Mechanisms of Cancer Invasion and Metastasis

  • Isaiah J. Fidler
Part of the Cancer book series (C, volume 4)


The spread of cancer cells from a primary site to a distant organ is called metastasis. It is one of the most intriguing phases in the pathogenesis of the disease; indeed, cancer metastasis is responsible for most therapeutic failures, as patients succumb to the multiple tumor growths. It would seem that, short of the complete prevention of cancer, the most urgent goal of oncologists should be the arrest and/or prevention of such tumor spread. In this regard, it is remarkable that current theories of the mechanisms responsible for cancer metastasis are fragmented and controversial. The following discussion is not intended to be totally inclusive or an exhaustive review of the literature. The prime intent is to summarize and consolidate early findings, hypotheses, and suggestions, and to describe some recent experiments. It is hoped that this presentation will promote further collaborative efforts to clarify and elucidate the mechanisms responsible for the pathogenesis of metastasis.


Lymph Node Tumor Cell Pulmonary Metastasis Circulate Tumor Cell Lymphatic System 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aaronson, S. A., and Todaro, G. J., 1968, Basis for the acquisition of malignant potential by mouse cells cultivated in vitro, Science 162:1024.PubMedCrossRefGoogle Scholar
  2. Abercrombie, M., and Ambrose, E. J., 1962, The surface properties of cancer cells: A review, Cancer Res. 22:525.PubMedGoogle Scholar
  3. Abercrombie, M., and Heaysman, J. E. M., 1954, Observations on the social behavior of cells in tissue culture. II. “Monolayering” of fibroblasts, Exp. Cell Res. 6:293.PubMedCrossRefGoogle Scholar
  4. Agosin, M., Christen, R., Badinez, Q., Gasic, G., Neghme, A., Pizarro, O., and Jarpa, A., 1952, Cortisone induced metastases of adenocarcinoma in mice, Proc. Soc. Exp. Biol. Med. 80:128.PubMedGoogle Scholar
  5. Agostino, D., and Cliffton, E. E., 1965, Organ localization and effect of trauma on the fate of circulating cancer cells, Cancer Res. 25:1728.PubMedGoogle Scholar
  6. Albert, D., and Zeidman, I., 1962, Relation of glucocorticoid activity of steroids to number of metastases, Cancer Res. 22:1297.PubMedGoogle Scholar
  7. Alexander, P., Evans, R., and Grant, C. K., 1972, The interplay of lymphoid cells and macrophages in tumor immunity, Ann. Inst. Pasteur 122:645.Google Scholar
  8. Ambrose, E. J., 1967, Biochemical and biophysical properties of cell membranes, in: Candian Cancer Conference: Proceedings of the Seventh Canadian Cancer Research Conference, Toronto, p. 247, Academic Press, New York.Google Scholar
  9. American Medical Association, 1951, Meeting of the Subcommittee on Steroids and Cancer, J. Am. Med. Assoc. 146:655.Google Scholar
  10. Arena, V., 1971, Ionizing Irradiation and Life, Mosby, St. Louis.Google Scholar
  11. Ballard, P. L., and Tomkins, G. M., 1970, Glucocorticoid induced alterations of the surface membrane of cultured hepatoma cells, J. Cell. Biol. 47:222.PubMedCrossRefGoogle Scholar
  12. Baserga, R., and Shubik, P., 1955, Action of cortisone on disseminated tumor cells after removal of the primary growth, Science 121:100.PubMedCrossRefGoogle Scholar
  13. Baserga, R., Kisieleski, W. E., and Halversen, K., 1960, A study on the establishment and growth of tumor metastases with tritiated thymidine, Cancer Res. 20:910.PubMedGoogle Scholar
