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Radiation enhancement of metastasis: a review

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Abstract

Virtually every modality employed in the treatment of cancer has demonstrated an adverse effect upon metastasis under some conditions. This review surveys the experimental and clinical literature pertaining to the untoward effects of ionizing radiation upon metastatic processes. Two processes are described: (1) enhancement of metastases following local tumor irradiation; (2) localization of metastasis in previously irradiated normal tissues. In the first process the experimental evidence indicates a local effect of irradiation upon the tumor-stroma interface. It predominates under conditions of non-curative radiation doses. There is no proof that this process occurs in clinical practice, but a review of data provides suggestive evidence for its existence following non-curative therapy. The second process is documented both experimentally and clinically. It requires the presence of viable, circulating tumor cells and appears mediated through vascular damage. The few clinical reports suggest that this effect is rare in practice. The clinical significance of both processes appears small under conditions of effective tumor therapy, but it is speculated that inadequate tumor irradiation, or irradiation of normal tissues with uncontrolled tumor elsewhere, may be deleterious.

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References

  1. Agostino, D., andClifton, E. E., 1962, Decrease of metastases of carcinosarcoma Walker 256 with irradiation and heparin or fibrinolytic agents.Radiology,79, 848–855.

    Google Scholar 

  2. Agostino, D., andClifton, E. E., 1965, Trauma as a cause of localization of blood-borne metastasis: preventive effect of heparin and fibrinolysin.Annals of Surgery,161, 97–102.

    Google Scholar 

  3. Anderson, P., andDische, S., 1981, Local tumor control and the subsequent incidence of distant metastatic disease.International Journal of Radiation Oncology,7, 1645–1648.

    Google Scholar 

  4. Ando, K., Muneyasu, U., Kenton, L., andKahn, J., 1987, Effect of thermochemo-therapy on the development of spontaneous lung metastases.International Journal of Hyperthermia,3, 453–458.

    Google Scholar 

  5. Aron, M. S., Wexler, H., Sabesin, S. M., andMantel, N., 1962, Effect of cortisone and amputation on metastases.Cancer,15, 227–231.

    Google Scholar 

  6. Baker, D., Constable, W., Elkon, D., andRinehart, L., 1981, The influence of ICRF-159 and Levamisole on the incidence of metastases following local irradiation of a solid tumor.Cancer,48, 2179–2183.

    Google Scholar 

  7. Baker, D., Elkon, D., Lim, M. L., Constable, W., andWanebo, H., 1981, Does local X-irradiation of a tumor increase the incidence of metastases?Cancer,48, 2394–2398.

    Google Scholar 

  8. Baker, D., Sager, H., andConstable, W., 1986, The influence of Levamisole and hyperthermia on the incidence of metastases from an X-irradiated tumor.Cancer Investigation,4, 287–292.

    Google Scholar 

  9. Baker, D. G., Sager, H., Constable, W., andGoodchild, N. T., 1984, Influence of ultrasound-induced hyperthermia and X-irradiation on the incidence of metastases from a solid tumor.Invasion and Metastasis,4, 111–124.

    Google Scholar 

  10. Barsky, S. H., andGopalakrishna, R., 1987, Increased invasion and spontaneous metastasis of BL16 melanoma with inhibition of the desmoplastic response in C57 BL/6 mice.Cancer Research,47, 1663–1667.

    Google Scholar 

  11. Baserga, R., andShubik, P., 1954, The action of cortisone on transplanted and induced tumors in mice.Cancer Research,14, 12–16.

    Google Scholar 

  12. Baumann, M., Beck-Bornholdt, H.-P., Becker, S., Maurer, T., andVolger, H., 1987, Radiotherapy of the R1H-tumour: induction of metastasis.International Journal of Radiation Biology,51, 917.

    Google Scholar 

  13. Baumann, M., Suit, H., andSedlacek, R. F., 1990, Metastases after fractionated radiation therapy of three murine tumor models.International Journal of Radiation Oncology, Biology and Physics,19, 367–370.

    Google Scholar 

  14. Beck-Bornholdt, H.-P., 1988, Parameters affecting the response of experimental tumours to fractionated radiotherapy.Strahlentherapie,164, 155–164.

    Google Scholar 

  15. Bonfil, R. D., Bustuoabad, R. A., Ruggerio, R. A., Meiss, R. P., andPasquanlini, C.D., 1988, Tumor necrosis can facilitate the appearance of metastases.Clinical and Experimental Metastasis,6, 121–130.

    Google Scholar 

  16. Brown, J. M., 1973, The effect of lung irradiation on the incidence of pulmonary metastases in mice.British Journal of Radiology,46, 613–618.

    Google Scholar 

  17. Brown, J. M., 1977, Effects of radiation and chemotherapeutic agents on the incidence and treatment of blood-borne metastases.Cancer Metastasis: Approaches to the Mechanism, Prevention, and Treatment edited by P. G. Stansly and H. Sato.GANN,20, 207–225.

