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COMEDO CARCINOMA (OR COMEDO-ADENOMA) O F THE
F E M A L E BREAST
JOSEPH COLT BLOODGOOD
I n 1893, forty-one years ago, I assisted Dr. Halstecl in exploring a
clinically benign tumor of the breast. The patient was sixty-seven
years of age and had observed a small tumor for about eleven months.
It was our custom then to cut into the tumor and decide on its pathological nature from the naked-eye appearance of the tissues. This
tumor was not encapsulated and not oystic, but distinctly circumscribed
and buried in a senile breast. The moment we cut into and pressed
on it, there exuded from its surface many grayish-white, granular cylinders, which I called at that time comedos. From the gross appearance the tumor was diagnosed as malignant, and the radical operation
was performed. The nodes were not involved, the breast was senile,
and there was no gross or microscopic evidence of chronic cystic mastitis. This patient lived nineteen years after operation, dying at the
age of eighty-six.
Since then I have been recording such cases and have divided them
into two groups-pure
comedo-adenocarcinoma and comedo-adenocarcinoma with areas of fully developed cancer of the breast. Examples of the latter group, in which areas of pure comedo tumor are
present in an otherwise fully developed cancer of the breast, are the
more frequent, and for this reason the operator must always bear in
mind the possibility of cancer when comedos are present in a tumor.
Hence, if the tumor is too large to exclude the presence of malignant
areas by frozen sections, a radical mastectomy should be done.
Until three years ago it was my practice to perform the complete
operation for cancer of the breast in all operable cases, whether of
pure comedo or of comedo with cancer. In reviewing the records of
these cases the striking feature is that none of the cases of pure
comedo-adenocarcinoma was associated with metastasis to the axillary
nodes, and not a single patient died of cancer. The majority have lived
over five years, a few over ten years, and two almost twenty years. I n
one case, in which the disease involved both breasts, the patient is living today, more than twenty-one years after the removal of the second
breast, and twenty-three years after removal of the first breast. In
two instances the tumors had broken down, ulcerated, and produced a
fungous growth. I n a third case the fungous tumor was recurrent in
the scar of a previous operation at which only the tumor had been removed. This is the first example of a permanent cure following radical mastectomy for recurrent cancer of the breast.
I n contrast to the pure comedo group, is the larger number of case8
in which pure comedo areas were found, both grossly and with the
1 Read
before the American Association for Cancer Research, Toronto, March 28, 1934.
842
COMEDO CARCINOMA OF THE FEMALE BREAST
843
microscope, to be associated with fully developed cancer of the breast.
Of these patients in whom nodes in the axilla were not involved, 30 per
cent died of metastasis. Among the large number with axillary involvement the percentage of five-year cures was identical with that in
fully developed cancer of the breast without comedo areas.
Pure comedo-adenocarcinoma is a rare but distinct tumor of the
breast, and I am confident it can be recognized on frozen section when
FIG,1. FUNQOUS
TUMORIN SCAR
AFpER REMOVAL
OF THE BREAST,
ONE YEAREARLIER,
FOR A
PRIMARY
TUMOROF EIGHTEEN
MONTHS’ DURATION.
PATE.No. 1705
Halsted’s complete operation was done. The nodes were not involved and the patient
lived more than fifteen years without recurrence. This was the first so-called recurrent breast
a n c e r treated in the Halstod Clinic without further recurrence five years or more after the
second operation. For gross and microscopic pictures, see Figs. 2 and 3.
Incidentally this picture, taken in 1897, is of historic interest, as it shows the sterile
gown in which patients were dressed at that time before leaving the ward for the operating
room, Original photograph by Dr. Harvey Gushing.
explored as a small tumor, removed by cutting through normal breast
tissue, and then bisected. In the past two years three such tumors
have come under my observation. All three were clinically benign;
all were completely excised, with immediate postoperative irradiation,
and none has recurred. MicroscopicalIy they were pure comedo. A
fourth case was seen by my associate, Dr. L. C. Cohn, who was so convinced that he was dealing with a pure comedo tumor that he did not
844
JOSEPH COLT BLOODGOOD
completely remove the mass occupying the upper hemisphere of the
breast, nor did he give postoperative irradiation. Today, after more
than three years, there is no induration left in the patient's breast,
there are no palpable nodes in the axilla, the other breast is not involved, and there is no evidence of internal metastasis. These additional cases, together with the late results in the earlier ones, lead to
the conclusion that when the tumor is small and the frozen section
shows a pure comedo neoplasm, it is sufficient to excise only the tumor.