  14. Batzdorf, U., 1973, Metastasis of primary central nervous system tumors including tissue culture studies, in: Chemotherapy of Cancer Dissemination and Metastasis (S. Garattini and G. Franchi, eds.), pp. 205–211, Raven Press, New York.Google Scholar
  15. Berg, J. W., Huvos, A. G., Axtell, L. M., and Robbins, G. Y., 1973, A new sign of favorable prognosis in mammary cancer: Hyperplastic reactive lymph nodes in the apex of the axilla, Ann. Surg. 177:8.PubMedCrossRefGoogle Scholar
  16. Berwick, L., and Coman, D. R., 1962, Some chemical factors in cellular adhesion and stickiness, Cancer Res. 22:982.Google Scholar
  17. Billingham, R. E., Brent, L., and Medawar, P. B., 1956, Quantitative studies on tissue transplantation immunity, Philos. Trans. R. Soc. London Ser. B 239:357.CrossRefGoogle Scholar
  18. Borberg, H., Oettgen, H. F., Choudry, K., and Beattie, E. J., Jr., 1972, Inhibition of established transplants of chemically induced sarcomas in syngeneic mice by lymphocytes from immunized donors, Int. J. Cancer 10:539.PubMedCrossRefGoogle Scholar
  19. Bosmann, H. B., Bieber, G. F., Brown, A. E., Case, K. R., Gersten, D. M., Kimmerer, T. W., and Lione, A., 1973, Biochemical parameters correlated with tumor cell implantation, Nature (London) 246:487.CrossRefGoogle Scholar
  20. Carnaud, C., Hoch, B., and Trainin, N., 1974, Influence of immunologic competence of the host on metastasis induced by the 3LL Lewis tumor in mice, J. Natl. Cancer Inst. 52:395.PubMedGoogle Scholar
  21. Cliffton, E. E., and Grossi, C. E., 1974, The rationaleof anticoagulants in the treatment of cancer, J. Med. 5:107.PubMedGoogle Scholar
  22. Coman, D. R., 1944, Decreased mutual adhesiveness, a property of cells from squamous cell carcinomas, Cancer Res. 4:625.Google Scholar
  23. Coman, D. R., 1953, Mechanisms responsible for the origin and distribution of blood-borne tumor metastases: A review, Cancer Res. 13:397.PubMedGoogle Scholar
  24. Coman, D. R., 1954, Cellular adhesiveness in relation to the invasiveness of cancer: Electron microscopy of liver perfused with a chelating agent, Cancer Res. 14:519.PubMedGoogle Scholar
  25. Coman, D. R., 1961, Adhesiveness and stickiness: Two independent properties of the cell surface, Cancer Res. 21:1436.PubMedGoogle Scholar
  26. Coman, D. R., Delong, R. P., and Mccutcheon, M., 1951, Studies on the mechanism of metastasis: The distribution of tumors in various organs in relation to the distribution of arterial emboli, Cancer Res. 11:648.PubMedGoogle Scholar
  27. Crile, G., 1969, Possible role of uninvolved regional nodes in preventing metastasis from breast cancer, Cancer 24:1283.PubMedCrossRefGoogle Scholar
  28. Curtis, A. S. G., and Buultjens, T. E. J., 1973, Cell adhesion and locomotion, in: Locomotion of Tissue Cells, Ciba Foundation Symposium 14, pp. 171–180, Associated Scientific Publishers, Amsterdam.Google Scholar
  29. Daniel, M. R., 1970, Diffusible factors from malignant cells which affect epidermal survival and differentiation, Br. J. Cancer 54:712.CrossRefGoogle Scholar
  30. Dao, T. L., and Yogo, H., 1967, Enhancement of pulmonary metastasis by x-irradiation in rats bearing mammary cancer, Cancer 20:2020.PubMedCrossRefGoogle Scholar
  31. David, J. R., 1971, Migration inhibitory factor and mediators of cellular hypersensitivity in vitro, in: Progress in Immunology (B. Amos, ed.), pp. 400–412, Academic Press, New York.Google Scholar
