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True local recurrences do not metastasize

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Abstract

Generally, the limits of local tumor control are in part connected with the term “field cancerization” and are known from oral, lung, prostate, or mammary cancer. With the example of breast cancer (BC), the problem of ipsilateral breast tumor recurrences (IBTR) after breast-conserving surgery will be reviewed. Three types of local recurrences are distinguished: true recurrences, new primaries, or residual tumors. Good data for BC allow the description of the time-dependent risk of these three types, relative to the diagnosis of the primary tumor, because the time of initiation and the growth duration of the IBTR can be estimated. Two hypotheses explain the data: first, local recurrences may be initiated years before the diagnosis of a primary tumor (PT) and can then appear as multifocal PT at diagnosis, and second, true local recurrences probably do not metastasize. The generalizability of these hypotheses for other tumors will be discussed.

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Abbreviations

BCS:

breast-conserving surgery

IBTR:

ipsilateral breast tumor recurrence

LR:

local recurrence

MET:

(distant) metastasization

NP:

new primary

PT:

primary (breast) tumor

RT:

residual tumor

TC(D):

tumor cell (dissemination)

TR:

true recurrence

References

  1. Benson, J. R., Jatoi, I., Keisch, M., Esteva, F. J., Makris, A., & Jordan, V. C. (2009). Early breast cancer. Lancet, 373(9673), 1463–1479. doi:10.1016/S0140-6736(09)60316-0.

    Article  PubMed  Google Scholar 

  2. Early Breast Cancer Trialists’ Collaborative Group. (2005). Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: An overview of the randomised trials. Lancet, 366(9503), 2087–2106.

    Google Scholar 

  3. Freedman, G. M., Anderson, P. R., Hanlon, A. L., Eisenberg, D. F., & Nicolaou, N. (2005). Pattern of local recurrence after conservative surgery and whole-breast irradiation. International Journal of Radiation Oncology, Biology, Physics, 61(5), 1328–1336.

    Article  PubMed  Google Scholar 

  4. Engel, J., Eckel, R., Aydemir, U., Aydemir, S., Kerr, J., Schlesinger-Raab, A., et al. (2003). Determinants and prognoses of locoregional and distant progression in breast cancer. International Journal of Radiation Oncology, Biology, Physics, 55(5), 1186–1195. doi:S0360301602044760.

    Article  PubMed  Google Scholar 

  5. Voogd, A. C., van Oost, F. J., Rutgers, E. J., Elkhuizen, P. H., van Geel, A. N., Scheijmans, L. J., et al. (2005). Long-term prognosis of patients with local recurrence after conservative surgery and radiotherapy for early breast cancer. European Journal of Cancer, 41(17), 2637–2644.

    Article  PubMed  CAS  Google Scholar 

  6. Munich Cancer Registry. (2011). Available from: http://www.Tumorregister-muenchen.De/facts/specific_analysis.Php.

  7. Hölzel, D., Eckel, R., Emeny, R., & Engel, J. (2010). Distant metastases do not metastasize. Cancer and Metastasis Reviews. doi:10.1007/s10555-010-9260-1.

    PubMed  Google Scholar 

  8. Recht, A., Silver, B., Schnitt, S., Connolly, J., Hellman, S., & Harris, J. R. (1985). Breast relapse following primary radiation therapy for early breast cancer. I. Classification, frequency and salvage. International Journal of Radiation Oncology, Biology, Physics, 11(7), 1271–1276.

    Article  PubMed  CAS  Google Scholar 

  9. Haffty, B. G., Carter, D., Flynn, S. D., Fischer, D. B., Brash, D. E., Simons, J., et al. (1993). Local recurrence versus new primary: Clinical analysis of 82 breast relapses and potential applications for genetic fingerprinting. International Journal of Radiation Oncology, Biology, Physics, 27(3), 575–583.

    Article  PubMed  CAS  Google Scholar 

  10. Komoike, Y., Akiyama, F., Iino, Y., Ikeda, T., Tanaka-Akashi, S., Ohsumi, S., et al. (2005). Analysis of ipsilateral breast tumor recurrences after breast-conserving treatment based on the classification of true recurrences and new primary tumors. Breast Cancer, 12(2), 104–111.

    Article  PubMed  Google Scholar 

  11. Smith, T. E., Lee, D., Turner, B. C., Carter, D., & Haffty, B. G. (2000). True recurrence vs. new primary ipsilateral breast tumor relapse: an analysis of clinical and pathologic differences and their implications in natural history, prognoses, and therapeutic management. International Journal of Radiation Oncology, Biology, Physics, 48(5), 1281–1289.

    Article  PubMed  CAS  Google Scholar 

  12. Goldstein, N. S., Vicini, F. A., Hunter, S., Odish, E., Forbes, S., & Kestin, L. L. (2005). Molecular clonality relationships in initial carcinomas, ipsilateral breast failures, and distant metastases in patients treated with breast-conserving therapy: Evidence suggesting that some distant metastases are derived from ipsilateral breast failures and that metastases can metastasize. American Journal of Clinical Pathology, 124(1), 49–57. doi:10.1309/2GAMH08G25JXVWHQ.

