581

METASTATIC TUMOR OF BONE IN A

TIAHUANACO FEMALE*
MARVIN J. ALLISON, Ph.D., and ENRIQUE GERSZTEN, M.D.
Department of Pathology, Medical College of Virginia
Health Sciences Division
Virginia Commonwealth University
Richmond, Virginia

JUAN MUNIZAGA, Ph.D.

Departamento de Ciencias Antropologicas y Arquelogicas
Universidad de Chile
Santiago, Chile

CALOGERO SANTORO, Ph.D.

Departamento de Antropologia
Universidad del Norte
Arica, Chile

MsETASTATIC carcinoma is the most common malignant tumor seen in

bone. By definition, it arises from detached fragments of a tumor
transported from a primary site, commonly through the lymphatics or blood
vessels, and must be differentiated from contiguous spread from the primary
growth. The usual site of initiation of these metastatic tumors is the bone
marrow, although they may occur also in the periosteum and are located
chiefly where the main foramina traverse cortical bone.
Table I lists the 15 most common sites of metastatic involvement in 1,000
consecutively autopsied cases of carcinoma from Montefiore Hospital in
New York for the years 1943-1947. In this series metastasis to bone is
seventh in frequency and the 27% figure rather a conservative estimate. This
frequency will depend on the types of tumor and the care exercised by the
pathologist in studying the skeleton at autopsy.
Six cases of metastatic tumor in the paleopathology literature of the Americas were reviewed by Steinbock,1 and an additional study on malignant
melanoma was reported by Urteaga and Pack.2
MATERIALS AND METHODS
A mummy bundle containing the skeleton of a female was excavated from
*This study was supported by the National Geographic Society.

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M.

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OTHERS

TABLE I. FIFTEEN MOST COMMON SITES OF METASTATIC INVOLVEMENT

IN 1,000 CONSECUTIVE AUTOPSIED CASES OF CARCINOMA2

Sites
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.

Abdominal nodes

49.5
49.4
46.5
42.1
27.7
27.4
27.2
27.0
26.9
20.4
18.3
13.1
12.6
11.6
11.1

Liver
Lungs

Mediastinal nodes
Pleura
Brain
Bone
Adrenal
Peritoneum
Gastrointestinal tract
Diaphragm
Pericardium
Kidney
Pancreas
Ovary

the cemetery site AZ71 located in San Miguel de Azapa near Arica, Chile, in
August 1978. The mummy bundle was dated archeologically on the basis of
the artifacts as about the 8th century A. D. Gross and radiographic examination of the skeleton was performed.
RESULTS

The mummy bundle was accompanied by the following offerings: one

wooden spoon, one gourd container, one metal working crucible, two plain
wool shirts, one wool shirt with embroidered designs, feathers, a large
amount of corn on the cob with husks. The artifacts present were of a type
associated with the Tiahuanaco culture, dating around 750 A.D.
The mummy bundle was unwrapped and contained the complete skeleton
and hair of a woman estimated to be 45 years old, based on remodeling of the
pelvic symphysis. Her hair was black, braided in a single long braid down the
back, 30 inches long and tied with a green cord.
A review of the complete skeleton showed that the teeth were worn but had
no cavities. Two teeth had been lost during life in the maxilla (left first molar
and right first premolar). Nine bones had gross evidence of disease: the skull,
the right and left innominate bones, the right femur, sacrum, the eighth
thoracic vertebra, the fourth and fifth lumbar vertebrae, and the sternum.
Bull. N.Y. Acad. Med.

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Fig. 1. The three principle cranial lesions may be seen here. The central lytic lesion has
punched-out openings in the inner and outer table. Two nonperforating lesions may be
noted at either side.

The parietal bones had three lesions near the sagittal suture. The largest
was a lytic lesion that began in the diploe and perforated the inner and outer
tables equally, leaving a ragged opening 35 x 30 mm. To the right of this
opening was a nonperforating lesion 17 x 16 mm. and to the left a smaller
nonperforating lesion 15 x 15 mm. The nonperforating lesions were observed as a roughening and incipient crumbling of the outer table (Figure 1).
Radiographically, these were considered sclerotic lesions (Figure 2). A third
nonperforating lesion about 10 x 10mm. was present in the central portion of
the occipital bone.
Both innominate bones were extensively attacked by disease, although that
seen in the right was more severe than the left. There was a large lytic lesion
of the right ischium that destroyed most of the bone below the obturator
foramen almost to the acetabulum, and a second lytic lesion in the pubic bone
between the obturator foramen and the symphysis pubis. A third large lesion
was noted at the sacroiliac joint. The left innominate bone had a small lytic
lesion below the obturator foramen near the pubisischium junction and a
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Fig. 2. The radiograph of the above lesions shows their sclerotic nature.

lesion in the ilium in the area of the posterior superior iliac spine. The sacrum
had a large lytic lesion on the right involving the articular surface with the
right hip bone. The lesions may be seen in Figure 3.
The right femur had a lytic lesion at the proximal end which involved the
neck but left the articular surface of the head intact. The right femur measured
370 mm. in length in contrast to the normal left femur that measured 400
mm.; thus there was a 30 mm. loss of bone due to the lesion. There were three
lesions of the vertebrae. The entire eighth thoracic vertebral body was destroyed. The fourth and fifth lumbar vertebrae each had a small incipient
lesion in the body. The sternum had a small lytic lesion at the level of costal
notch II.
In the case under study, it will never be possible precisely to identify
the site of the primary. Nevertheless, on the basis of present day knowledge of tumors, some good probabilities can be offered.
The frequency of modern cancer deaths in the female is seen in Table
II. On the basis of this table, the first consideration should be carcinoma
of the breast because it is the most common female malignant tumor and
Bull. N.Y. Acad. Mod.

