THE SURGICAL TREATMENT OF POST-RADIATION RECURRENT BASAL-CELL CARCINOMA OF THE FACE AND SCALP

THE SURGICAL TREATMENT OF POST-RADIATION RECURRENT BASAL-CELL CARCINOMA OF THE FACE AND SCALP By RANDELL CHAMPION, M.B.E., F.R.C.S.Ed., and ROBERT GIBB, M.B., Ch.B., D.M.R.T.(Eng.) From Christie Hospital and Holt Radium Institute, Manchester FOR some years now radiotherapy has been the accepted method of treatment of basal-cell carcinoma of the skin. Between 400 and 500 cases annually are treated in this manner at the Holt Radium Institute, and the results from a cosmetic, economic, and functional point of view are satisfactory. Even with careful radiotherapy, however, a certain number of cases develop recurrence in the irradiated area. Table I shows the percentage of primary recurrences at the fifth anniversary following radiation in early (Stages I and 2) cases of basal-cell carcinoma of the face and scalp treated in I938. Table II shows the recurrence rate after the third anniversary for cases treated in I947. Both these tables show a recurrence-free rate of over 90 per cent. An analysis of the I947 group (Table III) shows that there is only a very slight variation in the recurrence rates in the different sites. The high percentage in the chin region is insignificant with the overall number treated. TABLE I Basal-cell Carcinoma treated by Radiation Face and scalp : Stages I and 2 (Early). 1938 Number Treated. /. Number of Primary Recurrences, Fifth Anniversary. Percentage. 259 / 2i TABLE II Basal-cell Carcinoma treated by Radiation Face and scalp : Stages I and 2 (Early). I947 Number Treated, Number of Primary Recurrences, Third Anniversary. Percentage. 462 28 6 4 c 263

264 BRITISH JOURNAL OF PLASTIC SURGERY TABLE III Analysis of Cases treated in 1947 Area. Number Treated. Number of Primary Recurrences, Third Anniversary. Percentage. I --! Scalp and forehead... Ear, including pre-auricular and post-auricular area Eyelids.... Nose, including naso-labial fol~t Cheek Lips and chin IIO I7 ~48 87 75 I5 8 6 5 6 I 20 i The causes of failure of radiotherapy in primary cases of basal-cell carcinoma appear to be :-- 1. " Geographic miss "--a term coined in this hospital to denote failure in treatment, in which it can be shown that a small part of the treatment zone has either escaped radiation or has been inadequately radiated This is commonly due to slipping of a radium mould or an X-ray applicator. 2. Inadequate dosage of radiation. 3- The basal-cell cfircinoma which shows the adenoides cysticum pattern. This particular lesion is generally resistant to methods of radiation which cure a high percentage of skin basal-cell carcinomata. 4. Supralethal dose effects as noted by Paterson, who suggests that radiation above the optimum tumour-lethal dose may fail to produce a turnoutlethal effect. For post-radiation recurrences, radiotherapy is generally not advisable, and the treatment becomes a surgical problem. Surgical methods have lacked uniformity, and although the literature suggests that there is a general realisation of the importance of curing the lesion once and for all by adequate excision, there is little advice as to how to achieve this purpose. Further recurrence following excision is only too common, and this interim report is presented to show the need for a radical surgical outlook in such cases. It is the practice at the Christie Hospital that small excisions are undertaken by the plastic surgeon and gross excisions by the general surgeon. If possible, the repair is performed at the same time by the plastic surgeon. Before undertaking any treatment, the surgeon should have at his disposal a complete history of the case, as it is important to appreciate the original size of the lesion, the type of radiotherapy used, and the size of the area treated. A histological report is essential as basal-cell carcinomata show variations in pattern which are of importance from a treatment point of view. These variations can usefully be divided into three groups, though there is no clear demarcation between each.