    Article  PubMed  CAS  Google Scholar 

  13. Noguchi, S., Aihara, T., Koyama, H., Motomura, K., Inaji, H., & Imaoka, S. (1994). Discrimination between multicentric and multifocal carcinomas of the breast through clonal analysis. Cancer, 74(3), 872–877.

    Article  PubMed  CAS  Google Scholar 

  14. Kreike, B., Hart, A. A., van de Velde, T., Borger, J., Peterse, H., Rutgers, E., et al. (2008). Continuing risk of ipsilateral breast relapse after breast-conserving therapy at long-term follow-up. International Journal of Radiation Oncology, Biology, Physics, 71(4), 1014–1021. doi:10.1016/j.ijrobp.2007.11.029.

    Article  PubMed  Google Scholar 

  15. Fisher, B., Anderson, S., Fisher, E. R., Redmond, C., Wickerham, D. L., Wolmark, N., et al. (1991). Significance of ipsilateral breast tumour recurrence after lumpectomy. Lancet, 338(8763), 327–331.

    Article  PubMed  CAS  Google Scholar 

  16. Middleton, L. P., Vlastos, G., Mirza, N. Q., Eva, S., & Sahin, A. A. (2002). Multicentric mammary carcinoma: Evidence of monoclonal proliferation. Cancer, 94(7), 1910–1916. doi:10.1002/cncr.10452.

    Article  PubMed  Google Scholar 

  17. Cabioglu, N., Ozmen, V., Kaya, H., Tuzlali, S., Igci, A., Muslumanoglu, M., et al. (2009). Increased lymph node positivity in multifocal and multicentric breast cancer. Journal of the American College of Surgeons, 208(1), 67–74. doi:10.1016/j.jamcollsurg.2008.09.001.

    Article  PubMed  Google Scholar 

  18. Coombs, N. J., & Boyages, J. (2005). Multifocal and multicentric breast cancer: Does each focus matter? Journal of Clinical Oncology, 23(30), 7497–7502.

    Article  PubMed  Google Scholar 

  19. Andea, A. A., Bouwman, D., Wallis, T., & Visscher, D. W. (2004). Correlation of tumor volume and surface area with lymph node status in patients with multifocal/multicentric breast carcinoma. Cancer, 100(1), 20–27. doi:10.1002/cncr.11880.

    Article  PubMed  Google Scholar 

  20. Veronesi, U., Gatti, G., Luini, A., Intra, M., Ciocca, M., Sanchez, D., et al. (2003). Full-dose intraoperative radiotherapy with electrons during breast-conserving surgery. Archives of Surgery, 138(11), 1253–1256.

    Article  PubMed  Google Scholar 

  21. Bernier, J., Viale, G., Orecchia, R., Ballardini, B., Richetti, A., Bronz, L., et al. (2006). Partial irradiation of the breast: old challenges, new solutions. Breast, 15(4), 466–475.

    Article  PubMed  CAS  Google Scholar 

  22. Vaidya, J. S., Joseph, D. J., Tobias, J. S., Bulsara, M., Wenz, F., Saunders, C., et al. (2010). Targeted intraoperative radiotherapy versus whole breast radiotherapy for breast cancer (targit-a trial): An international, prospective, randomised, non-inferiority phase 3 trial. Lancet, 376(9735), 91–102.

    Article  PubMed  Google Scholar 

  23. Bartelink, H., Horiot, J. C., Poortmans, P., Struikmans, H., Van den Bogaert, W., Barillot, I., et al. (2001). Recurrence rates after treatment of breast cancer with standard radiotherapy with or without additional radiation. The New England Journal of Medicine, 345(19), 1378–1387.

    Article  PubMed  CAS  Google Scholar 

  24. Holland, R., Veling, S. H., Mravunac, M., & Hendriks, J. H. (1985). Histologic multifocality of tis, t1-2 breast carcinomas. Implications for clinical trials of breast-conserving surgery. Cancer, 56(5), 979–990.

    Article  PubMed  CAS  Google Scholar 

  25. Recht, A., Silen, W., Schnitt, S. J., Connolly, J. L., Gelman, R. S., Rose, M. A., et al. (1988). Time-course of local recurrence following conservative surgery and radiotherapy for early stage breast cancer. International Journal of Radiation Oncology, Biology, Physics, 15(2), 255–261.

    Article  PubMed  CAS  Google Scholar 

  26. Kurtz, J. M., Amalric, R., Brandone, H., Ayme, Y., & Spitalier, J. M. (1989). Local recurrence after breast-conserving surgery and radiotherapy. Helvetica Chirurgica Acta, 55(6), 837–842.

    PubMed  CAS  Google Scholar 

  27. Wise, A. M., Stamey, T. A., McNeal, J. E., & Clayton, J. L. (2002). Morphologic and clinical significance of multifocal prostate cancers in radical prostatectomy specimens. Urology, 60(2), 264–269. doi:S0090429502017284.

    Article  PubMed  Google Scholar 

  28. Flieder, D. B., Vazquez, M., Carter, D., Brambilla, E., Gazdar, A., Noguchi, M., et al. (2006). Pathologic findings of lung tumors diagnosed on baseline CT screening. The American Journal of Surgical Pathology, 30(5), 606–613. doi:10.1097/01.pas.0000202040.51967.d0.