It is my object in this paper to give a pic$we-Of the clinical possibilities and the gross microscopic characteristics of comedo car-
$'I&
2.
CBOSS sECfrON THBOUGH
FUNGOUS
TUlirOE AND
PECTORAL MUBCLE, PROM CASE SHOWN
IN FIQ1
Note the superficial nature of the fungous tumor.
cinoma. As the comedos may'not be present in the earliest and smallest tumors, the final diagnosis must rest upon the microscopic picture.
After the removal of the breast tumor, in the interval before the pathological report is received, the axillary nodes may be irradiated and, if
healing is completed, the breast may also be irradiated after ten days
have elapsed.
Larger ulcerating fungous tumors of the breast should be irradiated before being subjected to operation. A patient of sixty-five whom
I saw six months ago had a large, oozing, fungous ulcer in the periphery of the upper outer quadrant of the left breast (Fig. 4). She
was weak and anemic. The axillary nodes were palpable, but the
tumor was operable. Irradiation with deep x-rays checked the hemorrhage and the tumor has gradually receded to an ulcer less than 2 cm.
in diameter. Clinically, the patient is well in spite of the fact that the
supraclavicular nodes are now palpable. She is still receiving irradiation over the axillary and supraclavicular nodes. Frozen sections of
the fungus showed the tissue so infiltrated with blood and so much in-
COMEDO CARCINOMA OF THE FEMALE BREAST
845
flammatory reaction that it was impossible to tell whether o r not areas
of comedo were present. I am confident that if this patient had had
the complete operation for cancer there would have been a serious
risk of death from an infection such as occurred in another case after
an operation for a similar tumor. I mention t,hese two cases to emphasize that when on exploration a tumor too large f o r complete excision
is found, which is microscopically a comedo, it may be wiser to give
the patient the benefit of radiotherapy before, rather than after, radical
operation, since if the growth is a pure comedo it may disappear after
irradiation.
PURE COMEDO TUMOR,SHOWING
SOME SOLID
BASAL-CELL
FIo. 3. TYPICAL,FULLYDEVELOPED
DUCTADENOXATOUS
ALvEoLr WITHOUT CENTRAL AREASOF NECROSIS
From case shown in Figs. 1 and 2.
I will not discuss here the relationship, if any, of chronic cystic mastitis to pure comedo-adenocarcinoma. I n an earlier article (Arch.
Surg. 3: 445, 1921) I recorded (page 540) under the group solid adenoma, four types. The first three of these, (1) small alveolar adenoma, (2) large alveolar adenoma apparently in the ducts, and (3)
small, irregular stellate adenoma are present in chronic cystic mastitis,
while the fourth, comedo-adenoma, is not observed in chronic cystic
mastitis. It is quite possible that the large solid adenoma may be the
beginning of an area of pure comedo; but the typical pure comedo with
a central area of necrosis is not a frequent occurrence in the breast
the seat of chronic cystic mastitis. This subject, however, needs further investigation. Undoubtedly, the pure comedo tumors will be ob-
846
JOSEPH COLT ULOODQOOD
served much more frequently in clinically benign tumors of the breast
exposed at operation. Nevertheless, late cases will still be seen, and
when more clinically malignant tumors are given preoperative irradiation with and without biopsy, more comedo-adenomas will be found
and their radiosensitivity more fully determined. I believe that the
majority of pathologists class comedo-adenoma with duct cancer.
Comedo-adenoma is a basal-cell tumor and apparently arises in ducts,
but it is rarely, if ever, present in the zone of the nipple and areola.
The accompanying illustrations show the clinical, gross, and microscopic appearances of the typical comedo-adenoma tumor. To avoid
confusion I propose to call this pure comedo-adenoma tumor, since in
spite of clinical signs of cancer and gross and microscopic pictures of
malignancy, and in spite of recurrence after excision of the tumor,
FIO. 4.
