CUTANEOUS METASTASES O F MALIGNANT DISEASE '

OLIVE GATES, M.D.

(Fuo~tzthe Ltrborelori~,sof Pathology, Ht~ntingtonMrnzorial Hospital, New Engla~zd D P ~ ~ C O I I P S S
Hospital, and the Pondville Hospital)

Cutaneous metastases are important because of their accessibility, although

less frequent than lymph node and organ metastases. T o ascertain their
approximate frequency, cases of metastasis to the skin were selected from
2233 autopsies in which malignant disease was present, from the Huntington

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Memorial Hospital, New England Deaconess Hospital, Pondville Hospital,
and Harvard Medical School, and from approxim~tely80,000 surgical speci-
mens of all kinds from the three hospitals. One hundred and eighty-one cases
were originally diagnosed as metastatic tumor in the skin. Eighty-eight of
these were discarded because of inadequate data, leaving a total of 93 tumors
of all kinds, including surgical and autopsy specimens, nletastatic in the skin.
In addition, 349 cases have been assembled from the literature. One hundred
and fifteen of these were gathered by Suzuki (60) in 1918 and are incor-
porated in this material, even though many of the skin tumors were not biop-
sied. The cases selected for this study, with the exception of a few reported
by Suzuki, were examined microscopically and the possibility of direct ex-
tension was excluded. One hundred and seventeen of the cases from the
literature were autopsied. An exhaustive survey of the literature was not at-
tempted. The cases in this paper represent rather a fair sample of the type
of case with metastasis to the skin which is being reported constantly.
The different types of malignancy producing skin metastases in this series
are charted in Table I. Of 82,298 malignant and non-malignant specimens
93 (0.1 per cent) are metastatic malignant tumors localized in the skin: 29
(0.04 per cent) from 80,000 surgical specimens, and 64 (2.3 per cent) from
the autopsy series of 2298 malignant tumors. The autopsy series probably
represents more nearly the true frequency of occurrence, since many meta-
static skin tumors may be unobserved or may not be diagnosed microscopically
during life. There are iew adequate statistics on the incidence of metastatic
tumors in the skin. My figures are considerably higher than others which
have been published and approach those given by Nusbaum and Heyer (41)
for metastases to the heart, which vary from 0.02 to 3.15 per cent. In
Suzuki's article, various authors are cited as recording the frequency of sec-
ondary skin tumors from 0.01 to 0.7 per cent for all types of cases, malignant
and non-malignant.
In Table I1 the cases in this series plus those from the literature are classi-
fied according to the site of the primary tumor, the location of skin metastases,
the age, and the sex of the patient.
A little more than one-half or 58 of the secondary tumors of the skin in
1 Read before the American Association for Cancer Research, Chicago, Ill., March 24, 1937.
"Sixty-five of the autopsied cases had more than one tumor, making a total of 2298 malignant
tumors in the autopsy series.
718
 CUTANEOUS METASTASES OF MALIGNANT DISEASE 719
I : Tumors Metastatic lo Skin *
TABLE

No. of
No, of No. of Percentage Primary
Total No. Cases Cases of Cases Malignant
of Cases with with with Tumors in
Biopsy Autopsy Autopsy Autopsy
Series

Carcinolila 2031
Malignant melanoma 19
Lymphoma 85
Leukemia 50
Sarcoma 83
Hemangio-endothelioma 11

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Myeloma (Ewing's) 10
Neuroblastoma 6
Myeloma (multiple) 3

2298

* 65 of these represent cases of multiple malignancy.