  32. Delong, R. P., and Coman, D. R., 1950, Relative susceptibility of various organs to tumor transplantation, Cancer Res. 10:513.PubMedGoogle Scholar
  33. Delong, R. P., Coman, D. R., and Zeidman, I., 1950, The significance of low calcium and high potassium content in neoplastic tissue, Cancer 3:718.PubMedCrossRefGoogle Scholar
  34. Dorsey, J. K., and Roth, S., 1973, Adhesive specificity in normal and transformed mouse fibroblasts, Dev. Biol. 33:249.PubMedCrossRefGoogle Scholar
  35. Duff, R., Doller, E., and Rapp, F., 1973, Immunologic manipulation of metastases due to herpesvirus transformed cells, Science 180:79.PubMedCrossRefGoogle Scholar
  36. Easty, D. M., and Easty, G. C., 1974, Measurement of the ability of cells to infiltrate normal tissue in vitro, Br. J. Cancer 29:36.PubMedCrossRefGoogle Scholar
  37. Easty, G. C., and Easty, D. M., 1973, In vitro systems for the study of tumor infiltration, in: Chemotherapy of Cancer Dissemination and Metastasis (S. Garattini and G. Franchi, eds.), pp. 45–51, Raven Press, New York.Google Scholar
  38. Eaves, G., 1973, The invasive growth of malignant tumors as a purely mechanical process, J. Pathol. 109:233.PubMedCrossRefGoogle Scholar
  39. Engeset, A., 1959, Lymphaticovenous communications in the albino rat, J. Anat. 93:380.PubMedGoogle Scholar
  40. Evans, R., and Alexander, P., 1970, Cooperation of immune lymphoid cells with macrophages in tumor immunity, Nature (London) 228:620.CrossRefGoogle Scholar
  41. Fidler, I. J., 1970, Metastasis: Quantitative analysis of distribution and fate of tumor emboli labeled with 125I-5-iodo-2′-deoxyuridine, J. Natl. Cancer Inst. 45:775.Google Scholar
  42. Fidler, I. J., 1973a, The relationship of embolic homogeneity, number, size and viability to the incidence of experimental metastasis, Eur. J. Cancer 9:223.PubMedGoogle Scholar
  43. Fidler, I. J., 1973b, Selection of successive tumor lines for metastasis, Nature New Biol. 242:148.PubMedGoogle Scholar
  44. Fidler, I. J., 1974a, Immune stimulation-inhibition of experimental cancer metastasis, Cancer Res. 34:491.PubMedGoogle Scholar
  45. Fidler, I. J., 1974b, Inhibition of pulmonary metastasis by intravenous injection of specifically activated macrophages, Cancer Res. 34:1074.PubMedGoogle Scholar
  46. Fidler, I. J., and Lieber, S., 1972, Quantitative analysis of the mechanism of glucocorticoid enhancement of experimental metastasis, Res. Commun. Chem. Pathol. Pharmacol. 4:607.PubMedGoogle Scholar
  47. Fidler, I. J., and Zeidman, I., 1972, Enhancement of experimental metastasis by x-ray: A possible mechanism, J. Med. 3:172.PubMedGoogle Scholar
  48. Fidler, I. J., Mcwilliams, R. W., and Beck-Nielsen, S., 1974, Immune reactivity of lymphocytes obtained from original lymph node, distant lymph node, and peripheral blood to autochthonous neoplasms of the dog, Immunolog. Comm., in press, 1975.Google Scholar
  49. Fisher, B., and Fisher, E. R., 1965, Transmigration of lymph nodes by tumor cells, Science 152:1397.CrossRefGoogle Scholar
  50. Fisher, B., and Fisher, E. R., 1966, The interrelationship of hematogenous and lymphatic tumor cell dissemination, Surg. Gynecol. Obst. 122:791.Google Scholar
  51. Fisher, B., and Fisher, E. R., 1967a, The organ distribution of disseminated 51Cr-labeled tumor cells, Cancer Res. 27:9412.Google Scholar
