Solitary Bony Metastasis as the First Sign of Malignant Gastric Tumor or

of Its Recurrence

RAJENDRA K. BIRLA, M.D.,* LEMUEL BOWDEN, M.D.t

Symptomatic solitary bony metastasis as the First sign of asymptomatic gastric carcinoma is very infrequent. Only 8 cases reported by 7 authors have been found in the literature. Furthermore, solitary bony metastasis as the sole sign of recurrence after hopefully curative resections are so rare that none has been previously reported in the literature. Three additional instances of solitary and histologically proven osseous metastasis of malignant gastric neoplasms have been observed and treated at Memorial Hospital during the years 1949 through 1969, and are herewith reported.

From the Memorial Sloan Kettering Cancer Center, New York, New York rence. Abstracts of these three patients' clinical course follows:

Case Reports

N o TISSUE OR ORGAN is exempt from blood-borne metastases of gastric carcinoma. James Ewing,10 in his monograph, Neoplastic Diseases: A Treatise on Tumors, states that miscellaneous sites of metastases of gastric carcinoma include brain, bones, kidney and ad-

renal, and spinal cord and membranes. Others including Willis,31 Anderson,2 McNeer and Pack'7 also emphasize the rarity of bony metastases from malignant gastric tumors even in advanced stages of the disease. For distant metastases as the first clinical sign of gastric carcinoma an incidence of 5.4% was reported by LaDue et al.15 in a series of 1112 patients. None however, presented as bony metastasis. During the 21 years, 1949 through 1969, three patients who were observed and treated at Memorial Hospital were found to have not only osseous metastasis of a malignant gastric tumor but a solitary osseous metastasis, presenting as the first sign of tumor or of its recur-

Submitted for publication April 2, 1975. *Former Fellow in Surgery, Memorial Sloan Kettering Cancer Center, New York, N.Y. tConsultant, Memorial Sloan Kettering Cancer Center, New York, N.Y. Reprint requests: Lemuel Bowden, M.D., 177 East 79 Street, New York, N.Y. 10021

45

Case 1: M. R., a 59-year-old woman, was admitted to Memorial Hospital on May 7, 1967. Four months prior to admission she had noted the onset of pain in the right groin following insignificant trauma. Roentgenographic studies revealed an osteolytic lesion in the right pubic bone. An incisional biopsy of this lesion elsewhere was interpreted as metastatic adenocarcinoma.

Thorough investigation in Memorial Hospital, including chest x-ray and thoracic tomograms, intravenous pyelogram, barium enema, G.I. series, mammography, liver scan and multiple urine and sputum cytologic analyses failed to reveal the primary site. The combined blastic and lytic lesion of the right pubic bone was again noted (Fig. 1) and was also identifiable by bone scan. Review of the biopsy material was interpreted: "Metastatic adenocarcinoma; favor lung as primary site; would then consider GI tract and breast in that order of preference" (Fig. 2). A non-specific stellate density, seen in the mammogram of the right breast, was biopsied and several other random biopsies of the breast were taken as well, but primary mammary carcinoma was not demonstrated. Radiation therapy, employing 250KV technique, was administered to the known lesion of the right pubic bone; and the patient was placed empirically on oral androgen therapy in the belief that an occult mammary carcinoma existed. The patient did well for two months. In August 1967 she first noticed some epigastric discomfort and anorexia. Repeat G.I. series performed in October 1967 revealed an extensive polypoid and ulcerating tumor of the body of the stomach. Gastric cytology revealed "several clusters of suspicious glandular cells." A repeat skeletal survey did not show any new osseous lesion. Surgical exploration of the abdomen on October 24, 1967 revealed an extensive carcinoma involving stomach,

46

BIRLA AND BOWDEN

Ann.

