Department of Plastic Surgery, Rambam Government Hospital, Haifa, Israd
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1 INCURABLE RECURRENCES OF BASAL CELL CARCINOMA OF THE MID-FACE FOLLOWING RADIATION THERAPY By BERNARD HIRSHOWlTZ, F.R.C.S., and DAN MAHLER, M.D. Department of Plastic Surgery, Rambam Government Hospital, Haifa, Israd Basal cell carcinoma is the most common carcinoma affecting mankind. Its diagnosis is relatively easy since the lesions are generally superficial and present characteristic appearances. As a rule they are recognised fairly early and their cure rate, provided surgical treatment is adequate, should approximate loo per cent. Advanced untreated cases presenting for treatment are becoming less and less frequent probably because of patient and doctor awareness. "Why then are a significant number of deaths due to this disease continuing to occur every year? " (Macomber et al, 1959). Irradiation is still one of the most common methods of treatment and the recurrence rate is relatively high : 7"3 per cent (Shigematsu et al., 1966), 8.o per cent (Von Essen, 196o), lo"5 per cent (Stoll et al., 1964), 15 per cent (Gibson, 196o), 24 per cent (Hayes, 1962), 25 per cent (Stmdell et al, 1966). Published figures for recurrences following surgical treatment are much lower: I per cent (McCallum and Kinmont, I966), 1"4 per cent (Rank and Wakefield, I958), 1"5 per cent (.Gibson, I96O), 2 per cent (Mahler and Hirshowitz, I967), 3 per cent (Hayes, 1962). However, surgical excision for recurrences following irradiation carries with it a higher subsequent recurrence rate : 15 per cent (Sundell et al., I966), 20"5 per cent (Cobbett, 1965). Within the group of recurrences following irradiation, basal cell carcinoma of the mid-face can cause gross and hideous deformities (Gaisford et al, 1958 ; Gibson, 196o ; Hayes, 1962 ; Lewin, 1963 ; Cobbett, 1965 ; Baxter and Pirozynski, 1967). In their article Pierce et al. (1953) preface their remarks with the words" A living death, why? " These authors were the first to raise the spectre of this irradiation danger. No bibliography was included in their article and the authors requested information from others. Four cases of incurable basal cell carcinoma of the mid-face, all previously irradiated, are herewith presented. In contrast to these four cases, we present a patient with advanced basal cell carcinoma of the nose who developed recurrences after surgery but whose condition has eventually become stabilised. CASE REPORTS Case L--This woman aged 53 years, had some 20 years previously been irradiated for lupus vulgaris of her nose. No record is available of the irradiation dose that was given. Ten years later she developed a basal ceu carcinoma with epidermoid elements in the skin of the nose. This was treated by additional radiation therapy which proved unsuccessful in controlling the growth. Thereafter, most of the nose was radically excised and this was followed by immediate reconstruction by means of a Tagliacozzi arm flap. Further recurrences developed deep to the flap and a second radical excision was performed ; the nose was again reconstructed, this time by a chest flap. When first seen by us in 1959, deep recurrences had again developed and wide excisions were undertaken leading to extensive deformities (Fig. I). Intra-arterial perfusion of the left external carotid artery using Methotrexate, proved of no avail. The tumour spread to the ethmoid sinuses and finally to the dura. Enucleation of the left eye was performed and finally the "living death" came to its inevitable end. 205
2 206 BRITISH JOURNAL OF PLASTIC SURGERY Case 2.--When first seen by us in 1966, this woman was aged 61 years. A small turnout of the right side of the nose had been treated some 25 years previously by irradiation. The dosage of irradiation given is unknown. Recurrences of this tumour which proved to be basal cell carcinoma on histological examination, were dealt with by wide excision. The defect was repaired by means of a reconstructive rhinoplasty performed elsewhere. Deep spread under the flap led to invasion of the right maxillary antrum, the alveolar margin and the hard palate (Fig. 2) and eventually to the ethmoid sinuses. A feature of this patient was the unpleasant odour emanating from the necrotic tumour tissue which eventually confined her in isolation. Repeated local excisions of necrotic bone were made. Death claimed this patient after an excruciatingly slow progression of the lesion. FIG. I FIG. 2 Fig. i~z-shows severe deformity of the left raid-face, following wide resections for persistent recurrences of a previously irradiated basal cell carcinoma. Fig. 2.reAppearance of a patient showing invasion of the mid-face by an uncontrolled basal cell carcinoma. The hard palate, maxillary antrum and the ethmoid sinuses are all involved. Case 3.--This male aged 60 when first seen in I962 suffered from multi-focal basal cell carcinoma of the skin of the face. Over a period of 27 years he was repeatedly treated by irradiation. Recurrences developed in the region of the left upper eyelid spreading into the adjacent forehead and left medial canthal areas (Fig. 3). Wide excision of affected tissues was undertaken and a forehead rotation flap was used for repair. In the region of the inner canthus of the eye the excision proved to be incomplete with probable deep spread into the region of the ethmoid sinuses. An unsuccessful attempt was made to control the tumour spread by means ofintra-arterial (external carotid) perfusion with Methotrexate. An additional uncontrolled lesion involved the right lower eyelid and right external canthal region. The patient left our care for another medical centre and died three years later, ostensibly from the effects of tumour spread. Case 4.--In 195I, this man then aged 24, following trauma to the right cheek, developed a basal cell carcinoma of the skin of the cheek. Treatment was by means of radium needle implant ; 5ooo rads were administered.