my group are epithelial: in 49 cases the primary site is known, in 9 carci-

nomas the original site is undetermined. Of 2031 carcinomas in the autopsy
series, 43 or 2 per cent had skin metastases. I n the group taken from the
literature the number of skin metastases from mesenchymal and epithelial
tumors is practically the same, 176 sarcomas against 173 cases of carcinoma.
Carcinoma of the breast is the most important of my group, producing as
many secondary skin tumors as all other types of carcinoma together. Among
58 metastatic carcinomas to the skin, 25 originated in the breast. In order
to rule out the factor of direct extension in breast carcinoma, skin metastases
located solely on the anterior and lateral chest wall, neck, and upper arms
were excluded. In striking contrast to these figures are the collected cases
from the literature, which show only 8 out of 173 metastatic carcinomas
primary in the breast. This may be due partly to the fact that secondary
skin tumors from breast carcinoma are so common as to excite little interest
and partly to the common assumption that they result from lymphatic permea-
tion and are, therefore, not true metastases.
The remaining 24 cases in my series arose from 14 different organs: 4
from the lung; 3 each from the uterus and kidney; 2 each from the stomach,
rectum, and pancreas; and 1 each from the liver, adrenal, thyroid, tonsil, jaw,
urethra, prostate, and penis.
In the group from the literature carcinoma of the stomach (54 cases) pro-
duces the majority of secondary skin tumors. After the stomach, the order
of frequency is: uterus, 17 cases; lung, 15 cases; large intestine, 13 cases;
kidney and ovary, 10 cases each; esophagus, 5 cases; liver, 4 cases; urinary
bladder, 3 cases; tonsil, pharynx, trachea, adrenal, thyroid, 2 cases each;
nose, larynx, parotid, tongue, penis, and gallbladder, 1 case each.
In both groups, carcinomas of the lung, uterus, and kidney are, with the
exception of the breast and stomach, the most i m p ~ r t a n tsources of skin me-
tastases, the incidence varying from 5 to 9 per cent. If carcinoma of the
breast is withdrawn from both series, the incidence for different sources of
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 Location Median
No. of No. of Total Duration Sex i
Litera- No. of --- of T u m o r Median
ture Age *
cases Cases Entire Extrem- before
Cases Head Death M F
Trunk Body 1 ities

L iv6r 1 I 1 I 15 wks.
Gallbladder 64
Pancreas 2 3 12 wks. 3
Adrenal 1 I 1 1 16rks i :; 1 1 1
Thyroid 1 1 24 wks. 48 1 1 2
Breast 25 11 52 wks. 54 2 31
Origin Undetermined 9 6 22 wks. 63 10 6
-3
--
t
4
- Total 3 19 20 wks. 53 23 46
-
TOTALCIRCINOII~E I 58 T/I 231 I SO 1 1 4 2 15 I 56 I 12 r k s . I 52 I
Sarcoma 4 wks.
Malignant Melanoma 24 wks.
Hemangio-endothelioma 104 wks.
Lymphoma 68 wks.
Leukemia 24 wks.
Chordoma

Total other than carcinoma 1 35 1 176 1 211 1 51 1 94 1 54 1 81 1 32 wks. 47 ( 125 85

--
Total all cases 442 I 101 I 236 I 69 I 137 I 20 r k s .
1
* In 54 cases, age not stated. t In 29 cases, sex not stated.

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722 OLIVE GATES

epithelial skin metastases is practically unchanged for the literature group,

but is considerably raised for carcinon~asof my series. The incidence of
skin metastases from carcinoma of the lung, uterus and kidneys is thus raised
from 7, 5, and 5 per cent to 12, 9, and 9 per cent, respectively. Stomach
carcinoma, however, still remains abnormally low in my group, forming only
6 per cent of skin metastases as compared to 32 per cent in the literature group.
The stomach has long been considered the most important source of skin
metastasis. Statistics from large groups of reported cases, however, give
rather contradictory results and do not altogether substantiate this assump-
tion. Riechelmann, Gussenbauer and Winniwarter are quoted by Suzuki (60)
as finding no skin metastases in respective series of 208 and 903 carcinomas
of the stomach. Edel (21) cites Lubarsch and Redlich as reporting respec-

