Modified Radical Mastectomy: Why Not? HUGH
It is an honor and privilege to contribute to this issue honoring Dr George Humphrey% I was one of the last to bridge the transition, having interned under his much-beloved predecessor, Dr Allen 0 Whipple, later returning after World War II to serve a residency for four years under Dr Humphreys, and continuing on his staff to the present. It has been an interesting time in American surgery with the advent of many new concepts and technics, the most exciting of which has been the development of the surgeon’s ability to operate on any part of the body with relative safety and sureness. In cancer surgery the most radical operations were devised for a variety of malignant lesions and carried out successfully and with low mortality. During this period we achieved the goal of cancer surgeons; there were few organs that could not be removed, many completely, others subtotally. The great chance had finally come to learn the limits and possibilities of cure by radical surgical extirpation. The field of breast cancer shared in this movement with the advent of supraradical technics as described by Handley, Patey, and Hand [I], Dahl-Iversen [2], Lewis [3] and Wangensteen, Urban [4], and others in which internal mammary and supraclavicular nodes could be removed with massive en. bloc resection of these areas. Time, however, has shown that the increased morbidity and occasional mortality from such procedures, particularly when performed by those less skilled or experienced, were not clearly justified by the results in terms of five and ten year cure rates. Indeed it has been difficult to establish the superiority of any one of the large variety of procedures, from the most radical to the most conservative, with or without radiotherapy. The enormous number of reports, each arguing the merits of a particular approach, affords ample testimony to this fact. In short, what we are slowly learning and being forced to accept as the truth is that an individual’s chance of survival is determined more by the degree to which his own inherent immunologic defense mechanisms can hold in check, if not eventually eradicate, the malignant tumor rather than anything we, as surgeons, can do to remove it. This is not to say that surgery is ineffectual in the treatment of breast cancer, for I beFrom the Department of Surgery, College of Physicians and Surgeons, Columbia University. and the Surgical Service of the Presbyterian Hospital, New York, New York.
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AUCHINCLOSS,
MD, New York,
New York
lieve it very clearly is, especially in the stage I case (with no axillary metastases), but that the reason for its effectiveness lies in the ability of the patient’s defense mechanisms to confine the disease to the breast. In many instances tnese mechanisms seem to be overwhelmed totally by cancer from the outset; in others they operate successfully for a time and then collapse, and in yet others they remain effective and operative for the entire life span of the patient. In our present state of knowledge, or perhaps ignorance, how can we determine a rational approach? In attempting to arrive at this solution, at least for myself, the evolution of my own thinking has taken a somewhat tortuous course. I have the temerity to think that to trace its development to where I now stand might be of interest and perhaps help to others who are as perplexed as I have been and unfortunately still am! Such an account would seem to be an appropriate contribution to this issue of the Journd honoring the man under whose aegis it all took place. At the outset, I was strongly influenced by the radical approach to the cure of cancer. When one is thus inculcated by one’s teachers, among whom is one’s own much admired father, this becomes a powerful influence indeed. My father had developed the most radical and meticulous mastectomy of his day, long before the removal of internal mammary nodes was considered. His thesis was that many instances of postoperative local recurrence of disease could be attributed to inadequate removal of the dermal lymphatics of the skin overlying the breast and adjacent chest wall, which might be harboring malignant cells. He developed a “dermal dissection” technic [5] whereby virtually all of the superficial lymphatics were removed and the entire operative area, from clavicle to rectus muscle, from sternum to latissimus dorsi, was covered by a free, full thickness skin graft. These flaps received none of their blood supply from the periphery, depending for survival on their ability to become vascularized from the chest wall, as does any free graft. He performed this operation 152 times, with disappointing results. However, (he never lived to find this out, but the facts as I later analyzed them were as follows. The over-all ten year survival rate was 38.8 per cent and the local recurrence rate 14.5 per cent (twenty-two patients). In six of the twenty-two patients the local recurrence was widespread and occurred in patients with far advanced cancer at the time of mas-
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tectomy. In contrast, in the sixteen remaining cases, the local recurrence presented as either parasternal nodules, which are in reality an outgrowth of tumor from internal mammary lymph nodes, or as intercostal chest wall recurrences beneath the dermal dissection flaps. Since in the latter instances the skin flaps were really grafts and contained no subcutaneous tissues, it must be assumed that the local disease arose in the chest wall itself having already existed there in lymphatics prior to operation. This experience indicated that, except in very advanced cases, local recurrence of cancer on the chest wall bears little relation to the amount of skin removed, and is far more often a manifestation of tumor growing outward from internal mammary and chest wall lymphatics, which only then involves the skin. This does not mean that a reasonable amount of skin overlying the tumor, including the nipple and areola, should not be removed routinely; it should, and care should be taken to cut thin skin flaps we11 away from the underlying breast tissue since the latter can be extremely close to the skin in thin individuals. Up to this