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Published in: BMC Medicine 1/2020

Open Access 01-12-2020 | Rectal Cancer | Research article

Risk factors and risk prediction models for colorectal cancer metastasis and recurrence: an umbrella review of systematic reviews and meta-analyses of observational studies

Authors: Wei Xu, Yazhou He, Yuming Wang, Xue Li, Jane Young, John P. A. Ioannidis, Malcolm G. Dunlop, Evropi Theodoratou

Published in: BMC Medicine | Issue 1/2020

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Abstract

Background

There is a clear need for systematic appraisal of models/factors predicting colorectal cancer (CRC) metastasis and recurrence because clinical decisions about adjuvant treatment are taken on the basis of such variables.

Methods

We conducted an umbrella review of all systematic reviews of observational studies (with/without meta-analysis) that evaluated risk factors of CRC metastasis and recurrence. We also generated an updated synthesis of risk prediction models for CRC metastasis and recurrence. We cross-assessed individual risk factors and risk prediction models.

Results

Thirty-four risk factors for CRC metastasis and 17 for recurrence were investigated. Twelve of 34 and 4/17 risk factors with p < 0.05 were estimated to change the odds of the outcome at least 3-fold. Only one risk factor (vascular invasion for lymph node metastasis [LNM] in pT1 CRC) presented convincing evidence. We identified 24 CRC risk prediction models. Across 12 metastasis models, six out of 27 unique predictors were assessed in the umbrella review and four of them changed the odds of the outcome at least 3-fold. Across 12 recurrence models, five out of 25 unique predictors were assessed in the umbrella review and only one changed the odds of the outcome at least 3-fold.

Conclusions

This study provides an in-depth evaluation and cross-assessment of 51 risk factors and 24 prediction models. Our findings suggest that a minority of influential risk factors are employed in prediction models, which indicates the need for a more rigorous and systematic model construction process following evidence-based methods.
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Literature
2.
go back to reference Mekenkamp LJ, Koopman M, Teerenstra S, et al. Clinicopathological features and outcome in advanced colorectal cancer patients with synchronous vs metachronous metastases. Br J Cancer. 2010;103(2):159.PubMedPubMedCentralCrossRef Mekenkamp LJ, Koopman M, Teerenstra S, et al. Clinicopathological features and outcome in advanced colorectal cancer patients with synchronous vs metachronous metastases. Br J Cancer. 2010;103(2):159.PubMedPubMedCentralCrossRef
3.
go back to reference Duineveld LA, van Asselt KM, Bemelman WA, et al. Symptomatic and asymptomatic colon cancer recurrence: a multicenter cohort study. Ann Fam Med. 2016;14(3):215–20.PubMedPubMedCentralCrossRef Duineveld LA, van Asselt KM, Bemelman WA, et al. Symptomatic and asymptomatic colon cancer recurrence: a multicenter cohort study. Ann Fam Med. 2016;14(3):215–20.PubMedPubMedCentralCrossRef
4.
go back to reference Ryuk JP, Choi GS, Park JS, et al. Predictive factors and the prognosis of recurrence of colorectal cancer within 2 years after curative resection. Ann Surg Treatment Res. 2014;86(3):143–51.CrossRef Ryuk JP, Choi GS, Park JS, et al. Predictive factors and the prognosis of recurrence of colorectal cancer within 2 years after curative resection. Ann Surg Treatment Res. 2014;86(3):143–51.CrossRef
5.
go back to reference Dromain C, Caramella C, Dartigues P, et al. Liver, lung and peritoneal metastases in colorectal cancers: is the patient still curable? What should the radiologist know. Diagnostic Interventional Imaging. 2014;95(5):513–23.PubMedCrossRef Dromain C, Caramella C, Dartigues P, et al. Liver, lung and peritoneal metastases in colorectal cancers: is the patient still curable? What should the radiologist know. Diagnostic Interventional Imaging. 2014;95(5):513–23.PubMedCrossRef
6.
go back to reference Haggar FA, Boushey RP. Colorectal cancer epidemiology: incidence, mortality, survival, and risk factors. Clinics Colon Rectal Surg. 2009;22(04):191–7.CrossRef Haggar FA, Boushey RP. Colorectal cancer epidemiology: incidence, mortality, survival, and risk factors. Clinics Colon Rectal Surg. 2009;22(04):191–7.CrossRef
7.