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tively 8 cases (0.3 per cent) and 2 cases (0.4 per cent) of secondary skin tu-
mors in 2735 and 500 cases of carcinoma of the stomach. Edel (21) at-
tempted to compare the frequency of secondary skin tumors from carcinoma
of the stomach and from carcinoma of other organs and to this end collected
from the literature 75 cases of metastasis to the skin. Stomach carcinoma
held the first place with 2 7 cases (37 per cent); uterine carcinoma with 11
cases (15 per cent) and lung carcinoma with 6 cases (8 per cent) were the
only others of numerical importance. Strangely enough, only one case of
carcinon~aof the ovary is reported, and there is no case of renal carcinonla
in the group.
The percentage of carcinomas from a given organ which produce skin
metastases is difficult to determine, but is one of the most important factors
to be considered. Unfortunately there is very little information available
on this point. In an autopsy series of 156 carcinomas of the large intestine,
Warren (67) found 2 cases ( 1 per cent) with skin metastases. Riechelmann,
cited by Edel (2 I ) , found skin metastases in 0.9 per cent of 366 breast carci-
nomas. Busser (9) found only one case of skin metastasis among 94 carci-
nomas of the kidney. Simpson (58) reported a series of 139 cases of lung
carcinoma, 4 ( 3 per cent) of which had secondary tumors in the skin. Ask-
Upmark (4) collected statistics on the frequency and distribution of metas-
tases in carcinoma of the lung from 19 sources. Skin ranked thirteenth, with
32 cases, just after the spleen and the heart with 59 and 60 cases respectively.
Only 9 of the 19 authors, however, mentioned skin metastases. The inci-
dence of skin metastases reported by these 9 authors varies from 0.9 to 8
per cent; for the 1123 cases in the 9 series it is 3 per cent and for the entire
group of 2080 cases of lung carcinoma 2 per cent.
From this group of figures, it appears obvious that carcinoma metastatic
in the skin is frequently not recognized. No other explanation can ac-
count for the wide variation in figures such as those cited by Ask-Upmark
( 4 ) for carcinoma of the lung. However, in spite of discrepancies in per-
centages of incidence, there are a few epithelial tunlors which, when their oc-
currence is compared in three large groups of cases (Edel's, the cases from
the literature collected in this paper, and my series reported here) appear to
be consistently more important than others as sources of skin metastases. In
each of these three groups, lung carcinoma produced between 7 and 9 per cent,
and carcinoma of the uterus between 5 and 15 per cent of the skin metastases.
 CUTANEOUS METASTASES OF MALIGNANT DISEASE 72 3
I n two groups (Edel's and the collected literature cases) gastric carcinoma
produced 15 per cent and 31 per cent of the skin metastases. Renal carci-
noma produced 6 per cent of skin metastases in both of the groups of cases
reported in this paper. I t would, therefore, appear that a skin metastasis
of unknown origin is more likely to have arisen from one of these four organs
than from any other.
In the entire group of 442 cases reviewed in this paper there are 200 mesen-
chymal tumors. Lymphomas and leukemias make up 94 per cent of the
mesenchymal tumors and 43 per cent of the entire group. They will be dis-
cussed in a later paper. Aside from these there are only 11 mesenchymal tu-
mors in the series.
Mesenchymal tumors produced 23 per cent of the secondary skin tumors

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in my autopsy series. Of these, the lymphomas and leukemias are the most
important groups, secondary skin tumors being present in 8 (9 per cent) of
85 lymphoma autopsies and in 3 ( 6 per cent) of 50 leukemia autopsies. A
little over one-half of the lymphomas in the series are surgical specimens,
whereas all 3 lesions of leukemia cutis are from autopsies. T h e wide differ-
ence in the number of the two groups is due to the fact that in lymphoma cutis
the primary disease is less obvious than in leukemia and diagnosis frequently
depends on biopsy.
I have considered the melanomas as a distinct group because of their clin-
ical peculiarities and marked tendency to establish skin metastases. I n my
group there are 9 malignant melanomas producing definite and, in all but 2
cases, distant skin metastases. Six (31 per cent) of the 19 malignant mela-
nomas in the autopsy series produced skin metastases. Only two malignant
melanomas are included in the literature cases making a total of 11, or 2.3
per cent of 442 cases.
The distribution of metastases to the skin is of interest in regard to their
mode of spread and their relation to the primary disease. The most widely
placed tumors are the lymphomas and leukemias, which are more apt to be
present on all parts of the body surface than other mesenchymal or epithelial
tumors. I n 442 cases of metastasis to the skin, diffuse distribution over the en-
tire body was seen in only 69 instances, and 53 of these were either lymphoma
or leukemia. Carcinoma of the stomach, with 8 cases of diffuse skin involve-
ment, is the only other type of malignancy which approximates the widespread
skin metastases of these diseases. In only 20 per cent of the 189 cases of
leukemia and lymphoma were the tumors confined to one part of the body,
i.e., the trunk, head, and extremity, as compared to 38 per cent of all the
other malignant tumors which were thus located. However, involvement of
Inore than one part of the body surface is the rule with all metastatic skin
tumors. The trunk, including the neck, is involved more often than other
parts of the body, partly because of the larger area as compared to the head
and the extremities, and partly because it is the principal location for sec-
ondary tumors of the stomach and breast.
I n 72 of the 253 cases, excluding lymphoma and leukemia, the earliest skin
lnetastases were localized in the general vicinity of the primary tumors. For
example, skin metastases from carcinoma of the uterus and ovary were most
often seen first in the skin of the lower abdomen, groin or upper thigh; those
724 OLIVE GATES

