferred to the RVEEH for traditional surgical excision under general anaesthetic. The defect diameter was less than 1 cm in 25 patients, 1–1.99 cm in 65 patients, 2–2.99 cm in 18 patients, 3–3.9 cm in seven patients, 4–5 cm in six patients and greater than 5 cm in one patient. There was no defect size data for four patients and one did not tolerate procedure. The tumour was located on the lower lid in 84 patients (66 %). There were 29 medial canthal lesions (23 %) and 11 upper lid lesions (9 %). Three patients had lesions spanning from the upper to the lower lids. Reconstruction techniques included cheek flaps (n = 2), direct closures (n = 49), glabellar flaps (n = 10), Hughes flaps (n = 17), K flaps (n = 1), lid slides (n = 14), laissez faire closures (n = 1), periosteal flaps (n = 1), retroauricular skin grafts (n = 25), Tenzel slides (n = 17) conjunctival grafts and Z-flaps (n = 4). Some reconstructions included multiple techniques. There were 11 postoperative complications (8.66 %); five patients developed ectropion, two developed trichiasis, two had lid notches, one suffered a corneal ulcer due to postoperative suture abrasion and there was one case of cellulitis. The treating ophthalmologist successfully managed all of these complications. There have been no local recurrences identified to date. However, one of the patients with SCC had metastatic spread to the parotid gland requiring a parotidectomy and neck dissection. This metastatic deposit was diagnosed 2.9 months after the MMS and reconstruction was conducted.
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Discussion It is important to note that MMS is a tissue-sparing technique designed to minimise larger surgical margins . MMS can be used for non-melanoma skin cancers (NMSC) such as BCC and SCC . However, its use is not appropriate for melanocytic lesions . Malignant melanomas are aggressive tumours which can spread throughout the body . They require wide local excision down to fascia with at least a 5 mm margin and possible sentinel lymph node sampling depending on Breslow’s depth . The British Association of Dermatology has specific guidelines for the surgical management of melanomas . There are many methods for treatment of BCCs which include MMS, standard surgical excision, cryosurgery, curettage and electrodesiccation, radiotherapy, photo dynamic therapy, carbon dioxide laser surgery and medical treatments such as topical imiquimod . A recent Cochrane review concluded that excision is superior to the other treatment modalities . To date there is just one randomised controlled trial (RCT) comparing MMS to standard surgical excision and this showed that MMS is better for treating recurrent BCCs but only trended toward superiority for primary BCCs . This RCT has been criticised because it allowed MMS to be used as a rescue therapy for patients with primary BCCs assigned to the standard surgical excision group who did not have clear margins after the initial excision. In this trial, 23 % of the patients with positive biopsy margins after standard surgical excision for a primary tumour were rescued with MMS; this may have introduced bias in the results that reduced the apparent benefit of MMS over standard surgical excision for primary BCCs . The Cochrane reviews [9, 12] acknowledge that there is a paucity of RCT evidence; however, there have been several sizeable prospective case series and much literature published in Australia where BCC is a major public health concern [13, 14, 15]. Large non-randomised and retrospective studies suggest that standard excision has recurrence rates of 3–10 % for primary tumours and [17 % for recurrent tumours, [8, 16, 17] whereas, MMS yields recurrence rates of 1 % for primary tumours  and 5–7 % for recurrent tumours [19, 20, 21]. Many experts agree that MMS is preferable for high-risk BCC tumours located in the H-Zone (Fig. 1) . Cutaneous neoplasms appear to respect the boundaries of embryological fusion planes and tend to invade deeply before continuing superficial spread that would cross a fusion plane . This leads to a higher risk of surprisingly deep infiltration and subsequent failure of standard surgical excision to fully clear tumours located in this H-Zone. The recurrence risk of individual lesions is determined by
various factors including the size of the lesion, the duration of tumour before surgery, the histological subtype and whether the tumour was already a recurrence . Where MMS has been conducted, the stage of MMS required for clearance of tumour margins and the defect size can offer some further prognostic information . Tumours excised by MMS requiring greater numbers of MMS stages and with larger defect size tend to have a worse prognosis . Basal cell carcinomas are classified according to histological subtypes based on their microscopic appearance. Recognised BCC subtypes include nodular (50 %) infiltrative (10–20 %), micronodular (15 %), mixed (10–15 %), morphoeic (5 %) and fibroepithelioma (1 %). Of these, micronodular, infiltrative and morphoeic are more likely to recur after excision [22, 23, 24]. Seventy-five per cent of BCC recurrences happen within the first 3 years following excision [25, 26]. For primary BCCs 5 year follow-up is considered optimal and for recurrent tumours 7–10 years have been suggested . The patients presented in this study had a mean follow-up of 2 years (range 0.25–6.5 years). We intend to continue following these patients to obtain five-year data. It is known that 70 % of periocular BCCs are located on the lower lid . This was supported by our data, where 66 % of the tumours were lower lid lesions. In our group of patients there were five who had MMS for recurrence of a previous BCC. Three of these recurring tumours were located on the medial canthus, which seemed to be disproportionate to the total percentage of medial canthal tumours (20 %). However, this is consistent with the literature because medial canthal tumours are known to be more likely to recur than similar-sized tumours located in other periocular tissues . Squamous cell carcinomas represent 20 % of cutaneous malignancies and 5–10 % of eyelid malignancies . They are more aggressive tumours than BCCs and have more potential to cause death . SCCs can display perineural invasion and undergo metastatic spread to the lymph nodes and distant sites . Current accepted practice for the removal of SCCs by standard surgical excision is to take a wide 6 mm margin of normal tissue including subcutaneous fat as 30 % invade to this level . Incomplete excision increases the risk of metastatic spread . MMS is less well-established as the gold standard treatment of SCC; however, it seems to be particularly useful in localised cutaneous lesions where it can provide a cure rate of 97 % . Studies of MMS for SCCs report low recurrence rates for the periocular region with just 3.4 % at 5-year follow-up . Some authorities suggest that the final reconstructive surgery following MMS for SCC should be delayed in case there is a delay in the diagnosis of recurrence, which could be masked by
Ir J Med Sci Fig. 2 Diagnostic biopsy technique. a Pre-biopsy lesion on lower lid. b Small piece of tissue removed from centre of lesion for histology. c Postbiopsy appearance with obvious margins
flaps or grafts. However, this approach is normally impractical for eyelid tumours due to the functional importance of the periocular tissues . One of the five patients with SCC treated in our study was found to have metastatic spread to the parotid gland shortly after undergoing MMS for the primary tumour. This patient did not display any evidence of local recurrence and it is thought that the metastatic spread probably occurred prior to the MMS being undertaken. Sebaceous gland carcinoma (SGC) accounts for 1–5.5 % of all periocular malignancies [35, 36]. The periocular area is the most common site for SGC though it can also arise elsewhere on the body. It usually occurs on the upper eyelid reflecting the preponderance of meibomian glands there. These tumours can sometimes be mistaken for chalazions. SGC has a recurrence rate of 11–30 % and metastatic spread occurs in 3–25 % . MMS has been shown to offer low recurrence rates in the treatment of SGC ; however, SGC tends to exhibit multicentricity, pagetoid spread and non-contiguous growth making the determination of negative margins difficult . In the USA approximately 30 % of all BCCs and 25 % of all SCCs are excised using MMS . A much higher proportion of facial non-melanoma skin cancers (NMSC) are referred for MMS than those situated elsewhere in the body . In Europe, MMS is not as readily available and it is undertaken, almost exclusively, in tertiary referral centres . MMS is more expensive than standard surgical excision and it has been shown to be economically inefficient to use MMS in excision of all BCCs . The increased economic cost of MMS is directly linked to the length of procedure. One Mohs cycle, takes around 45 min to complete . Therefore, complex cases requiring numerous Mohs stages are more expensive. However, when the analysis is extended to include the cost of recurrence in patients treated with
standard surgical excision, MMS is shown to be more efficient . Furthermore, the requirement for less extensive reconstruction, or in some cases no reconstruction at all, reduces the relative cost of MMS . The tissuesparing qualities and improved cosmetic result are cited as enhancing the value of MMS . In our series nine patients had non-malignant lesions excised by MMS, which might be considered a waste of resources. One way to avoid performing unnecessary MMS would be to take a diagnostic or excisional biopsy prior to surgery. There is no consensus on the merits of taking excisional biopsies in the case of BCCs; it can be difficult to find the location of residual tumour if an excisional biopsy site has healed  but the clinical efficacy in diagnosing BCC without a tissue biopsy is only 60–70 % [45, 46]. If it is necessary to take a biopsy prior to definitive treatment, we advocate removing a small piece of tissue from the centre of the lesion for diagnostic purposes rather than attempting to remove the entire lesion (Fig. 2). This has the advantage of leaving the tumour intact thus making subsequent MMS more straightforward. The oculoplastic reconstruction complication rates in our study compare favourably with the literature. One published study reported that 36 % have complications including corneal ulcers (4.5 %), ectropion (12 %), granulation tissue (4.5 %), excess tearing (13.5 %) and diplopia (1.5 %) . Another study reported that 7 % developed either trichiasis or granulomas . In conclusion, Mohs surgery is available in Ireland and should be considered in appropriate patients. Suitable patients might include those with facial tumours along embryological fusion lines known as the ‘‘H-Zone’’, those with histologically aggressive tumour subtypes, those with large tumours and especially those with recurring basal cell carcinomas. More RCT data would be desirable to conclusively prove that MMS is indicated in the case of primary BCC.
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