  18. Brown, J. M., andMarsa, G. W., 1978, Effect of dose fractionation on the enhancement by radiation of cyclophosphamide on artificial pulmonary metastases.British Journal of Cancer,37, 1020–1025.

    Google Scholar 

  19. Brown, J. M., andParker, E. T., 1979, Host treatments affecting artificial pulmonary metastases: interpretation of loss of radioactively labelled cells from lungs.British Journal of Cancer,40, 677–688.

    Google Scholar 

  20. Cole, H., andHalnan, K. E., 1971, Facilitation of tumor spread in irradiated tissue after prophylactic post-operative X-ray therapy for breast cancer.Clinical Radiology,22, 133–135.

    Google Scholar 

  21. Crile, G. Jr, 1968, The effect on metastasis of removing or irradiating regional nodes of mice.Surgery, Gynecology and Obstetrics,126, 1270–1272.

    Google Scholar 

  22. Crile, G. Jr, andDeodhar, S. D., 1971, Role of preoperative irradiation in prolonging concomitant immunity and preventing metastasis in mice.Cancer,27, 629–634.

    Google Scholar 

  23. Cuzick, J., Steward, H., Peto, R., Baum, M., Fisher, B., Host, H., Lythgoe, J. P., Ribeiro, G., Scheurlen, H., andWallgren, A., 1987, Overview of randomized trials of postoperative adjuvant radiotherapy in breast cancer.Cancer Treatment Reports,71, 15–29.

    Google Scholar 

  24. Dao, T. L., andKovaric, J., 1962, Incidence of pulmonary and skin metastases in woman with breast cancer who received postoperative irradiation.Surgery,52, 203–212.

    Google Scholar 

  25. Dao, T. L., andMoore, G. E., 1961, Clinical observations of conditions which apparently enhance malignant cell survival.Surgery, Gynecology and Obstetrics,112, 191–195.

    Google Scholar 

  26. Dao, T., andYogo, H., 1967, Enhancement of pulmonary metastases by X-irradiation in rats bearing mammary cancer.Cancer,20, 2020–2025.

    Google Scholar 

  27. dela Monte, S. M., Hutchins, G. M., Grover, M., andMoore, G. W., 1988, Altered metastatic behavior of small cell carcinoma of the lung after chemotherapy and radiation.Cancer,61, 2176–2182.

    Google Scholar 

  28. DeRuiter, J., Cramer, S. J., Lelieveld, P., andVan Putten, L. M., 1982, Comparison of metastatic disease after local tumour treatment with radiotherapy or surgery in various tumour models.European Journal of Cancer,18, 281–289.

    Google Scholar 

  29. Dickson, J. A., andEllis, H. A., 1974, Stimulation of tumour cell dissemination by raised temperature (42°C) in rats with transplanted Yoshida tumours.Nature,248, 354–358.

    Google Scholar 

  30. Diehl, L. F., Hurwitz, A., Johnson, S. A., Butler, W. M., andTaylor, H. G., 1984, Skin metastases confined to a field of previous irradiation.Cancer,53, 1864–1868.

    Google Scholar 

  31. Dixon, B., andBagnall, D. A., 1985, Metastasis and the excision of irradiated LMC1 tumours in the rat.Radiotherapy and Oncology,4, 153–161.

    Google Scholar 

  32. Dubravsky, N. B., Dubrawsky, C., Jampolis, S., Mason, K., Hunter, N., andWithers, H. R., 1981, Long-term effects of pulmonary damage in mice on lung weight, compliance, hydroxyproline content and formation of metastases.British Journal of Radiology,54, 1075–1080.

    Google Scholar 

  33. Dubravsky, N., Hunter, N., Mason, K., Dubrawsky, C., andWithers, H. R., 1976, Development of pulmonary metastases from a transplanted mammary carcinoma in leg. II. Studies of a possible ‘factor’ released as a result of the irradiation of the tumor-bearing limb.Radiation Research,67, 642.

    Google Scholar 

  34. Eccles, S. A., andAlexander, P., 1975, Immunologically-mediated restraint of latent tumour metastases.Nature,257, 52–53.

    Google Scholar 

  35. Feder, B. H., Stein, J. J., Smith, T. K., Schaeflein, J. W., Boutelle, J. L., Conroy, R. M., 1968, The effect of hyperbaric oxygen on pulmonary metastases in C3H mice.Radiology,6, 1181–1184.

    Google Scholar 

  36. Fidler, I. J., andZeidman, I., 1972, Enhancement of experimental metastases by X-ray: a possible mechanism.Journal of Medicine,3, 172–177.

    Google Scholar 

  37. Fisher, B., Fisher, E. R., andFedusko, N., 1967, Trauma and the localization of tumor cells.Cancer,20, 23–30.

    Google Scholar 

  38. Fisher, B., Saffer, E. A., andDeutsch, M., 1986, Influence of irradiation of a primary tumor on the labelling index and estrogen receptor index in a distant tumor focus.International Journal of Radiation Oncology, Biology and Physics,12, 879–885.

