Oligometastasis and oligo-recurrence: more than a mirage

Radiation Oncology

Kunyu Yang¹  Gang Wu¹  Fang Huang¹ 

[1] Wuhan Union Hospital, TongJi Medical College, Huazhong University of Science and Technology, Wuhan 430022, Hubei, China

关键词: Survival;    SBRT;    Surgery;    Oligo-recurrence;    Oligometastasis;   

Others  :  1151017
DOI  :  10.1186/s13014-014-0230-6

 received in 2014-05-07, accepted in 2014-10-04,  发布年份 2014

【 摘 要 】

The standard treatment choice for cancer metastasis has been systemic management, including cytotoxic chemotherapy, hormonal manipulation, and targeted therapy. Emerging evidence has shown an oligometastatic state, an intermediate state between limited primary cancer and polymetastatic cancer, in which local therapy for metastatic lesions results in satisfactory survival comparable to non-metastatic disease. We provide a comprehensive introduction of evidence from experimental and clinical studies in favor of the oligometastatic phenotype, we review the efficacy and safety of surgery and stereotactic body radiotherapy in the treatment of oligometastases, and finally, we discuss the way to differentiate the oligometastatic state from polymetastasis.

【 授权许可】

   
2014 Huang et al.; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Weichselbaum RR, Hellman S: Oligometastases revisited. Nat Rev Clin Oncol 2011, 8:378-382.
• [2]Hellman S, Weichselbaum RR: Oligometastases. J Clin Oncol 1995, 13:8-10.
• [3]Niibe Y, Hayakawa K: Oligometastases and oligo-recurrence: the new era of cancer therapy. Jpn J Clin Oncol 2010, 40:107-111.
• [4]Niibe Y, Chang JY: Novel insights of oligometastases and oligo-recurrence and review of the literature. Pulm Med 2012, 2012:261096.
• [5]Navin N, Kendall J, Troge J, Andrews P, Rodgers L, McIndoo J, Cook K, Stepansky A, Levy D, Esposito D, Muthuswamy L, Krasnitz A, McCombie R, Wigler M: Tumour evolution inferred by single-cell sequencing. Nature 2011, 472:90-94.
• [6]Fidler IJ, Kripke ML: Metastasis results from preexisting variant cells within a malignant tumor. Science (New York, NY) 1977, 197:893-895.
• [7]Shindo-Okada N, Takeuchi K, Nagamachi Y: Establishment of cell lines with high- and low-metastatic potential from PC-14 human lung adenocarcinoma. Jpn J Cancer Res 2001, 92:174-183.
• [8]Li Y, Tang ZY, Ye SL, Liu YK, Chen J, Xue Q, Chen J, Gao DM, Bao WH: Establishment of cell clones with different metastatic potential from the metastatic hepatocellular carcinoma cell line MHCC97. World J Gastroenterol 2001, 7:630-636.
• [9]Chambers AF, Hill RP, Ling V: Tumor heterogeneity and stability of the metastatic phenotype of mouse KHT sarcoma cells. Cancer Res 1981, 41:1368-1372.
• [10]Yachida S, Jones S, Bozic I, Antal T, Leary R, Fu B, Kamiyama M, Hruban RH, Eshleman JR, Nowak MA, Velculescu VE, Kinzler KW, Vogelstein B, Iacobuzio-Donahue CA: Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 2010, 467:1114-1117.
• [11]Wuttig D, Baier B, Fuessel S, Meinhardt M, Herr A, Hoefling C, Toma M, Grimm MO, Meye A, Rolle A, Wirth MP: Gene signatures of pulmonary metastases of renal cell carcinoma reflect the disease-free interval and the number of metastases per patient. Int J Cancer 2009, 125:474-482.
• [12]Tomlinson JS, Jarnagin WR, DeMatteo RP, Fong Y, Kornprat P, Gonen M, Kemeny N, Brennan MF, Blumgart LH, D¿Angelica M: Actual 10-year survival after resection of colorectal liver metastases defines cure. J Clin Oncol 2007, 25:4575-4580.
• [13]Bergenfeldt M, Jensen BV, Skjoldbye B, Nielsen D: Liver resection and local ablation of breast cancer liver metastases¿a systematic review. Eur J Surg Oncol 2011, 37:549-557.
• [14]Saxena A, Chua TC, Perera M, Chu F, Morris DL: Surgical resection of hepatic metastases from neuroendocrine neoplasms: a systematic review. Surg Oncol 2012, 21:e131-141.