time I had been excising almost all the skin overlying the breast and covering the defect with dermatome skin grafts as described by Haagensen [6]. I now began to remove less skin, continued to cut thin flaps, but practiced primary closure using a conventional vertical skin incision in nearly all cases. The cosmetic effect was clearly improved. When I later learned that a transverse incision afforded similarly good access to the axilla, the eventual appearance of the chest wall was even better, and patients were able to wear low-cut dresses with no visible scar. Thus, if surgical results were to be improved, a new approach was indicated. The work of Handley and Thackray [7] on the incidence of internal mammary node metastases suggested such an approach both to themselves and to several other innovative surgeons. The most notable and persistent among these was Urban [4,8] whose radical mastectomy in continuity with en bloc resection of the internal mammary lymph node chain opened a new era in the surgical treatment of breast cancer. Even before this, in 1948 at Presby-
TABLE
I
Ten Year Results: Forty-Two Patients after Extended Presbyterian Hospital from 1952-1961
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terian Hospital, Dr Humphreys undertook in three cases to dissect the internal mammary nodes through a parasternal intrathoracic approach, following this in a few weeks by radical mastectomy. Commenting on one such case Haagensen wrote, “Since the carcinoma lies closer to the internal mammary chain of nodes than it does to the axillary nodes, it seems reasonable to remove the internal mammary nodes also, if we hope to cure her.” In only one of the three cases were the internal mammary nodes involved, and this patient died of cancer a year later. No further efforts were made in this direction at Presbyterian Hospital at this time. However, after Urban’s initial report, I undertook to follow his example and performed his operation on thirty-five selected patients from 1952 to 1961. During the same period seven such procedures were carried out by four other surgeons, making a total of forty-two. In all instances the tumor was located in either the inner half or the subareolar portion of the breast. There was no operative mortality and few significant complications. Table I shows the results. Internal mammary nodes were positive in only nine of the forty-two cases. In other words the Urban operation could have been helpful in only nine patients; actually it has proved possibly curative for two patients, or 5 per cent of the total. These two patients, alive and apparently free of cancer at the time of this writing, are indeed quite remarkable. One patient (MKT) was thirty-eight years of age at the time of operation in 1953 for a 2.5 cm tumor located over the second interspace close to the sternum. The pathology report indicated one positive axillary (central) node out of twenty-eight and a 5 mm positive internal mammary node in the second interspace. The second patient (T deM) was forty-eight years of age at the time of operation in 1955 for a 3.5 cm tumor in the lower central portion of the breast close to the areola. The pathology report indicated three positive axillary (central) nodes out of forty-one and two positive internal mammary nodes in the second interspace. The first patient received no postoperative. radiotherapy; the second received a tumor dose of
Radical Mastectomy
(Urban)
at
Number of Patients
Living Free of Cancer
Died or Living with Cancer
Diedwithout
Lostto
Cancer
Follow-up Study
All negative Axillary only, pOSitiVe Internal mammary only,
19 14
12 5
4 7
2 2
1 0
positive Both axiilary and internal mammary, positive
1
0
1
0
0
6
0 4
0 1
Status of Nodes
Total
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ia
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3,950 r with 250 kv to the supraclavicular and internal mammary areas. Despite these two exceptions, the beneficial results of the operation were discouragingly small. As time went on it did not seem justifiable to subject a large number of patients to the extended operation which either they did not need or, if needed, could seldom produce cure. For this reason and because of increasing evidence [9-II] to suggest that supervoltage irradiation (cobalt 60 or 2 million volts) was far more effective than 250 kv in arresting and possibly even completely eradicating breast cancer, the use of extended radical mastectomy was discontinued. Guttmann [II] states that autopsy findings show that, “there is no doubt that localized metastatic disease to internal mammary lymph nodes (less than 3 cm in size) can be sterilized with an adequate dosage of radiation.” With this background, the concept began to emerge that although radical mastectomy has a definite place in the treatment of breast cancer, it can only be effective in a limited number of patients and may be unnecessarily radical. Furthermore, if this limit could be defined more accurately, the conventional radical operation could be modified to make it less deforming and thus more acceptable without sacrificing any of its effectiveness. In attempting to answer this question and to define as accurately as possible the extent to which radical mastectomy need be carried, a retrospective study comprising the ten year results of conventional radical mastectomy performed on 107 patients who had proved axillary metastases was undertaken [22]. The operative specimens of these patients had been subjected to meticulous dissection by a single pathologist using a clearing technic to determine the number and to plot the exact location of each metastatic axillary lymph node. The principal finding was that only 30 of 107 patients with proved axillary metastases at the time of conventional radical mastectomy were alive and free of cancer more than ten years (revised as of 1969) ; of these, twenty-seven had involvement of four nodes or less which, with four exceptions, were located in the lower two thirds of the axilla. This was significant since it is perfectly possible to remove these nodes by simple mastectomy and subtotal axillary dissection. Such a modified radical mastectomy does not accomplish removal of the highest apical or subclavicular group of nodes since the chance of effecting permanent cure of the cancer, if these are involved, is minimal if not impossible. Indeed, thirtyfour of thirty-eight patients in the series who had involvement of these nodes did have recurrence. The four exceptions must be considered just that, and survival should be ascribed more to the patients’ innate immunologic resistance than to radical surgery. Inci-
