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Radiologic T staging of colon cancer: renewed interest for clinical practice

  • Special Section: Rectal Cancer
  • Published:
Abdominal Radiology Aims and scope Submit manuscript

Abstract

Radiologic imaging, especially MRI, has long been the mainstay for rectal cancer staging and patient selection for neoadjuvant therapy prior to surgical resection. In contrast, colonoscopy and CT have been the standard for colon cancer diagnosis and metastasis staging with T and N staging often performed at the time of surgical resection. With recent clinical trials exploring the expansion of the use of neoadjuvant therapy beyond the anorectum to the remainder of the colon, the current and future state of colon cancer treatment is evolving with a renewed interest in evaluating the role radiology may play in the primary T staging of colon cancer. The performance of CT, CT colonography, MRI, and FDG PET-CT for colon cancer staging will be reviewed. N staging will also be briefly discussed. It is expected that accurate radiologic T staging will significantly impact future clinical decisions regarding the neoadjuvant versus surgical management of colon cancer.

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References

  1. Siegel RL, Miller KD, Fuchs HE, Jemal A (2022) Cancer statistics, 2022. CA Cancer J Clin 72 (1):7-33. doi:https://doi.org/10.3322/caac.21708

    Article  PubMed  Google Scholar 

  2. Rahib L, Wehner MR, Matrisian LM, Nead KT (2021) Estimated Projection of US Cancer Incidence and Death to 2040. JAMA Netw Open 4 (4):e214708. doi:https://doi.org/10.1001/jamanetworkopen.2021.4708

    Article  PubMed  PubMed Central  Google Scholar 

  3. Chen FW, Sundaram V, Chew TA, Ladabaum U (2017) Advanced-Stage Colorectal Cancer in Persons Younger Than 50 Years Not Associated With Longer Duration of Symptoms or Time to Diagnosis. Clin Gastroenterol Hepatol 15 (5):728-737 e723. doi:https://doi.org/10.1016/j.cgh.2016.10.038

    Article  PubMed  Google Scholar 

  4. Osterman E, Glimelius B (2018) Recurrence Risk After Up-to-Date Colon Cancer Staging, Surgery, and Pathology: Analysis of the Entire Swedish Population. Dis Colon Rectum 61 (9):1016-1025. doi:https://doi.org/10.1097/DCR.0000000000001158

    Article  PubMed  Google Scholar 

  5. Bockelman C, Engelmann BE, Kaprio T, Hansen TF, Glimelius B (2015) Risk of recurrence in patients with colon cancer stage II and III: a systematic review and meta-analysis of recent literature. Acta Oncol 54 (1):5-16. doi:https://doi.org/10.3109/0284186X.2014.975839

    Article  PubMed  Google Scholar 

  6. Wilkinson NW, Yothers G, Lopa S, Costantino JP, Petrelli NJ, Wolmark N (2010) Long-term survival results of surgery alone versus surgery plus 5-fluorouracil and leucovorin for stage II and stage III colon cancer: pooled analysis of NSABP C-01 through C-05. A baseline from which to compare modern adjuvant trials. Ann Surg Oncol 17 (4):959-966. doi:https://doi.org/10.1245/s10434-009-0881-y

    Article  PubMed  PubMed Central  Google Scholar 

  7. Shi Q, Andre T, Grothey A, Yothers G, Hamilton SR, Bot BM, Haller DG, Van Cutsem E, Twelves C, Benedetti JK, O'Connell MJ, Sargent DJ (2013) Comparison of outcomes after fluorouracil-based adjuvant therapy for stages II and III colon cancer between 1978 to 1995 and 1996 to 2007: evidence of stage migration from the ACCENT database. J Clin Oncol 31 (29):3656-3663. doi:https://doi.org/10.1200/JCO.2013.49.4344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Benson AB, Venook AP, Al-Hawary MM, Arain MA, Chen YJ, Ciombor KK, Cohen S, Cooper HS, Deming D, Garrido-Laguna I, Grem JL, Gunn A, Hoffe S, Hubbard J, Hunt S, Kirilcuk N, Krishnamurthi S, Messersmith WA, Meyerhardt J, Miller ED, Mulcahy MF, Nurkin S, Overman MJ, Parikh A, Patel H, Pedersen K, Saltz L, Schneider C, Shibata D, Skibber JM, Sofocleous CT, Stoffel EM, Stotsky-Himelfarb E, Willett CG, Johnson-Chilla A, Gurski LA (2020) NCCN Guidelines Insights: Rectal Cancer, Version 6.2020. J Natl Compr Canc Netw 18 (7):806-815. doi:https://doi.org/10.6004/jnccn.2020.0032