3 INCURABLE RECURRENCES OF BASAL CELL CARCINOMA When first seen by us in 1959, the patient was suffering from radiation injury to the skin of the right cheek and lower eyelid with ectropion. The excised skin showed basal cell carcinomatous elements in the margins. A large full thickness skin graft was applied. Four years later recurrences appeared over the skin of the nose and right lower eyelid. The lesions were widely excised and skin grafted. After a further four years the patient showed new recurrences in the nose, right lower eyelid and right cheek. XO7 FIG. 3 A case with multi-focal basal cell carcinoma of the face and neck, showing a deeply invading growth of the left upper eyelid and medial canthal regions. FIG. 4 A, A widely invading basal cell carcinoma of the right side of the face. Spread has involved the lower eyelid medial canthal re#on, nose and ethmoid sinuses. B, Present state, after wide excision of the tumour including enucleation of the right eye. The frontal maxillary and ethmoidal sinuses were excised, as well as the soft tissues and part of the nose, the area being coveredby split thickness skin graft.
4 208 BRITISH JOURNAL OF PLASTIC SURGERY A recent extensive operation included exenteration of the right orbit, deroofing of both right frontal and maxillary sinuses with removal of all mucous membrane lining, removal of most of the right ethmoid sinuses and excision of most of the right side of the nose. Figure 4 shows the present situation which may well progress to a fatal conclusion. Case 5.--This 7o-year-old man had an advanced basal cell carcinoma of his nose which had not previously been treated. The lesion was widely excised on four occasions with the application of split skin grafts to the defects. On each occasion, excision of the lesion was histologically proved to be complete. However, on three occasions recurrences appeared in the excised margins of the defect but following the last excision four years ago, no further evidence of spread has been noted. Figure 5 shows the present "stabilised " situation. FIG. 5 An advanced basal cell carcinoma of the nose treated initially by surgery. Four wide excisions have resulted in control of the growth. DISCUSSION In discussing the action of irradiation on basal cell carcinoma, two questions arise : I. In "successfully" treated cases are all the malignant cells destroyed by irradiation? If not, does the fibrosis resulting from the irradiation stop the turnour spread by encapsulating the remaining tumour cells? To quote from Pierce et al. (I953) ; " Some irradiated basal cell epitheliomata may become locked up for years in the scarred atrophic skin resulting from that treatment, then break out and grow suddenly and widely, invading tissue much more rapidly than did the original turnout. It is this type that we fear most, especially when it invades the nasal mucosa and then invades the bone." z. In recurrences, is there a change in the "turnout-host relationship "? In other words, are there biological or structural changes in the tumour cell leading to greater invasivencss? Have the natural defcnces of the host's tissue been so weakened as a rcsult of the irradiation that there is no longer an effective barrier to tumour spread, or are there still other factors participating in this process?
