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METASTATIC TUMOR OF BONE IN ATIAHUANACO FEMALE*

MARVIN J. ALLISON, Ph.D., and ENRIQUE GERSZTEN, M.D.Department of Pathology, Medical College of Virginia

Health Sciences DivisionVirginia Commonwealth University

Richmond, VirginiaJUAN MUNIZAGA, Ph.D.

Departamento de Ciencias Antropologicas y ArquelogicasUniversidad de Chile

Santiago, ChileCALOGERO SANTORO, Ph.D.

Departamento de AntropologiaUniversidad del Norte

Arica, Chile

MsETASTATIC carcinoma is the most common malignant tumor seen inbone. By definition, it arises from detached fragments of a tumor

transported from a primary site, commonly through the lymphatics or bloodvessels, and must be differentiated from contiguous spread from the primarygrowth. The usual site of initiation of these metastatic tumors is the bonemarrow, although they may occur also in the periosteum and are locatedchiefly where the main foramina traverse cortical bone.

Table I lists the 15 most common sites of metastatic involvement in 1,000consecutively autopsied cases of carcinoma from Montefiore Hospital inNew York for the years 1943-1947. In this series metastasis to bone isseventh in frequency and the 27% figure rather a conservative estimate. Thisfrequency will depend on the types of tumor and the care exercised by thepathologist in studying the skeleton at autopsy.

Six cases of metastatic tumor in the paleopathology literature of the Ameri-cas were reviewed by Steinbock,1 and an additional study on malignantmelanoma was reported by Urteaga and Pack.2

MATERIALS AND METHODSA 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. J. ALLISON AND OTHERS

TABLE I. FIFTEEN MOST COMMON SITES OF METASTATIC INVOLVEMENTIN 1,000 CONSECUTIVE AUTOPSIED CASES OF CARCINOMA2

Sites %

1. Abdominal nodes 49.52. Liver 49.43. Lungs 46.54. Mediastinal nodes 42.15. Pleura 27.76. Brain 27.47. Bone 27.28. Adrenal 27.09. Peritoneum 26.9

10. Gastrointestinal tract 20.411. Diaphragm 18.312. Pericardium 13.113. Kidney 12.614. Pancreas 11.615. Ovary 11.1

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

RESULTS

The mummy bundle was accompanied by the following offerings: onewooden spoon, one gourd container, one metal working crucible, two plainwool shirts, one wool shirt with embroidered designs, feathers, a largeamount of corn on the cob with husks. The artifacts present were of a typeassociated with the Tiahuanaco culture, dating around 750 A.D.

The mummy bundle was unwrapped and contained the complete skeletonand hair of a woman estimated to be 45 years old, based on remodeling of thepelvic symphysis. Her hair was black, braided in a single long braid down theback, 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 molarand right first premolar). Nine bones had gross evidence of disease: the skull,the right and left innominate bones, the right femur, sacrum, the eighththoracic vertebra, the fourth and fifth lumbar vertebrae, and the sternum.

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Fig. 1. The three principle cranial lesions may be seen here. The central lytic lesion haspunched-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 largestwas a lytic lesion that began in the diploe and perforated the inner and outertables equally, leaving a ragged opening 35 x 30 mm. To the right of thisopening was a nonperforating lesion 17 x 16 mm. and to the left a smallernonperforating lesion 15 x 15 mm. The nonperforating lesions were ob-served as a roughening and incipient crumbling of the outer table (Figure 1).Radiographically, these were considered sclerotic lesions (Figure 2). A thirdnonperforating lesion about 10 x 10mm. was present in the central portion ofthe occipital bone.

Both innominate bones were extensively attacked by disease, although thatseen in the right was more severe than the left. There was a large lytic lesionof the right ischium that destroyed most of the bone below the obturatorforamen almost to the acetabulum, and a second lytic lesion in the pubic bonebetween the obturator foramen and the symphysis pubis. A third large lesionwas noted at the sacroiliac joint. The left innominate bone had a small lyticlesion below the obturator foramen near the pubisischium junction and a

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583TUMOR OF BONE

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 sacrumhad a large lytic lesion on the right involving the articular surface with theright hip bone. The lesions may be seen in Figure 3.

The right femur had a lytic lesion at the proximal end which involved theneck but left the articular surface of the head intact. The right femur measured370 mm. in length in contrast to the normal left femur that measured 400mm.; thus there was a 30 mm. loss ofbone due to the lesion. There were threelesions of the vertebrae. The entire eighth thoracic vertebral body was de-stroyed. The fourth and fifth lumbar vertebrae each had a small incipientlesion in the body. The sternum had a small lytic lesion at the level of costalnotch II.