    Article  PubMed  Google Scholar 

  29. Holland, R., Connolly, J. L., Gelman, R., Mravunac, M., Hendriks, J. H., Verbeek, A. L., et al. (1990). The presence of an extensive intraductal component following a limited excision correlates with prominent residual disease in the remainder of the breast. Journal of Clinical Oncology, 8(1), 113–118.

    PubMed  CAS  Google Scholar 

  30. Kreike, B., Halfwerk, H., Armstrong, N., Bult, P., Foekens, J. A., Veltkamp, S. C., et al. (2009). Local recurrence after breast-conserving therapy in relation to gene expression patterns in a large series of patients. Clinical Cancer Research, 15(12), 4181–4190. doi:1078-0432.CCR-08-2644.

    Article  PubMed  CAS  Google Scholar 

  31. Voogd, A. C., Peterse, J. L., Crommelin, M. A., Rutgers, E. J., Botke, G., Elkhuizen, P. H., et al. (1999). Histological determinants for different types of local recurrence after breast-conserving therapy of invasive breast cancer. Dutch Study Group on Local Recurrence After Breast Conservation (BORST). European Journal of Cancer, 35(13), 1828–1837.

    Article  PubMed  CAS  Google Scholar 

  32. Fredriksson, I., Liljegren, G., Palm-Sjovall, M., Arnesson, L. G., Emdin, S. O., Fornander, T., et al. (2003). Risk factors for local recurrence after breast-conserving surgery. The British Journal of Surgery, 90(9), 1093–1102. doi:10.1002/bjs.4206.

    Article  PubMed  CAS  Google Scholar 

  33. Hill-Kayser, C. E., Harris, E. E., Hwang, W. T., & Solin, L. J. (2006). Twenty-year incidence and patterns of contralateral breast cancer after breast conservation treatment with radiation. International Journal of Radiation Oncology, Biology, Physics, 66(5), 1313–1319.

    Article  PubMed  Google Scholar 

  34. Oh, J. L., Dryden, M. J., Woodward, W. A., Yu, T. K., Tereffe, W., Strom, E. A., et al. (2006). Locoregional control of clinically diagnosed multifocal or multicentric breast cancer after neoadjuvant chemotherapy and locoregional therapy. Journal of Clinical Oncology, 24(31), 4971–4975.

    Article  PubMed  Google Scholar 

  35. Gentilini, O., Botteri, E., Rotmensz, N., Da Lima, L., Caliskan, M., Garcia-Etienne, C. A., et al. (2009). Conservative surgery in patients with multifocal/multicentric breast cancer. Breast Cancer Research and Treatment, 113(3), 577–583. doi:10.1007/s10549-008-9959-7.

    Article  PubMed  Google Scholar 

  36. Houssami, N., Ciatto, S., Macaskill, P., Lord, S. J., Warren, R. M., Dixon, J. M., et al. (2008). Accuracy and surgical impact of magnetic resonance imaging in breast cancer staging: systematic review and meta-analysis in detection of multifocal and multicentric cancer. Journal of Clinical Oncology, 26(19), 3248–3258.

    Article  PubMed  Google Scholar 

  37. Lehman, C. D., Gatsonis, C., Kuhl, C. K., Hendrick, R. E., Pisano, E. D., Hanna, L., et al. (2007). Mri evaluation of the contralateral breast in women with recently diagnosed breast cancer. The New England Journal of Medicine, 356(13), 1295–1303. doi:NEJMoa065447.

    Article  PubMed  CAS  Google Scholar 

  38. Sardanelli, F., Giuseppetti, G. M., Panizza, P., Bazzocchi, M., Fausto, A., Simonetti, G., et al. (2004). Sensitivity of mri versus mammography for detecting foci of multifocal, multicentric breast cancer in fatty and dense breasts using the whole-breast pathologic examination as a gold standard. AJR. American Journal of Roentgenology, 183(4), 1149–1157.

    PubMed  Google Scholar 

  39. Peer, P. G., van Dijck, J. A., Hendriks, J. H., Holland, R., & Verbeek, A. L. (1993). Age-dependent growth rate of primary breast cancer. Cancer, 71(11), 3547–3551.

    Article  PubMed  CAS  Google Scholar 

  40. Kuroishi, T., Tominaga, S., Morimoto, T., Tashiro, H., Itoh, S., Watanabe, H., et al. (1990). Tumor growth rate and prognosis of breast cancer mainly detected by mass screening. Japanese Journal of Cancer Research, 81(5), 454–462.

    PubMed  CAS  Google Scholar 

  41. Fisher, B., Anderson, S., Bryant, J., Margolese, R. G., Deutsch, M., Fisher, E. R., et al. (2002). Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. The New England Journal of Medicine, 347(16), 1233–1241. doi:10.1056/NEJMoa022152.

    Article  PubMed  Google Scholar 

  42. Husemann, Y., Geigl, J. B., Schubert, F., Musiani, P., Meyer, M., Burghart, E., et al. (2008). Systemic spread is an early step in breast cancer. Cancer Cell, 13(1), 58–68. doi:S1535-6108(07)00372-8.

