Long term results after surgical basal cellcarcinoma excision in the eyelid region

Stefan Pieh, Andreas Kuchar, Philipp Novak, Rainer Kunstfeld, Gunda Nagel,F J Steinkogler

AbstractAims—To evaluate the data for patientswith basal cell carcinoma (BCC) in theeyelid region, to demonstrate histologi-cally controlled tumour excision, and toprove the eYcacy of the treatment on thebasis of long term observations.Methods—Retrospective analysis of 382microscopically controlled BCC excisionsin the eyelid apparatus (350 patients) in afollow up study over 5.7 (SD 1.1) years.Tumour location, tumour size, and histo-logical results were recorded. The sameprocedure was followed for recurrences.Follow up examinations were carried out1, 3, 6, and 12 months after the operation,and then annually for a further 4 years orlonger.Results—A recurrence rate of 5.36% wasobserved after the primary operation.60.3% of first recurrences occurred in themedial canthus, 41.2% showed in depthextension, and sclerosing types wereoverly represented at 35.3%. After the sec-ond operation the recurrence rate in-creased to 14.7% and reached 50% after athird and fourth operation.Conclusions—The greatest risk of recur-rence exists for BCCs of the medialcanthus with in depth extension, and forsclerosing types. The recurrence rateincreases after every operation. For highrisk cases, consideration should be givento adjuvant treatment such as radio-therapy.(Br J Ophthalmol 1999;83:85–88)

Basal cell carcinoma (BCC) is the commonestskin cancer of the eyelid, accounting for80–90% of cases.1 The most important riskfactors for BCC are fair skin, inability to tan,and chronic exposure to sunlight.2 BCC gener-ally grows slowly, invading and destroying theadjacent tissues; it rarely metastasises.3 Aggres-sive types of BCC are occasionally observed,4

especially in young patients. The various typesof treatment described in the literature includesurgical excision,5 cryotherapy,6 radiotherapy,7

laser surgery,8 and photodynamic therapy.9

This study involved exclusively surgical exci-sion with microscopic control of the woundmargins.

The technique of removing all histologicallyvisible tumour was first described in 1941 byFrederick Mohs.10 The original procedureusing zinc chloride paste was too destructivefor periocular tissues11 and was thereforereplaced by cryosurgery. Free autologous skin

transplants are necessary for covering thewounds resulting from removal of extendedtumours. The literature describes severalmethods for ensuring primary healing of thetransplant. The technique using pressurebandages was introduced in 1966 byMustarde,12 and in 1979 Metha13 developed asuture technique for free transplants thatsecures the contact with the wound bed. Theintroduction in the early 1980s of fibrin sealingfor skin transplants14 15 was a fundamentalinnovation which has since become the stand-ard technique for wound covering of freeautologous skin transplants.

Subjects and methodsPATIENTS AND TUMOUR CLASSIFICATION

This study involved the evaluation of 382 radi-cal BCC excisions in the eyelid region (350patients) carried out between 1980 and 1993.Fifty two of these patients underwent primarysurgical tumour excision at other hospitals andwere then assigned to our hospital for treat-ment of the recurrences. Clinical and macro-scopic diagnosis was carried out. In cases ofwidespread and infiltrating tumours the exten-sion was verified by echography, computedtomography, and magnetic resonance imagingfor purposes of planning the operation.

Tumour localisation was classified as upperor lower lid and medial or lateral canthus. TheBCCs were divided according to macroscopi-cally or echographically measured tumour sizeinto the groups 1–4 mm, 5–9 mm, 10–14 mm,15–19 mm, and 20 mm or larger. Tumoursgrowing deeply into the orbicularis oculi mus-cle are strictly classified as BCCs with an indepth extension. Histological results weredivided into three groups corresponding to theliterature.16 17 The histological patterns of BCCare determined by the relative amounts of cel-lular and stromal elements and by the extent ofcellular diVerentiation.

First groupNodular BCC, clinically the most commontype of BCC, is characterised by relativelyundiVerentiated cells and tumour masses con-taining a small proportion of connective tissue.Nodular BCC appears histologically in a solid,keratotic or adenoidal form. In solid types theperipheral cell layer of the tumour mass showsa characteristic palisade arrangement. Kera-totic types are characterised by parakeratoticcells and horn cysts in addition to undiVerenti-ated cells. The adenoid BCC resembles gland-like structures and the tumour has a mucoidappearance.