ULCERATED
FUNQOUS
TUXOROF BBEASTAFTER X-RAY
PATH.No. 62418
HEMORRHAOE.
See also Figs. 5 and 8,
IlLRAnIATSON
HAD CHECKED
there has never been, in this group, metastasis to nodes nor death from
cancer. As has been said, however, when this tumor occurs with fully
developed cancer of the breast, it behaves like cancer of the breast.
Fig. 1 shows a recurrent tumor developing into a fungus after
simple excision of the breast. There are three such cases among our
25 comedo tumors, two of them primary, one recurrent. The recurrent
tumor in the case illustrated was of one year’s duration; the primary
tumor was of eighteen months’ duration. The very superficial growth
of this fungous tumor in the scar is shown in Fig. 2, its histology in
Fig. 3. This case is the best evidence we have of the relative benignancy of the pure comedo tumor. The tumor was clinically malignant,
it recurred after excision of the breast, and is the first permanently
cured recurrent tumor of the breast observed in Halsted’s clinic at
Johns Hopkins. Yet the presence of the comedos in the gross specimen and the characteristic histological picture placed it in 1897 with
the first case of comedo tumor observed in 1893. Up to that time there
COMEDO CARUINOMA OF THE FEMALE B&PIAST
847
had been three other cases. Subsequently we have observed 22 additional cases.
Figs. 4,5, and 6 introduce the subject of irradiation for ulcerating
and fungous tumors of the breast. When Fig. 4 was photographed,
Nov. 23, 1933, bleeding from the fungous tumor of the left breast had
ceased as the result of x-ray irradiation, and the tumor was beginning
to shrink. By the following June only an ulcer some 2 cm. in diameter
remained. When irradiation was first given, in November, the axillary
nodes were palpable. Under continued irradiation they became
smaller, but have not yet completely disappeared, while the supraclavicular nodes have enlarged. This patient is clinically well. We
cannot tell the exact nature of this fungous growth, since the tumor
tissue was ohscured hy blood and inflammatory reaction. I am in-
FIG&
3
S H O W N IN FIff. 4 TWO MONTHSA N D SEVEN MONTHSLATER
6. PATIEKT
The tumor has been reduced to au ulcer about 2 em. in diameter.
AND
clined to feel that it is largely a cbmedo tumor, but in view of the involvement of the nodes, it probably contains cancer areas. This patient refused operation, but had she consented to it, irradiation would
still have been continued.
The specimen shown in Fig. 7 was a clinically benign tumor. The
surgeon, Dr. Ben Johnson of Richmond, Virginia, wrote me: “I am
sending you two specimens f o r microscopic examination. One is a
small lump taken from the b&st of a young woman twenty-six years
old. She noticed this little button about two and a half months ago.
I removed it under cocaine yesterday and am of the opinion that it is
benign.” I am inclined t o think today that ,Johnson was right, but not
until about one year ago did I encounter a similar lump and then I did
what Johnson had done in 1907-1 removed only the tumor, recognized it a s benign comedo-adenoma in the frozen section, closed the
FIG.1. SPECIMEN
TYPICALGROSSLYAND MICROSCOPICALLY
OF PURE
COMEDO
TUMOR. CASE
OF DR. JOHNSON.
PATH.
No. 8349
This is the type we may expect to see more frequently today. The complete operation for
cantor was advised.
FIG.8. SECTION
THROUGH TISSUE REMOVED
IN COMPLETEBREASTOPE~ATION
FOR CANCER,
SHOWIKG
PURE
COMEDOTUMOR. CASEOF DR. JAB.
F. M I T C H ~ L .PATH. No. 4819
This specimen shows more comedos than that in Fig. 7.
FIG. 9.
COMPLETEINVOLVEMENT OF BREAST
BY PURE COMEDO ADENOMA.PATH. NO. 15427
The patient is well more than twenty-one years after removal of the breast.
848
COMEDO CARCINOMA OF THE FEMALE BREAST
849
wound, and gave immediate irradiation. My patient is well today.
Dr. Johnson’s patient was lost track of after having been followed for
more than ten years.