In the case under study, it will never be possible precisely to identifythe site of the primary. Nevertheless, on the basis of present day knowl-edge of tumors, some good probabilities can be offered.

The frequency of modern cancer deaths in the female is seen in TableII. On the basis of this table, the first consideration should be carcinomaof the breast because it is the most common female malignant tumor and

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Fig. 3. The extent of the lesions in the two innominated bones and the sacrum may beappreciated in this illustration. The nature of our material is such that postmortem damageis 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, breastcarcinoma is also the most common tumor from the age of 15 to 74.4 Thefrequency of bones involved in metastatic breast carcinoma is first pelvis,followed by vertebrae, proximal femur, ribs, and skull.5 The radiologicalpicture of this tumor in bone tends to show mixed sclerotic lesions similarto the present case.

Renal carcinoma produces a similar radiological picture but is consider-ably less common in women, tends to occur later in life, and the mostcommon sites of bone metastases are, first, humerus followed by verte-brae, femur, pelvis, ribs, and skull.6Tumors of the colon, rectum, and ovary are common in women, and do

occur below 50 years of age in significant numbers, but have a lowfrequency of metastasis to bone. Radiologically, these metastases areusually not sclerotic. Tumors of the lung are associated with death inwomen about half as frequently as tumors of the breast and produce abouthalf 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 Bone metastasis %

Breast 32,800 73.12Colon and rectum 20,900 9.3-12.62Lung 18,600 32.52Uterus 11,000Ovary 10,800 9.02Pancreas 8,700 15.62Stomach 5,900 10.92Urinary organs 5,500 24.02

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

alternative along with a number of others not discussed here. It isobviously difficult to locate the primary site in some cases of metastaticcarcinoma even today. One that may be identified with certainty ismalignant melanoma such as that described by Urteaga and Pack,2 buteven this depends upon the production of melanin pigment.

The other problem facing modern investigators in interpreting data isthat no one can be sure which tumors were common 1,000 years ago. It isonly necessary to go back about 45 years to see uterocervical carcinoma asa leading cause of death in women whereas today it is in fourth placeamong tumors, and a recent study shows cancer of the lung in women tobe the second most common type and rapidly approaching carcinoma ofthe breast in frequency.7 In men, carcinoma of the lung went from fourper 100,000 to more than 50 in the same time span. Hopefully, continuedstudy of mummies, particularly those with surviving soft tissue, mighthelp to resolve some of these problems in the epidemiology of tumors.

DISCUSSIONSix cases of possible metastatic carcinoma were reviewed by Steinbock.

These were two Pueblo Indians, two Peruvians, and two Eskimos-allincomplete skeletons, and in two cases only the skull was available.

This paucity of tumors reported in the paleopathology literature is surpris-ing in view of the large numbers of skeletons that have been studied during thelast 100 or so odd years. This is perhaps due to two causes: The custom of ar-cheologists and anthropologists for many years of concentrating on the cra-

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nium and ignoring the postcranial bones, and the fact that most early peopledied younger than 40, before tumors could become fully developed. Thislatter point is underlined by reviewing figures for carcinoma of the breast in amodem population. Under the age of 49 the number of cases would be only48.5/100,000 in the population at risk, while over the age of 49 there are366.4 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 becausedifferent tumors metastasize at different frequencies; breast and prostate, forexample, yield bone lesions in more than 70% of the cases,3 whereascarcinoma of the uterus varies greatly, depending upon whether its origin iscervical or endometrial, the former metastasizing in nearly 40%o to distantsites whereas the latter is commonly limited to lymphatic drainage areas orlocal direct extension.8 A third factor to consider is the different geographicdistribution of tumors among the world's population today, differences prob-ably present also in earlier times. Modern epidemiological data must also beused with caution because new diagnostic methods and treatment constantlyalter tumor frequencies and disease distribution.

REFERENCES

1. Steinbock, R. T.: Paleopathological Di-agnosis and Interpretation. Springfield,I1., Thomas, 1976, pp. 316-97.

2. Urteaga, O. B. and Pack, G. T.: On theantiquity of melanoma. Cancer 19:607-10, 1966.

3. Abrams, H. L., Spiro, R., and Gold-stein, N.: Metastases in carcinoma.Cancer 3:74-85, 1950.

4. Silverberg, E.: Cancer statistics. CA27:26-41, 1977.

5. Lenz, M. and Freid, J. R.: Metastases tothe skeleton, brain and spinal cord from

cancer of the breast and the effects ofradiotherapy. Ann. Surg. 93:278-93,1931.

6. Copeland, M. M.: Skeletal metastaspsarising from carcinoma and from sarco-ma. Arch. Surg. 23:581-654, 1931.

7. Silverberg, E.: Cancer statistics. CA30:23-38, 1980.

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

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