go back to reference Beaton C, Twine CP, Williams GL, et al. Systematic review and meta-analysis of histopathological factors influencing the risk of lymph node metastasis in early colorectal cancer. Color Dis. 2013;15(7):788–97.CrossRef Beaton C, Twine CP, Williams GL, et al. Systematic review and meta-analysis of histopathological factors influencing the risk of lymph node metastasis in early colorectal cancer. Color Dis. 2013;15(7):788–97.CrossRef
8.
go back to reference Choi JY, Jung S, Shim KN, et al. Meta-analysis of predictive clinicopathologic factors for lymph node metastasis in patients with early colorectal carcinoma. J Korean Med Sci. 2015;30(4):398–406.PubMedPubMedCentralCrossRef Choi JY, Jung S, Shim KN, et al. Meta-analysis of predictive clinicopathologic factors for lymph node metastasis in patients with early colorectal carcinoma. J Korean Med Sci. 2015;30(4):398–406.PubMedPubMedCentralCrossRef
9.
go back to reference Ha GW, Kim JH, Lee MR. Oncologic impact of anastomotic leakage following colorectal cancer surgery: a systematic review and meta-analysis. Ann Surg Oncol. 2017;24(11):3289–99.PubMedCrossRef Ha GW, Kim JH, Lee MR. Oncologic impact of anastomotic leakage following colorectal cancer surgery: a systematic review and meta-analysis. Ann Surg Oncol. 2017;24(11):3289–99.PubMedCrossRef
10.
go back to reference Rekhraj S, Aziz O, Prabhudesai S, et al. Can intra-operative intraperitoneal free cancer cell detection techniques identify patients at higher recurrence risk following curative colorectal cancer resection: a meta-analysis. Ann Surg Oncol. 2008;15(1):60–8.PubMedCrossRef Rekhraj S, Aziz O, Prabhudesai S, et al. Can intra-operative intraperitoneal free cancer cell detection techniques identify patients at higher recurrence risk following curative colorectal cancer resection: a meta-analysis. Ann Surg Oncol. 2008;15(1):60–8.PubMedCrossRef
11.
go back to reference Moher D, Shamseer L, Clarke M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Systematic Reviews. 2015;4(1):1.PubMedPubMedCentralCrossRef Moher D, Shamseer L, Clarke M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Systematic Reviews. 2015;4(1):1.PubMedPubMedCentralCrossRef
12.
13.
go back to reference IntHout J, Ioannidis JP, Borm GF. The Hartung-Knapp-Sidik-Jonkman method for random effects meta-analysis is straightforward and considerably outperforms the standard DerSimonian-Laird method. BMC Med Res Methodol. 2014;14(1):25.PubMedPubMedCentralCrossRef IntHout J, Ioannidis JP, Borm GF. The Hartung-Knapp-Sidik-Jonkman method for random effects meta-analysis is straightforward and considerably outperforms the standard DerSimonian-Laird method. BMC Med Res Methodol. 2014;14(1):25.PubMedPubMedCentralCrossRef
16.
go back to reference Ioannidis JP. Clarifications on the application and interpretation of the test for excess significance and its extensions. J Math Psychol. 2013;57(5):184–7.CrossRef Ioannidis JP. Clarifications on the application and interpretation of the test for excess significance and its extensions. J Math Psychol. 2013;57(5):184–7.CrossRef
17.
go back to reference He Y, Li X, Gasevic D, et al. Statins and multiple noncardiovascular outcomes: umbrella review of meta-analyses of observational studies and randomized controlled trials. Ann Intern Med. 2018;169(8):543–53. . He Y, Li X, Gasevic D, et al. Statins and multiple noncardiovascular outcomes: umbrella review of meta-analyses of observational studies and randomized controlled trials. Ann Intern Med. 2018;169(8):543–53. .