    Google Scholar 

  39. Fisher, E. R., andFisher, B., 1969, Effects of X-irradiation on parameters of tumor growth, histology, and ultrastructure.Cancer,24, 39–55.

    Google Scholar 

  40. Fisher, M. S., andCifone, M. A., 1981, Enhanced metastatic potential of murine fibrosarcoma treatedin vitro with ultraviolet radiation.Cancer Research,41, 3018–3023.

    Google Scholar 

  41. Florentin, I., Nolibe, D., andGiroud, J. P., 1986, Enhancement of lung metastases and inhibition of NK activity of lung intracapillary cells by an acute inflammation.Bulletin du Cancer,73, 217–218.

    Google Scholar 

  42. Gorelik, E., Segal, S., andFeldman, M., 1978, Growth of a local tumor exerts a specific inhibitory effect on progression of lung metastases.International Journal of Cancer,21, 617–625.

    Google Scholar 

  43. Gunduz, N., Fisher, B., andSaffer, E. A., 1979, Effect of surgical removal on the growth kinetics of residual tumor.Cancer Research,39, 3861–3865.

    Google Scholar 

  44. Hahn, E. W., Alfieri, A. A., andKim, J. H., 1979, The significance of local tumor hyperthermia/radiation on the production of disseminated disease.International Journal of Radiation Oncology, Biology and Physics,5, 819–823.

    Google Scholar 

  45. Hanna, N., andBurton, R. C., 1981, Definitive evidence that natural killer (NK) cells inhibit experimental tumor metastasisin vivo.Journal of Immunology,127, 1754–1758.

    Google Scholar 

  46. Heisel, M. A., Lang, W. E., Stowe, S. M., andJones, P. A., 1984, Effects of X-irradiation on artificial blood vessel wall degradation by invasive tumor cells.Cancer Research,44, 2441–2445.

    Google Scholar 

  47. Hewitt, H. B., andBlake, E. R., 1977, Facilitation of nodal metastasis from a non-immunogenic murine carcinoma by previous whole-body irradiation of tumour recipients.British Journal of Cancer,36, 23–34.

    Google Scholar 

  48. Hill, R. P., Bush, R. S., 1969, A lung-colony assay to determine the radiosensitivity of the cells of a solid tumor.International Journal of Radiation Biology,15, 415–444.

    Google Scholar 

  49. Hill, S. A., andDenekamp, J., 1982, Does local tumour heating in mice influence metastatic spread?British Journal of Radiology,55, 444–451.

    Google Scholar 

  50. Hill, S. A., andDenekamp, J., 1988, Therapeutic benefit from combined heat and radiation.Recent Results in Cancer Research,109, 28–34.

    Google Scholar 

  51. Hirata, H., andTanaka, K., 1984, Artificial metastases and decrease of fibrinolysis in the nude mouse after hemithoracic irradiation.Clinical and Experimental Metastasis,2, 311–319.

    Google Scholar 

  52. Hong, W. K., Bromer, R. H., Amato, D. A., Shapshay, S., Vincent, M., Vaughan, C., Willett, B., Katz, A., Welch, J., Fofonoff, S., andStrong, M. S., 1985, Patterns of relapse in locally advanced head and neck cancer in patients who achieved complete remission after combined modality therapy.Cancer,56, 1242–1245.

    Google Scholar 

  53. Hubbard, N. E., andErickson, K. L., 1987, Enhancement of metastasis from a transplantable mouse mammary tumor by dietary linoleic acid.Cancer Research,48, 6171–6175.

    Google Scholar 

  54. Hunter, N., Dubravsky, N., Mason, K., andWithers, H. R., 1976, Development of pulmonary metastases from a transplanted mammary carcinoma in leg. I. Effect of irradiation of the primary tumor.Radiation Research,67, 642.

    Google Scholar 

  55. Inch, W. R., andMcCredie, J. A., 1961, Effect of radiation of primary tumour on incidence of distant metastases. Ontario Cancer Treatment and Research Foundation Annual Report, 1960–61, Toronto, Canada, pp. 68–69.

  56. Ito, H., Kubo, A., Shigematsu, N., andHashimoto, S., 1984, Skin metastases within the previous radiation field after prophylactic postoperative radiotherapy for breast cancer.Clinical and Experimental Metastasis,2, 235–239.

    Google Scholar 

  57. Ivarsson, L., 1976, Pulmonary metastasis formation after trauma.Acta Chirurgica Scandinavica (Suppl.),463, 1–46.

    Google Scholar 

  58. Jaffe, D. R., Williamson, J. F., andBowden, G. T., 1987, Ionizing radiation enhances malignant progression of mouse skin tumors.Carcinogenesis,8, 1753–1755.

    Google Scholar 

  59. Kaae, S., 1953, Metastatic frequency of spontaneous mammary carcinoma in mice following local roentgen irradiation.Cancer Research,13, 744–749.

    Google Scholar 

  60. Kamby, C., Ejlertsen, J., Andersen, N. E., Birkler, L., Zedeler, K., andRose, C., 1988, The pattern of metastases in human breast cancer.Acta Oncologica,27, 715–719.