Fig. 8 is another example of comedo-adenoma, recognized in the
gross by Dr. J a s F. Mitchell.
Fig. 9 is the photograph of a gross section through the left breast.
I n this instance the entire breast was involved by pure comedo tumor.
This patient had been operated on by me some three years previously
for a pure comedo tumor of the right breast. It was a small tumor,
and the complete operation was performed; but the nodes were not involved. The patient returned once a year for examination and at the
SECTION OF THE FIRST PURE COMEDO ADENOMA
OPERATED ON IN 1893. PATH. NO. 123
This photomicrograph was made from a section thirty-seveu years old. It is typical of
the older pictures of pure comedo tumor.
PIQ. 10.
last examination a nodule was present in the remaining breast. At
that time I was persuading many of my breast cancer patients to allow
me to remove the remaining breast because of the greater danger of
cancer in that breast-at least 6 to 8 per cent more than that of primary cancer. For this reason the breast was completely removed.
Figs. 10 and 11are microscopic pictures which should be compared
with Fig. 3. There is nothing particularly difficult in the recognition
of the pure comedo tumor in its fresh appearance, or in frozen and
permanelit sections. But as this tumor often occurs with fully developed and metastasizing cancer of the breast, the latter must always
be looked for. When the palpable tumor is small and can be completely excised by cutting through normal breast tissue and closing
850
JOSEPH COLT BLOODQOOD
the wound without injury to the symmetry of the breast, there is no
reason why the breast should not be saved without danger to the patient. Older women may be spared the complete operation for cancer
by an aspiration biopsy, when pure comedo tumor involving a large
part of, or the entire breast, is recognized.
An interesting case was observed by Dr. (3. A. MacCallum, of Dunnville, Ontario, and the specimen was sent to me in August 1899. The
letter from which I am about to quote was sent to me by his son, Dr.
TI7. G. MacCallum. The case is remarkable clinically as both breasts
were involved. Dr. MacCallum wrote that he operated simply to make
FIG. 11.
PURE
COMEDO TUMORWITHOUT ALVFXILI
OF
PSEUDO-LACTATION
TYPE, PATH.No.
20198
the woman more comfortable for the time she had to live. The tumors
in each breast proved to be pure comedo tumors. The nodes in the
axilla were not involved. The patient died about fifteen years later
(1914), at the age of sixty-seven, without any evidence of external or
internal malignant disease.
Dr. MacCallum’s letter of Nov. 28, 1901, reads as follows: “Mrs. B.,
aged fifty-two, presented herself at my office on August 1, 1899, in a
very weakened condition. On examination, I found her right breast
much enlarged, very hard and with an open, red, fungating mass about
an inch and a half in diameter, below the nipple. She said she suffered intense pain and could get no rest. I found a mass of enlarged
nodes in the right axilla. The left breast also contained a tumor as
large as a goose egg and there were enlarged nodes in the left axilla.”
The swelling of the right breast had been present two years and the
patient had not observed any growth in the left breast. ‘(1, however,
COMEDO CARCINOMA OF THE FEMALE BREAST
851
told her,” wrote Dr. MacCallum, “that if we could remove the tumor
of the right breast she would probably have less pain and would probably be relieved for a time. Accordingly next day I did Halsted’s opeverything went
eration, having to graft a large piece of skin
well, and in two weeks the wound was nearly healed.” Dr. MaeCallum
later performed the complete operation on the left breast, and the patient fully recovered.
As I read this letter, thirty-three years after it was written, I am
more and more impressed that it is the best of evidence for the relative
benignancy of the pure comedo tumor. It may involve the entire breast,
...
FIQ.12. MOST8tISPICIOUS AREAFROM A PURE COMEDO TUMOREXPLORED
AND PARTIALLY
REMOVED,
THREEYEARS AQO. CASE OF DR. COHN. PATH. NO. 44244
This patient received no preoperative or postoperative irradiation. The breast is now
nermal both to palpation aiid transillumination.
occur at the same time in both breasts, produce a fungous tumor and
palpable nodes in the axilla, and yet the patient remain well and free
from recurrence sixteen years after operation. I n this case only the
tumor from the right breast was sent t o the laboratory, and I described
this in my original note as “pure comedo-adenocarcinoma, ” comparing
its gross and microscopic appearances with the tumors in Figs. 3 and
10. It was the fifth pure comedo tumor observed in the laboratory.
Fig. 12 shows the most suspicious microscopic area in the pure
comedo tumor explored more than three years ago and incompletely
removed by my colleague Dr. L. C. Cohn (see above). The tumor involved too much of the breast to remove it completely. I n the gross
it was a typical comedo tumor and comedo cylinders could be expressed.