  52. Fisher, B., and Fisher, E. R., 1967b, Barrier function of lymph node to tumor cells and erythrocytes. I. Normal nodes, Cancer 20:1907.PubMedCrossRefGoogle Scholar
  53. Fisher, E. R., and Fisher, B., 1967c, Recent observations on the concept of metastasis, Arch. Pathol. 83:321.PubMedGoogle Scholar
  54. Fisher, B., Fisher, E. R., and Feduska, N., 1967, Trauma and the localization of tumor cells, Cancer 20:23.PubMedCrossRefGoogle Scholar
  55. Fisher, B., Saffer, E. A., and Fisher, E. R., 1972, Experience with lymphocyte immunotherapy in experimental tumor systems, Cancer 27:771.CrossRefGoogle Scholar
  56. Fisher, B., Saffer, E. A., and Fisher, E. R., 1974, Studies concerning the regional lymph node in cancer. IV. Tumor inhibition by regional lymph node cells, Cancer 33:631.PubMedCrossRefGoogle Scholar
  57. Franks, L. M., 1973, Structure and biological malignancy of tumors, in: Chemotherapy of Cancer Dissemination and Metastasis (S. Garattin and G. Franchi, eds.), pp. 71–78, Raven Press, New York.Google Scholar
  58. Gasic, G. J., and Gasic, T. B., 1962, Removal of sialic acid from the cell coat in tumor cells and vascular endothelium and its effects on metastasis, Proc. Natl. Acad. Sci. U.S.A. 48:1172.PubMedCrossRefGoogle Scholar
  59. Gasic, G. J., Gasic, T. B., and Stewart, C. C., 1968, Antimetastatic effects associated with platelet reduction, Proc. Natl. Acad. Sci. U.S.A. 61:46.PubMedCrossRefGoogle Scholar
  60. Gasic, G. J., Gasic, T. B., Galanti, N., Johnson, T., and Murphy, S., 1973, Platelet-tumor cell interaction in mice: The role of platelets in the spread of malignant disease, Int. J. Cancer 11:704.PubMedCrossRefGoogle Scholar
  61. Goldie, H., Jeffries, B. R., Jones, A. M., and Walker, M., 1953, Detection of metastatic tumor cells by intraperitioneal inoculation of organ brei from tumor bearing mice, Cancer Res. 13:566.PubMedGoogle Scholar
  62. Greene, H. S. N., and Harvey, E. K., 1964, The relationship between the dissemination of tumor cells and the distribution of metastases, Cancer Res. 24:799.PubMedGoogle Scholar
  63. Griffiths, J. F., 1960, The dissemination of cancer cells during operative procedures, Ann. Roy. Coll. Surg. Engl. 27:14.Google Scholar
  64. Hagmar, B., 1972a, Cell surface charge and metastasis formation, Acta Pathol. Microbiol. Scand. Sect. A 80:357.Google Scholar
  65. Hagmar, B., 1972b, Defibrination and metastasis formation: Effects of arvin on experimental metastases in mice, Eur. J. Cancer 8:17.PubMedGoogle Scholar
  66. Hagmar, B., and Norrby, K., 1973, Influence of cultivation, trypsinization and aggregation on the transplantability of melanoma B16 cells, Int. J. Cancer 11:663.PubMedCrossRefGoogle Scholar
  67. Handley, W. S., 1922, Cancer of the Breast and Its Treatment, Harper and Row, New York.Google Scholar
  68. Hashimoto, K., Yamanishi, Y., Maeyens, E., Dabbous, M. K., and Kanzaki, T., 1973, Collagenolytic activities of squamous cell carcinoma of the skin, Cancer Res. 33:2790.PubMedGoogle Scholar
  69. Hellström, I., Hellström, K. E., Sjögren, H. O., and Warner, G. A., 1971, Demonstration of cell mediated immunity to human neoplasms of various histological types, Int. J. Cancer 7:1.PubMedCrossRefGoogle Scholar
  70. Heppner, G. H., 1972, Blocking antibodies and enhancement, Ser. Haematol. 4:41.Google Scholar
  71. Herman, P. G., Benninghoff, D. L., and Mellins, H. Z., 1968, Radiation effect on the barrier function of the lymph node, Radiology 91:698.PubMedGoogle Scholar