    Google Scholar 

  61. Kanclerz, A., andChapman, J. D., 1988, Influence of misonidazole, SR-2508, RSU-1069 and WR-2721 on spontaneous metastases in C57BL mice.International journal of Radiation Oncology, Biology and Physics,14, 309–316.

    Google Scholar 

  62. Kaplan, H. S., Murphy, E. D., 1949, The effect of local roentgen irradiation on the biological behavior of a transplantable mouse carcinoma. I. Increased frequency of pulmonary metastasis.Journal of the National Cancer Institute,9, 407–413.

    Google Scholar 

  63. Katzav, S., Shapiro, J., Segal, S., andFeldman, M., 1986, General anesthesia during excision of a mouse tumor accelerates postsurgical growth of metastases by suppression of natural killer cell activity.Israel Journal of Medical Science,22, 339–345.

    Google Scholar 

  64. Kerbel, R. S., andDavies, A. J. S., 1982, Facilitation of tumour progression by cancer therapy.Lancet,2, 977–978.

    Google Scholar 

  65. Kinjo, M., 1978, Lodgement and extravasation of tumour cells in blood-borne metastasis: an electron microscope study.British Journal of Cancer,38, 293–301.

    Google Scholar 

  66. Koike, A., Nakazato, H., andMoore, G. E., 1963, The fate of Ehrlich cells injected into the portal system.Cancer,16, 715–720.

    Google Scholar 

  67. Kramer, R. H., Gonzalez, R., andNicolson, G. L., 1980, Metastatic tumor cells adhere preferentially to the extracellular matrix underlying vascular endothelial cells.International Journal of Cancer,26, 639–645.

    Google Scholar 

  68. Krebs, C., 1929, The effect of roentgen irradiation on the interrelation between malignant tumors and their hosts.Acta Radiologica (Suppl. VIII).

  69. Liotta, L. A., 1986, Tumor invasion and metastases—role of the extracellular matrix.Cancer Research,48, 1–7.

    Google Scholar 

  70. Lollini, P.-L., De Giovanni, C., Del Re, B., Nicoletti, G., Prodi, G., andNanni, P., 1987, Interferon-mediated enhancement of metastasis. Are MHC antigens involved?Clinical and Experimental Metastasis,5, 277–287.

    Google Scholar 

  71. Lord, P. F., Knapp, D. S., andMorrow, D., 1981, Increased skeletal metastases of spontaneous canine osteosarcoma after fractionated systemic hyperthermia and local X-irradiation.Cancer Research,41, 4331–4334.

    Google Scholar 

  72. Maor, M. H., 1988, Dermatophytosis confined to irradiated skin. A case report.International Journal of Radiation Oncology, Biology and Physics,14, 825–826.

    Google Scholar 

  73. Marley, N. F., andMarley, W. M., 1982, Skin metastases in an area of radiation dermatitis.Archives of Dermatology,118, 129–131.

    Google Scholar 

  74. McCredie, J. A., Inch, W. R., andCowie, H. C., 1976, Effect of excision or local radiotherapy to a tumour and its regional nodes on metastases.Cancer,31, 983–987.

    Google Scholar 

  75. McMillan, T.J., andHart, I. R., 1986, Enhanced experimental metastatic capacity of a murine melanoma following pre-treatment with anti-cancer drugs.Clinical and Experimental Metastasis,4, 285–292.

    Google Scholar 

  76. McMillan, T. J., andHart, I. R., 1987, Can cancer chemotherapy enhance the malignant behaviour of tumours?Cancer and Metastasis Reviews,6, 503–519.

    Google Scholar 

  77. Meltzer, J., Ahmed, S. A., andArchambeau, J. O., 1981, The development of metastases within a field of previous irradiation.Cancer,48, 717–720.

    Google Scholar 

  78. Merino, O. R., Lindberg, R. D., andFletcher, G. H., 1977, An analysis of distant metastases from squamous cell carcinoma of the upper respiratory and digestive tracts.Cancer,40, 145–151.

    Google Scholar 

  79. Milas, L., Daly, N., Hunter, N., Meoz, R., andPeters, L. J., 1983, Enhancement by misonidazole of metastatic tumor nodule formation in the lungs of mice.Clinical and Experimental Metastasis,1, 61–70.

    Google Scholar 

  80. Milas, L., Hirata, H., Hunter, N., andPeters, L. J., 1988, Effect of radiation-induced injury of tumor bed stroma on metastatic spread of murine sarcomas and carcinomas.Cancer Research,48, 2116–2120.

    Google Scholar 

  81. Milas, L., Hunter, N., andBasic, I., 1985, Treatment with cortisone plus heparin or hexuronyl hexoaminoglycan sulfates of murine tumors and their lung deposits.Clinical and Experimental Metastasis,3, 247–255.

    Google Scholar 

  82. Milas, L., Hunter, N., Basic, I., Volpe, J. P., andTofilon, P. J., 1986, Effect of the radiosensitizer misonidazole and the radioprotector diethyldithiocarbamate on spontaneous metastasis formation of murine tumors.International Journal of Radiation Oncology, Biology and Physics,12, 1071–1074.