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dentally, only one of these four patients received postoperative irradiation. From this study, together with a larger series assembled by Harvey and Auchincloss [ 131 comprising 415 survivors of radical mastectomy performed between the years 1951 and 1958, and from the on-going work of Handley [14] along similar lines in London, the now firm conviction developed that conventional radical mastectomy could indeed be modified safely. Such an operation consists of removing all breast tissue through a transverse elliptic incision, preserving both pectoral muscles, and including nearly total axillary lymph node dissection with primary skin closure. The technic of this operation has been described elsewhere [12]. It should be emphasized, however, that this operation is in no way simpler or less time-consuming than is conventional radical mastectomy. Axillary dissection must be performed from beneath the pectoral muscles, and it is absolutely essential that all the fascial investments of these muscles be removed carefully with the specimen if so-called Rotter’s nodes between the muscles and pectoral nodes, which may lie on the pectoral fascia just lateral to the anterior axillary fold, are to be included, Furthermore, the skin flaps must be developed carefully so that all breast tissue is removed. Finally, and especially important, the initial biopsy must never be allowed to penetrate through or even to the pectoral fascia; therefore, incisional rather than excisional biopsy is preferable unless the tumor is very small and superficial. Invasion of pectoral fascia or muscle is a rare occurrence. If it does exist, or if clinical evidence suggests it may, a plaque of pectoral muscle should definitely be included with the specimen. This modified operation has now been performed seventy-five times since 1956, so far with no unexpected results or untoward events and with no local pectoral muscle recurrence. I used it initially in only carefully selected patients, but in recent years, as confidence in the procedure has increased, I consider it the operation of choice in virtually all primary, operable cancers of the breast. Because of the high incidence of internal mammary metastases, 20 per cent in clinical stage I [8], it is followed by cobalt 60 or 2 million volts irradiation (5,000 rads in five weeks) to the internal mammary and supraclavicular areas in all cases in which the tumor is located in the medial half or subareolar portion of the breast, and in most cases in which pathologic examination shows more than minimal axillary node involvement, that is, one or two lower nodes. The early patients in the series were carefully selected and all had relatively benign types of cancer, without axillary metastases. The more recent cases, unselected since 1962, are too few and the follow-up
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interval too short to have statistical significance. Nevertheless, during the years 1962 to 1964, there were thirty-three patients, thirteen of whom had positive nodes. Nineteen (58 per cent) are alive and apparently free of cancer at the time of this writing. It is hoped, and confidently expected, that by use of this approach the best of both worlds, surgery and radiotherapy, may be achieved, modifying each in a conservative direction. The operation is far more acceptable to the average patient and is quite superior from a cosmetic and functional standpoint, As physicians, we should be aware that the quality of life is often at least as important as the quantity. When the former can be improved without sacrificing any of the latter, why should it not be? Summary The author traces the evolution of his surgical treatment of breast cancer from conventional, through extended, and finally to a modified, conservative, radical mastectomy as the treatment of choice for all primary operable carcinomas. The justification for this is outlined, and a case is made for the use of postoperative supervoltage irradiation in selected patients. References
2.
3. 4.
5. 6. 7.
8. 9.
10.
11.
12.
13.
1. Handley
RS, Patey DH, Hand BH: Excision of the internal mammary chain in radical mastectomy. Lancet 1: 457, 1956.
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Dahl-lversen E: Carcinoma of the breast. Official Transactions of the Northern Surgical Association, p 150. Copenhagen, 1951. Lewis FJ: Extended or super-radical mastectomy for cancer of the breast. Minn Med 36: 763, 1953. Urban JA: Radical excision of the chest wall for mammary cancer. Cancer 4: 1263, 1951; 5: 992, 1952. Auchincloss H: The nature of local recurrence following radical mastectomy. Cancer 11: 611, 1958. Haagensen CD: Diseases of the Breast, p 594. Saunders, Philadelphia, 1956. Handley RS, Thackray AC: Invasion of the internal mammary lymph glands in carcinoma of the breast. f3rit J Cancer 1: 15, 1947. Urban JA: What is the rationale for an extended radical procedure in early cases? JAMA 199: 742, 1967. Guttmann RJ: Survival and results after 2-million volt irradiation in treatment of primary operable carcinoma of the breast with proved positive internal mammary and/or highest axillary nodes. Cancer 15: 383, 1962. Guttman RJ: Radiotherapy in the treatment of primary operable carcinoma of the breast with proved lymph node metastases. Amer J Roentgen 89: 58, 1963. Guttmann RJ: Role of supervoltage irradiation of regional lymph node bearing areas in breast cancer. Amer J Roentgen 96: 560.1966. Auchincloss H: Significance of location and number of axillary metastases in carcinoma of the breast: a justification for a conservative operation, Ann Surg 158: 37, 1963. Harvey HD, Auchincloss H: Metastases to lymph nodes from carcinomas that were arrested. Cancer 21: 684, 1968. Handley RS: Observations and reflections on breast cancer. J Roy Golf Surg Edinb 6: 1, 1960.
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