    Article  PubMed  CAS  Google Scholar 

  43. Klein, C. A., & Hölzel, D. (2006). Systemic cancer progression and tumor dormancy: mathematical models meet single cell genomics. Cell Cycle, 5(16), 1788–1798. doi:3097.

    Article  PubMed  CAS  Google Scholar 

  44. Engel, J., Eckel, R., Kerr, J., Schmidt, M., Furstenberger, G., Richter, R., et al. (2003). The process of metastasisation for breast cancer. European Journal of Cancer, 39(12), 1794–1806. doi:S0959804903004222.

    Article  PubMed  CAS  Google Scholar 

  45. Fisher, B., & Anderson, S. J. (2010). The breast cancer alternative hypothesis: Is there evidence to justify replacing it? Journal of Clinical Oncology, 28(3), 366–374. doi:JCO.2009.26.8292.

    Article  PubMed  Google Scholar 

  46. Demicheli, R., Terenziani, M., & Bonadonna, G. (1998). Estimate of tumor growth time for breast cancer local recurrences: Rapid growth after wake-up? Breast Cancer Research and Treatment, 51(2), 133–137.

    Article  PubMed  CAS  Google Scholar 

  47. Naumov, G. N., Akslen, L. A., & Folkman, J. (2006). Role of angiogenesis in human tumor dormancy: Animal models of the angiogenic switch. Cell Cycle, 5(16), 1779–1787. doi:3018.

    Article  PubMed  CAS  Google Scholar 

  48. Komoike, Y., Akiyama, F., Iino, Y., Ikeda, T., Akashi-Tanaka, S., Ohsumi, S., et al. (2006). Ipsilateral breast tumor recurrence (ibtr) after breast-conserving treatment for early breast cancer: Risk factors and impact on distant metastases. Cancer, 106(1), 35–41. doi:10.1002/cncr.21551.

    Article  PubMed  Google Scholar 

  49. Zahl, P. H., Maehlen, J., & Welch, H. G. (2008). The natural history of invasive breast cancers detected by screening mammography. Archives of Internal Medicine, 168(21), 2311–2316. doi:168/21/2311.

    Article  PubMed  Google Scholar 

  50. Bories, N., Dalle, S., Debarbieux, S., Balme, B., Ronger-Savle, S., & Thomas, L. (2008). Dermoscopy of fully regressive cutaneous melanoma. The British Journal of Dermatology, 158(6), 1224–1229. doi:BJD8501.

    Article  PubMed  CAS  Google Scholar 

  51. Chlebowski, R. T., Kuller, L. H., Prentice, R. L., Stefanick, M. L., Manson, J. E., Gass, M., et al. (2009). Breast cancer after use of estrogen plus progestin in postmenopausal women. The New England Journal of Medicine, 360(6), 573–587. doi:360/6/573.

    Article  PubMed  CAS  Google Scholar 

  52. Perry, N., Broeders, M., de Wolf, C., Tornberg, S., Holland, R., & von Karsa, L. (2008). European guidelines for quality assurance in breast cancer screening and diagnosis. Fourth edition—summary document. Annals of Oncology, 19(4), 614–622. doi:mdm481.

    Article  PubMed  CAS  Google Scholar 

  53. Jorgensen, K. J., & Gotzsche, P. C. (2009). Overdiagnosis in publicly organised mammography screening programmes: Systematic review of incidence trends. British Medical Journal, 339, b2587.

    Article  PubMed  Google Scholar 

  54. Bear, H. D., Anderson, S., Brown, A., Smith, R., Mamounas, E. P., Fisher, B., et al. (2003). The effect on tumor response of adding sequential preoperative docetaxel to preoperative doxorubicin and cyclophosphamide: Preliminary results from national surgical adjuvant breast and bowel project protocol b-27. Journal of Clinical Oncology, 21(22), 4165–4174. doi:10.1200/JCO.2003.12.005.

    Article  PubMed  CAS  Google Scholar 

  55. Rastogi, P., Anderson, S. J., Bear, H. D., Geyer, C. E., Kahlenberg, M. S., Robidoux, A., et al. (2008). Preoperative chemotherapy: Updates of national surgical adjuvant breast and bowel project protocols b-18 and b-27. Journal of Clinical Oncology, 26(5), 778–785. doi:26/5/778.

    Article  PubMed  Google Scholar 

  56. Phillips, T. M., McBride, W. H., & Pajonk, F. (2006). The response of cd24(−/low)/cd44+ breast cancer-initiating cells to radiation. Journal of the National Cancer Institute, 98(24), 1777–1785. doi:98/24/1777.

    Article  PubMed  Google Scholar 

  57. Joergensen, L. E., Gunnarsdottir, K. A., Lanng, C., Moeller, S., & Rasmussen, B. B. (2008). Multifocality as a prognostic factor in breast cancer patients registered in Danish Breast Cancer Cooperative Group (DBCG) 1996–2001. Breast, 17(6), 587–591. doi:S0960-9776(08)00153-7.