18.
go back to reference Li X, Meng X, Timofeeva M, et al. Serum uric acid levels and multiple health outcomes: umbrella review of evidence from observational studies, randomised controlled trials, and Mendelian randomisation studies. BMJ. 2017;357:j2376.PubMedPubMedCentralCrossRef Li X, Meng X, Timofeeva M, et al. Serum uric acid levels and multiple health outcomes: umbrella review of evidence from observational studies, randomised controlled trials, and Mendelian randomisation studies. BMJ. 2017;357:j2376.PubMedPubMedCentralCrossRef
19.
go back to reference Shea BJ, Reeves BC, Wells G, et al. AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both. Bmj. 2017;358:j4008.PubMedPubMedCentralCrossRef Shea BJ, Reeves BC, Wells G, et al. AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both. Bmj. 2017;358:j4008.PubMedPubMedCentralCrossRef
20.
go back to reference Guyatt GH, Oxman AD, Sultan S, et al. GRADE guidelines: 9. Rating up the quality of evidence. J Clin Epidemiol. 2011;64(12):1311–6.PubMedCrossRef Guyatt GH, Oxman AD, Sultan S, et al. GRADE guidelines: 9. Rating up the quality of evidence. J Clin Epidemiol. 2011;64(12):1311–6.PubMedCrossRef
21.
go back to reference He Y, Ong Y, Li X, et al. Performance of prediction models on survival outcomes of colorectal cancer with surgical resection: a systematic review and meta-analysis. Surg Oncol. 2019;29:196–202. He Y, Ong Y, Li X, et al. Performance of prediction models on survival outcomes of colorectal cancer with surgical resection: a systematic review and meta-analysis. Surg Oncol. 2019;29:196–202.
22.
go back to reference Macias-Garcia F, Celeiro-Muñoz C, Lesquereux-Martinez L, et al. A clinical model for predicting lymph node metastasis in submucosal invasive (T1) colorectal cancer. Int J Color Dis. 2015;30(6):761–8.CrossRef Macias-Garcia F, Celeiro-Muñoz C, Lesquereux-Martinez L, et al. A clinical model for predicting lymph node metastasis in submucosal invasive (T1) colorectal cancer. Int J Color Dis. 2015;30(6):761–8.CrossRef
23.
go back to reference Taylor I, Mullee MA, Campbell MJ. Prognostic index for the development of liver metastases in patients with colorectal cancer. Br J Surg. 1990;77(5):499–501.PubMedCrossRef Taylor I, Mullee MA, Campbell MJ. Prognostic index for the development of liver metastases in patients with colorectal cancer. Br J Surg. 1990;77(5):499–501.PubMedCrossRef
24.
go back to reference Segelman J, Akre O, Gustafsson UO, et al. Individualized prediction of risk of metachronous peritoneal carcinomatosis from colorectal cancer. Color Dis. 2014;16(5):359–67.CrossRef Segelman J, Akre O, Gustafsson UO, et al. Individualized prediction of risk of metachronous peritoneal carcinomatosis from colorectal cancer. Color Dis. 2014;16(5):359–67.CrossRef
25.
go back to reference Huang YQ, Liang CH, He L, et al. Development and validation of a radiomics nomogram for preoperative prediction of lymph node metastasis in colorectal cancer. J Clin Oncol. 2016;34(18):2157–64.PubMedCrossRef Huang YQ, Liang CH, He L, et al. Development and validation of a radiomics nomogram for preoperative prediction of lymph node metastasis in colorectal cancer. J Clin Oncol. 2016;34(18):2157–64.PubMedCrossRef
26.
go back to reference Hu T, Wang S, Huang L, et al. A clinical-radiomics nomogram for the preoperative prediction of lung metastasis in colorectal cancer patients with indeterminate pulmonary nodules. Eur Radiol. 2019;29(1):439–49.PubMedCrossRef Hu T, Wang S, Huang L, et al. A clinical-radiomics nomogram for the preoperative prediction of lung metastasis in colorectal cancer patients with indeterminate pulmonary nodules. Eur Radiol. 2019;29(1):439–49.PubMedCrossRef
27.