• [15]Mariani P, Piperno-Neumann S, Servois V, Berry MG, Dorval T, Plancher C, Couturier J, Levy-Gabriel C, Lumbroso-Le Rouic L, Desjardins L, Salmon RJ: Surgical management of liver metastases from uveal melanoma: 16 years¿ experience at the Institut Curie. Eur J Surg Oncol 2009, 35:1192-1197.
• [16]Ercolani G, Grazi GL, Ravaioli M, Ramacciato G, Cescon M, Varotti G, Del Gaudio M, Vetrone G, Pinna AD: The role of liver resections for noncolorectal, nonneuroendocrine metastases: experience with 142 observed cases. Ann Surg Oncol 2005, 12:459-466.
• [17]Adam R, Chiche L, Aloia T, Elias D, Salmon R, Rivoire M, Jaeck D, Saric J, Le Treut YP, Belghiti J, Mantion G, Mentha G: Hepatic resection for noncolorectal nonendocrine liver metastases: analysis of 1,452 patients and development of a prognostic model. Ann Surg 2006, 244:524-535.
• [18]Reddy SK, Barbas AS, Marroquin CE, Morse MA, Kuo PC, Clary BM: Resection of noncolorectal nonneuroendocrine liver metastases: a comparative analysis. J Am Coll Surg 2007, 204:372-382.
• [19]Hoffmann K, Franz C, Hinz U, Schirmacher P, Herfarth C, Eichbaum M, Buchler MW, Schemmer P: Liver resection for multimodal treatment of breast cancer metastases: identification of prognostic factors. Ann Surg Oncol 2010, 17:1546-1554.
• [20]Rehders A, Peiper M, Stoecklein NH, Alexander A, Boelke E, Knoefel WT, Rogiers X: Hepatic metastasectomy for soft-tissue sarcomas: is it justified? World J Surg 2009, 33:111-117.
• [21]Small R, Lubezky N, Ben-Haim M: Current controversies in the surgical management of colorectal cancer metastases to the liver. Isr Med Assoc J 2007, 9:742-747.
• [22]Lawrence TS, Robertson JM, Anscher MS, Jirtle RL, Ensminger WD, Fajardo LF: Hepatic toxicity resulting from cancer treatment. Int J Radiat Oncol Biol Phys 1995, 31:1237-1248.
• [23]Mendez Romero A, Hoyer M: Radiation therapy for liver metastases. Curr Opin Support Palliat Care 2012, 6:97-102.
• [24]Wada H, Takai Y, Nemoto K, Yamada S: Univariate analysis of factors correlated with tumor control probability of three-dimensional conformal hypofractionated high-dose radiotherapy for small pulmonary or hepatic tumors. Int J Radiat Oncol Biol Phys 2004, 58:1114-1120.
• [25]Sawrie SM, Fiveash JB, Caudell JJ: Stereotactic body radiation therapy for liver metastases and primary hepatocellular carcinoma: normal tissue tolerances and toxicity. Cancer Control 2010, 17:111-119.
• [26]Lanciano R, Lamond J, Yang J, Feng J, Arrigo S, Good M, Brady L: Stereotactic body radiation therapy for patients with heavily pretreated liver metastases and liver tumors. Front Oncol 2012, 2:23.
• [27]Katz AW, Carey-Sampson M, Muhs AG, Milano MT, Schell MC, Okunieff P: Hypofractionated stereotactic body radiation therapy (SBRT) for limited hepatic metastases. Int J Radiat Oncol Biol Phys 2007, 67:793-798.
• [28]Herfarth KK, Debus J, Lohr F, Bahner ML, Rhein B, Fritz P, Hoss A, Schlegel W, Wannenmacher MF: Stereotactic single-dose radiation therapy of liver tumors: results of a phase I/II trial. J Clin Oncol 2001, 19:164-170.
• [29]Kavanagh BD, Schefter TE, Cardenes HR, Stieber VW, Raben D, Timmerman RD, McCarter MD, Burri S, Nedzi LA, Sawyer TE, Gaspar LE: Interim analysis of a prospective phase I/II trial of SBRT for liver metastases. Acta Oncol 2006, 45:848-855.
• [30]Lee MT, Kim JJ, Dinniwell R, Brierley J, Lockwood G, Wong R, Cummings B, Ringash J, Tse RV, Knox JJ, Dawson LA: Phase I study of individualized stereotactic body radiotherapy of liver metastases. J Clin Oncol 2009, 27:1585-1591.