    Google Scholar 

  83. Milas, L., Hunter, N., Basic, I., andWithers, H. R., 1974, Protection by Corynebacterium granulosum against radiation-induced enhancement of artificial pulmonary metastases of a murine fibrosarcoma.Journal of the National Cancer Institute,52, 1875–1880.

    Google Scholar 

  84. Milas, L., Hunter, N., andPeters, L. J., 1987, The tumor bed effect: Dependence of tumor take, growth rate, and metastasis on the time interval between irradiation and tumor cell transplantation.International Journal of Radiation Oncology, Biology and Physics,13, 379–383.

    Google Scholar 

  85. Milas, L., Iwakawa, M., andHunter, N., 1987, Enhancement of lung colony formation by admixing irradiated with viable tumor cells: dependence on host status.Clinical and Experimental Metastasis,5, 213–217.

    Google Scholar 

  86. Milas, L., andPeters, L. J., 1984, Conditioning of tissues for metastasis formation by radiation and cytotoxic drugs.Cancer Invasion and Metastasis: Biologic and Therapeutic Aspects, edited by G. L. Nicholson and L. Milas (New York: Raven Press), pp. 321–336.

    Google Scholar 

  87. Moore, J. V., andDixon, B., 1977, Metastasis of a transplantable mammary tumour in rats treated with cyclophosphamide and/or irradiation.British Journal of Cancer,36, 221–226.

    Google Scholar 

  88. Nolibe, D., andPoupon, M. F., 1986, Enhancement of pulmonary metastasis induced by decreased lung natural killer cell activity.Journal of the National Cancer Institute,77, 99–103.

    Google Scholar 

  89. O'Brien, C. J., Smith, J. W., Soong, S. J., Unst, M. M., andMaddox, W. A., 1986, Neck dissection with and without radiotherapy: Prognostic factors, patterns of recurrence, and survival.American Journal of Surgery,152, 456–463.

    Google Scholar 

  90. Ohno, M., Nakata, H., andMatsuura, K., 1980, Enhancement of metastatic pulmonary malignant lymphoma following lung irradiation.Nippon Acta Radiologica,40, 1183–1188.

    Google Scholar 

  91. Olch, P. D., Eck, R. V., andSmith, R. R., 1959, An experimental study of the effect of external irradiation on a ‘primary’ tumor and its distance metastases.Cancer,12, 23.

    Google Scholar 

  92. Olch, P. D., Stevenson, J. K., andHarkens, H. N., 1960, Further studies of the effect of local sublethal tumor irradiation on the development of distant metastases.Surgical Forum,11, 61–64.

    Google Scholar 

  93. Orr, F. W., Adamson, I. Y. R., andYoung, L., 1986, Promotion of pulmonary metastasis in mice by bleomycin-induced endothelial injury.Cancer Research,46, 891–897.

    Google Scholar 

  94. Orr, F. W., andWarner, D. J., 1987, Effects of neutrophil-mediated pulmonary endothelial injury on the localization and metastasis of circulating Walker carcinosarcoma cells.Invasion and Metastasis,7, 183–196.

    Google Scholar 

  95. Owen, L., 1975, Influence of radiotherapy.Intravascular Events in Cancer Dissemination. Proceedings of EORTC Metastasis Club.European Journal of Cancer,11, 35–36.

    Google Scholar 

  96. Owen, L. N., andBostock, D. E., 1973, Prophylactic X-irradiation of the lung in canine tumours with particular reference to osteosarcoma.European Journal of Cancer,9, 747–752.

    Google Scholar 

  97. Papaioannou, A. N., 1985, Hypothesis: increasingly intensive locoregional treatment of breast cancer may promote recurrence.Journal of Surgical Oncology,30, 33–41.

    Google Scholar 

  98. Peters, L. J., 1974, The potentiating effect of prior local irradiation of the lungs on the development of pulmonary metastases.British Journal of Cancer,47, 827–829.

    Google Scholar 

  99. Peters, L. J., 1975, A study of the influence of various diagnostic and therapeutic procedures applied to a murine squamous carcinoma on its metastatic behaviour.British Journal of Radiology,32, 355–365.

    Google Scholar 

  100. Peters, L. J., Mason, K. A., McBride, W. J., andPatt, Y. Z., 1978, Enhancement of lung colony forming efficiency by local thoracic irradiation: interpretation of labeled cell studies.Radiology,126, 499–505.

    Google Scholar 

  101. Peters, L. J., Mason, K. A., andWithers, H. R., 1980, Effect of lung irradiation on metastases: radiobiological studies and clinical correlations.Radiation Biology in Cancer Research, edited by R. E. Meyn and H. R. Withers (New York: Raven Press), pp. 515–529.

    Google Scholar 

  102. Piro, A. J., andHellman, S., 1978, Effect of primary treatment modality on the metastatic pattern of mammary carcinoma.Cancer Treatment Reports,62, 1275–1279.