    Article  Google Scholar 

  9. Costas-Chavarri A, Nandakumar G, Temin S, Lopes G, Cervantes A, Cruz Correa M, Engineer R, Hamashima C, Ho GF, Huitzil FD, Malekzadeh Moghani M, Sharara AI, Stern MC, Teh C, Vazquez Manjarrez SE, Verjee A, Yantiss R, Shah MA (2019) Treatment of Patients With Early-Stage Colorectal Cancer: ASCO Resource-Stratified Guideline. J Glob Oncol 5:1-19. doi:https://doi.org/10.1200/JGO.18.00214

    Article  PubMed  Google Scholar 

  10. Labianca R, Nordlinger B, Beretta GD, Mosconi S, Mandala M, Cervantes A, Arnold D, Group EGW (2013) Early colon cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 24 Suppl 6:vi64–72. doi:https://doi.org/10.1093/annonc/mdt354

  11. Benson AB, Venook AP, Al-Hawary MM, Arain MA, Chen YJ, Ciombor KK, Cohen S, Cooper HS, Deming D, Farkas L, Garrido-Laguna I, Grem JL, Gunn A, Hecht JR, Hoffe S, Hubbard J, Hunt S, Johung KL, Kirilcuk N, Krishnamurthi S, Messersmith WA, Meyerhardt J, Miller ED, Mulcahy MF, Nurkin S, Overman MJ, Parikh A, Patel H, Pedersen K, Saltz L, Schneider C, Shibata D, Skibber JM, Sofocleous CT, Stoffel EM, Stotsky-Himelfarb E, Willett CG, Gregory KM, Gurski LA (2021) Colon Cancer, Version 2.2021, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw 19 (3):329-359. doi:https://doi.org/10.6004/jnccn.2021.0012

    Article  PubMed  Google Scholar 

  12. Andre T, Boni C, Navarro M, Tabernero J, Hickish T, Topham C, Bonetti A, Clingan P, Bridgewater J, Rivera F, de Gramont A (2009) Improved overall survival with oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment in stage II or III colon cancer in the MOSAIC trial. J Clin Oncol 27 (19):3109-3116. doi:https://doi.org/10.1200/JCO.2008.20.6771

    Article  CAS  PubMed  Google Scholar 

  13. Kubicka S (2016) [Capecitabine Plus Oxaliplatin Compared With Fluorouracil/Folinic Acid As Adjuvant Therapy for Stage III Colon Cancer: Final Results of the NO16968 Randomized Controlled Phase III Trial]. Strahlenther Onkol 192 (7):505-506. doi:https://doi.org/10.1007/s00066-016-0991-y

    Article  PubMed  Google Scholar 

  14. Yothers G, O'Connell MJ, Allegra CJ, Kuebler JP, Colangelo LH, Petrelli NJ, Wolmark N (2011) Oxaliplatin as adjuvant therapy for colon cancer: updated results of NSABP C-07 trial, including survival and subset analyses. J Clin Oncol 29 (28):3768-3774. doi:https://doi.org/10.1200/JCO.2011.36.4539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Andre T, Boni C, Mounedji-Boudiaf L, Navarro M, Tabernero J, Hickish T, Topham C, Zaninelli M, Clingan P, Bridgewater J, Tabah-Fisch I, de Gramont A, Multicenter International Study of Oxaliplatin/5-Fluorouracil/Leucovorin in the Adjuvant Treatment of Colon Cancer I (2004) Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer. N Engl J Med 350 (23):2343-2351. doi:https://doi.org/10.1056/NEJMoa032709

    Article  CAS  PubMed  Google Scholar 

  16. Des Guetz G, Nicolas P, Perret GY, Morere JF, Uzzan B (2010) Does delaying adjuvant chemotherapy after curative surgery for colorectal cancer impair survival? A meta-analysis. Eur J Cancer 46 (6):1049-1055. doi:https://doi.org/10.1016/j.ejca.2010.01.020

    Article  PubMed  Google Scholar 

  17. Gao P, Huang XZ, Song YX, Sun JX, Chen XW, Sun Y, Jiang YM, Wang ZN (2018) Impact of timing of adjuvant chemotherapy on survival in stage III colon cancer: a population-based study. BMC Cancer 18 (1):234. doi:https://doi.org/10.1186/s12885-018-4138-7

    Article  PubMed  PubMed Central  Google Scholar 

  18. Biagi JJ, Raphael MJ, Mackillop WJ, Kong W, King WD, Booth CM (2011) Association between time to initiation of adjuvant chemotherapy and survival in colorectal cancer: a systematic review and meta-analysis. JAMA 305 (22):2335-2342. doi:https://doi.org/10.1001/jama.2011.749

    Article  CAS  PubMed  Google Scholar 

  19. Beijers AJ, Mols F, Tjan-Heijnen VC, Faber CG, van de Poll-Franse LV, Vreugdenhil G (2015) Peripheral neuropathy in colorectal cancer survivors: the influence of oxaliplatin administration. Results from the population-based PROFILES registry. Acta Oncol 54 (4):463-469. doi:https://doi.org/10.3109/0284186X.2014.980912