go back to reference Guan X, Ma CX, Quan JC, et al. A clinical model to predict the risk of synchronous bone metastasis in newly diagnosed colorectal cancer: a population-based study. BMC Cancer. 2019;19(1):704.PubMedPubMedCentralCrossRef Guan X, Ma CX, Quan JC, et al. A clinical model to predict the risk of synchronous bone metastasis in newly diagnosed colorectal cancer: a population-based study. BMC Cancer. 2019;19(1):704.PubMedPubMedCentralCrossRef
28.
go back to reference Oh JR, Park B, Lee S, et al. Nomogram development and external validation for predicting the risk of lymph node metastasis in T1 colorectal cancer. Cancer Res Treat. 2019;51(4):1275–84. Oh JR, Park B, Lee S, et al. Nomogram development and external validation for predicting the risk of lymph node metastasis in T1 colorectal cancer. Cancer Res Treat. 2019;51(4):1275–84.
29.
go back to reference Goossens-Beumer IJ, Derr RS, Buermans HP, et al. MicroRNA classifier and nomogram for metastasis prediction in colon cancer. Cancer Epidemiol Prevention Biomarkers. 2015;24(1):187–97.CrossRef Goossens-Beumer IJ, Derr RS, Buermans HP, et al. MicroRNA classifier and nomogram for metastasis prediction in colon cancer. Cancer Epidemiol Prevention Biomarkers. 2015;24(1):187–97.CrossRef
30.
go back to reference Wang X, Chi P, Lin H, et al. Establishment of nomogram model to predict peritoneal metastasis in colon cancer patients without distant metastasis by preoperative imaging examination. Zhonghua Wei Chang Wai Ke Za Zhi. 2017;20(12):1387–92.PubMed Wang X, Chi P, Lin H, et al. Establishment of nomogram model to predict peritoneal metastasis in colon cancer patients without distant metastasis by preoperative imaging examination. Zhonghua Wei Chang Wai Ke Za Zhi. 2017;20(12):1387–92.PubMed
31.
go back to reference Van Gijn W, Van Stiphout R, Van De Velde CJ, et al. Nomograms to predict survival and the risk for developing local or distant recurrence in patients with rectal cancer treated with optional short-term radiotherapy. Ann Oncol. 2015;26(5):928–35.PubMedCrossRef Van Gijn W, Van Stiphout R, Van De Velde CJ, et al. Nomograms to predict survival and the risk for developing local or distant recurrence in patients with rectal cancer treated with optional short-term radiotherapy. Ann Oncol. 2015;26(5):928–35.PubMedCrossRef
32.
go back to reference Valentini V, Van Stiphout RG, Lammering G, et al. Nomograms for predicting local recurrence, distant metastases, and overall survival for patients with locally advanced rectal cancer on the basis of European randomized clinical trials. J Clin Oncol. 2011;29(23):3163–72.PubMedCrossRef Valentini V, Van Stiphout RG, Lammering G, et al. Nomograms for predicting local recurrence, distant metastases, and overall survival for patients with locally advanced rectal cancer on the basis of European randomized clinical trials. J Clin Oncol. 2011;29(23):3163–72.PubMedCrossRef
33.
go back to reference Sun Y, Lin H, Lu X, et al. A nomogram to predict distant metastasis after neoadjuvant chemoradiotherapy and radical surgery in patients with locally advanced rectal cancer. J Surg Oncol. 2017;115(4):462–9.PubMedCrossRef Sun Y, Lin H, Lu X, et al. A nomogram to predict distant metastasis after neoadjuvant chemoradiotherapy and radical surgery in patients with locally advanced rectal cancer. J Surg Oncol. 2017;115(4):462–9.PubMedCrossRef
34.
go back to reference Hoshino N, Hasegawa S, Hida K, et al. Nomogram for predicting recurrence in stage II colorectal cancer. Acta Oncol. 2016;55(12):1414–7.PubMedCrossRef Hoshino N, Hasegawa S, Hida K, et al. Nomogram for predicting recurrence in stage II colorectal cancer. Acta Oncol. 2016;55(12):1414–7.PubMedCrossRef
35.
go back to reference Renfro LA, Grothey A, Xue Y, et al. ACCENT-based web calculators to predict recurrence and overall survival in stage III colon cancer. J National Cancer Institute. 2014;106(12):dju333.CrossRef Renfro LA, Grothey A, Xue Y, et al. ACCENT-based web calculators to predict recurrence and overall survival in stage III colon cancer. J National Cancer Institute. 2014;106(12):dju333.CrossRef
36.