Surg. * July 1975

COMMENT: Solitary symptomatic bony metastasis as the first sign of gastric carcinoma. Case 2: W. D., a 72-year-old caucasian man, was admitted to Memorial Hospital on September 21, 1969 with a history of progressive dysphagia and a 10 pound weight loss. Roentegenographic studies prior to admission had revealed a partially obstructing lesion involving the distal 10cm of the esophagus. Physical examination was unremarkable. Esophagoscopy on September 29, 1969 revealed a granular obstructing lesion 37cm

FIG. 1. (M.R.) X-ray of pelvis: Combined blastic and lytic lesion of the superior ramus of the right pubic bone.

and adjacent lymph nodes, with metastases to both lobes of liver and to omentum. Suitable biopsies were subsequently reported as "Adenocarcinoma consistent with pancreato-biliary origin with stomach as next possibility." Radiation therapy employing 60Co technique was administered to the upper abdomen for a total dose of 4600r delivered in 5 weeks. The patient received little benefit from this therapy, her condition steadily deteriorated, and she died on June 7, 1968. pancreas,

from the upper alveolar arch and biopsy of this tissue was reported as adenocarcinoma. On September 30, 1969, through a thoraco-abdominal approach, resection of the distal half of esophagus, upper half of stomach, spleen, a portion of diaphragm and the greater omentum was performed. After a very stormy postoperative course the patient was discharged on 54th postoperative day. Pathological study of the resected specimen showed adenocarcinoma grade II with focal epidermoid metaplasia arising in stomach at the gastroesophageal junction. The patient did well for next 7 months. He then noticed a mass in the left hip with local pain and difficulty in locomotion. This mass measured 8 x 8 cm, was tender and fixed to the lateral aspect of the wing of the left ilium (Fig. 3). Aspiration biopsy of this mass was reported to show fragments of carcinoma similar to previously resected gastric tumor (Fig. 4). Subsequent chest roentgenograms disclosed multiple nodules in both lung fields, suggestive of metastatic disease. The patient developed dyspnoea rather abruptly and required tracheostomy. There was rapid progression of the lung lesions, the patient's condition worsened and he expired on July 5, 1970. At autopsy metastases involving both lungs, gastroduodenal and pulmonary hilar nodes were found. The liver and the rest of the skeleton were free of metastatic disease.

FIGS. 2 a and b (M.R.) (left) Incisional biopsy from the superior ramus of the right pubic bone showing metastatic adenocarcinoma (x230). (right) Primary gastric adenocarcinoma (x 230).

A :ellWE-

MALIGNANT GASTRIC TUMOR

Vol. 182- No. I

47

complicated by a left empyema which required thoracotomy with drainage and subsequent decortication. He was discharged improved on May 1, 1949. He was readmitted in August 1949 because of loss of weight

FIG. 3. (W.D.) Lytic lesion in the wing of the left ilium. Arrows deliniate the extent of the lesion.

COMMENT: Solitary symptomatic bony metastasis as the first sign of recurrence of gastric adenocarcinoma. Case 3: A. J., a 60-year-old man, first experienced melena in 1944. A diagnosis of gastric ulcer was made at another hospital and under dietary management he did well until 1948 when melena recurred. Exploratory lapratomy on June 10, 1948 revealed an "inoperable" carcinoma of the cardia of the stomach. Biopsy of this tumor however revealed a low-grade leiomyosarcoma. The patient was ultimately admitted to Memor-al Hospital and on March 21, 1949 underwent total gastrectomy, splenectomy and distal pancreatectomy through a thoracoabdominal approach. His postoperative course was stormy,

FIGS. 4 a and b (W.D.) (left) adenocarMetastatic cinoma (x 93): aspiration

,

w-

biopsy from the wing of the left ilium. (right) Primary

gastric adenocarcinoma

i

(x 140) previously resected.