    Article  CAS  PubMed  Google Scholar 

  20. Seretny M, Currie GL, Sena ES, Ramnarine S, Grant R, MacLeod MR, Colvin LA, Fallon M (2014) Incidence, prevalence, and predictors of chemotherapy-induced peripheral neuropathy: A systematic review and meta-analysis. Pain 155 (12):2461-2470. doi:https://doi.org/10.1016/j.pain.2014.09.020

    Article  PubMed  Google Scholar 

  21. Reinert T, Henriksen TV, Christensen E, Sharma S, Salari R, Sethi H, Knudsen M, Nordentoft I, Wu HT, Tin AS, Heilskov Rasmussen M, Vang S, Shchegrova S, Frydendahl Boll Johansen A, Srinivasan R, Assaf Z, Balcioglu M, Olson A, Dashner S, Hafez D, Navarro S, Goel S, Rabinowitz M, Billings P, Sigurjonsson S, Dyrskjot L, Swenerton R, Aleshin A, Laurberg S, Husted Madsen A, Kannerup AS, Stribolt K, Palmelund Krag S, Iversen LH, Gotschalck Sunesen K, Lin CJ, Zimmermann BG, Lindbjerg Andersen C (2019) Analysis of Plasma Cell-Free DNA by Ultradeep Sequencing in Patients With Stages I to III Colorectal Cancer. JAMA Oncol 5 (8):1124-1131. doi:https://doi.org/10.1001/jamaoncol.2019.0528

    Article  PubMed  PubMed Central  Google Scholar 

  22. Tie J, Cohen JD, Lahouel K, Lo SN, Wang Y, Kosmider S, Wong R, Shapiro J, Lee M, Harris S, Khattak A, Burge M, Harris M, Lynam J, Nott L, Day F, Hayes T, McLachlan SA, Lee B, Ptak J, Silliman N, Dobbyn L, Popoli M, Hruban R, Lennon AM, Papadopoulos N, Kinzler KW, Vogelstein B, Tomasetti C, Gibbs P, Investigators D (2022) Circulating Tumor DNA Analysis Guiding Adjuvant Therapy in Stage II Colon Cancer. N Engl J Med 386 (24):2261-2272. doi:https://doi.org/10.1056/NEJMoa2200075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Tie J, Cohen JD, Lo SN, Wang Y, Li L, Christie M, Lee M, Wong R, Kosmider S, Skinner I, Wong HL, Lee B, Burge ME, Yip D, Karapetis CS, Price TJ, Tebbutt NC, Haydon AM, Ptak J, Schaeffer MJ, Silliman N, Dobbyn L, Popoli M, Tomasetti C, Papadopoulos N, Kinzler KW, Vogelstein B, Gibbs P (2021) Prognostic significance of postsurgery circulating tumor DNA in nonmetastatic colorectal cancer: Individual patient pooled analysis of three cohort studies. International journal of cancer 148 (4):1014-1026. doi:https://doi.org/10.1002/ijc.33312

    Article  CAS  PubMed  Google Scholar 

  24. Tie J, Cohen JD, Wang Y, Christie M, Simons K, Lee M, Wong R, Kosmider S, Ananda S, McKendrick J, Lee B, Cho JH, Faragher I, Jones IT, Ptak J, Schaeffer MJ, Silliman N, Dobbyn L, Li L, Tomasetti C, Papadopoulos N, Kinzler KW, Vogelstein B, Gibbs P (2019) Circulating Tumor DNA Analyses as Markers of Recurrence Risk and Benefit of Adjuvant Therapy for Stage III Colon Cancer. JAMA Oncol 5 (12):1710-1717. doi:https://doi.org/10.1001/jamaoncol.2019.3616

    Article  PubMed  PubMed Central  Google Scholar 

  25. Tie J, Vogelstein B, Gibbs P (2020) Circulating Tumor DNA as a Prognostic Marker in Stage III Colon Cancer-Reply. JAMA Oncol 6 (6):932-933. doi:https://doi.org/10.1001/jamaoncol.2020.0289

    Article  PubMed  Google Scholar 

  26. Tie J, Wang Y, Tomasetti C, Li L, Springer S, Kinde I, Silliman N, Tacey M, Wong HL, Christie M, Kosmider S, Skinner I, Wong R, Steel M, Tran B, Desai J, Jones I, Haydon A, Hayes T, Price TJ, Strausberg RL, Diaz LA, Jr., Papadopoulos N, Kinzler KW, Vogelstein B, Gibbs P (2016) Circulating tumor DNA analysis detects minimal residual disease and predicts recurrence in patients with stage II colon cancer. Sci Transl Med 8 (346):346ra392. doi:https://doi.org/10.1126/scitranslmed.aaf6219