from carcinoma of the stomach, first a t the umbilicus or in the epigastrium;

and those from breast carcinoma, on the thoracic wall. Secondary skin tu-
mors in 3 of the 11 cases of malignant melanoma and jn all of the hemangio-
endotheliomas were in the same general part of the body as the primary tumor,
although not closely adjacent.
Some tumors appear to have a predilection for certain sites. Twelve of
33 breast carcinomas presented secondary tumors on the scalp; 6 of these
were from my series and 6 from the literature. I n 5 (20 per cent) of my
cases of carcinoma other than breast carcinoma and in one case from the
literature, secondary skin tumors were confined to the scalp. One carcinoma
of the colon, from the literature, had a solitary skin metastasis on the scalp,
and in one case of carcinoma of the rectum, in my series, the only secondary

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skin tumor was located on the scalp. I n 13 cases of renal carcinoma me-
tastasizing to the skin, the head was the site of secondary deposits in S cases
and the scalp alone in 4 cases: 3 from the literature and one from my series.
Other parts of the body rarely show solitary skin metastases. Two cases
from the literature, with tumor originating in trachea and tongue, had sec-
ondary skin tumors confined to the face. In 2 cases of carcinoma of the
cervix from my group, skin metastases were present only on the lower ex-
tremities, and in one patient with a chorionepithelioma a single secondary
skin tumor presented on the thigh. Zoon (69) reported an interesting case
of chorionepithelioma which metastasized to the toes of the right foot and
to the left upper eyelid.
Secondary tumors in the upper abdomen or umbilical region comnlonly
originate from the stomach, ovary, or uterus. They are frequently associated
with metastatic nodules in the liver and may travel by the lymphatics of the
ligamentum teres. Burckhardt, according to Edel (21), found 11 out of 26
carcinomas of the umbilicus secondary to gastric carcinoma. Criep (13) col-
lected 137 cases of carcinoma of the stomach with inetastases in the skin, the
majority of which were in the umbilical region. Cullen (15) also supports
the view that umbilical carcinoma is most often secondary to malignancy in
the stomach.
T h e gross appearance of skin metastases is not distinctive and they have
been mistaken for such different lesions as tertiary syphilis, infected hair fol-
licles, and the nodules of periarteritis nodosa. There are, however, certain
characteristics which are helpful in differentiating secondary carcinomatous,
lymphomatous, and leukemic skin tumors. Secondary skin t~imorsof carci-
nomatous and sarcomatous origin are discrete rounded or oval masses.
Plaque-like forms rarely occur except in lyn~phomaor leukemia. Cancer en
cuirasse, which corresponds to the diffuse form of leukemia, differs from the
latter in that it is not a true metastasis, but rather a direct infiltration of the
skin from a neighboring tumor. T h e tumors are usually moderately firm,
and a t first may be resilient. This is particularly true of the metastatic renal
carcinomas, which, occurring frequently in the scalp, are often mistaken for
sebaceous cysts. Tumors secondary to breast carcinoma are more apt to be
quite firm and scirrhous. T h e overlying skin is usually movable, but may be
adherent, and is often a deep pink or violaceous color. Pigmentation is rarely
seen, though, Newcomb (39) described a case of secondary skin nodules from
 CUTANEOUS METASTASES OF MALIGNANT DISEASE 72 5
carcinoma of the breast with such marked pigmentation that the diagnosis of
melanotic sarcoma was made. Scirrhous lymphoblastoma is the only type of
malignancy, other than melanoma, which con~monly produces pigmented
cutaneous tumors or a diffusc pigmentation of the skin. Cutaneous metastases
of melanoma are more often colorless than not, and when pigment is present
it is very apt to be bluish rather than brown.
Ulceration is fairly common in l y n ~ p h o n ~and
a leukemia but is rarely seen
in other secondary skin tumors. The size of secondary skin tumors ranges
from 0.5 to 4 or 5 cm. Tumors over 4 cm. in diameter are relatively rare.
T h e majority are 1 to 2 cm, in diameter. Very large skin tumors, occasionally
8 to 10 cm. in diameter, are usually secondary to lymphoma.
The number of skin tumors ~ ~ a r i efroin
s one to several hundred. Single

