{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,17]],"date-time":"2026-06-17T02:02:43Z","timestamp":1781661763046,"version":"3.54.5"},"reference-count":41,"publisher":"Springer Science and Business Media LLC","issue":"6","license":[{"start":{"date-parts":[[2003,6,1]],"date-time":"2003-06-01T00:00:00Z","timestamp":1054425600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nat Rev Cancer"],"published-print":{"date-parts":[[2003,6]]},"DOI":"10.1038\/nrc1098","type":"journal-article","created":{"date-parts":[[2003,5,30]],"date-time":"2003-05-30T18:07:33Z","timestamp":1054318053000},"page":"453-458","source":"Crossref","is-referenced-by-count":3723,"title":["The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited"],"prefix":"10.1038","volume":"3","author":[{"given":"Isaiah J.","family":"Fidler","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","reference":[{"key":"BFnrc1098_CR1","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1023\/A:1010646304844","volume":"19","author":"L Weiss","year":"2000","unstructured":"Weiss, L. Metastasis of cancer: a conceptual history from antiquity to the 1990s. Cancer Metastasis Rev. 19, 193\u2013400 (2000).","journal-title":"Cancer Metastasis Rev."},{"key":"BFnrc1098_CR2","doi-asserted-by":"publisher","first-page":"571","DOI":"10.1016\/S0140-6736(00)49915-0","volume":"1","author":"S Paget","year":"1889","unstructured":"Paget, S. The distribution of secondary growths in cancer of the breast. Lancet 1, 571\u2013573 (1889).","journal-title":"Lancet"},{"key":"BFnrc1098_CR3","volume-title":"Neoplastic Diseases","author":"J Ewing","year":"1928","unstructured":"Ewing, J. Neoplastic Diseases edn 6 (W. B. Saunders, Philadelphia, 1928)."},{"key":"BFnrc1098_CR4","first-page":"2281","volume":"40","author":"IR Hart","year":"1980","unstructured":"Hart, I. R. & Fidler, I. J. Role of organ selectivity in the determination of metastatic patterns of the B16 melanoma. Cancer Res. 40, 2281\u20132287 (1980).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR5","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0147-0272(79)80008-2","volume":"3","author":"EV Sugarbaker","year":"1979","unstructured":"Sugarbaker, E. V. Cancer metastasis: a product of tumour-host interactions. Curr. Probl. Cancer 3, 1\u201359 (1979).","journal-title":"Curr. Probl. Cancer"},{"key":"BFnrc1098_CR6","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1038\/283139a0","volume":"283","author":"G Poste","year":"1979","unstructured":"Poste, G. & Fidler, I. J. The pathogenesis of cancer metastasis. Nature 283, 139\u2013146 (1979).","journal-title":"Nature"},{"key":"BFnrc1098_CR7","doi-asserted-by":"publisher","first-page":"498","DOI":"10.1046\/j.1432-0436.2002.700904.x","volume":"70","author":"IJ Fidler","year":"2002","unstructured":"Fidler, I. J. The organ microenvironment and cancer metastasis. Differentiation 70, 498\u2013505 (2002).","journal-title":"Differentiation"},{"key":"BFnrc1098_CR8","first-page":"648","volume":"11","author":"DR Coman","year":"1951","unstructured":"Coman, D. R., de Long, R. P. & McCutcheon, M. Studies on the mechanism of metastasis: the distribution of tumours in various organs in relation to the distribution of arterial emboli. Cancer Res. 11, 648\u2013654 (1951).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR9","first-page":"734","volume":"12","author":"B Lucke","year":"1952","unstructured":"Lucke, B. et al. Differential growth of metastatic tumours in liver and lung: experiments with rabbit V2 carcinoma. Cancer Res. 12, 734\u2013738 (1952).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR10","first-page":"357","volume":"10","author":"I Zeidman","year":"1950","unstructured":"Zeidman, I., McCutcheon, M. & Coman, D. R. Factors affecting the number of tumour metastases, experiments with a transplantable mouse tumour. Cancer Res. 10, 357\u2013364 (1950).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR11","first-page":"731","volume":"12","author":"I Zeidman","year":"1952","unstructured":"Zeidman, I. & Buss, J. M. Transpulmonary passage of tumour cell emboli. Cancer Res. 12, 731\u2013737 (1952).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR12","first-page":"321","volume":"83","author":"ER Fisher","year":"1967","unstructured":"Fisher, E. R. & Fisher B. Recent observations on concepts of metastasis. Arch. Pathol. 83, 321\u2013324 (1967).","journal-title":"Arch. Pathol."},{"key":"BFnrc1098_CR13","first-page":"157","volume":"17","author":"I Zeidman","year":"1957","unstructured":"Zeidman, I. Metastasis: a review of recent advances. Cancer Res. 17, 157\u2013164 (1957).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR14","first-page":"412","volume":"27","author":"B Fisher","year":"1967","unstructured":"Fisher, B. & Fisher, E. R. The organ distribution of disseminated 51Cr-labeled tumour cells. Cancer Res. 27, 412\u2013419 (1967).