    Article  PubMed  CAS  Google Scholar 

  58. Yerushalmi, R., Kennecke, H., Woods, R., Olivotto, I. A., Speers, C., & Gelmon, K. A. (2008). Does multicentric/multifocal breast cancer differ from unifocal breast cancer? An analysis of survival and contralateral breast cancer incidence. Breast Cancer Research and Treatment. doi:10.1007/s10549-008-0265-1.

    PubMed  Google Scholar 

  59. Veronesi, U., Cascinelli, N., Mariani, L., Greco, M., Saccozzi, R., Luini, A., et al. (2002). Twenty-year follow-up of a randomized study comparing breast-conserving surgery with radical mastectomy for early breast cancer. The New England Journal of Medicine, 347(16), 1227–1232. doi:10.1056/NEJMoa020989.

    Article  PubMed  Google Scholar 

  60. van Dongen, J. A., Voogd, A. C., Fentiman, I. S., Legrand, C., Sylvester, R. J., Tong, D., et al. (2000). Long-term results of a randomized trial comparing breast-conserving therapy with mastectomy: European Organization for Research and Treatment of Cancer 10801 trial. Journal of the National Cancer Institute, 92(14), 1143–1150.

    Article  PubMed  Google Scholar 

  61. Sobin, L., Gospodarowicz, M., & Wittekind, C. (Eds.). (2009). UICC: TNM classification of malignant tumors (7th ed.). UK: Wiley-Blackwell.

    Google Scholar 

  62. Anderson, S. J., Wapnir, I., Dignam, J. J., Fisher, B., Mamounas, E. P., Jeong, J. H., et al. (2009). Prognosis after ipsilateral breast tumor recurrence and locoregional recurrences in patients treated by breast-conserving therapy in five national surgical adjuvant breast and bowel project protocols of node-negative breast cancer. Journal of Clinical Oncology, 27(15), 2466–2473. doi:JCO.2008.19.8424.

    Article  PubMed  Google Scholar 

  63. de Bock, G. H., van der Hage, J. A., Putter, H., Bonnema, J., Bartelink, H., & van de Velde, C. J. (2006). Isolated loco-regional recurrence of breast cancer is more common in young patients and following breast conserving therapy: Long-term results of European Organisation for Research and Treatment of Cancer Studies. European Journal of Cancer, 42(3), 351–356. doi:S0959-8049(05)00893-2.

    Article  PubMed  Google Scholar 

  64. Jones, H. A., Antonini, N., Hart, A. A., Peterse, J. L., Horiot, J. C., Collin, F., et al. (2009). Impact of pathological characteristics on local relapse after breast-conserving therapy: A subgroup analysis of the EORTC boost versus no boost trial. Journal of Clinical Oncology. doi:JCO.2008.21.5764.

    Google Scholar 

  65. Vicini, F. A., Kestin, L., Huang, R., & Martinez, A. (2003). Does local recurrence affect the rate of distant metastases and survival in patients with early-stage breast carcinoma treated with breast-conserving therapy? Cancer, 97(4), 910–919.

    Article  PubMed  Google Scholar 

  66. de Bock, G. H., Putter, H., Bonnema, J., van der Hage, J. A., Bartelink, H., & van de Velde, C. J. (2009). The impact of loco-regional recurrences on metastatic progression in early-stage breast cancer: A multistate model. Breast Cancer Research and Treatment, 117(2), 401–408. doi:10.1007/s10549-008-0300-2.

    Article  PubMed  CAS  Google Scholar 

  67. Gujral, D. M., Sumo, G., Owen, J. R., Ashton, A., Bliss, J. M., Haviland, J., et al. (2011). Ipsilateral breast tumor relapse: Local recurrence versus new primary tumor and the effect of whole-breast radiotherapy on the rate of new primaries. International Journal of Radiation Oncology, Biology, Physics, 79(1), 19–25.

    Article  PubMed  Google Scholar 

  68. Vicini, F. A., Antonucci, J. V., Wallace, M., Gilbert, S., Goldstein, N. S., Kestin, L., et al. (2007). Long-term efficacy and patterns of failure after accelerated partial breast irradiation: A molecular assay-based clonality evaluation. International Journal of Radiation Oncology, Biology, Physics, 68(2), 341–346. doi:S0360-3016(06)03636-4.

    Article  PubMed  Google Scholar 

  69. Whipp, E., Beresford, M., Sawyer, E., & Halliwell, M. (2010). True local recurrence rate in the conserved breast after magnetic resonance imaging-targeted radiotherapy. International Journal of Radiation Oncology, Biology, Physics, 76(4), 984–990.

    Article  PubMed  Google Scholar 

  70. Wapnir, I. L., Anderson, S. J., Mamounas, E. P., Geyer, C. E., Jr., Jeong, J. H., Tan-Chiu, E., et al. (2006). Prognosis after ipsilateral breast tumor recurrence and locoregional recurrences in five national surgical adjuvant breast and bowel project node-positive adjuvant breast cancer trials. Journal of Clinical Oncology, 24(13), 2028–2037. doi:24/13/2028.

    Article  PubMed  Google Scholar 

  71. Cheng, L., Song, S. Y., Pretlow, T. G., Abdul-Karim, F. W., Kung, H. J., Dawson, D. V., et al. (1998). Evidence of independent origin of multiple tumors from patients with prostate cancer. Journal of the National Cancer Institute, 90(3), 233–237.