• [31]Mendez Romero A, Wunderink W, Hussain SM, De Pooter JA, Heijmen BJ, Nowak PC, Nuyttens JJ, Brandwijk RP, Verhoef C, Ijzermans JN, Levendag PC: Stereotactic body radiation therapy for primary and metastatic liver tumors: A single institution phase i-ii study. Acta Oncol 2006, 45:831-837.
• [32]Rule W, Timmerman R, Tong L, Abdulrahman R, Meyer J, Boike T, Schwarz RE, Weatherall P, Chinsoo Cho L: Phase I dose-escalation study of stereotactic body radiotherapy in patients with hepatic metastases. Ann Surg Oncol 2011, 18:1081-1087.
• [33]Rusthoven KE, Kavanagh BD, Cardenes H, Stieber VW, Burri SH, Feigenberg SJ, Chidel MA, Pugh TJ, Franklin W, Kane M, Gaspar LE, Schefter TE: Multi-institutional phase I/II trial of stereotactic body radiation therapy for liver metastases. J Clin Oncol 2009, 27:1572-1578.
• [34]Schefter TE, Kavanagh BD, Timmerman RD, Cardenes HR, Baron A, Gaspar LE: A phase I trial of stereotactic body radiation therapy (SBRT) for liver metastases. Int J Radiat Oncol Biol Phys 2005, 62:1371-1378.
• [35]Long-term results of lung metastasectomy: prognostic analyses based on 5206 cases. The International Registry of Lung Metastases.J Thorac Cardiovasc Surg 1997, 113:37¿49
• [36]Choong PF, Pritchard DJ, Rock MG, Sim FH, Frassica FJ: Survival after pulmonary metastasectomy in soft tissue sarcoma Prognostic factors in 214 patients. Acta Orthop Scand 1995, 66:561-568.
• [37]Casiraghi M, De Pas T, Maisonneuve P, Brambilla D, Ciprandi B, Galetta D, Borri A, Gasparri R, Petrella F, Tessitore A, Guarize J, Donghi SM, Veronesi G, Solli P, Spaggiari L: A 10-year single-center experience on 708 lung metastasectomies: the evidence of the ¿international registry of lung metastases¿. J Thorac Oncol 2011, 6:1373-1378.
• [38]Pfannschmidt J, Hoffmann H, Muley T, Krysa S, Trainer C, Dienemann H: Prognostic factors for survival after pulmonary resection of metastatic renal cell carcinoma. Ann Thorac Surg 2002, 74:1653-1657.
• [39]Kanemitsu Y, Kato T, Hirai T, Yasui K: Preoperative probability model for predicting overall survival after resection of pulmonary metastases from colorectal cancer. Br J Surg 2004, 91:112-120.
• [40]Petersen RP, Hanish SI, Haney JC, Miller CC 3rd, Burfeind WR Jr, Tyler DS, Seigler HF, Wolfe W, D¿Amico TA, Harpole DH Jr: Improved survival with pulmonary metastasectomy: an analysis of 1720 patients with pulmonary metastatic melanoma. J Thorac Cardiovasc Surg 2007, 133:104-110.
• [41]Saito Y, Omiya H, Kohno K, Kobayashi T, Itoi K, Teramachi M, Sasaki M, Suzuki H, Takao H, Nakade M: Pulmonary metastasectomy for 165 patients with colorectal carcinoma: A prognostic assessment. J Thorac Cardiovasc Surg 2002, 124:1007-1013.
• [42]Welter S, Jacobs J, Krbek T, Krebs B, Stamatis G: Long-term survival after repeated resection of pulmonary metastases from colorectal cancer. Ann Thorac Surg 2007, 84:203-210.
• [43]Meimarakis G, Angele M, Staehler M, Clevert DA, Crispin A, Ruttinger D, Lohe F, Preissler G, Hatz RA, Winter H: Evaluation of a new prognostic score (Munich score) to predict long-term survival after resection of pulmonary renal cell carcinoma metastases. Am J Surg 2011, 202:158-167.
• [44]Liu D, Abolhoda A, Burt ME, Martini N, Bains MS, Downey RJ, Rusch VW, Bosl GJ, Ginsberg RJ: Pulmonary metastasectomy for testicular germ cell tumors: a 28-year experience. Ann Thorac Surg 1998, 66:1709-1714.
• [45]Suri RM, Deschamps C, Cassivi SD, Nichols FC 3rd, Allen MS, Schleck CD, Pairolero PC: Pulmonary resection for metastatic malignant fibrous histiocytoma: an analysis of prognostic factors. Ann Thorac Surg 2005, 80:1847-1852.