SURGICAL TREATMENT OF POST-RADIATION RECURRENT BASAL-CELL CARCINOMA 265 I. The more usual pattern where the basal cells form clumps beneath the basal layer of the dermis. 2. The cases in which the adenoides cysticum pattern is predominant. This type of lesion is very slow-growing, generally resistant to radiation, and usually of low-grade malignancy. 3. In this group basal-cell tumours develop a palisade pattern, the cells of which tend to infiltrate beyond the basal layer. They are most commonly seen in the skin of the nose, particularly of the ala nasi and the nasolabial fold, but they do occur less frequently in skin lesions elsewhere in the body. It is the most difficult type to eradicate because of its infiltrating properties. During the four years under review, 1947 to 1951, forty-five cases of postradiation recurrent basal-cell carcinoma were treated by plastic surgery. To date, there has been one local recurrence which was of the nasolabial fold (Case 7) and two deaths. One patient died post-operatively, and the second patient died within a month from another pathological condition. The forty-five cases treated have been divided into the following sites detailed in Table III. I. Scalp area 2. Ear region 3. Eyelids 4. Nose 5. Cheek 6. Lips and chin region Some of the cases treated are now discussed in the following text. I. Scalp Area, including the Forehead and Temple.--When the lesion is confined to the skin and subcutaneous tissue, as indicated by its free mobility over the underlying structures, excision should include the lesion and the radiated area with a margin of o. 5 to I cm. In the case of lesions which are adherent to underlying structures and where there is likelihood of infiltration of the deeper layers, including bone, though this latter may be difficult to demonstrate radiologically, the whole thickness of skull in the affected area with o-5 to I cm. margin should be excised. The following case illustrates a recurrent lesion at the periphery due to a " geographic miss." Case i (Fig. I).--Male, aged 34 in I946. History.--Five months previously noticed small nodule on scalp which caught on comb and bled. October 1946. Patient presented with a typical basal-cell carcinoma, size I-5 by x cm., which was treated by low-voltage X-rays--2,25o r single exposure. November 1947. A marginal recurrence (Fig. 1, A) was excised with the radiated area and 0"5 cm. margin. Repair was performed with a rotation flap. Histology.--Basal-cell carcinoma. Patient has remained well since the operation. 15 2 4 2O 3 I

266 BRITISH JOURNAL OF PLASTIC SURGERY In general, lesions of the scalp area, whether superficial or deep, respond well to treatment, as the scalp and underlying bone are readily accessible and the area lends itself to repair. A FIG. I--Case I. A, November 1947- Superficial marginal recurrent lesion. B, November 1947. One week after excision and rotation flap. remained well since operation. B Patient has 2. Pre-auricular and Post-auricular Areas.--Superficial lesions of this region should be treated in the same manner as that indicated for the scalp. With deeper lesions there is often a tendency to undertake minimal excision in depth in order to preserve the underlying structures such as the facial nerve and temporomandibular joint. These mental anxieties often lead to inadequate removal with the likelihood of subsequent recurrence. In such cases, not only should the lesion be excised widely, but the underlying structures should be sacrificed to ensure that the turnout has been completely removed. The following case demonstrates inadequate surgery following a post-radiation recurrence and indicates the depth to which excision had to be carried at the second surgical operation. Case 2 (Fig. 2).--Female, aged 48 in 1942. History.--Three years previously noticed small ulcer commencing on birthmark on left pre-auricular area. December I942. Patient presented with large lesion extending from outer canthus to ear (Fig. 2, A) which was treated with radium mould and gold seed implant to a dose of 6,ooo r in eight days. Histology.--Basal-cell carcinoma (Fig. 2, B). February I944. A recurrence in the pre-auricular area (Fig. 2, c) was excised and the raw surface covered with a forehead flap. Histology.--Basal-cell carcinoma tending to become cystic (Fig. 2, D).