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skin tumors were present in 28 cases of the entire group of 442 tumors; 19 of
these were epithelial tumors, 10 were skin tumors of lymphoma and leukemia.
The microscopic appearances vary chiefly with the type of metastasizing
cell. Tumor cells are found in all layers of the corium. I n some early tu-
mors scattered individual cells are present in the upper corium and papillary
bodies and, in distinction from lymphoma and leukemia, show no tendency to
collect around capillaries and lymphatics. I t is more common to find the cells
in the middle or lower layers of the corium whence they spread toward the
epidermis and into the subcutaneous tissue. Epidermal infiltration has not
been encountered in these cases. There is rarely evidence of the mode of
spread, whether by blood vessels or lymphatics. A certain amount of fibrosis
is usually present and in some tumors this is marked. The inflammatory re-
action is usually not great unless ulceration is present. T h e chief changes
in the skin structures may be attributed to pressure. Tumors of the deep
subcutaneous tissue and muscle are of infrequent occurrence but may occur
either alone or with tunlors of the true skin. Only the latter are considered
in this paper.
The type of carcinoma seems to be of relatively slight importance as a
factor in determining metastasis to the skin. Criep (13) found that adeno-
carcinoma more often gave rise to skin metastasis than scirrhous carcinoma.
More than one-half of Suzuki's cases were adenocarcinomas. I n my series
there are 18 cases of adenocarcinoma, 28 cases of carcinoma simplex, 7 of
epidermoid carcinoma, and 2 of papillary adenocarcinoma. T h e cases fro111
the literature are somewhat more difficult to classify because of the difference
in terminology. Among these, there are 8 cases of adenocarcinoma, 2 of carci-
noma simplex, 31 of unclassified carcinoma, 2 of colloid carcinoma, 2 of papil-
lary adenocarcinoma, 9 of scirrhous carcinoma, and 5 of epiderinoid carcinoma.
Because of resemblance between primary skin tumors and metastases of
squamous-cell carcinoma to the skin, certain cases are doubtful. One patient
in my series first developed an ulcerated tumor on his knee, measuring approx-
imately 3 cm. in diameter. This was excised and diagnosed epidermoid carci-
noma, grade 11. Because of the extensive ulceration there was no definite
evidence of origin from the epidermis, but the architecture was that of a pri-
mary skin tumor. Four years later, tumors of similar size without ulceration
developed on the scalp and trunk. Autopsy a few months after their appear-
ance revealed a carcinoma of the bronchus with widespread visceral metastases
726 OLIVE GATES

as well as secondary skin tumors. These were less well differentiated than
the tumor which had been excised four years previously but had the same ar-
chitectural structure. I t is impossible to say whether or not this is a case
of very early metastasis to the skin or one of multiple malignancy, although
the latter seems more probable.
The interval between the appearance of skin metastasis and death is often
difficult to determine with accuracy. The duration is stated in relatively few
cases. Many of the secondary carcinomas remain unnoticed during life, only
the unusually large or numerous tumors being remarked. I n my series, the
average length of life was longest in breast carcinoma; 9 patient? living an
average of sixteen months after the appearance of skin metastases. Four of
these lived one year, 1 lived two years and 3 lived three years. Only 3 died