Br J Ophthalmol 1999;83:85–88 85

Department ofOphthalmology,University of Vienna,Medical School,Vienna, AustriaS PiehA KucharP NovakG NagelF J Steinkogler

Department ofDermatology,University of Vienna,Medical School,Vienna, AustriaR Kunstfeld

Correspondence to:Stefan Pieh, MD, UniversityEye Clinic Vienna,Währinger Gürtel 18–20,A-1090 Wien, Austria.

Accepted for publication31 July 1998

Second groupSclerosing (morphoea-like) BCC—The histo-logical pattern is determined by a highproportion of fibrous stroma. Tumour cellsform strands which often penetrate deeplyinto the dermis. Furthermore, sclerosing BCCis characterised by the loss of palisadeformation, especially in the deeper lying partsof the tumour.

Third groupSuperficial multicentric BCC shows irregularproliferation of tumour tissue attached to theunderside of the epidermis. In most cases thereis little penetration into the dermis. Theperipheral cell layer of the tumour formationshows palisading.

SURGICAL TECHNIQUE

The operation was performed under localanaesthesia in 375 cases; general anaesthesiawas necessary in six cases because of the extentof the tumour. Our technique corresponds tothe principles of Mohs’s micrographicsurgery.10 18 19 The first step is resection of themacroscopically visible tumour. The next criti-cal step is the excision of thin layers of tissuecircumferential to the debulking defect. Allspecimens must be marked with sutures inorder to indicate their in situ position. Thespecimens are taken to the histopathologicallaboratory where frozen sections tangential tothe surgical margin are prepared using amicrotome and then stained. The results ofmicroscopic examination are reported to theoperating theatre as quickly as possible andused for deciding whether additional tissueresections are necessary. Wound closure shouldnot be performed until total removal of thetumour has been verified histologically. Thedesired primary skin closure after tumour exci-sion may be achieved by undermining thewound margins if the suture tension does notrestrict the eyelid function. If the tumour wasextensive, primary skin closure is often impos-sible. In such cases we used skin transplantsfrom the upper lid or the postauricular region.

POSTOPERATIVE EXAMINATION

Routinely, macroscopic clinical examinationswere carried out 1, 3, 6, and 12 months afterthe operation. Further examinations took placeannually for a further 4 years or longer. Themean follow up period for the patients was 5.7(SD 1.1) years.

ResultsThe ratio of female to male patients was 1.4:1(204 and 146). The mean age of the femalepatients was 69.0 years; that of the malepatients was 67.1 years.

The primary tumour locations were distrib-uted as follows: 196 cases (56.0%) on the lowerlid, 95 cases (27.1%) on the medial canthus, 29cases (8.3%) on the upper lid, 30 cases (8.6%)on the lateral canthus (Fig 1A).

The size of the BCCs at diagnosis were dis-tributed as follows: 1–4 mm in 19.1% (57patients), 5–9 mm in 40.9% (122 patients),10–14 mm in 20.5% (61 patients), 15–19 mm

in 9.1% (27 patients), 20 mm or more in 6.7%(20 patients), BCC with in depth extension in3.7% (11 patients) (Fig 1B).

The histological types of the primarytumour were distributed as follows: sclerosingin 14.4% (43 patients), nodular types in 73.5%(219 patients), and superficial multicentrictypes in 12.1% (36 patients) (Fig 1C).

Primary wound closure was possible in 333cases. In this group neither wound infectionsnor other complications of wound healing were

Figure 1 (A) Location, (B) size, and (C) histologicalresults of basal cell carcinoma in the eyelid region.

86 Pieh, Kuchar, Novak, et al

observed. In the remaining 49 cases the woundcovering was performed by free autologoustransplant using the fibrin sealing technique.This method was simple to use. Complicationssuch as infection were not observed.

For the group of 298 cases whose primaryoperation was performed at our hospital, therecurrence rate was 5.36% (16 patients).

The locations of the 68 first recurrences (16patients first operated at our hospital and 52patients referred to our hospital for first recur-rent surgery) were distributed as follows:60.3% (41 patients) on the medial canthus,22.0% (15 patients) on the lower lid, 11.8%(eight patients) on the upper lid, 5.9% (fourpatients) on the lateral canthus (Fig 2A).

Of these first recurrences, 41.2% (28 pa-tients) showed an in depth extension, 4.4%(three patients) had a tumour size of 1–4 mm,8.8% (six patients) of 5–9 mm, 14.7% (10patients) of 10–14 mm, 14.7% (10 patients) of15–19 mm and 16.2% (11 patients) of 20 mmor greater (Fig 2B).

Histological analysis of the 68 first recur-rences revealed the sclerosing type of BCC in35.3% (24 patients), nodular types in 55.9%(38 patients), and superficial multicentrictypes in 8.8% (six patients) (Fig 2C).