SURGICAL TREATMENT OF POST-RADIATION RECURRENT BASAL-CELL CARCINOMA 267 December I947. A further recurrence in the pre-auricular area was excised with diathermy. June I947. Lesion again recurred in the same area and was treated by diathermy and excision. A FIG. 2--Case 2. A, December 1942. Before radiotherapy. B, December 1942. Histology--basal-cell carcinoma. 18. November I947. A further recurrence of the lesion (Fig. 2, E) was excised widely and deeply and the raw surface covered with a rotation flap from the neck. At operation the tumour was found lying deep to the neck of the condyle. Excision necessitated

268 BRITISH JOURNAL OF PLASTIC SURGERY removing most of the ascending ramus with the coronoid and condyle, as well as a small portion of the base of the skull of the middle fossa. C I3 FIG. 2--Case 2. C, February 1944. Post-radiation recurrence. D~ February I944. Histology--tendency to form cystic pattern, x 18. Histology.--Basal-cell carcinoma with well-developed adenoides cysticum pattern (Fig. 2, F). Patient has remained well since operation (Fig. 2, G).

SURGICAL TREATMENT OF POST-RADIATION RECURRENT BASAL-CELL CARCINOMA 269 This case illustrates two interesting points. Firstly, the initial excision was inadequate, and this may have been due either to failure to appreciate the original size of the lesion and its probable deep penetration or to reluctance to sacrifice the temporo-mandibular joint at operation. Secondly, the histological pattern E F FIG. 2--Case 2. E, November 1947. Recurrence in flap. F, November 1947. FlistologyIadenoides cysticum pattern, x 18. shows a basal-cell carcinoma which has tended to assume the adenoides cysticum pattern. In this particular case it is probable that the histological type of the basal-cell carcinoma was the reason for its slow growth and low-grade malignancy. 3-The Eyelids. I Lesions, involving skin only, require excision with 0. 5 cm. margin and free grafting.

270 BRITISH JOURNAL OF PLASTIC SURGERY When the eyelid margin is involved and when the tumour cells have infiltrated on to the conjunctiva of the eyelid, the full thickness of the eyelid must be removed, taking a minimum of 0. 5 cm. to ensure complete extirpation of the lesion. When the eyelid conjunctiva has been removed, lining for reconstruction is obtained by raising conjunctiva from the eyeball, while local flaps provide skin covering. Although post-operatively there is some limitation in mobility of the eyeball, it is not gross enough to interfere with vision. G FIG. 2--Case 2. G, August i95 I. Three and a half years after second excision and repair. Patient has remained well since operation. Invasion of the ocular conjunctiva by tumour cells is an indication for removal of the eyeball. Too often inadequate treatment has been performed on this type of case in order to save the eye, and this has resulted in the lesion becoming untreatable. The following two cases demonstrate basal-cell carcinoma involving the full thickness of the eyelid. Case 3 (Fig. 3).--Male, aged 64 in I949. History.--Five years previously patient noticed small wart on lower eyelid. February I949. Patient presented with a typical basal-cell carcinoma of the lower eyelid with ectropion. The lesion extended to the lid margin and involved the conjunctiva of the lateral half of the eyelid (Fig. 3, A). It was treated with low-voltage X-rays, 2,25 r single exposure. October I949. Recurrence at outer canthus (Fig. 3, B) was excised with o" 5 cm. margin round the irradiated area. Lining was obtained by raising conjunctiva from the eyeball and covering by a local forehead flap. Patient has remained well since operation (Fig. 3, c).

SURGICAL TREATMENT OF POST-RADIATION RECURRENT BASAL-CELL CARCINOMA 271 A B c FIG. 3--Case 3. A, February I949. Before radiotherapy. B~ October I949. Small recurrence at outer canthus. C, January I95o. Three months after excision of recurrence. Patient has remained well since operation. Case 4 (Fig. 4).--Male, aged 45 in I947. History.--A small hard lump appeared on the lower eyelid near the inner canthus. October I947- Patient presented with a typical crusted basal-cell carcinoma, size I "5 by I cm., which was treated by gold seed implant, 7,ooo r. December I948. A recurrence of the lesion (Fig. 4, A) was excised with the radiated area and a o'5 to I cm. margin. The excision necessitated removal of about one-third of the lower eyelid plus the inner canthus and I cm. of the upper eyelid. Lining for the repair was obtained by raising the conjunctiva from the eyeball, and skin covering by a midline forehead rotation flap. The donor site was closed by direct suturing. Histology.--Basal-cell carcinoma (Fig. 4, B). Patient has remained well since operation (Fig. 4, c). These two cases indicate the nature of the surgical treatment considered ~aecessary, and although repair of the eyelids may present problems, these are not insurmountable. In both patients the conjunctiva was raised from the eyeball without gross interference of function.