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR15","first-page":"773","volume":"45","author":"IJ Fidler","year":"1970","unstructured":"Fidler, I. J. Metastasis: quantitative analysis of distribution and fate of tumour emboli labeled with 125I-5-iodo-2\u2032-deoxyuridine. J. Natl Cancer Inst. 45, 773\u2013782 (1970).","journal-title":"J. Natl Cancer Inst."},{"key":"BFnrc1098_CR16","first-page":"1","volume":"3","author":"L Weiss","year":"1986","unstructured":"Weiss, L. Metastatic inefficiency: causes and consequences. Cancer Metastasis Rev. 3, 1\u201324 (1986).","journal-title":"Cancer Metastasis Rev."},{"key":"BFnrc1098_CR17","first-page":"6130","volume":"50","author":"IJ Fidler","year":"1990","unstructured":"Fidler, I. J. Critical factors in the biology of human cancer metastasis: twenty-eighth G.H.A. Clowes memorial award lecture. Cancer Res. 50, 6130\u20136138 (1990).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR18","first-page":"2259","volume":"44","author":"G Heppner","year":"1984","unstructured":"Heppner, G. Tumour heterogeneity. Cancer Res. 44, 2259\u20132265 (1984).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR19","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1007\/BF00047691","volume":"3","author":"GL Nicolson","year":"1984","unstructured":"Nicolson, G. L. Generation of phenotypic diversity and progression in metastatic tumour cells. Cancer Metastasis Rev. 3, 25\u201342 (1984).","journal-title":"Cancer Metastasis Rev."},{"key":"BFnrc1098_CR20","first-page":"327","volume":"14","author":"L Foulds","year":"1954","unstructured":"Foulds, L. The experimental study of tumour progression. Cancer Res. 14, 327\u2013339 (1954).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR21","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1126\/science.959840","volume":"194","author":"PC Nowell","year":"1976","unstructured":"Nowell, P. C. The clonal evolution of tumour cell populations. Science 194, 23\u201328 (1976).","journal-title":"Science"},{"key":"BFnrc1098_CR22","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1093\/genetics\/28.6.491","volume":"28","author":"SE Luria","year":"1943","unstructured":"Luria, S. E. & Delbruck, M. Mutations of bacteria from virus sensitive to virus resistance. Genetics 28, 491\u2013511 (1943).","journal-title":"Genetics"},{"key":"BFnrc1098_CR23","doi-asserted-by":"publisher","first-page":"6949","DOI":"10.1073\/pnas.78.11.6949","volume":"78","author":"MA Cifone","year":"1981","unstructured":"Cifone, M. A. & Fidler, I. J. Increasing metastatic potential is associated with increasing genetic instability of clones isolated from murine neoplasms. Proc. Natl Acad. Sci. USA 78, 6949\u20136952 (1981).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnrc1098_CR24","first-page":"87","volume":"2","author":"IR Hart","year":"1991","unstructured":"Hart, I. R. & Easty, D. Tumour cell progression and differentiation in metastasis. Semin. Cancer Biol. 2, 87\u201397 (1991).","journal-title":"Semin. Cancer Biol."},{"key":"BFnrc1098_CR25","first-page":"148","volume":"242","author":"IJ Fidler","year":"1973","unstructured":"Fidler, I. J. Selection of successive tumour lines for metastasis. Nature 242, 148\u2013149 (1973).","journal-title":"Nature"},{"key":"BFnrc1098_CR26","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1007\/BF00048224","volume":"1","author":"G Poste","year":"1982","unstructured":"Poste, G. Experimental systems for analysis of the malignant phenotype. Cancer Metastasis Rev. 1, 141\u2013200 (1982).","journal-title":"Cancer Metastasis Rev."},{"key":"BFnrc1098_CR27","first-page":"175","volume":"948","author":"GL Nicolson","year":"1988","unstructured":"Nicolson, G. L. Cancer metastasis: tumour cell and host organ properties important in metastasis to specific secondary sites. Biochem. Biophys. Acta 948, 175\u2013224 (1988).","journal-title":"Biochem. Biophys. Acta"},{"key":"BFnrc1098_CR28","doi-asserted-by":"publisher","first-page":"893","DOI":"10.1126\/science.887927","volume":"197","author":"IJ Fidler","year":"1977","unstructured":"Fidler, I. J. & Kripke, M. L. Metastasis results from pre-existing variant cells within a malignant tumour. Science 197, 893\u2013895 (1977).","journal-title":"Science"},{"key":"BFnrc1098_CR29","first-page":"947","volume":"67","author":"IJ Fidler","year":"1981","unstructured":"Fidler, I. J. et al. Demonstration of multiple phenotype diversity in a murine melanoma of recent origin. J. Natl Cancer Inst. 67, 947\u2013956 (1981).","journal-title":"J. Natl Cancer Inst."