In the group of 68 secondary operations therecurrence rate was 14.7% (10 patients). Inseven of these 10 patients the recurrent tumourwas located on the medial canthus, in five casesthe tumour possessed an in depth extensionand seven of these 10 recurrences wereclassified as sclerosing.

In the 10 patients requiring a third opera-tion, a recurrence was diagnosed in four cases.Three of these four recurrences were in themedial canthus, two showed an in depth exten-sion, and all were of the sclerosing type.

In the final group of four patients requiring afourth operation, two recurrences occurredduring the follow up period, were located onthe medial canthus, showed an in depth exten-sion, and were classified as sclerosing.

DiscussionThe introduction of microscopically controlledtumour excision by Mohs in 1941 and the fur-ther development of the cryogenic techniquehave led to considerable improvements in sur-gical tumour excision. According to previouslypublished reports, residual tumours remain inthe margins of resection after up to 50% ofsurgical BCC excisions performed without his-tological control.20 21

The great majority of patients with a BCC inthe lid region are over 60 years old, the mostcommon location being the lower lid. In mostof the cases the tumour size at diagnosis wasflat and between 5 and 9 mm: 73% of theBCCs are histologically classified as nodulartypes.

Our follow up period involving examin-ations 1, 3, 6, and 12 months after theoperation and then annually for a further 4years, is in accordance with the literaturerecommendation.22

A recurrence rate of 5.36% was observed forthe 298 patients undergoing histologically con-

trolled tumour resection in our hospital. Closecooperation with the pathologist and uninter-rupted preparation of the layered sections areimportant factors in ensuring that the histo-logical results can be relied on. Surgical instru-ments which have previously been used fortumour debulking must not be reused. Exci-sion of the layered segments must be carriedout using a separate set of instruments.

It is evident from the group of 68 first recur-rences that a BCC on the medial canthus ismore likely to recur than one located anywhereelse in the lid region (Fig 2A). This may be dueto the complex anatomy of the medial canthal

Figure 2 (A) Location, (B) size, and (C) histologicalresults of basal cell carcinoma recurrences in the eyelidregion.

Long term results after surgical basal cell carcinoma excision in the eyelid region 87

tendon, of the canalicular system, and of theorbital septal attachments. Not only are thesepredisposed to early in depth extension of thetumour, but the lacrimal drainage systeminduces the surgeon to be more cautiousduring tumour excision than is the case atother locations in the lid region. Analysis of thetumour extension also reveals that most recur-rences are associated with in depth extension(Fig 2B). A possible explanation would be thatprecise excision of a thin layer of tissue formicroscopic control is easier at the peripherythan underneath the debulking defect resultingfrom primary tumour excision.

A total of 14.4% of the group of histologi-cally evaluated primary tumours were scleros-ing BCCs compared with 35.3% of the groupof 68 primary recurrences. This indicates thatthe sclerosing type has a higher potential forrecurrence compared with other types.

After the first reoperation, the recurrencerate increases from 5.36% to 14.7%. This mayindicate that the recurrent tumours consist ofcells with a greater invasive potential. This“surgical selection” of aggressive tumour celltypes would also explain the increase in therecurrence rate after the second and thirdreoperation. The evaluation of recurrencesafter the first reoperation confirms that thegreatest risk of recurrence exists for BCCs inthe medial canthus, for those with an in depthextension, and for the sclerosing type. Therecurrence rate increases to 50% for patientswho have undergone a second or thirdoperation. Analysis of these recurrences con-firms yet again the critical factors of medialcanthus, in depth extension, and sclerosingtype.

The fibrin sealing technique proved to be aneasy method for fixing autologous transplantsand since its introduction has replaced othertechniques such as pressure bandages12 andsutures.13 In addition to the practical advan-tages of the fibrin sealing technique, good cos-metic results have also been achieved.

In our opinion microscopic control of thewound margins ought to become standardpractice in the surgical treatment of BCC.Correct diagnosis at an early stage permitstumour eradication in accordance with Mohs,preserving functionally important tissues, andallowing primary wound closure with resultant

simplification of the surgical procedure. Rou-tine ophthalmological examinations shouldtherefore be used as an opportunity to detectlesions in the eyelid region, especially withpatients over 60. It should be borne in mindthat surgical excision of a BCC in the medialcanthus or with in depth extension is a sophis-ticated procedure. This applies particularly torecurrence excisions. In high risk cases—forexample, a recurrent operation in the medialcanthus with a histologically evaluated sclero-dermiform type confirmed by the primaryexcision—the application of adjuvant radio-therapy should be considered.

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