  72. Hibbs, L. B., Jr., Lambert, L. H., Jr., and Remington, J. S., 1972, Control of carcinogenesis: A possible role for the activated macrophage, Science 177:990.CrossRefGoogle Scholar
  73. Hutchin, P., Amos, D. B., and Prioleau, W. H., 1967, Interaction of humoral antibodies and immune lymphocytes, Transplantation 5:68.CrossRefGoogle Scholar
  74. Joansson, O., 1958, The viability of circulating tumor cells in experimental cancer, Surg. Forum 9:577.Google Scholar
  75. Klein, G., and Klein, E., 1956, Conversion of solid neoplasms into ascites tumors, Ann. N. Y. Acad. Sci. 63:640.PubMedCrossRefGoogle Scholar
  76. Kripke, M. L., and Borsos, T., 1974, Immune surveillance revisited, J. Natl. Cancer Inst. 52:1393.PubMedGoogle Scholar
  77. Lane, M., Goksel, H., Salerno, R. A., and Haagensen, C. D., 1961, Clinicopathologic analysis of the surgical curability of breast cancers: A minimum ten-year study of a personal series, Ann. Surg. 153:483.PubMedCrossRefGoogle Scholar
  78. Lilien, J. E., and Moscona, A. A., 1967, Cell aggregation: Its enhancement by a supernatant from cultures of homologous cells, Science 157:70.PubMedCrossRefGoogle Scholar
  79. Lubarsch, E., 1912, Die Bedeutung des Traumas für Entstehung und Wachstum krankhafter Gewächse, Med. Klin. 8:1651.Google Scholar
  80. Lucké, B., Breedis, C., Woo, Z. P., Berwick, L., and Nowell, P., 1952, Differential growth of metastatic tumors in liver and lung: Experiments with rabbit V2 carcinoma, Cancer Res. 12:734.PubMedGoogle Scholar
  81. Ludwig, J., and Titus, J. L., 1967, Experimental tumor cell emboli in lymph nodes, Arch, Pathol. 84:304.Google Scholar
  82. Majno, G., Shea, S. M., and Leventhal, M., 1969, Endothelial contraction induced by histamine-type mediators, J. Cell Biol. 42:647.PubMedCrossRefGoogle Scholar
  83. Malmgren, R. A., 1967, Studies of circulating tumor cells in cancer patients, in: Mechanisms of Invasion of Cancer (P. Deroix, ed.), pp. 108–117, Springer, New York.CrossRefGoogle Scholar
  84. Martinez-Palomo, Braislovsky, C., and Bernhard, W., 1969, Ultrastructural modifications of the cell surface and intercellular contacts of some transformed cell strains, Cancer Res. 29:925.PubMedGoogle Scholar
  85. Milas, L., Hunter, N., Mason, K., and Withers, H. R., 1974, Immunological resistance to pulmonary metastases in C3Hf/Bu mice bearing syngeneic fibrosarcoma of different sizes, Cancer Res. 34:61.PubMedGoogle Scholar
  86. O’Meara, R. A. Q., 1958, Coagulative properties of cancers, Ir. J. Med. Sci. 394:474.PubMedGoogle Scholar
  87. O’Meara, R. A. Q., 1964, Fibrinolytic treatment of cancer, Lancet ii:963.CrossRefGoogle Scholar
  88. Ossowski, L., Unkeless, J. C., Tobia, A., Quigley, J. P., Rifkin, D. B., and Reich, E., 1973, An enzymatic function associated with transformation of fibroblasts by oncogenic viruses. II. Mammalian fibroblast cultures transformed by DNA and RNA viruses, J. Exp. Med. 137:113.CrossRefGoogle Scholar
  89. Ozaki, T., Yoshida, K., Ushijima, K., and Hayashi, H., 1971, Studies on the mechanisms of invasion in cancer. II. In vivo effects of a factor chemotactic for cancer cells, Int. J. Cancer 7:93.PubMedCrossRefGoogle Scholar
  90. Paget, S., 1889, The distribution of secondary growths in cancer of the breast, Lancet i:571.CrossRefGoogle Scholar