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in less than six months. The mean duration for my group of 24 carcinomas
of all types was twelve months as compared to the 15 carcinomas exclusive
of the breast, which was eleven months. Nine of the latter group lived less
than six months. T h e 2 in which survival was of longer duration both had
carcinomas of the kidney and lived twelve months and eighteen nlonths fol-
lowing the appearance of skin metastases. One patient with adamantino~na
of the mandible died of distant metastasis three years after secondary tumors
appeared on the temple. There are 2 cases of secondary skin carcinomas
of long duration from the literature: a patient with carcinoma of the uterus
lived two years, and one with carcinoma of the stomach lived eighteen months.
I n 18 of my cases of lymphoma and leukemia, the duration of the skin
tumors is known. T h e time varied from less than six months to six years:
4 patients lived less than three months after the appearance of tumor; 14
lived six months or longer and 5 more than a year. Three patients are still
alive six years, two years, and one year respectively after the first appearance
of skin tumors. All the patients living more than a year had scirrhous lymph-
oblastoma. The average duration for my cases of lymphoma is nine months.
T h e duration of skin tumors in melanoma is known in only 3 cases. In
2 of these it was five and six months; in one case it was a year.
T h e cases from the literature are much more difficult to analyze in regard
to the time element inasmuch as the information is very indefinite. I n general
the skin metastases from carcinoma appear to be of shorter duration than in
my cases, averaging between five and six months, while the lymphomas and
leukemias are of longer duration than in my series, averaging two years for
lymphoma and one year for leukemia. I n Suzuki's group the duration of
the secondary skin tumor is known in 38 cases, 36 of these being carcinomas.
Twenty-two patients died within three months and only 4 lived more than
six months. T h e average duration of life after development of secondary
skin tumors was seven months. T h e majority of Suzuki's cases are of primary
gastro-intestinal neoplasms.
T h e behavior of secondary skin tumors, in general, gives no indication
of the growth of the primary tumor. Individual tumors may grow rapidly
for a time, remain stationary, or regress. At times, they are remarkably
indolent; at other times they grow rapidly and appear in showers. Spontane-
ous partial regression is very rare except in lymphoma and leukemia. Du Bois
(19) described an interesting case of carcinoma of the tongue which was ex-
 CUTANEOUS METASTASES OF MALIGNANT DISEASE 727
cised and the site treated with radium. This was followed by very marked
lingual and cervical edema. Three months after operation numerous small
nodules developed about the face which were diagnosed as papular syphilide.
Antiluetic treatment was of no benefit. The papules developed into tumors
of variable size symmetrically distributed over the face. They were oval,
red, painless, and not ulcerated. Numerous biopsies showed metastatic epi-
dermoid carcinoma. Six months after the appearance of the face tumors, the
first nodules disappeared spontaneously and new ones appeared. This was
repeated four months later. N o enlarged lymph nodes had appeared. Al-
though the patient's health failed, he was still alive at the time of the report.
Variations in growth do not necessarily correspond with similar changes in
the primary tumor. In terminal stages of the disease, rapid growth of the