5 INCURABLE RECURRENCES OF BASAL CELL CARCINOMA 209 This " tumour-host relationship" can also be altered by repeated inadequate surgery. The chances of this happening however, arc small indeed if one considers the very low post-cxcisional recurrence rate of 1-3 per cent. The technique of excisional biopsy which should be performed in all cases will reveal those lesions which have been incompletcly excised and a careful follow-up survey will as a rule detect any early recurrence. If this is adequately dealt with, the same chances of success should attend this re-excision as after primary excision since little, if any, "biological deterioration" should follow surgery. Two clinical observations with regard to the mid-third face area may indicate the manner in which irradiation may cause further damage in these areas and contribute to the uncontrollable spread of recurrent basal cell carcinoma : (a) The mid-third of the face has the highest incidence of basal cell carcinoma. It may be that particularly in this region, changes in the skin structure occur which arc the precursor to the appearance of basal cell carcinomas. This initially damaged skin is more likely, therefore, to suffer from irradiation treatment than skin in other parts of the body. (b) The skin and subcutaneous tissues of the mid-face are relatively thin and the underlying bone, cartilage, sinuses and cavities are in close proximity to the surface. Again the diploic bones of the mid-third of the face have only a thin cortical layer. Accordingly, radiation therapy of the mid-face could adversely affect not only the skin but also the deep structures as well. One can therefore assume that irradiation of the mid-third of the face is potentially hazardous as the skin is already relatively damaged and the deeper structures being so near the skin surface, are particularly liable to be adversely affected by irradiation. The spread of uncontrolled basal cell carcinoma of the mid-third of the face can be likened to a field fire in that recurrences develop at widely separated points. According to Gibson (r96o), bone and cartilage provide a natural barrier to the spread of the tumour. " These tissues resist penetration for quite a long time while the tumour is spreading along their surface." Figure 6 shows spread of the carcinoma into bone. A depressing feature of this disease is that after a recurrence has been radically excised through "healthy" tissues, further recurrences may appear in the healed margins of the defect. Histological FIG. 6 reports on the excised lesions confirm that a complete Histological appearance of an unconexcision had been effected. Unfortunately, only trolled basal cell carcinoma (Case 4) invading the deep structures of the too often in these post-irradiation recurrences, face. This preparation shows infiltra- complete excision confirmed histologically, is illusory, Another substantiation of the invasiveness of this tumour is the occurrence of metastases. More than 7o cases of metastasising basal cell carcinoma have appeared in the world literature (Hirshowitz and Mahler, I968). As far as can be ascertained from the available case reports, all lesions were of long standing and most had been treated initially by irradiation. tion of bone by the tumour. No doubt deep penetration of the mid-third of the face does occur in advanced non-irradiated basal cell carcinoma. Once the tumour spreads to the nasal mucous
6 210 BRITISH JOURNAL OF PLASTIC SURGERY membrane, then its subsequent eradication is made more difficult. But as stated previously, this is rarely met with following surgery which carries with it such a high cure rate. Correlation between the initial radiation dose, tumour size and recurrences.--to quote again from Pierce et al. (I953), " Some of the radiologists argue that the initial turnout dose is not adequate and when questioned as to adequate treatment, state that 30oo-5oo0 roentgen units to one half centimetre beyond the growth is adequate. Yet we have seen recurrences with the skin almost destroyed by irradiation and others with the skin badly scarred." Shigematsu et al. (1966) in their series had a 7"3 per cent recurrence rate, a figure which includes lesions which failed to regress following irradiation. The technique which they used most frequently was 35 rad skin dose x 13, in 17 to 19 days--the total irradiation dose per lesion being 455 fads. These authors state that increasing lesion size does not significamly augment the likelihood of recurrence for lesions in the region of the nose and eye. Stoll et al. (1964) in reporting their results of radiation treatment for basal cell carcinoma, had a failure rate of lo'53 per cent. The total irradiation dose given to individual lesions in the course of their work was between 4000 and 8000 rad. In their opinion there was no correlation between tumour size and failure rate. According to our records, three of the four uncontrollable cases had small lesions initially. Suggestions for handling basal cell recurrences post-irradiation.--pierce et al. (1953) state : "We are convinced that if the first irradiation fails to eradicate, and if there is a recurrence, surgery only should be done and at once ". " The excision should include, where applicable, the natural tissue barriers, namely, cartilage and bone" (Gibson, I96o). Because of the insidious spread of these recurrences, no major reconstructive procedures should be undertaken if possible, for a period of at least two years following radical excision. From the radiological literature, this time lapse also appears to be valid. According to Shigematsu et al. (1966) "the peak of recurrence post-irradiation is between one half and two years after complete turnout regression. All recurrences which were uncontrolled occurred before two years had elapsed." The use of split skin grafts to cover the operative defect offers the best means for detecting a recurrence because of the thinness of the overlying skin. Flap cover, which by its nature is much thicker, can conceal a recurrence for a long period during which it may progress to inoperable dimensions. It has been noted that some patients become acutely aware of a recurrence in that they feel a constant "itchiness " in the suspicious site.' This should put the surgeon on his guard when the question of a recurrence is being considered. In conclusion, there is no doubt that the most effective way to reduce the morbidity and the mortality of this disease is to desist from irradiating basal cell carcinoma of the mid-face. Surgery offers the best chances of cure and incidentally the best cosmetic result. McCallum and Kinmont (1966) say," While there is as yet no single treatment that is universally satisfactory, the plastic surgeon has a major contribution to make in the treatment of basal cell carcinoma, especially if he has an opportunity to treat it in its early phase " SUMMARY Irradiation of basal cell carcinoma of the mid-face is complicated in certain cases by uncontrolled spread of the turnout.