},{"key":"BFnrc1098_CR30","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1093\/jnci\/72.1.93","volume":"72","author":"RS Kerbel","year":"1984","unstructured":"Kerbel, R. S., Man, M. S. & Dexter, D. A model of human cancer metastasis: extensive spontaneous and artificial metastasis of a human pigmented melanoma and derived variant sublines in nude mice. J. Natl Cancer Inst. 72, 93\u2013108 (1984).","journal-title":"J. Natl Cancer Inst."},{"key":"BFnrc1098_CR31","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1126\/science.6953592","volume":"217","author":"JE Talmadge","year":"1982","unstructured":"Talmadge, J. E., Wolman, S. R. & Fidler, I. J. Evidence for the clonal origin of spontaneous metastasis. Science 217, 361\u2013363 (1982).","journal-title":"Science"},{"key":"BFnrc1098_CR32","first-page":"5167","volume":"46","author":"IJ Fidler","year":"1986","unstructured":"Fidler, I. J. & Talmadge, J. E. Evidence that intravenously derived murine pulmonary melanoma metastases can originate from the expansion of a single tumour cell. Cancer Res. 46, 5167\u20135171 (1986).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR33","doi-asserted-by":"publisher","first-page":"749","DOI":"10.1136\/bmj.288.6419.749","volume":"288","author":"D Tarin","year":"1984","unstructured":"Tarin, D. et al. Clinicopathological observations on metastasis in man studied in patients treated with peritoneovenous shunts. BMJ 288, 749\u2013751 (1984).","journal-title":"BMJ"},{"key":"BFnrc1098_CR34","first-page":"3584","volume":"44","author":"D Tarin","year":"1984","unstructured":"Tarin, D. et al. Mechanisms of human tumour metastasis studied in patients with peritoneovenous shunts. Cancer Res. 44, 3584\u20133592 (1984).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR35","first-page":"3478","volume":"48","author":"G Schackert","year":"1988","unstructured":"Schackert, G. & Fidler, I. J. Site-specific metastasis of mouse melanomas and a fibrosarcoma in the brain or the meninges of syngeneic animals. Cancer Res. 48, 3478\u20133484 (1988).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR36","doi-asserted-by":"publisher","first-page":"272","DOI":"10.1016\/S0168-9525(98)01489-9","volume":"14","author":"NL Simone","year":"1998","unstructured":"Simone, N. L. et al. Laser capture microdissection: opening the microscopic frontier to molecular analysis. Trends Genet. 14, 272\u2013276 (1998).","journal-title":"Trends Genet."},{"key":"BFnrc1098_CR37","doi-asserted-by":"publisher","first-page":"364","DOI":"10.1038\/380364a0","volume":"380","author":"R Pasqualini","year":"1996","unstructured":"Pasqualini, R. & Ruoslahti, E. Organ targeting in vivo using phage display peptide libraries. Nature 380, 364\u2013366 (1996).","journal-title":"Nature"},{"key":"BFnrc1098_CR38","doi-asserted-by":"publisher","first-page":"458","DOI":"10.1093\/jnci\/95.6.458","volume":"95","author":"H Uehara","year":"2003","unstructured":"Uehara, H. et al. Effects of blocking platelet-derived growth factor-receptor signaling in a mouse model of experimental prostate cancer bone metastases.. J. Natl Cancer Inst. 95, 458\u2013470 (2003).","journal-title":"J. Natl Cancer Inst."},{"key":"BFnrc1098_CR39","first-page":"467","volume":"46","author":"J Folkman","year":"1986","unstructured":"Folkman, J. How is blood vessel growth regulated in normal and neoplastic tissue? G.H.A. Clowes memorial award lecture. Cancer Res. 46, 467\u2013743 (1986).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR40","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0065-230X(08)60034-2","volume":"46","author":"LA Liotta","year":"1986","unstructured":"Liotta, L. A. Tumour invasion and metastasis \u2014 role of the extracellular matrix: Rhoads memorial award lecture. Cancer Res. 46, 1\u20137 (1986).","journal-title":"Cancer Res."},{"key":"BFnrc1098_CR41","first-page":"791","volume":"122","author":"B Fisher","year":"1966","unstructured":"Fisher, B. & Fisher, E. R. The interrelationship of hematogenous and lymphatic tumour cell dissemination. Surg. Gynecol. Obstet. 122, 791\u2013797 (1966).","journal-title":"Surg. Gynecol. Obstet."}],"container-title":["Nature Reviews Cancer"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/nrc1098.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/nrc1098","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/nrc1098.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,19]],"date-time":"2023-05-19T00:25:29Z","timestamp":1684455929000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/nrc1098"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2003,6]]},"references-count":41,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2003,6]]}},"alternative-id":["BFnrc1098"],"URL":"https:\/\/doi.org\/10.1038\/nrc1098","relation":{},"ISSN":["1474-175X","1474-1768"],"issn-type":[{"value":"1474-175X","type":"print"},{"value":"1474-1768","type":"electronic"}],"subject":[],"published":{"date-parts":[[2003,6]]}}}