!A Pg:

and anorexia. A mass was felt in the mid-abdomen. Resection of this mass, which involved multiple loops of small bowel, was carried out with suitable anastomosis. The resected specimen did not show tumor. Convalescence was complicated by development of fecal fistula and subsequent to this an acute myocardial infarction. While still hospitalized the patient inadvertently fell and sustained a fracture of the upper left femur (Fig. 5) which was treated in balanced traction suspension for 7 weeks. Aspiration biopsy of fracture site showed metastatic leiomyosarcoma, similar in histological picture to the gastric primary (Fig. 6). The patient's further course was downhill and he expired on January 27, 1950, 10 months after the initial resection. Autopsy revealed recurrent gastric leiomyosarcoma in the region of the tail of the pancreas with metastases to liver and lungs. Except for the pathological fracture site no other bony metastasis was found. COMMENT: Solitary bony metastasis presenting as a pathological fracture as the first sign of recurrence of gastric leiomyosarcoma.

Discussion

It has already been stated that osseous metastases from primary gastric neoplasms are uncommon, and it is probable that solitary osseous metastasis from this source is quite rare. Willis32 however states that it is probable that bony metastases from gastric carcinoma occur more often than is actually demonstrated by x-ray examination. He explains this as due to impracticality of total skeletal study at

necropsy.

McNeer and Pack18 be-

BIRLA AND BOWDEN

48

Ann Surg. * July 19 75

TABLE 1. Incidence of Osseous Metastasis in Gastric Carcinoma

Author & year

Jenkinson, 192312 Moore, 191919 Winiwarter, 193233 Copeland, 19317 Bertin, 19444 Lawton, 193816 FIG. 5. (A.J.) Pathological fracture Warwick, 192829 left upper femur. Kerr & Berger, 193513 Stein, 193913 Willis, 196031 Walther, 194828 Ackerman & Spjut, 1%21 Stout & Horn, 194324 Donn & McNeer, 1967w

Number of Cases

% of Metastasis

Comment*

00.00 00.00 00.00 1.30 1.33 2.02 2.20 2.40 2.65 5-10 7.00 11.00 11.20 17.50

0/1600 0/903 7/537 1/75 3/606 4/176 3/123 9/340 -

-/368 14/80

Autopsy Autopsy Autopsy Autopsy Autopsy **

Autopsy

*Clinical series except where otherwise stated **Clinical and autopsy material lieve that the incidence is

assiduity of from

directly proportional

search. The incidence of

osseous

gastric carcinoma,

to 17.5%

as variously reported varies from (Table 1). Higginbotham and Marcove1' from

the bone tumor

instances of

registry of Memorial Hospital found 1800 metastases in 6,842 patients re-

osseous

corded from 1931 to 1964, in which 191 had

pathological gastric carcinoma. gastric carcinoma hepatic metastases occur fre-

fractures, but In

to the

metastases

none

from

quently and early, pulmonary metastases seldom and late, and bony metastases very rarely. The development of skeletal metastases is believed to

occur as a

discon-

tinuous, hematogenous process. In abdominal cancer the

liver

the first filter to tumor emboli from the metastases once established may send tumor emboli to the second filter, the lungs. It is possible that the hepatic filter may be by-passed via the thoracic duct. However, once the pulmonary bed is serves as

primary site. Hepatic

A~FIGS.

6

a

and b (A.J.) (left)

Aspiration biopsy from left

upper

femur

showing

metastatic leiomyosarcoma

(x120). (right) Rep-

resentative section of pre-

_ viously resected gastric _ _ leiomyosarcoma (x120).