  91. Prehn, R. T., 1972, Neoplasia, in: Principles of Pathobiology (M. F. Lavia and R. B. Hill, eds.), pp. 191–232, Oxford University Press, New York.Google Scholar
  92. Prehn, R. T., and Lappé, M. A., 1971, An immunostimulation theory of tumor development, Transplant. Rev. 7:26.PubMedGoogle Scholar
  93. Purdam, L., Ambrose, E. J., and Klein, G., 1958, A correlation between electrical surface charge and some biological characteristics during the stepwise progression of a mouse sarcoma, Nature (London) 181:1586.CrossRefGoogle Scholar
  94. Romsdahl, M. D., Chu, E. W., Hume, R., and Smith, R.R., 1961, The timeof metastasis and release of circulating tumor cells as determined in an experimental system, Cancer 14:883.PubMedCrossRefGoogle Scholar
  95. Sandberg, A. A., and Moore, E. G., 1957, Examination of blood for tumor cells, J. Natl. Cancer Inst. 12:1.Google Scholar
  96. Schleich, A., 1973, The confrontation of normal and malignant cells in vitro: An experimental system in tumor invasion studies, in: Chemotherapy of Cancer Dissemination and Metastasis (S. Garattini and G. Franchi, eds.), pp. 51–57, Raven Press, New York.Google Scholar
  97. Steinberg, M. S., 1958, On the chemical bonds between animal cells: A mechanism for tight, specific cell association, Am. Nat. 92:65.CrossRefGoogle Scholar
  98. Steinberg, M. S., 1973, Cell movement in confluent monolayers: A reevaluation of the causes of “contact inhibition” in: Locomotion of Tissue Cells, Ciba Foundation Symposium 14, pp. 333–341, Associated Scientific Publishers, Amsterdam.Google Scholar
  99. Stoker, M. P. G., and Rubin, H., 1967, Density dependent inhibition of growth in culture, Nature (London) 215:172.CrossRefGoogle Scholar
  100. Strauli, P., 1970, The barrier function of lymph nodes: A review of experimental studies and their implications for cancer surgery, in: Surgical Oncology (F. Saegesser, ed.), pp. 161–176, Hans Huber, Bern.Google Scholar
  101. Sugarbaker, E. D., 1952, The organ selectivity of experimentally induced metastases in rats, Cancer 5:606.PubMedCrossRefGoogle Scholar
  102. Sylvan, B., 1973, Biochemical and enzymatic factors involved in cellular detachment, in: Chemotherapy of Cancer Dissemination and Metastasis (S. Garattini and G. Franchi, eds.), pp. 129–138, Raven Press, New York.Google Scholar
  103. Taptiklis, N., 1968, Dormancy by dissociated thyroid cells in the lungs of mice, Eur. J. Cancer 4:59.PubMedGoogle Scholar
  104. Thornes, R. D., 1972, Warfarin as maintenance therapy for cancer, J. Ir. Coll. Physicians Surg. 2:2.Google Scholar
  105. Unkeless, J. C., Tobia, A., Ossowski, L., Quigley, J. P., Rifkin, D. B., and Reich, E., 1973, An enzymatic function associated with transformation of fibroblasts by oncogenic viruses. I. Chick embryo fibroblast cultures transformed by avian RNA tumor viruses, J. Exp. Med. 137:85.PubMedCrossRefGoogle Scholar
  106. Vaage, J., 1973, Humoral and cellular immune factors in the systemic control of artificially-induced metastases in C3Hf mice, Cancer Res. 33:1957.PubMedGoogle Scholar
  107. Vaage, J., Doroshow, J. H., and Dubois, T. T., 1974, Radiation induced changes in established tumor immunity, Cancer Res. 34:129.PubMedGoogle Scholar
  108. Virchow, R., 1860, Cellular Pathology (transl. from 2nd ed. by Frank Chance), R. M. De Witt, New York.Google Scholar
  109. Ward, P. A., 1971, Inflammation, in: Principles of Pathobiology (M. F. Lavia and R. B. Hill, eds.), pp. 96–126, Oxford University Press, New York.Google Scholar