• [46]Clavero JM, Deschamps C, Cassivi SD, Allen MS, Nichols FC 3rd, Barrette BA, Larson DR, Pairolero PC: Gynecologic cancers: factors affecting survival after pulmonary metastasectomy. Ann Thorac Surg 2006, 81:2004-2007.
• [47]Garcia Franco CE, Torre W, Tamura A, Guillen-Grima F, San-Julian M, Martin-Algarra S, Pardo FJ: Long-term results after resection for bone sarcoma pulmonary metastases. Eur J Cardiothorac Surg 2010, 37:1205-1208.
• [48]Guckenberger M, Wulf J, Mueller G, Krieger T, Baier K, Gabor M, Richter A, Wilbert J, Flentje M: Dose¿response relationship for image-guided stereotactic body radiotherapy of pulmonary tumors: relevance of 4D dose calculation. Int J Radiat Oncol Biol Phys 2009, 74:47-54.
• [49]Hamamoto Y, Kataoka M, Yamashita M, Nogami N, Sugawara Y, Kozuki T, Sawada S, Suehisa H, Shinohara S, Nakajima N, Shinkai T: Factors affecting the local control of stereotactic body radiotherapy for lung tumors including primary lung cancer and metastatic lung tumors. Jpn J Radiol 2012, 30:430-434.
• [50]Norihisa Y, Nagata Y, Takayama K, Matsuo Y, Sakamoto T, Sakamoto M, Mizowaki T, Yano S, Hiraoka M: Stereotactic body radiotherapy for oligometastatic lung tumors. Int J Radiat Oncol Biol Phys 2008, 72:398-403.
• [51]Okunieff P, Petersen AL, Philip A, Milano MT, Katz AW, Boros L, Schell MC: Stereotactic Body Radiation Therapy (SBRT) for lung metastases. Acta Oncol 2006, 45:808-817.
• [52]Ricardi U, Filippi AR, Guarneri A, Ragona R, Mantovani C, Giglioli F, Botticella A, Ciammella P, Iftode C, Buffoni L, Ruffinie E, Scagliottif GV: Stereotactic body radiation therapy for lung metastases. Lung Cancer 2012, 75:77-81.
• [53]Takahashi W, Yamashita H, Niibe Y, Shiraishi K, Hayakawa K, Nakagawa K: Stereotactic body radiotherapy for metastatic lung cancer as oligo-recurrence: an analysis of 42 cases. Pulmonary medicine 2012, 2012:454107.
• [54]Takahashi W, Nakajima M, Yamamoto N, Yamada S, Yamashita H, Nakagawa K, Tsuji H, Kamada T: Carbon ion radiotherapy for oligo-recurrent lung metastases from colorectal cancer: a feasibility study. Radiat Oncol 2014, 9:68. BioMed Central Full Text
• [55]Rusthoven KE, Kavanagh BD, Burri SH, Chen C, Cardenes H, Chidel MA, Pugh TJ, Kane M, Gaspar LE, Schefter TE: Multi-institutional phase I/II trial of stereotactic body radiation therapy for lung metastases. J Clin Oncol 2009, 27:1579-1584.
• [56]Hof H, Hoess A, Oetzel D, Debus J, Herfarth K: Stereotactic single-dose radiotherapy of lung metastases. Strahlenther Onkol 2007, 183:673-678.
• [57]Fritz P, Kraus HJ, Muhlnickel W, Hammer U, Dolken W, Engel-Riedel W, Chemaissani A, Stoelben E: Stereotactic, single-dose irradiation of stage I non-small cell lung cancer and lung metastases. Radiat Oncol 2006, 1:30. BioMed Central Full Text
• [58]Hamamoto Y, Kataoka M, Yamashita M, Shinkai T, Kubo Y, Sugawara Y, Inoue T, Sakai S, Aono S, Takahashi T, Semb T, Uwatsu K: Local control of metastatic lung tumors treated with SBRT of 48 Gy in four fractions: in comparison with primary lung cancer. Jpn J Clin Oncol 2010, 40:125-129.
• [59]Takeda A, Kunieda E, Ohashi T, Aoki Y, Koike N, Takeda T: Stereotactic body radiotherapy (SBRT) for oligometastatic lung tumors from colorectal cancer and other primary cancers in comparison with primary lung cancer. Radiother Oncol 2011, 101:255-259.