Vol. 182 No. I

MALIGNANT GASTRIC TUMOR

TABLE 2. Summary of Previously Reported Cases of Solitary Metastasis of Gastric Carcinoma

Author & Year 1. Tilling, 190825 2. Konjentzny, 193814 1938 3. Barclay, 19403 4. Bertin, 19444 5. Bockus, 19635 6. Catone & Henry, it

19698 7. Debernardi et al., 19698

Age & Sex

Bone involved

Histological Diagnosis

Humerus

Elderly, F Os calsis Elderly, M Humerus Left clavicle 34, M Left tibia 70, F Thirties, M Vertebra L4

Adenocarcinoma Adenocarcinoma Adenocarcinoma Adenocarcinoma Not mentioned

52, M

Left mandible Adenocarcinoma

55,M

Right mandible Adenocarcinoma

seeded there would seem to be limitless possibilities to the number and location of metastases via the systemic circulation. It is curious however that metastases from gastric carcinoma are found much less frequently in lungs and beyond, than are metastases from colon carcinoma. Schinz et al.22 stated that the tumor emboli of both adenocarcinoma and leiomyosarcoma are clumps of cells, rather than individual cells, and as such have a greater chance of being trapped in the first filter. A solitary skeletal metastasis can easily be mistaken for a primary bone tumor. Schinz et al.22 stated, "After age 40 every bone tumor must first be approached as a metastasis as long as contrary can't be proved." Walther," in a study of 2088 autopsies in patients with potentially metastasizing tumors, stated, "Bony metastases in the pelvic girdle almost exclusively present as part of generalized skeletal carcinomatosis; rarely as a bizarre solitary metastasis". Interestingly enough in two of our cases the solitary metastasis was in the pelvic girdle, one in the pubic bone and the other in the ilium. Crest of ilium is said to be a favorite site in this bone.20 The predilection of metastatic disease for the flat bones compared to long bones30 is said to be due to prevalence of red marrow. 21,26,27 Previously reported cases of solitary osseous metastasis are summarized in Table 2. Case 1 presents an example of symptomatic solitary bony metastasis as the first sign of gastric adenocarcinoma. Case 2 provides an example of solitary symptomatic bony metastasis as the first sign of recurrence of gastric adenocarcinoma. Case 3 is similar to Case 2 except that the primary lesion was a leiomyosarcoma.

References 1. Ackerman, L. V. and Spjut, H. J.: Atlas of Tumor Pathology; Tumors of Bone and Cartilage; Section II-Fascile 4, Washington, D.C., Armed Forces Institute of Pathology, 1962; pp. F4-262. 2. Anderson, W. A. D.: Pathology, Volume II, 6th Edition, St. Louis, The C. V. Mosby Company, 1971. 3. Barclay, I. B.: Two Unusual Gastro-intestinal Cases. Br. J.

Radiol., 13: 273-278, 1940. 4. Bertin, E. J.: Metastasis to Bone as the First Symptoms of Cancer