  110. Warren, B. A., 1973, Environment of the blood-bor ne tumor embolus adherent to vessel wall, J. Med. 4:150.PubMedGoogle Scholar
  111. Weiss, L., and Hauschka, T. S., 1970, Malignancy, electrophoretic mobilities and sialic acids at the electrokinetic surface of TA3 cells, Int. J. Cancer 6:270.PubMedCrossRefGoogle Scholar
  112. Wexler, H., Ryan, J. J., and Ketcham, A., 1969, The study of circulating tumor cells by the formation of pulmonary embolic tumor growths in a secondary host, Cancer 23:946.PubMedCrossRefGoogle Scholar
  113. Willis, R. A., 1960, Pathology of Tumors, 3rd ed., Butterworths, Washington, D.C.Google Scholar
  114. Wood, S., Jr., 1958, Pathogenesis of metastasis formation observed in vivo in the rabbit ear chamber, Arch. Pathol. 66:550.Google Scholar
  115. Wood, S., Jr., 1964, Experimental studies of the intravascular dissemination of ascites V2 carcinoma cells in the rabbit with special reference to fibrinogen and fibrinolytic agents, Bull. Schweiz. Akad. Med. Wiss. 20:12.Google Scholar
  116. Wood, S., Jr., Holyoke, E. D., and Yardley, J. H., 1961, Mechanisms of metastasis production by blood-borne cancer cells, Can. Cancer Conf. 4:167.Google Scholar
  117. Wood, S., Jr., Baker, R. R., and Marzocchi, B., 1967, Locomotion of cancer cells in vivo compared with normal cells, in: Mechanisms of Invasion in Cancer (P. Denoix, ed.), pp. 26–30, Springer-Verlag, Berlin.CrossRefGoogle Scholar
  118. Young, J. S., 1959, The invasive growth of malignant tumors: An experimental interpretation based on elastic-jelly models, J. Pathol. Bacteriol. 77:321.PubMedCrossRefGoogle Scholar
  119. Zeidman, I., 1957, Metastasis: A review of recent advances, Cancer Res. 17:157.PubMedGoogle Scholar
  120. Zeidman, I., 1961, The fate of circulating tumor cells. I. Passage of cells through capillaries, Cancer Res. 21:38.PubMedGoogle Scholar
  121. Zeidman, I., 1962, The fate of circulating tumor cells. II. A mechanism of cortisone action in increasing metastases, Cancer Res. 22:501.PubMedGoogle Scholar
  122. Zeidman, I., 1965, Fate of circulating tumor cells. III. Comparison of metastatic growth produced by tumor cell emboli in veins and lymphatics, Cancer Res. 3:324.Google Scholar
  123. Zeidman, I., and Buss, J. M., 1952, Transpulmonary passage of tumor cell emboli, Cancer Res. 12:731.PubMedGoogle Scholar
  124. Zeidman, I., and Buss, J. M., 1954, Experimental studies on the spread of cancer in the lymphatic system. I. Effectiveness of the lymph node as a barrier to the passage of embolic tumor cells, Cancer Res. 14:403.PubMedGoogle Scholar
  125. Zeidman, I., and Fidler, I. J., 1970, Effect of irradiation on experimental metastases via lymph and blood stream, J. Med. 1:9.PubMedCrossRefGoogle Scholar
  126. Zeidman, I., Mccutcheon, M., and Coman, D. R., 1950, Factors affecting the number of tumor metastases, experiments with a transplantable mouse tumor, Cancer Res. 10:357.PubMedGoogle Scholar
  127. Zeidman, I., Gamble, W. J., and Clovis, W. L., 1956, Immediate passage of tumor cell emboli through the liver and kidney, Cancer Res. 16:814.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1975

Authors and Affiliations

  • Isaiah J. Fidler
    • 1
  1. 1.Department of PathologyUniversity School of Medicine, University of PennsylvaniaPhiladelphiaUSA

Personalised recommendations