go back to reference Tian X, Zhu X, Yan T, et al. Recurrence-associated gene signature optimizes recurrence-free survival prediction of colorectal cancer. Mol Oncol. 2017;11(11):1544–60.PubMedPubMedCentralCrossRef Tian X, Zhu X, Yan T, et al. Recurrence-associated gene signature optimizes recurrence-free survival prediction of colorectal cancer. Mol Oncol. 2017;11(11):1544–60.PubMedPubMedCentralCrossRef
37.
go back to reference Peng J, Wang Z, Chen W, et al. Integration of genetic signature and TNM staging system for predicting the relapse of locally advanced colorectal cancer. Int J Color Dis. 2010;25(11):1277–85.CrossRef Peng J, Wang Z, Chen W, et al. Integration of genetic signature and TNM staging system for predicting the relapse of locally advanced colorectal cancer. Int J Color Dis. 2010;25(11):1277–85.CrossRef
38.
go back to reference Ying HQ, Deng QW, He BS, et al. The prognostic value of preoperative NLR, d-NLR, PLR and LMR for predicting clinical outcome in surgical colorectal cancer patients. Med Oncol. 2014;31(12):305.PubMedCrossRef Ying HQ, Deng QW, He BS, et al. The prognostic value of preoperative NLR, d-NLR, PLR and LMR for predicting clinical outcome in surgical colorectal cancer patients. Med Oncol. 2014;31(12):305.PubMedCrossRef
39.
40.
go back to reference Kim C, Kim WR, Kim KY, et al. Predictive nomogram for recurrence of stage i colorectal cancer after curative resection. Clin Colorectal Cancer. 2018;17(3):e513–8.PubMedCrossRef Kim C, Kim WR, Kim KY, et al. Predictive nomogram for recurrence of stage i colorectal cancer after curative resection. Clin Colorectal Cancer. 2018;17(3):e513–8.PubMedCrossRef
41.
go back to reference Miyoshi N, Ohue M, Yasui M, et al. Novel prognostic prediction models for patients with stage IV colorectal cancer after concurrent curative resection. ESMO Open. 2016;1(3):e000052.PubMedPubMedCentralCrossRef Miyoshi N, Ohue M, Yasui M, et al. Novel prognostic prediction models for patients with stage IV colorectal cancer after concurrent curative resection. ESMO Open. 2016;1(3):e000052.PubMedPubMedCentralCrossRef
42.
go back to reference Saso K, Myoshi N, Fujino S, et al. A novel prognostic prediction model for recurrence in patients with stage II colon cancer after curative resection. Mol Clin Oncol. 2018;9(6):697–701.PubMedPubMedCentral Saso K, Myoshi N, Fujino S, et al. A novel prognostic prediction model for recurrence in patients with stage II colon cancer after curative resection. Mol Clin Oncol. 2018;9(6):697–701.PubMedPubMedCentral
43.
go back to reference Hida K, Okamura R, Park SY, et al. A new prediction model for local recurrence after curative rectal cancer surgery: development and validation as an Asian collaborative study. Dis Colon Rectum. 2017;60(11):1168–74.PubMedCrossRef Hida K, Okamura R, Park SY, et al. A new prediction model for local recurrence after curative rectal cancer surgery: development and validation as an Asian collaborative study. Dis Colon Rectum. 2017;60(11):1168–74.PubMedCrossRef
44.
go back to reference van Wyk HC, Roxburgh CS, Horgan PG, et al. The detection and role of lymphatic and blood vessel invasion in predicting survival in patients with node negative operable primary colorectal cancer. Crit Rev Oncol Hematol. 2014;90(1):77–90.PubMedCrossRef van Wyk HC, Roxburgh CS, Horgan PG, et al. The detection and role of lymphatic and blood vessel invasion in predicting survival in patients with node negative operable primary colorectal cancer. Crit Rev Oncol Hematol. 2014;90(1):77–90.PubMedCrossRef
45.