    Google Scholar 

  103. Ramani, P., andBalkwill, F. R., 1987, Enhanced metastases of a mouse carcinoma after the vitro treatment with murine interferon gamma.International Journal of Cancer,40, 830.

    Google Scholar 

  104. Ramsay, J., Suit, H. D., andSedlacek, R., 1988, Experimental studies on the incidence of metastases after failure of radiation treatment and the effect of salvage surgery.International Journal of Radiation Oncology, Biology and Physics,14, 1165–1168.

    Google Scholar 

  105. Rappaport, D. S., andBrown, J. M., 1979, Influence of localized preinoculation irradiation of the foot on lymphatic metastasis from a primary tumor growing in the foot.Radiation Research,78, 108–121.

    Google Scholar 

  106. Rappaport, D. S., andBrown, J. M., 1980, A study of the mechanism by which localized preinoculation irradiation enhances the rate of lymphatic spread.Radiation Research,83, 566–578.

    Google Scholar 

  107. Revesz, L., 1958, Effect of lethally damaged tumor cells upon the development of admixed viable cells.Journal of the National Cancer Institute,20, 1157–1186.

    Google Scholar 

  108. Riggins, R. S., andKetcham, A. S., 1965, Effects of incisional biopsy on the development of experimental tumor metastases.Journal of Surgical Research,5, 200–206.

    Google Scholar 

  109. Robinson, K. P., andHoppe, E., 1962, The development of blood-borne metastases, effect of local trauma and ischemia.Archives of Surgery,85, 720–724.

    Google Scholar 

  110. Rockwell, S., Nierenburg, M., andIrvin, C. G., 1984, Enhancement of artificial lung metastases by misonidazole.International Journal of Radiation Oncology, Biology and Physics,10, 1395–1398.

    Google Scholar 

  111. Roos, E., andDingemans, K. P., 1978, Mechanisms of metastasis.Biochimica et Biophysica Acta,560, 135–166.

    Google Scholar 

  112. Schantz, S. P., andGoepfert, H., 1987, Multimodality therapy and distant metastases: the impact of natural killer cell activity.Archives of Otolaryngology,113, 1207–1213.

    Google Scholar 

  113. Schurch, O., 1935, Ueber Hautmetastasen im Bestrahlungsfeld bei Pyloruscarcinom.Zeitschrift für Krebsforschung,41, 47–50.

    Google Scholar 

  114. Schwarz, G., 1935, Ueber die Nachbestrahlung bei operiertem Mammarkarzinom.Strahlentherapie,53, 674–681.

    Google Scholar 

  115. Sell, S., Stillman, D., Michaelsen, M., Alaimo, J., andvon Essen, C. F., 1977, Prevention of pulmonary metastases by irradiation of the lung.Radiation Research,69, 54–64.

    Google Scholar 

  116. Sheldon, P. W., 1974, The effect of irradiating a transplanted solid sarcoma on the subsequent development of metastases.British Journal of Cancer,30, 416–420.

    Google Scholar 

  117. Sheldon, P. W., Begg, A. C., Fowler, J. F., andLansley, I. F., 1974, The incidence of lung metastases in C3H mice after treatment of implanted solid tumours with X-rays or surgery.British Journal of Cancer,30, 342–348.

    Google Scholar 

  118. Sheldon, P. W., andFowler, J. F., 1973, The effect of irradiating a transplanted murine lymphosarcoma on the subsequent development of metastases.British Journal of Cancer,28, 508–514.

    Google Scholar 

  119. Sheldon, P. W., andFowler, J. F., 1976, The effect of low-dose pre-operative X-irradiation of implanted mouse mammary carcinomas on local recurrence and metastasis.British Journal of Cancer,34, 401–407.

    Google Scholar 

  120. Shen, R.-N., Hornback, N. B., Shidnia, H., Lu, L., Montebello, J. F., andBrahmi, Z., 1988, A comparison of lung metastases and natural killer cell activity in daily fractions and weekly fractions of radiation therapy on murine B16a melanoma.Radiation Research,114, 354–360.

    Google Scholar 

  121. Shewell, J., 1980, Effect of hemithorax irradiation of young mice on pulmonary metastatic deposits from subsequently developing spontaneous mammary tumors.Metastasis: Clinical and Experimental Aspects. Proceedings of EORTC Metastasis Group International Conference. (The Hague: Martinus Nijhoff),Developments in Oncology,4, 368.

    Google Scholar 

  122. Sikov, M. R., Chapman, B. B., andLofstrom, J. E., 1967, Factors in the development of metastases after irradiation of the L-1 lymphosarcoma.Radiology,88, 1007–1008.

    Google Scholar 

  123. Sikov, M. R., Cook, B. B., andLofstrom, J. E., 1960, Metastatic spread of lymphosarcoma as influenced by radiation.Federation Proceedings,19, 399.

    Google Scholar 

  124. Slotman, G. J., Mohit, T., Raina, S., Swaminathan, A. P., Ohanian, M., andRush, B. F., 1984, The incidence of metastases after multimodal therapy of cancer of the head and neck.Cancer,54, 2009–2014.