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Fig. 3. The extent of the lesions in the two innominated bones and the sacrum may be
appreciated in this illustration. The nature of our material is such that postmortem damage
is easily recognizable due to fragments of bone found in mummy wrappings. All changes in
bone seen in this individual are antemortem.

produces bone metastasis in nearly 75% of the cases.3 In women, breast

carcinoma is also the most common tumor from the age of 15 to 74.4 The
frequency of bones involved in metastatic breast carcinoma is first pelvis,
followed by vertebrae, proximal femur, ribs, and skull.5 The radiological
picture of this tumor in bone tends to show mixed sclerotic lesions similar
to the present case.
Renal carcinoma produces a similar radiological picture but is considerably less common in women, tends to occur later in life, and the most
common sites of bone metastases are, first, humerus followed by vertebrae, femur, pelvis, ribs, and skull.6
Tumors of the colon, rectum, and ovary are common in women, and do
occur below 50 years of age in significant numbers, but have a low
frequency of metastasis to bone. Radiologically, these metastases are
usually not sclerotic. Tumors of the lung are associated with death in
women about half as frequently as tumors of the breast and produce about
half the number of bone lesions. This must be considered a possible
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TABLE II. ESTIMATED CANCER DEATHS IN THE FEMALE 1976

Primary site

Number

Breast
Colon and rectum
Lung
Uterus
Ovary
Pancreas
Stomach
Urinary organs

32,800
20,900
18,600
11,000
10,800
8,700
5,900
5,500

Bone metastasis %
73.12

9.3-12.62
32.52
9.02
15.62
10.92
24.02

Modified from Anderson and Kissane: Pathology, Chapter 17, Neoplasia, Table 17-18 p. 686, seventh
edition. St. Louis, Mosby, 1977.

alternative along with a number of others not discussed here. It is

obviously difficult to locate the primary site in some cases of metastatic
carcinoma even today. One that may be identified with certainty is
malignant melanoma such as that described by Urteaga and Pack,2 but
even this depends upon the production of melanin pigment.
The other problem facing modern investigators in interpreting data is
that no one can be sure which tumors were common 1,000 years ago. It is
only necessary to go back about 45 years to see uterocervical carcinoma as
a leading cause of death in women whereas today it is in fourth place
among tumors, and a recent study shows cancer of the lung in women to
be the second most common type and rapidly approaching carcinoma of
the breast in frequency.7 In men, carcinoma of the lung went from four
per 100,000 to more than 50 in the same time span. Hopefully, continued
study of mummies, particularly those with surviving soft tissue, might
help to resolve some of these problems in the epidemiology of tumors.
DISCUSSION
Six cases of possible metastatic carcinoma were reviewed by Steinbock.
These were two Pueblo Indians, two Peruvians, and two Eskimos-all
incomplete skeletons, and in two cases only the skull was available.
This paucity of tumors reported in the paleopathology literature is surprising in view of the large numbers of skeletons that have been studied during the
last 100 or so odd years. This is perhaps due to two causes: The custom of archeologists and anthropologists for many years of concentrating on the craBull. N.Y. Acad. Med.

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nium and ignoring the postcranial bones, and the fact that most early people
died younger than 40, before tumors could become fully developed. This
latter point is underlined by reviewing figures for carcinoma of the breast in a
modem population. Under the age of 49 the number of cases would be only
48.5/100,000 in the population at risk, while over the age of 49 there are
366.4 About sevenfold more cases occur in a population over 50 years of age.
This is further emphasized when one has only a skeleton to study because
different tumors metastasize at different frequencies; breast and prostate, for
example, yield bone lesions in more than 70% of the cases,3 whereas
carcinoma of the uterus varies greatly, depending upon whether its origin is
cervical or endometrial, the former metastasizing in nearly 40%o to distant
sites whereas the latter is commonly limited to lymphatic drainage areas or
local direct extension.8 A third factor to consider is the different geographic
distribution of tumors among the world's population today, differences probably present also in earlier times. Modern epidemiological data must also be
used with caution because new diagnostic methods and treatment constantly
alter tumor frequencies and disease distribution.
REFERENCES
1. Steinbock, R. T.: Paleopathological Diagnosis and Interpretation. Springfield,
I1., Thomas, 1976, pp. 316-97.
2. Urteaga, O. B. and Pack, G. T.: On the
antiquity of melanoma. Cancer 19:60710, 1966.
3. Abrams, H. L., Spiro, R., and Goldstein, N.: Metastases in carcinoma.
Cancer 3:74-85, 1950.
4. Silverberg, E.: Cancer statistics. CA
27:26-41, 1977.
5. Lenz, M. and Freid, J. R.: Metastases to
the skeleton, brain and spinal cord from

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cancer of the breast and the effects of

radiotherapy. Ann. Surg. 93:278-93,
1931.
6. Copeland, M. M.: Skeletal metastasps
arising from carcinoma and from sarcoma. Arch. Surg. 23:581-654, 1931.
7. Silverberg, E.: Cancer statistics. CA

30:23-38, 1980.
8. Novak, E. R. and Woodruff, J. D.:
Gynecologic and Obstetric Pathology.
Philadelphia, Saunders, 1974, 7th ed.,
Chapters 5, 9.