go back to reference Stacker SA, Baldwin ME, Achen MG. The role of tumor lymphangiogenesis in metastatic spread. FASEB J. 2002;16(9):922–34.PubMedCrossRef Stacker SA, Baldwin ME, Achen MG. The role of tumor lymphangiogenesis in metastatic spread. FASEB J. 2002;16(9):922–34.PubMedCrossRef
46.
go back to reference Bosch SL, Teerenstra S, de Wilt JH, et al. Predicting lymph node metastasis in pT1 colorectal cancer: a systematic review of risk factors providing rationale for therapy decisions. Endoscopy. 2013;45(10):827–41.PubMedCrossRef Bosch SL, Teerenstra S, de Wilt JH, et al. Predicting lymph node metastasis in pT1 colorectal cancer: a systematic review of risk factors providing rationale for therapy decisions. Endoscopy. 2013;45(10):827–41.PubMedCrossRef
47.
go back to reference Longatto-Filho A, Pinheiro C, Ferreira L, et al. Peritumoural, but not intratumoural, lymphatic vessel density and invasion correlate with colorectal carcinoma poor-outcome markers. Virchows Arch. 2008;452(2):133–8.PubMedCrossRef Longatto-Filho A, Pinheiro C, Ferreira L, et al. Peritumoural, but not intratumoural, lymphatic vessel density and invasion correlate with colorectal carcinoma poor-outcome markers. Virchows Arch. 2008;452(2):133–8.PubMedCrossRef
48.
go back to reference Desolneux G, Burtin P, Lermite E, et al. Prognostic factors in node-negative colorectal cancer: a retrospective study from a prospective database. Int J Color Dis. 2010;25(7):829–34.CrossRef Desolneux G, Burtin P, Lermite E, et al. Prognostic factors in node-negative colorectal cancer: a retrospective study from a prospective database. Int J Color Dis. 2010;25(7):829–34.CrossRef
49.
go back to reference Matsumoto K, Nakayama Y, Inoue Y, et al. Lymphatic microvessel density is an independent prognostic factor in colorectal cancer. Dis Colon Rectum. 2007;50(3):308–14.PubMedCrossRef Matsumoto K, Nakayama Y, Inoue Y, et al. Lymphatic microvessel density is an independent prognostic factor in colorectal cancer. Dis Colon Rectum. 2007;50(3):308–14.PubMedCrossRef
50.
go back to reference Ha RK, Han KS, Sohn DK, et al. Histopathologic risk factors for lymph node metastasis in patients with T1 colorectal cancer. Ann Surg Treatment Res. 2017;93(5):266–71.CrossRef Ha RK, Han KS, Sohn DK, et al. Histopathologic risk factors for lymph node metastasis in patients with T1 colorectal cancer. Ann Surg Treatment Res. 2017;93(5):266–71.CrossRef
51.
go back to reference Yamauchi H, Togashi K, Kawamura H, et al. Tumor budding and pathological differentiation are predictive markers for lymph node metastasis in T1 colorectal cancer. Gastrointest Endosc. 2006;63(5):AB216.CrossRef Yamauchi H, Togashi K, Kawamura H, et al. Tumor budding and pathological differentiation are predictive markers for lymph node metastasis in T1 colorectal cancer. Gastrointest Endosc. 2006;63(5):AB216.CrossRef
52.
go back to reference Tateishi Y, Nakanishi Y, Taniguchi H, et al. Pathological prognostic factors predicting lymph node metastasis in submucosal invasive (T1) colorectal carcinoma. Mod Pathol. 2010;23(8):1068.PubMedCrossRef Tateishi Y, Nakanishi Y, Taniguchi H, et al. Pathological prognostic factors predicting lymph node metastasis in submucosal invasive (T1) colorectal carcinoma. Mod Pathol. 2010;23(8):1068.PubMedCrossRef
53.
go back to reference Van Wyk HC, Park J, Roxburgh C, et al. The role of tumour budding in predicting survival in patients with primary operable colorectal cancer: a systematic review. Cancer Treat Rev. 2015;41(2):151–9.PubMedCrossRef Van Wyk HC, Park J, Roxburgh C, et al. The role of tumour budding in predicting survival in patients with primary operable colorectal cancer: a systematic review. Cancer Treat Rev. 2015;41(2):151–9.PubMedCrossRef
54.