49

of Gastro-intestinal Tract; Report of Three Cases. Am. J. Roentgenol. Radium Ther. Nucl. Med., 51: 614-622, 1944. 5. Bockus, H. L.: Gastroenterology, Volume 1, 2nd. Ed., Philadelphia and London, W. R. Saunders Co., 1963; p. 758. 6. Catone, G. A. and Henny, F. A.: Metastatic Adenocarcinoma of Mandible: Report of a Case. J. Oral Surg., 27: 36-40, 1969. 7. Copeland, M. M.: Skeletal Metastases Arising from Carcinoma and from Sarcoma. Arch. Surg., 23: 581-654, 1931. 8. Debernardi, G., Roccia, L. and Guasta, G.: A Case of Precocious Mandibular Metastasis from Initially Silent Gastric Adenocarcinoma. Minerva Stomatol., 17: 679-685, 1968. 9. Donn, F. and McNeer, G.: Metastases of Gastric Carcinoma to Other Organs In: Neoplasms of Stomach, McNeer, G. & Pack, G. T. (eds.), Philadelphia & Toronto, J. B. Lippincott Company, 1967; p. 437. 10. Ewing, J.: Neoplastic Diseases, A Treatise on Tumors, Fourth Ed., Philadelphia and London, W. B. Saunders Company, 1940. 11. Higginbotham, N. L. and Marcove, R. C.: The Management of Pathological Fractures. J. Trauma, 5: 792, 1965. 12. Jenkinson, E. L.: Primary Carcinoma of Gastro-intestinal Tract Accompanied by Bone Metastases. Am. J. Roentgenol. Radium Ther. Nucl. Med., 11:411, 1923. 13. Kerr, H.D. and Berger, R. A.: Bone Metastases in Carcinoma of Stomach. Am. J. Cancer, 25:518, 1935. 14. Konjetzny, G. E.: Der Magenkrebs, Stuttgart, Ferdinand Enke Verlag, 1938. 15. LaDue, J.S., Murison, P.J., McNeer, G. and Pack, G. T.: Symptomatology and Diagnosis of Gastric Cancer. Arch. Surg., 60:305, 1950. 16. Lawton, S. E.: Bone Metastases from Carcinoma of Stomach. Surgery, 3:121, 1938. 17. McNeer, G. and Pack G. T.: Neoplasms of Stomach, Philadelphia and Toronto, J. B. Lippincott Company, 1967. 18. McNeer, G. and Pack, G. T.: Malignant Tumors of Stomach In: Treatment of Cancer and Allied Diseases, Volume V. 2nd Edition. Pack, G. T. and Ariei, I. M. (eds), Harper & Row, 1962; pp. 111-254. 19. Moore, A. B.: Roentgenologic Study of Metastatic Malignancy of the Bones. Am. J. Roentgenol., 6:589-593, 1919. 20. Patey, D. H.: Some Notes on Clinical Features and Distribution of Secondary Deposits in Bone Following Carcinoma of Breast. Brt. J. Surg., 15:182, 1927. 21. Piney, A.: Metastasis in Bone Marrow. J. Pathol., 25:140, 1922. 22. Schinz, H. R., Baensch, W. E., Friedl, E. and Uehlinger, E.: Roentgen-Diagnostics, Vol. II, New York, Grune & Stratton, 1952; pp. 977-1014. (First American Edition based on Fifth German Edition, translation arranged and edited by James T. Case, M.D., D.M.R.E.) 23. Stein, J. J.: Metastasis to Bone from Carcinoma of Gastro-intestinal Tract. Radiology, 35:486, 1940. 24. Stout, A. P.: Tumors of Stomach, Atlas of Tumor Pathology, Section VI/Fascile 21, Washington, D.C., Armed Forces Institute of Pathology, 1953. 25. Tilling, quoted by Martin In, Modern Medicine, Its Theory and Practice, William Osler, (ed.) Philadelphia, Lea Brothers & Company, 1908. 26. Turner, J.W. and Jaffe, H.L.: Metastatic Neoplasms, Am. J. Roentgenol. Radium Ther. Nucl. Med., 43:479, 1940. 27. von Recklinghausen, quoted by Willis, R. A. In: The Spread of Tumours in the Human Body, 2nd. Edition, London, Butterworth, 1952; p. 239. 28. Walther, H. E.: Krebmetasten. Basel, Benno Swabe, 1948. 29. Warwick, M.: Analysis of 176 Cases of Carcinoma of Stomach Submitted to Autopsy. Ann. Surg., 88:216, 1928. 30. Welch, C. E.: Pathological Fractures Due to Malignant Disease. Surg. Gynecol. Obstet., 62:735, 1936. 31. Willis R. A.: Pathology of Tumors, London, Butterworth, 1960. 32. Willis, R. A.: The Spread of Tumors in the Human Body, 2nd. Edition, London, Butterworth, 1952. 33. Winiwarter, quoted by Kerr & Berger In: Bone Metastasis in Carcinoma of Stomach. Am. J. Cancer, 25:518, 1935.

Solitary bony metastasis as the first sign of malignant gastric tumor or of its recurrence.

Symptomatic solitary bony metastasis as the First sign of asymptomatic gastric carcinoma is very infrequent. Only 8 cases reported by 7 authors have b...
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