• [60]Baschnagel AM, Mangona VS, Robertson JM, Welsh RJ, Kestin LL, Grills IS: Lung metastases treated with image-guided stereotactic body radiation therapy. Clin Oncol 2013, 25:236-241.
• [61]Muth A, Persson F, Jansson S, Johanson V, Ahlman H, Wangberg B: Prognostic factors for survival after surgery for adrenal metastasis. Eur J Surg Oncol 2010, 36:699-704.
• [62]Zheng QY, Zhang GH, Zhang Y, Guo YL: Adrenalectomy may increase survival of patients with adrenal metastases. Oncology letters 2012, 3:917-920.
• [63]Suzuki H: Laparoscopic adrenalectomy for adrenal carcinoma and metastases. Curr Opin Urol 2006, 16:47-53.
• [64]Chawla S, Chen Y, Katz AW, Muhs AG, Philip A, Okunieff P, Milano MT: Stereotactic body radiotherapy for treatment of adrenal metastases. Int J Radiat Oncol Biol Phys 2009, 75:71-75.
• [65]Torok J, Wegner RE, Burton SA, Heron DE, Torok J, Wegner RE, Burton SA, Heron DE: Stereotactic body radiation therapy for adrenal metastases: a retrospective review of a noninvasive therapeutic strategy. Future Oncol 2011, 7:145-151.
• [66]Chamberlain MC: Spinal metastases from lung cancer¿who benefits from decompression surgery? Nat Clin Pract Neurol 2007, 3:188-189.
• [67]Choi D, Morris S, Crockard A, Albert T, Bunger C, Fehlings M, Harrop J, Kawahara N, Martin JA, Massicotte EM, Mazel C, Oner FC, Peul W, Tomita K, Wang M: Assessment of quality of life after surgery for spinal metastases: position statement of the Global Spine Tumour Study Group. World Neurosurg 2013, 80:e175-179.
• [68]Lo SS, Sahgal A, Wang JZ, Mayr NA, Sloan A, Mendel E, Chang EL: Stereotactic body radiation therapy for spinal metastases. Discov Med 2010, 9:289-296.
• [69]Lopes JC, Navarro A, Sole JM, Martinez M, Guedea F: Stereotactic body radiation therapy for spinal metastases. Clin Transl Oncol 2010, 12:639-642.
• [70]Cunha MV, Al-Omair A, Atenafu EG, Masucci GL, Letourneau D, Korol R, Yu E, Howard P, Lochray F, da Costa LB, Fehlings MG, Sahgal A: Vertebral compression fracture (VCF) after spine stereotactic body radiation therapy (SBRT): analysis of predictive factors. Int J Radiat Oncol Biol Phys 2012, 84:e343-349.
• [71]Boehling NS, Grosshans DR, Allen PK, McAleer MF, Burton AW, Azeem S, Rhines LD, Chang EL: Vertebral compression fracture risk after stereotactic body radiotherapy for spinal metastases. J Neurosurg Spine 2012, 16:379-386.
• [72]Widder J, Klinkenberg TJ, Ubbels JF, Wiegman EM, Groen HJ, Langendijk JA: Pulmonary oligometastases: metastasectomy or stereotactic ablative radiotherapy? Radiother Oncol 2013, 107:409-413.
• [73]de Vin T, Engels B, Gevaert T, Storme G, De Ridder M: Stereotactic radiotherapy for oligometastatic cancer: a prognostic model for survival. Ann Oncol 2014, 25:467-471.
• [74]Milano MT, Katz AW, Zhang H, Okunieff P: Oligometastases treated with stereotactic body radiotherapy: long-term follow-up of prospective study. Int J Radiat Oncol Biol Phys 2012, 83:878-886.
• [75]Goslin R, Steele G Jr, Zamcheck N, Mayer R, MacIntyre J: Factors influencing survival in patients with hepatic metastases from adenocarcinoma of the colon or rectum. Dis Colon Rectum 1982, 25:749-754.
• [76]Choti MA, Sitzmann JV, Tiburi MF, Sumetchotimetha W, Rangsin R, Schulick RD, Lillemoe KD, Yeo CJ, Cameron JL: Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg 2002, 235:759-766.
• [77]Giuliante F, Ardito F, Vellone M, Ranucci G, Federico B, Giovannini I, Nuzzo G: Role of the surgeon as a variable in long-term survival after liver resection for colorectal metastases. J Surg Oncol 2009, 100:538-545.