go back to reference Glynne-Jones R, Wyrwicz L, Tiret E, et al. Rectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2017;28(suppl_4):iv22–40.PubMedCrossRef Glynne-Jones R, Wyrwicz L, Tiret E, et al. Rectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2017;28(suppl_4):iv22–40.PubMedCrossRef
55.
go back to reference Knijn N, Mogk SC, Teerenstra S, et al. Perineural invasion is a strong prognostic factor in colorectal cancer. Am J Surg Pathol. 2016;40(1):103–12.PubMedCrossRef Knijn N, Mogk SC, Teerenstra S, et al. Perineural invasion is a strong prognostic factor in colorectal cancer. Am J Surg Pathol. 2016;40(1):103–12.PubMedCrossRef
56.
go back to reference Benson AB, Venook AP, Cederquist L, et al. Colon cancer, version 1.2017, NCCN clinical practice guidelines in oncology. J Natl Compr Cancer Netw. 2017;15(3):370–98.CrossRef Benson AB, Venook AP, Cederquist L, et al. Colon cancer, version 1.2017, NCCN clinical practice guidelines in oncology. J Natl Compr Cancer Netw. 2017;15(3):370–98.CrossRef
57.
58.
go back to reference Poeschl EM, Pollheimer MJ, Kornprat P, et al. Perineural invasion: correlation with aggressive phenotype and independent prognostic variable in both colon and rectum cancer. J Clin Oncol. 2010;28(21):e358–60.PubMedCrossRef Poeschl EM, Pollheimer MJ, Kornprat P, et al. Perineural invasion: correlation with aggressive phenotype and independent prognostic variable in both colon and rectum cancer. J Clin Oncol. 2010;28(21):e358–60.PubMedCrossRef
59.
go back to reference Peng J, Sheng W, Huang D, et al. Perineural invasion in pT3N0 rectal cancer: the incidence and its prognostic effect. Cancer. 2011;117(7):1415–21.PubMedCrossRef Peng J, Sheng W, Huang D, et al. Perineural invasion in pT3N0 rectal cancer: the incidence and its prognostic effect. Cancer. 2011;117(7):1415–21.PubMedCrossRef
60.
go back to reference Huh JW, Kim HR, Kim YJ. Prognostic value of perineural invasion in patients with stage II colorectal cancer. Ann Surg Oncol. 2010;17(8):2066–72.PubMedCrossRef Huh JW, Kim HR, Kim YJ. Prognostic value of perineural invasion in patients with stage II colorectal cancer. Ann Surg Oncol. 2010;17(8):2066–72.PubMedCrossRef
61.
go back to reference Taylor FG, Swift RI, Blomqvist L, et al. A systematic approach to the interpretation of preoperative staging MRI for rectal cancer. Am J Roentgenol. 2008;191(6):1827–35.CrossRef Taylor FG, Swift RI, Blomqvist L, et al. A systematic approach to the interpretation of preoperative staging MRI for rectal cancer. Am J Roentgenol. 2008;191(6):1827–35.CrossRef
62.
go back to reference Talbot IC, Ritchie S, Leighton MH, et al. The clinical significance of invasion of veins by rectal cancer. Br J Surg. 1980;67(6):439–42.PubMedCrossRef Talbot IC, Ritchie S, Leighton MH, et al. The clinical significance of invasion of veins by rectal cancer. Br J Surg. 1980;67(6):439–42.PubMedCrossRef
63.
go back to reference Günther K, Dworak O, Remke S, et al. Prediction of distant metastases after curative surgery for rectal cancer. J Surg Res. 2002;103(1):68–78.PubMedCrossRef Günther K, Dworak O, Remke S, et al. Prediction of distant metastases after curative surgery for rectal cancer. J Surg Res. 2002;103(1):68–78.PubMedCrossRef
64.
go back to reference Smith NJ, Barbachano Y, Norman AR, et al. Prognostic significance of magnetic resonance imaging-detected extramural vascular invasion in rectal cancer. Br J Surg. 2008;95(2):229–36.PubMedCrossRef Smith NJ, Barbachano Y, Norman AR, et al. Prognostic significance of magnetic resonance imaging-detected extramural vascular invasion in rectal cancer. Br J Surg. 2008;95(2):229–36.PubMedCrossRef
65.