272 BRITISH JOURNAL OF PLASTIC SURGERY A, December I948. Recurrent lesion. B, December I948. Histology--basal-cell carcinoma. 3o. C, February. I95 o. Fourteen months after excision. Patient has remained well since operation. FIG. 4--Case 4.

SURGICAL TREATMENT OF POST-RADIATION RECURRENT BASAL-CELL CARCINOMA 273 4. The Nose.--Cases of basal-cell carcinoma which terminate in death often start as a small nodule on or adjacent to the nose. While radiotherapy may be repeated and over-enthusiastic, surgery is often inadequate because of the " bogy" of repair. The histological pattern of basal-cell carcinoma of the nose, and in particular of the ala nasi, tends to differ from other lesions inasmuch as the tumour cells are arranged in palisades and tend to infiltrate well beyond the basal layer. This infiltration of tumour cells in the nose has a very significant bearing on the treatment. Of the ten cases treated where the ala nasi was involved, all showed this type of histological pattern. The following case illustrates the tragedy of repeated radiotherapy and inadequate excision. FIG. 5--Case 5. A, June 1944. Before radiotherapy. B, December 195o. Recurrent lesion at nasolabial fold after further radiotherapy in May 1945, which was followed by necrosis. C, March 1951. Further recurrence left side of nose following inadequate excision in December 195. A B C Case 5 (Fig. 5).--Male, aged 46 in x944. History.hDuring the past two years small pimple appeared at the left ala nasi. June I944. Patient presented with a typical basal-cell carcinoma 2 cm. in diameter with deep induration over 4 by 3 cm. on the left nasolabial fold (Fig. 5, A). It was treated with low-voltage X-rays, I,Soo r single exposure.

274 BRITISH JOURNAL OF PLASTIC SURGERY D E F FIG. 5--Case 5. D, May I95i. Histology--infiltrative type of basal-cell carcinoma. Io. E, June r95i. After radical excision of right side of nose. First stage of thoracic flap for lining in situ. F, August r95i. One month after primary reconstructive operation. Plastic treatment not completed.

SURGICAL TREATMENT OF POST-RADIATION RECURRENT BASAL-CELL CARCINOMA 275 May 1945- A definite recurrence present in the middle of the treated area, probably due to inadequate dosage of X-ray therapy. Bearing in mind that surgery might well be necessary in any case, it was decided to re-treat the lesion by gold seed implant, 6,ooo r. May 1946. There was necrosis and a suspicion of recurrence at the left nasolabial fold. April 1948. Small sequestrum of the maxilla removed. December 195o. Again there was recurrence (Fig. 5, B) proved by histology. Excision was performed, taking a minimal margin of barely o. 5 cm. around the whole ulcer, and the raw area was grafted. May 1951. Further recurrence noted in the region of the left side of the nose (Fig. 5, c). Radical excision was carried out, taking I-5 cm. margin, which included all the left side of the nose. Histology (Fig. 5, D) shows infiltrating type of basal-cell carcinoma. The result of this operation and the first stage of the thoracic flap which provided lining,are shown in Fig. 5, E. June and July 1951. Reconstructive operations were performed, lining for the cheek and nose was obtained by a thoracic flap moved up in two stages, and skin covering by a forehead flap, based on the temporal artery. On discharge home (Fig. 5, F) there was a very noticeable improvement in the patient's psychological outlook and he has now returned to work. He will require further reconstructive treatment. The following case illustrates radical excision following post-radiation recurrence on the ala nasi. A FIG. 6--Case 6. A, September 1947. Before radiation. Blue pencil mark on ala indicating the limits of radiated area. B~ October 195 o. Recurrent lesion of the ala nasi. Case 6 (Fig. 6).--Male, aged 39 in 1947. History.--Some months previously an ulcer developed following a scratch on ala nasi. September 1947. Patient presented with typical basal-cell carcinoma, size I cm. in diameter (Fig. 6, A), which was treated with low-voltage X-rays, 2,25o r single exposure. October 195 o. Recurrence of the lesion on the left ala (Fig. 6, B) was excised, removing all the radiated area plus I cm. margin. B