    Article  PubMed  CAS  Google Scholar 

  72. Johnson, B. E., Cortazar, P., & Chute, J. P. (1997). Second lung cancers in patients successfully treated for lung cancer. Seminars in Oncology, 24(4), 492–499.

    PubMed  CAS  Google Scholar 

  73. Machens, A., Hauptmann, S., & Dralle, H. (2007). Increased risk of lymph node metastasis in multifocal hereditary and sporadic medullary thyroid cancer. World Journal of Surgery, 31(10), 1960–1965. doi:10.1007/s00268-007-9185-1.

    Article  PubMed  Google Scholar 

  74. Jensen, A. R., Nellemann, H. M., & Overgaard, J. (2007). Tumor progression in waiting time for radiotherapy in head and neck cancer. Radiotherapy and Oncology, 84(1), 5–10. doi:S0167-8140(07)00153-3.

    Article  PubMed  Google Scholar 

  75. Belt, E. J., van Stijn, M. F., Bril, H., de Lange-de Klerk, E. S., Meijer, G. A., Meijer, S., et al. (2010). Lymph node negative colorectal cancers with isolated tumor deposits should be classified and treated as stage III. Annals of Surgical Oncology, 17(12), 3203–3211.

    Article  PubMed  Google Scholar 

  76. Sauer, R., Becker, H., Hohenberger, W., Rodel, C., Wittekind, C., Fietkau, R., et al. (2004). Preoperative versus postoperative chemoradiotherapy for rectal cancer. The New England Journal of Medicine, 351(17), 1731–1740. doi:351/17/1731.

    Article  PubMed  CAS  Google Scholar 

  77. Camma, C., Giunta, M., Fiorica, F., Pagliaro, L., Craxi, A., & Cottone, M. (2000). Preoperative radiotherapy for resectable rectal cancer: A meta-analysis. Journal of the American Medical Association, 284(8), 1008–1015. doi:jma00002.

    Article  PubMed  CAS  Google Scholar 

  78. O’Daly, B. J., Sweeney, K. J., Ridgway, P. F., Quinn, C., McDermott, E. W., O’Higgins, N. J., et al. (2007). The accuracy of combined versus largest diameter in staging multifocal breast cancer. Journal of the American College of Surgeons, 204(2), 282–285.

    Article  PubMed  Google Scholar 

  79. Nagtegaal, I. D., & Quirke, P. (2007). Colorectal tumour deposits in the mesorectum and pericolon; a critical review. Histopathology, 51(2), 141–149. doi:HIS2720.

    Article  PubMed  CAS  Google Scholar 

  80. Tresserra, F., Rodriguez, I., Garcia-Yuste, M., Grases, P. J., Ara, C., & Fabregas, R. (2007). Tumor size and lymph node status in multifocal breast cancer. The Breast Journal, 13(1), 68–71.

    Article  PubMed  Google Scholar 

  81. Slaughter, D. P., Southwick, H. W., & Smejkal, W. (1953). Field cancerization in oral stratified squamous epithelium; clinical implications of multicentric origin. Cancer, 6(5), 963–968.

    Article  PubMed  CAS  Google Scholar 

  82. Braakhuis, B. J., Tabor, M. P., Kummer, J. A., Leemans, C. R., & Brakenhoff, R. H. (2003). A genetic explanation of slaughter’s concept of field cancerization: Evidence and clinical implications. Cancer Research, 63(8), 1727–1730.

    PubMed  CAS  Google Scholar 

  83. Heaphy, C. M., Griffith, J. K., & Bisoffi, M. (2009). Mammary field cancerization: Molecular evidence and clinical importance. Breast Cancer Research and Treatment, 118(2), 229–239. doi:10.1007/s10549-009-0504-0.

    Article  PubMed  Google Scholar 

  84. Dakubo, G. D., Jakupciak, J. P., Birch-Machin, M. A., & Parr, R. L. (2007). Clinical implications and utility of field cancerization. Cancer Cell International, 7, 2. doi:1475-2867-7-2.

    Article  PubMed  Google Scholar 

  85. Utsunomiya, T., Shimada, M., Imura, S., Morine, Y., Ikemoto, T., & Mori, M. (2010). Molecular signatures of noncancerous liver tissue can predict the risk for late recurrence of hepatocellular carcinoma. Journal of Gastroenterology, 45(2), 146–152.

    Article  PubMed  CAS  Google Scholar 

  86. Doll, R., Peto, R., Wheatley, K., Gray, R., & Sutherland, I. (1994). Mortality in relation to smoking: 40 years’ observations on male british doctors. British Medical Journal, 309(6959), 901–911.

    PubMed  CAS  Google Scholar 

  87. Wang, X., Wang, M., MacLennan, G. T., Abdul-Karim, F. W., Eble, J. N., Jones, T. D., et al. (2009). Evidence for common clonal origin of multifocal lung cancers. Journal of the National Cancer Institute, 101(8), 560–570. doi:djp054.