852
JOSEPH COLT BLOOMOOD
Under the microscope, in frozen and permanent sections, the majority
of areas are pure comedo. Undoubtedly this is the most interesting
among the recent border-line tumors in which the breast has not been
removed, because not all the tumor tissue was excised, and there was
no preoperative or postoperative irradiation.
Fig. 13 is a section from a very small tumor of the breast which T
completely removed more than one year ago. After making a frozen
section of the entire tumor, and diagnosing it a pure comedo tumor,
I dosed the defect in the breast and gave a course of irradiation.
FIQ. 13. SECTION
OF
A TUMOR1.5 CM. IN DIAMETE~L
PRESENTFOR
PERIPHERY OF THE BBEAETOF A THIN WOMAN. PATH.
THE- WEEKS IN THE
NO. 61020
This tumor was completely excised under local anesthesia and was diagnosed as pure
comedo tumor. The patient L well more than a year later. There were no gross comedos
in the fresh tumor, which was circumscribed but not encapsulated.
There is no sign of trouble today. This tumor, in the gross, had no
comedos. Since that date I have explored another pure comedo tumor
after a thorough course of irradiation, which had changed the morphology of the cells more than the gross appearance of the tumor. The
tumor had been aspirated before it was explored and from examination
of the stained aspirated cells we could only decide that they suggested
a malignant tumor. We did not recognize the comedo tumor.
SUMMARY
AND CONCLUSIONS
In 1908, in Chapter 31 of Kelly and Noble’s Gyfiecology amd Abdo+nnifiaZSurgery (Vol. 11),I described the comedo tumor of the breast
COMEDO CARCINOMA O F THE F E M A L E BREAST
853
and classified it among the adenocarcirwmas as adenocarcinoma comedo
I wrote: “Among 12 cases of the pure type I have yet to observe metastasis to the axilla. All so f a r have been permanently cured. I n one
the tumor was bilateral (specimen sent t o me by MacCallum of Canada), The only positive cure of a recurrent carcinoma belongs to this
group.” I used at that time many of the illustrations which are again
shown here.
I n 1917, in Chapter XXIII on Lesions of the Female Breast, in
Binney’s Regional Surgery (page 611) I again described comedoadenocarcinoma with illustrations. At that time I wrote: “At the exploratory incision this (tumor) has such a distinct gross appearance
that one should never fail to recognize it.” Now I know that in the
earlier tumor the typical comedos may be absent. I n this article, also,
I used the term duct cancer f o r comedo-adenocarcinoma.
I n the past two years I have restudied all the cases of pure comedo
and also those cases in which the comedo tumor was mixed with fully
developed cancer. There is but one conclusion, and that is that pathologists can learn to recognize the pure comedo tumor in all its histological pictures by repeatedly studying the actual sections in the cases
in which the tumors have been removed, the breasts saved, and the
patients followed. Less difficulty is found in recognizing the later
picture of pure comedo, as shown in Figs. 3,lO and 11,than the earlier
cases, shown in Figs. 12 and 13.
The pure comedo tumor takes its place among the border-line tumors
of the breast, which are growing in importance. It must be recognized
in frozen and permanent sections if progress is to be made in diagnosis
and treatment.
NOTE(Nov. 23, 1934) : I t is now over four months since this paper was completed.
All the patients mentioned as living are still alive. The patient shown in Fig. 4, in
whom the fungous tumor disappeared under x-ray irradiation, is clinically well. The
glands in the axilla and neck are still palpable. No new cases are added and all the
evidence is that the pure comedo-adenoma does not give metastases, and can be cured
by excision of the local tumor only. When the tumor is of fungous nature or is too
large f o r local excision, irradiation should be tried first.