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primary tumor may be reflected in the large number and rapid growth of the
skin tumors. These usually attain their maximum size early and then remain
stationary, although slow continuous growth is sometimes seen. Metastatic
carcinomas or sarcomas of the skin are usually of slower, more even growth
than the secondary skin tumors of the lymphon~asand leukemias.
Pain is almost unknown in connection with metastatic skin tumors.
Askanazy ( 3 ) , however, reports a case of carcinoma of the breast with wide-
spread skin metastases which were preceded by a definite painful sensation.
This made it possible for the patient to foretell accurately the location of the
tumor which attained its maximum size of approximately 1 cm. in twenty-four
hours. Biopsy showed small nerves completely surrounded by tumor.
The factors influencing the location and mode of spread of metastases to
the skin are variable and may be difficult to determine in a given case. A
great many tumor cells undoubtedly reach the skin through the blood stream.
Distant solitary skin metastases, such as those of the scalp seen in carcinoma
of the kidney, would be difficult to explain otherwise. Zoon's (69) case of
metastasis of a chorionepithelioma to the skin of toes and eyelid, which has
already been cited, is an excellent example of hematogenous spread. In this
case, metastases were established in the lung before they appeared in the skin.
Metastasis to the scalp in breast carcinoma could conceivably be due either
to retrograde lymphatic spread from carcinoma metastases in the cervical
or supraclavicular nodes, or to hematogenous spread. The vascularity and
comparative immobility of the scalp may also be contributing factors favoring
the localization of tumors in this region. One of the few cases in which there
is histologic evidence of the mode of spread is that of Askanazy (3) previously
cited, in which lymph emboli were definitely responsible for the skin tumors.
The fact that many of the metastases appear first in the general region
of a deep-seated primary tumor seems to suggest a local lymphatic spread.
Subsequent tumors involving all parts of the skin cannot be explained, how-
ever, on the basis of spread through dermal lymphatics. Local lymph node
involvement, producing outcropping skin nodules, must always be considered
as a source of distant skin metastases. But the most plausible route of mul-
tiple diffusely scattered skin metastasis is through the blood stream.
I n 40 of the 253 cases, excluding lymphoma and leukemia, definite inetas-
tases were localized in the skin before any lymph node or internal metastases
728 OLIVE GATES

were demonstrable. Sixteen of these were distant from the primary growth,
which in 8 cases was in the kidney and in 4 cases in the breast.
There are only 104 cases, all carcinomas, with sufficient information avail-
able from which to draw conclusions as to lymphatic or hematogenous dissem-
ination. Although one may be convinced of the probable mode of transmission
of tumor cells in a given case, generalizations may be misleading and are open
to criticism. The following figures must, therefore, be considered as merely
suggestive. In classifying the cases several factors were considered: the num-
ber of skin metastases in a given case, the location of the first skin metastasis
and other metastases, the time of occurrence before death and the autopsy
findings. In 72 of these cases the skin tumors are considered as probably due
to lymphatic spread as against 32 cases in which the distribution was ex-

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plained best by blood stream invasion by the primary tumor. Lymphatic
dissemination is seen chiefly in carcinomas of the breast (16 cases), stomach
(30 cases), uterus and ovary (10 cases). In 3 of the 9 melanoma cases the
location of the skin tumor suggested lymphatic spread. Hematogenous dis-
semination was seen mainly in carcinomas of the breast, uterus, ovary and
kidney. Widespread organ and usually lymph node involvement was present
in all but 9 of the autopsied cases in which metastases occurred as follows:
lung only, 5 cases; lung and lymph nodes 2 cases; lung and one other organ
2 cases. Six of the 9 cases had a solitary skin metastasis. There is no sup-
port for the supposition that there are tissues of predilection for metastases
of certain tumors. The chief organs involved in cases of carcinoma and sar-
coma with skin metastases were as follows: heart 12 times, lung 44, spleen 15,
liver 33, adrenal 22, bone 2 2 times. This clearly demonstrates the fact that
those tumors which produce extensive metastases in the internal organs are
those most likely to metastasize to the skin.

Metastases to the skin occur more often than has been supposed. In an
autopsy series of 2298 malignant tumors of various types 2.7 per cent had
metastases to the skin. Their importance lies in the fact that they are not un-
commonly the first evidence of the existence of malignancy and also of metas-
tasis. Contrary to current belief, metastases to the skin do not always herald
approaching death but may precede the terminal event by months or even
years. They are of limited value in prognosis since the behaviour of the skin
tumors does not necessarily indicate rate of growth of the primary tumor.

1. ABADIEA N D MONTPELLIER, J.: Bull. Assoc. franc. p. l'ktude du cancer 25: 25, 1936.
2. ARNDT:Zentralbl. f . Haut. u. Geschlechtskr. 10: 10, 1924, cited by Riehl.
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730 OLIVE GATES

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