    Article  PubMed  CAS  Google Scholar 

  88. Gazdar, A. F., & Minna, J. D. (2009). Multifocal lung cancers—clonality vs. field cancerization and does it matter? Journal of the National Cancer Institute, 101(8), 541–543. doi:djp059.

    Article  PubMed  Google Scholar 

  89. Shimizu, S., Yatabe, Y., Koshikawa, T., Haruki, N., Hatooka, S., Shinoda, M., et al. (2000). High frequency of clonally related tumors in cases of multiple synchronous lung cancers as revealed by molecular diagnosis. Clinical Cancer Research, 6(10), 3994–3999.

    PubMed  CAS  Google Scholar 

  90. Riquet, M., Cazes, A., Pfeuty, K., Ngabou, U. D., Foucault, C., Dujon, A., et al. (2008). Multiple lung cancers prognosis: What about histology? The Annals of Thoracic Surgery, 86(3), 921–926. doi:S0003-4975(08)01119-3.

    Article  PubMed  Google Scholar 

  91. Fisher, B., Land, S., Mamounas, E., Dignam, J., Fisher, E. R., & Wolmark, N. (2001). Prevention of invasive breast cancer in women with ductal carcinoma in situ: An update of the national surgical adjuvant breast and bowel project experience. Seminars in Oncology, 28(4), 400–418. doi:S0093775401001531.

    Article  PubMed  CAS  Google Scholar 

  92. Houghton, J., George, W. D., Cuzick, J., Duggan, C., Fentiman, I. S., & Spittle, M. (2003). Radiotherapy and tamoxifen in women with completely excised ductal carcinoma in situ of the breast in the UK, Australia, and New Zealand: Randomised controlled trial. Lancet, 362(9378), 95–102. doi:S0140673603138597.

    Article  PubMed  Google Scholar 

  93. Bijker, N., Meijnen, P., Peterse, J. L., Bogaerts, J., Van Hoorebeeck, I., Julien, J. P., et al. (2006). Breast-conserving treatment with or without radiotherapy in ductal carcinoma-in-situ: ten-year results of european organisation for research and treatment of cancer randomized phase III trial 10853—a study by the EORTC Breast Cancer Cooperative Group and EORTC Radiotherapy Group. Journal of Clinical Oncology, 24(21), 3381–3387. doi:JCO.2006.06.1366.

    Article  PubMed  Google Scholar 

  94. Page, D. L., Dupont, W. D., Rogers, L. W., Jensen, R. A., & Schuyler, P. A. (1995). Continued local recurrence of carcinoma 15–25 years after a diagnosis of low grade ductal carcinoma in situ of the breast treated only by biopsy. Cancer, 76(7), 1197–1200.

    Article  PubMed  CAS  Google Scholar 

  95. Guerra, L. E., Smith, R. M., Kaminski, A., Lagios, M. D., & Silverstein, M. J. (2008). Invasive local recurrence increased after radiation therapy for ductal carcinoma in situ. American Journal of Surgery, 196(4), 552–555. doi:S0002-9610(08)00457-1.

    Article  PubMed  Google Scholar 

  96. Glaves, D., Huben, R. P., & Weiss, L. (1988). Haematogenous dissemination of cells from human renal adenocarcinomas. British Journal of Cancer, 57(1), 32–35.

    Article  PubMed  CAS  Google Scholar 

  97. Klein, C. A. (2009). Parallel progression of primary tumours and metastases. Nature Reviews. Cancer, 9(4), 302–312. doi:nrc2627.

    Article  PubMed  CAS  Google Scholar 

  98. Wikman, H., Vessella, R., & Pantel, K. (2008). Cancer micrometastasis and tumour dormancy. APMIS, 116(7–8), 754–770. doi:APMapm_1033.

    Article  PubMed  CAS  Google Scholar 

  99. Cheng, L., Jones, T. D., Pan, C. X., Barbarin, A., Eble, J. N., & Koch, M. O. (2005). Anatomic distribution and pathologic characterization of small-volume prostate cancer (<0.5 ml) in whole-mount prostatectomy specimens. Modern Pathology, 18(8), 1022–1026. doi:3800431.

    Article  PubMed  Google Scholar 

  100. Landthaler, M., Braun-Falco, O., Leitl, A., Konz, B., & Holzel, D. (1989). Excisional biopsy as the first therapeutic procedure versus primary wide excision of malignant melanoma. Cancer, 64(8), 1612–1616.

    Article  PubMed  CAS  Google Scholar 

  101. Weyers, W. (1997). Excision of melanoma in historical perspective: Triumph of irrationality for nearly a century. Dermatopathology, 3, 238–246.

    Google Scholar 

  102. Thompson, I. M., Jr., Tangen, C. M., Paradelo, J., Lucia, M. S., Miller, G., Troyer, D., et al. (2006). Adjuvant radiotherapy for pathologically advanced prostate cancer: A randomized clinical trial. Journal of the American Medical Association, 296(19), 2329–2335. doi:296/19/2329.

    Article  PubMed  CAS  Google Scholar 

  103. Bolla, M., van Poppel, H., Collette, L., van Cangh, P., Vekemans, K., Da Pozzo, L., et al. (2005). Postoperative radiotherapy after radical prostatectomy: a randomised controlled trial (EORTC trial 22911). Lancet, 366(9485), 572–578. doi:S0140-6736(05)67101-2.