    Google Scholar 

  125. Stephens, T. C., Adams, K., andPeacock, J. H., 1980, Metastasis of Lewis lung carcinoma regrowing after cytotoxic treatments.Metastasis: Clinical and Experimental Aspects, edited by P. Hilgard and S. Eccles (The Hague: Martinus Nijhoff), pp. 411–415.

    Google Scholar 

  126. Stjernswärd, J., 1974, Decreased survival related to irradiation post-operatively in early operable breast cancer.Lancet,2, 1285–1286.

    Google Scholar 

  127. Stjernswärd, J., andDouglas, P., 1977, Immunosuppression and metastasis: biological mechanisms and therapy.Cancer Invasion and Metastases, edited by S. B. Day, W. D. Laird Myers, P. Stansly, S. Garattini and M. G. Lewis (New York: Raven Press), pp. 319–331.

    Google Scholar 

  128. Strong, M. S., Vaughan, C. W., Kayne, H. I., Aral, I. M., Ucmakli, A., Feldman, M., andHealy, G. B., 1978, A randomized trial of preoperative radiotherapy in cancer of the oropharynx and hypopharynx.American Journal of Surgery,136, 494–500.

    Google Scholar 

  129. Suit, H. D., Sedlacek, R. S., andGillette, E. L., 1970, Examination for a correlation between probabilities of development of distant metastasis and of local recurrence.Radiology,95, 189–194.

    Google Scholar 

  130. Suzuki, N., 1983, Spontaneous versus artificial lung metastasis: discrepant effect of whole-body irradiation in NFSA2ALM and NFSA1SLM tumor systems.Journal of the National Cancer Institute,71, 835–839.

    Google Scholar 

  131. Talmadge, J. E., andFidler, I. J., 1982, Enhanced metastatic potential of tumor cells harvested from spontaneous metastases of heterogeneous murine tumors.Journal of the National Cancer Institute,69, 975–985.

    Google Scholar 

  132. Tanaka, Y., 1976, Effect of lung irradiation on the incidence of pulmonary metastases and its mechanism.Acta Radiologica (Ther.),15, 142–148.

    Google Scholar 

  133. Tannock, I. F., andBrowman, G., 1986, Lack of evidence for a role of chemotherapy in the routine management of locally advanced head and neck cancer.Journal of Clinical Oncology,4, 1121–1126.

    Google Scholar 

  134. Terz, J. J., 1981, Pre-operative irradiation for head and neck cancer: results of a prospective study.Surgery,89, 449–453.

    Google Scholar 

  135. Thompson, S. C., 1974, Tumor colony growth in the irradiated mouse lung.British Journal of Cancer,30, 337–341.

    Google Scholar 

  136. Todoroki, T., andSuit, H. D., 1985, Therapeutic advantage in preoperative single-dose radiation combined with conservative and radical surgery in different size murine fibrosarcomas.Journal of Surgical Oncology,29, 207–215.

    Google Scholar 

  137. Todoroki, T., andSuit, H. D., 1986, Effect of fractionated irradiation prior to conservative and radical surgery on therapeutic gain in a spontaneous fibrosarcoma of the C3H mouse.Journal of Surgical Oncology,31, 279–286.

    Google Scholar 

  138. Travis, E. L., Reinartz, G., Chu, A. M., Down, J. D., andFowler, J. F., 1981, Effect of cyclophosphamide or X-rays on spontaneously occurring metastases from tumors transplanted into the tails of mice.Cancer Research,41, 1803–1807.

    Google Scholar 

  139. Tubiana, M., 1981, Does postoperative radiotherapy facilitate metastatic dissemination?Immunopharmacologic Effects of Radiation Therapy, edited by J. B. Dubois, B. Serrou and C. Rosenfeld (New York: Raven Press), pp. 399–414.

    Google Scholar 

  140. Vaage, J., Doroshow, J. H., andDuBois, T. T., 1974, Radiation-induced changes in established tumor immunity.Cancer Research,34, 129–137.

    Google Scholar 

  141. van den Brenk, H. A. S., Burch, W. M., Orton, C., andSharpington, C., 1973, Stimulation of clonogenic growth of tumour cells and metastases in the lungs by local X-radiation.British Journal of Cancer,27, 291–306.

    Google Scholar 

  142. van den Brenk, H. A. S., Crowe, M. C., andStone, M. G., 1977, Reactions of the tumour bed to lethally irradiated tumour cells, and the Revesz effect.British Journal of Cancer,36, 94–104.

    Google Scholar 

  143. van den Brenk, H. A. S., andKelly, H., 1973, Stimulation of growth of metastases by local X-irradiation in kidney and liver.British Journal of Cancer,28, 349–353.

    Google Scholar 

  144. van den Brenk, H. A. S., andKelly, H., 1974, Potentiating effect of prior local irradiation of the lungs on pulmonary metastases.British Journal of Radiology,47, 332–336.