go back to reference Slesser AA, Khan F, Chau I, et al. The effect of a primary tumour resection on the progression of synchronous colorectal liver metastases: an exploratory study. Eur J Surg Oncol. 2015;41(4):484–92.PubMedCrossRef Slesser AA, Khan F, Chau I, et al. The effect of a primary tumour resection on the progression of synchronous colorectal liver metastases: an exploratory study. Eur J Surg Oncol. 2015;41(4):484–92.PubMedCrossRef
66.
go back to reference Hugen N, Van de Velde CJ, De Wilt JH, et al. Metastatic pattern in colorectal cancer is strongly influenced by histological subtype. Ann Oncol. 2014;25(3):651–7.PubMedPubMedCentralCrossRef Hugen N, Van de Velde CJ, De Wilt JH, et al. Metastatic pattern in colorectal cancer is strongly influenced by histological subtype. Ann Oncol. 2014;25(3):651–7.PubMedPubMedCentralCrossRef
67.
go back to reference Grant MJ, Booth A. A typology of reviews: an analysis of 14 review types and associated methodologies. Health Information Libraries J. 2009;26(2):91–108.CrossRef Grant MJ, Booth A. A typology of reviews: an analysis of 14 review types and associated methodologies. Health Information Libraries J. 2009;26(2):91–108.CrossRef
68.
go back to reference Ioannidis JP. The mass production of redundant, misleading, and conflicted systematic reviews and meta-analyses. Milbank Quarterly. 2016;94(3):485–514.PubMedCrossRefPubMedCentral Ioannidis JP. The mass production of redundant, misleading, and conflicted systematic reviews and meta-analyses. Milbank Quarterly. 2016;94(3):485–514.PubMedCrossRefPubMedCentral
69.
go back to reference Greco T, Zangrillo A, Biondi-Zoccai G, Landoni G. Meta-analysis: pitfalls and hints. Heart Lung Vessel. 2013;5(4):219–25.PubMedPubMedCentral Greco T, Zangrillo A, Biondi-Zoccai G, Landoni G. Meta-analysis: pitfalls and hints. Heart Lung Vessel. 2013;5(4):219–25.PubMedPubMedCentral
70.
go back to reference Bellou V, Belbasis L, Tzoulaki I, et al. Environmental risk factors and Parkinson’s disease: an umbrella review of meta-analyses. Parkinsonism Relat Disord. 2016;23:1–9.PubMedCrossRef Bellou V, Belbasis L, Tzoulaki I, et al. Environmental risk factors and Parkinson’s disease: an umbrella review of meta-analyses. Parkinsonism Relat Disord. 2016;23:1–9.PubMedCrossRef
71.
go back to reference Theodoratou E, Tzoulaki I, Zgaga L, et al. Vitamin D and multiple health outcomes: umbrella review of systematic reviews and meta-analyses of observational studies and randomised trials. Bmj. 2014;348:g2035.PubMedPubMedCentralCrossRef Theodoratou E, Tzoulaki I, Zgaga L, et al. Vitamin D and multiple health outcomes: umbrella review of systematic reviews and meta-analyses of observational studies and randomised trials. Bmj. 2014;348:g2035.PubMedPubMedCentralCrossRef
72.
go back to reference Belbasis L, Savvidou MD, Kanu C, et al. Birth weight in relation to health and disease in later life: an umbrella review of systematic reviews and meta-analyses. BMC Med. 2016;14(1):147.PubMedPubMedCentralCrossRef Belbasis L, Savvidou MD, Kanu C, et al. Birth weight in relation to health and disease in later life: an umbrella review of systematic reviews and meta-analyses. BMC Med. 2016;14(1):147.PubMedPubMedCentralCrossRef
Metadata
Title
Risk factors and risk prediction models for colorectal cancer metastasis and recurrence: an umbrella review of systematic reviews and meta-analyses of observational studies
Authors
Wei Xu
Yazhou He
Yuming Wang
Xue Li
Jane Young
John P. A. Ioannidis
Malcolm G. Dunlop
Evropi Theodoratou
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2020
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/s12916-020-01618-6

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