    Article  PubMed  Google Scholar 

  104. Gazdar, A. F. (2010). Epidermal growth factor receptor inhibition in lung cancer: The evolving role of individualized therapy. Cancer and Metastasis Reviews, 29(1), 37–48.

    Article  PubMed  CAS  Google Scholar 

  105. Heidenreich, A., Richter, S., Thuer, D., & Pfister, D. (2010). Prognostic parameters, complications, and oncologic and functional outcome of salvage radical prostatectomy for locally recurrent prostate cancer after 21st-century radiotherapy. European Urology, 57(3), 437–443.

    Article  PubMed  Google Scholar 

  106. Trock, B. J., Han, M., Freedland, S. J., Humphreys, E. B., DeWeese, T. L., Partin, A. W., et al. (2008). Prostate cancer-specific survival following salvage radiotherapy vs observation in men with biochemical recurrence after radical prostatectomy. Journal of the American Medical Association, 299(23), 2760–2769. doi:299/23/2760.

    Article  PubMed  CAS  Google Scholar 

  107. International Multicentre Pooled Analysis of Colon Cancer Trials (IMPACT) investigators. (1995). Efficacy of adjuvant fluorouracil and folinic acid in colon cancer. Lancet, 345(8955), 939–944.

    Article  Google Scholar 

  108. MacFarlane, J. K., Ryall, R. D., & Heald, R. J. (1993). Mesorectal excision for rectal cancer. Lancet, 341(8843), 457–460. doi:0140-6736(93)90207-W.

    Article  PubMed  CAS  Google Scholar 

  109. Swedish Rectal Cancer Trial. (1997). Improved survival with preoperative radiotherapy in resectable rectal cancer. New England Journal of Medicine, 336(14), 980–987.

    Article  Google Scholar 

  110. Formenti, S. C., & Demaria, S. (2009). Systemic effects of local radiotherapy. The Lancet Oncology, 10(7), 718–726. doi:S1470-2045(09)70082-8.

    Article  PubMed  Google Scholar 

  111. Camara, O., Rengsberger, M., Egbe, A., Koch, A., Gajda, M., Hammer, U., et al. (2007). The relevance of circulating epithelial tumor cells (cetc) for therapy monitoring during neoadjuvant (primary systemic) chemotherapy in breast cancer. Annals of Oncology, 18(9), 1484–1492. doi:18/9/1484.

    Article  PubMed  CAS  Google Scholar 

  112. Pachmann, K., Camara, O., Kavallaris, A., Krauspe, S., Malarski, N., Gajda, M., et al. (2008). Monitoring the response of circulating epithelial tumor cells to adjuvant chemotherapy in breast cancer allows detection of patients at risk of early relapse. Journal of Clinical Oncology, 26(8), 1208–1215. doi:26/8/1208.

    Article  PubMed  Google Scholar 

  113. Cristofanilli, M., Budd, G. T., Ellis, M. J., Stopeck, A., Matera, J., Miller, M. C., et al. (2004). Circulating tumor cells, disease progression, and survival in metastatic breast cancer. The New England Journal of Medicine, 351(8), 781–791. doi:10.1056/NEJMoa040766.

    Article  PubMed  CAS  Google Scholar 

  114. Nimeus-Malmstrom, E., Krogh, M., Malmstrom, P., Strand, C., Fredriksson, I., Karlsson, P., et al. (2008). Gene expression profiling in primary breast cancer distinguishes patients developing local recurrence after breast-conservation surgery, with or without postoperative radiotherapy. Breast Cancer Research, 10(2), R34.

    Article  PubMed  CAS  Google Scholar 

  115. Punglia, R. S., Morrow, M., Winer, E. P., & Harris, J. R. (2007). Local therapy and survival in breast cancer. The New England Journal of Medicine, 356(23), 2399–2405. doi:356/23/2399.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

We thank the many doctors and clinicians who cooperate within the complex network of the Munich Cancer Registry (MCR). The Munich Cancer Centre, the Bavarian State Ministry of the Environment and Public Health, and in the past the Deutsche Krebshilfe have supported the MCR. The MCR has been developed to serve as an infrastructure for Health Service Research with online access to long-term results of patients and to provide substantial feedback for quality management in patient care.

Conflicts of interest

We declare that we have no conflicts of interest.

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Authors and Affiliations

  1. Munich Cancer Registry (MCR, Director J. Engel) of the Munich Cancer Center (MCC) at the Institute of medical Informatics, Biometry and Epidemiology (IBE), Ludwig-Maximilians-University (LMU) Munich, Munich, Germany

    Dieter Hölzel, Rebecca T. Emeny & Jutta Engel

  2. Tumorregister München, Klinikum Grosshadern, 81377, Munich, Germany

    Jutta Engel

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  1. Dieter Hölzel
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Correspondence to Dieter Hölzel.

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Hölzel, D., Emeny, R.T. & Engel, J. True local recurrences do not metastasize. Cancer Metastasis Rev 30, 161–176 (2011). https://doi.org/10.1007/s10555-011-9275-2

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