    Google Scholar 

  145. van den Brenk, H. A. S., Moore, V., Sharpington, C., andOrton, C., 1972, Production of metastases by a primary tumour irradiated under aerobic and anaerobic conditions,in vivo.British Journal of Cancer,26, 402–412.

    Google Scholar 

  146. van den Brenk, H. A. S., andSharpington, C., 1971, Effect of local X-irradiation of a primary sarcoma in the rat on dissemination and growth of metastases: dose-response characteristics.British Journal of Cancer,25, 812–830.

    Google Scholar 

  147. van Putten, L. M., Kram, L. K. J., van Dierendonck, H. H. C., Snimk, T., andFuzy, M., 1975, Enhancement by drugs of metastatic lung nodule formation after intravenous tumour cell injection.International Journal of Cancer,15, 588–595.

    Google Scholar 

  148. van Putten, L. M., de Ruiter, J., andMulder, J. H., 1983, Enhancement and reduction of metastases by anticancer drugs.Proceedings 13th International Congress of Chemotherapy,103, 34–39.

    Google Scholar 

  149. Vikram, B., Strong, E. W., Shah, J. P., andSpiro, R., 1984, Failure at distant sites following multimodality treatment for advanced head and neck cancer.Head and Neck Surgery,6, 730–733.

    Google Scholar 

  150. Vlodavsky, I., Atiav, Y., Atzmon, R., andFuks, Z., 1982, Tumor cell attachment to the vascular endothelium and subsequent degradation of the subendothelial extracellular matrix.Experimental Cell Research,140, 149–159.

    Google Scholar 

  151. von Essen, C. F., andKaplan, H. S., 1952, Further studies on metastasis of a transplantable mouse mammary carcinoma after roentgen irradiation.Journal of the National Cancer Institute,12, 883–892.

    Google Scholar 

  152. von Essen, C. F., andStjernswärd, J., 1978, Radiotherapy and metastases.Secondary Spread of Cancer, edited by R. W. Baldwin (New York: Academic Press), pp. 73–99.

    Google Scholar 

  153. Voutilainen, A., 1957, Experimental investigations on the influence of roentgen irradiation on the growth of multiple tumours.Acta Radiologica,47, 149–156.

    Google Scholar 

  154. Walker, A., McCullum, H. M., Wheldon, T. E., Nias, A. W. H., andAbdellal, A. S., 1987, Promotion of metastasis of C3H mouse mammary carcinoma by local hyperthermia.British Journal of Cancer,38, 561–563.

    Google Scholar 

  155. Weiss, L., andHolyoke, E. D., 1943, Some effects of hypervitaminosis A on metastasis of spontaneous breast cancer in mice.Journal of National Cancer Institute,43, 1045–1054.

    Google Scholar 

  156. Weiss, L., Orr, F., andHonn, K., 1988, Interactions of cancer cells with the microvasculature during metastasis.FASEB Journal,2, 12–21.

    Google Scholar 

  157. Wexler, H., Chretien, P. B., Ketcham, A. S., andSindelar, W. F., 1975, Induction of pulmonary metastases in both immune and nonimmune mice: effect of the removal of a transplanted primary tumor.Cancer,36, 2042–2047.

    Google Scholar 

  158. Withers, H. R., andMilas, L., 1973, Influence of preirradiation of lung on development of artificial pulmonary metastases of fibrosarcoma in mice.Cancer Research,33, 1931–1936.

    Google Scholar 

  159. Wood, J. S., Holyoke, E. D., Clason, W. P. C., Sommers, S. C., andWarren, S., 1954, An experimental study of the relationship between tumor size and number of lung metastases.Cancer,7, 437–443.

    Google Scholar 

  160. Woodruff, M. F. A., 1961, New approaches to the treatment of cancer.Journal of the Royal College of Surgeons (Edinburgh),6, 75–92.

    Google Scholar 

  161. Yamamoto, T., 1936, Experimental study on effect of X-ray on metastasis of malignant tumor, especially in bones.Japanese Journal of Obstetrics and Gynecology,19, 559–569.

    Google Scholar 

  162. Yerushalmi, A., 1976, Influence on metastatic spread of whole body or local tumor hyperthermia.European Journal of Cancer,12, 455–463.

    Google Scholar 

  163. Young, S. D., Marshall, R. S., andHill, 1988, Hypoxia induces DNA overreplication and enhances metastatic potential of murine tumor cells.Proceedings of the National Academy of Sciences, USA,85, 9533–9537.

    Google Scholar 

  164. Zeidman, I., andFidler, I. J., 1970, Effect of irradiation on experimental metastases via lymph and blood streams.Journal of Medicine,1, 9–14.

    Google Scholar 

  165. Zwaan, F. E., Jansen, J., andNoordiijk, E. M., 1980, Graft-versus-host disease limited to area of irradiated skin.Lancet,1, 1081.

    Google Scholar 

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von Essen, C.F. Radiation enhancement of metastasis: a review. Clin Exp Metast 9, 77–104 (1991). https://doi.org/10.1007/BF01756381

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