7 INCURABLE RECURRENCES OF BASAL CELL CARCINOMA 2II Four such cases are presented of widespread local infiltration by the turnout. A slow painful death, resultant directly from the effects of local invasion, occurred in three of the patients with the fourth patient tragically moving to the same inevitable conclusion. The anatomical features of the mid-face may account for this type of spread. There may also be an alteration of tumour-host relationship following radiotherapy. Surgery, rather than irradiation, is the treatment of choice for basal cell carcinoma of the mid-face. The authors wish to express their gratitude to Dr Eliezer Robinson, Head of the Oncological Department of their hospital, for his advice in the preparation of this paper. Their thanks are also extended to Dr Haim Lichtig for preparing the histological section and to Mrs Barbara Kulka for her excellent photographs. REFERENCES BAXTER, H. A. and PIROZYNSKI, W. J. (1967). Metastasizing basal cell carcinoma. American Journal of Clinical Pathology, 48, COBBETT, J. R. (1965). Recurrence of rodent ulcers after radiotherapy. Brmsh Journal of Surgery, 52, GAISFOV~O, J. C., HANNA, D. C. and SISSEN, A. F. (1.958). Major resection of scalp and skull for cancer with immediate complete reconstruction ; fourteen cases. Plastic and Reconstructive Surgery, 21, GIBSON, E. W. (I96O). Some aspects of the management of the recurrent basal cell carcinoma. In Transactions of the International Society of Plastic Surgeons, 2nd Congr. 1959, P. I IO. Edinburgh : Livingstone. HAYES, H. (I962). Basal cell carcinoma: The East Grinstead experience. Plastic and Reconstructive Surgery, 30, o. HmSHOWITZ, B. and MAHLER, D. (1968). Unusual case of multiple basal cell carcinoma with metastasis to the parotid lymph gland. Cancer, zz, LEWIN, M. L. (1963). Basal cell carcinoma. Plastic andreconstruetive Surgery, 3z, MCCALLUM, D. I. and KINMONT, P. D. (1966). Basal cell carcinoma. British Journal of Dermatology, 78, MACOMBER, W. B., WANG, M. K. H. and SULLIVAN, J. G. (I959). Cutaneous epithelioma. Plastic and Reconstructive Surgery, ~4, MAHLER, D. and HIRSHOWITZ, B. (I967). The clinical appearance of basal cell carcinoma. Harefuah, 7z, 453- PIERCE, C. W., KLABUNDE, E. H. and BROBST, H. T. (I953). Preliminary report on improper selection of treatment for basal cell epithelioma in the region of the orbit and the nose. Plastic and Reconstructive Surgery, II, I47-I5I. RANK, B. K. and WAKEFIELD, A. R. (1958). Surgery of basal cell carcinoma. BHtish Journal of Surgery, 45, SHIGEMATSU, Y., WEBSTER, J. H. and BRICOUT, P. (1966). Results of radiotherapy of skin cancer, with especial emphasis on treatment failure. Radiology, 86, 9o STOLL, H. L. Jr., MILGRAM, H. and TRAENKLE, H. L. (1964). Results of roentgen therapy of carcinoma of the nose. Archives of Dermatology, 90, o. SUNDELL, B., GYLLING, U. and SoIwo, A. I. (1966). Treatment of basal cell carcinoma by plastic surgery. Acta chirurgiea seandinavica, I3X, VON ESSEN, C. F. (196o). Roentgen therapy of skin and lip carcinoma : Factors influencing success and failure. American Journal of Roentgenology, Radium Therapy and Nuclear Medicine, 83,
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