276 BRITISH JOURNAL OF PLASTIC SURGERY Histology (Fig. 6, c).--basal-cell carcinoma infiltrating deeply. February I95I. Forehead rhinoplasty was perfolmed. Patient has remained well since operation (Fig. 6, D). C /i~!~! ~ ~7 ili!!i!i FIG. 6--Case 6. C, October I95O. Histology--showing palisade infiltrative type of basal-cell carcinoma. D, March I95I. Two months after rhinoplasty. Patient has remained well since operation. D The histology of both these cases shows an infiltrating type of basal-cell carcinoma which has penetrated deeply and which required radical surgical treatment.

SURGICAL TREATMENT OF POST-RADIATION RECURRENT BASAL-CELL CARCINOMA 277 It is interesting to note that Gillies in his paper to the Royal Society of Medicine, 1949, describes a recurrent carcinoma of the ala nasi, and Eckhoff in 1951 in this journal illustrates cases of recurrence in the nasolabial fold, though the histological type of the basal-cell carcinoma was not mentioned in either case. Lesions of the nose in the region of the inner canthus do show the infiltrating type of basal-cell carcinoma, but more often they develop the adenoides cysticum pattern. Of seven cases treated in this site, six showed the cystic pattern, while three showed the infiltrating pattern in addition to the cystic type. Case 7 (Fig. 7).--Male, aged 57 in 1947. History.--First noticed nodule on right side of nose in region of inner canthus two,~ years previously. November 1947. Patient presented with a typical basal-cell carcinoma, size I cm. in diameter, which was treated by a gold seed implant, 6,1oo r. December 1948. Lesion recurred and was treated surgically (Fig. 7, A). The excision entailed I cm. margm around the radiated area and the underlying nasal bone was removed, leaving the nasal mucous membrane intact. The FIG. 7--Case 7. raw surface was covered by a midline A, December I948. Post-radiation recurrent lesion forehead flap, the donor site being closed of nose in region of inner canthus, by direct suturing. Histology.--Infiltrating pattern (Fig. 7, B (i)) and adenoides cysticum pattern (Fig. 7, B (ii)) of basal-cell carcinoma, from the one lesion. Patient has remained well since operation (Fig. 7, c). 5. The Cheek.--Recurrent lesions of the cheek lend themselves readily for treatment, as they can be widely excised and close easily. 6. The Lip and Chin Region.--Recurrent lesions of the lip and chin are not common and, as they are usually localised to the skin, they render few problems to treatment by surgery. CONCLUSIONS Radiotherapy for early primary basal-cell carcinoma of the face and scalp gives a recurrence-free rate of over 90 per cent. Post-radiation recurrences should be treated by bold and radical excision, and the surgical treatment should be based on the previous size of the lesion, the area radiated, and the histological pattern. In the series reported the infiltrative type of basal-cell carcinoma has been found to occur more often in the skin of the nose than in other regions. Radical surgical removal of this type of lesion entails a I to I-5 cm. wide excision of the malignant process.

278 BRITISH JOURNAL OF PLASTIC SURGERY B (i) C FIG. 7--Case 7. B (i), December 1948. Histology--showing infiltrating type of basal-cell carcinoma lying deep to the muscle marked with arrow. 3o. B (ii), December 1948. H i s t o l o g y - - showing cystic pattern, x 7. C, February I949. Two months after repair. Patient has remained well since operation. i B (ii) The writers are indebted to Dr Ralston Paterson for his encouragement and interest in this work, and to Dr R. Taylor for her assistance with the histological sections. They woum also like to thank Miss E. Gibbon, Mr S. H. Heaton, and Mr F. Vdardlaw for the photographs and photomicrographs.