• [78]Simmonds PC, Primrose JN, Colquitt JL, Garden OJ, Poston GJ, Rees M: Surgical resection of hepatic metastases from colorectal cancer: a systematic review of published studies. Br J Cancer 2006, 94:982-999.
• [79]Suemitsu R, Takeo S, Kusumoto E, Hamatake M, Ikejiri K, Saitsu H: Results of a pulmonary metastasectomy in patients with colorectal cancer. Surg Today 2011, 41:54-59.
• [80]Inoue M, Ohta M, Iuchi K, Matsumura A, Ideguchi K, Yasumitsu T, Nakagawa K, Fukuhara K, Maeda H, Takeda S, Minami M, Ohno Y, Matsuda H: Benefits of surgery for patients with pulmonary metastases from colorectal carcinoma. Ann Thorac Surg 2004, 78:238-244.
• [81]Salah S, Watanabe K, Welter S, Park JS, Park JW, Zabaleta J, Ardissone F, Kim J, Riquet M, Nojiri K, Gisabella M, Kim SY, Tanaka K, Ali BA: Colorectal cancer pulmonary oligometastases: pooled analysis and construction of a clinical lung metastasectomy prognostic model. Ann Oncol 2012, 23:2649-2655.
• [82]Meimarakis G, Ruttinger D, Stemmler J, Crispin A, Weidenhagen R, Angele M, Fertmann J, Hatz RA, Winter H: Prolonged overall survival after pulmonary metastasectomy in patients with breast cancer. Ann Thorac Surg 2013, 95:1170-1180.
• [83]Ashworth A, Rodrigues G, Boldt G, Palma D: Is there an oligometastatic state in non-small cell lung cancer? A systematic review of the literature. Lung Cancer 2013, 82:197-203.
• [84]Patchell RA, Tibbs PA, Walsh JW, Dempsey RJ, Maruyama Y, Kryscio RJ, Markesbery WR, Macdonald JS, Young B: A randomized trial of surgery in the treatment of single metastases to the brain. N Engl J Med 1990, 322:494-500.
• [85]Andrews DW, Scott CB, Sperduto PW, Flanders AE, Gaspar LE, Schell MC, Werner-Wasik M, Demas W, Ryu J, Bahary JP, Souhami L, Rotman M, Mehta MP, Curran WJ: Whole brain radiation therapy with or without stereotactic radiosurgery boost for patients with one to three brain metastases: phase III results of the RTOG 9508 randomised trial. Lancet 2004, 363:1665-1672.
• [86]Spelt L, Andersson B, Nilsson J, Andersson R: Prognostic models for outcome following liver resection for colorectal cancer metastases: A systematic review. Eur J Surg Oncol 2012, 38:16-24.
• [87]Kanzaki R, Higashiyama M, Fujiwara A, Tokunaga T, Maeda J, Okami J, Nishimura K, Kodama K: Long-term results of surgical resection for pulmonary metastasis from renal cell carcinoma: a 25-year single-institution experience. Eur J Cardiothorac Surg 2011, 39:167-172.
• [88]Rees M, Tekkis PP, Welsh FK, O¿Rourke T, John TG: Evaluation of long-term survival after hepatic resection for metastatic colorectal cancer: a multifactorial model of 929 patients. Ann Surg 2008, 247:125-135.
• [89]Konopke R, Kersting S, Distler M, Dietrich J, Gastmeier J, Heller A, Kulisch E, Saeger HD: Prognostic factors and evaluation of a clinical score for predicting survival after resection of colorectal liver metastases. Liver Int 2009, 29:89-102.
• [90]Malik HZ, Prasad KR, Halazun KJ, Aldoori A, Al-Mukhtar A, Gomez D, Lodge JP, Toogood GJ: Preoperative prognostic score for predicting survival after hepatic resection for colorectal liver metastases. Ann Surg 2007, 246:806-814.
• [91]Minagawa M, Yamamoto J, Kosuge T, Matsuyama Y, Miyagawa S, Makuuchi M: Simplified staging system for predicting the prognosis of patients with resectable liver metastasis: development and validation. Arch Surg 2007, 142:269-276. discussion 277
• [92]Lussier YA, Khodarev NN, Regan K, Corbin K, Li H, Ganai S, Khan SA, Gnerlich JL, Darga TE, Fan H, Karpenko O, Paty PB, Posner MC, Chmura SJ, Hellman S, Ferguson MK, Weichselbaum RR: Oligo- and polymetastatic progression in lung metastasis(es) patients is associated with specific microRNAs. PLoS One 2012, 7:e50141.