  27. Wang Y, Li L, Cohen JD, Kinde I, Ptak J, Popoli M, Schaefer J, Silliman N, Dobbyn L, Tie J, Gibbs P, Tomasetti C, Kinzler KW, Papadopoulos N, Vogelstein B, Olsson L (2019) Prognostic Potential of Circulating Tumor DNA Measurement in Postoperative Surveillance of Nonmetastatic Colorectal Cancer. JAMA Oncol 5 (8):1118-1123. doi:https://doi.org/10.1001/jamaoncol.2019.0512

    Article  PubMed  PubMed Central  Google Scholar 

  28. Pages F, Mlecnik B, Marliot F, Bindea G, Ou FS, Bifulco C, Lugli A, Zlobec I, Rau TT, Berger MD, Nagtegaal ID, Vink-Borger E, Hartmann A, Geppert C, Kolwelter J, Merkel S, Grutzmann R, Van den Eynde M, Jouret-Mourin A, Kartheuser A, Leonard D, Remue C, Wang JY, Bavi P, Roehrl MHA, Ohashi PS, Nguyen LT, Han S, MacGregor HL, Hafezi-Bakhtiari S, Wouters BG, Masucci GV, Andersson EK, Zavadova E, Vocka M, Spacek J, Petruzelka L, Konopasek B, Dundr P, Skalova H, Nemejcova K, Botti G, Tatangelo F, Delrio P, Ciliberto G, Maio M, Laghi L, Grizzi F, Fredriksen T, Buttard B, Angelova M, Vasaturo A, Maby P, Church SE, Angell HK, Lafontaine L, Bruni D, El Sissy C, Haicheur N, Kirilovsky A, Berger A, Lagorce C, Meyers JP, Paustian C, Feng Z, Ballesteros-Merino C, Dijkstra J, van de Water C, van Lent-van Vliet S, Knijn N, Musina AM, Scripcariu DV, Popivanova B, Xu M, Fujita T, Hazama S, Suzuki N, Nagano H, Okuno K, Torigoe T, Sato N, Furuhata T, Takemasa I, Itoh K, Patel PS, Vora HH, Shah B, Patel JB, Rajvik KN, Pandya SJ, Shukla SN, Wang Y, Zhang G, Kawakami Y, Marincola FM, Ascierto PA, Sargent DJ, Fox BA, Galon J (2018) International validation of the consensus Immunoscore for the classification of colon cancer: a prognostic and accuracy study. Lancet 391 (10135):2128-2139. doi:https://doi.org/10.1016/S0140-6736(18)30789-X

  29. Taieb J, Zaanan A, Le Malicot K, Julie C, Blons H, Mineur L, Bennouna J, Tabernero J, Mini E, Folprecht G, Van Laethem JL, Lepage C, Emile JF, Laurent-Puig P (2016) Prognostic Effect of BRAF and KRAS Mutations in Patients With Stage III Colon Cancer Treated With Leucovorin, Fluorouracil, and Oxaliplatin With or Without Cetuximab: A Post Hoc Analysis of the PETACC-8 Trial. JAMA Oncol 2 (5):643-653. doi:https://doi.org/10.1001/jamaoncol.2015.5225

    Article  PubMed  Google Scholar 

  30. Chakrabarti S, Peterson CY, Sriram D, Mahipal A (2020) Early stage colon cancer: Current treatment standards, evolving paradigms, and future directions. World J Gastrointest Oncol 12 (8):808-832. doi:https://doi.org/10.4251/wjgo.v12.i8.808

    Article  PubMed  PubMed Central  Google Scholar 

  31. Bertagnolli MM, Redston M, Compton CC, Niedzwiecki D, Mayer RJ, Goldberg RM, Colacchio TA, Saltz LB, Warren RS (2011) Microsatellite instability and loss of heterozygosity at chromosomal location 18q: prospective evaluation of biomarkers for stages II and III colon cancer--a study of CALGB 9581 and 89803. J Clin Oncol 29 (23):3153-3162. doi:https://doi.org/10.1200/JCO.2010.33.0092

    Article  PubMed  PubMed Central  Google Scholar 

  32. Boland CR, Goel A (2010) Microsatellite instability in colorectal cancer. Gastroenterology 138 (6):2073-2087 e2073. doi:https://doi.org/10.1053/j.gastro.2009.12.064

    Article  CAS  PubMed  Google Scholar 

  33. Koenig JL, Toesca DAS, Harris JP, Tsai CJ, Haraldsdottir S, Lin AY, Pollom EL, Chang DT (2019) Microsatellite Instability and Adjuvant Chemotherapy in Stage II Colon Cancer. Am J Clin Oncol 42 (7):573-580. doi:https://doi.org/10.1097/COC.0000000000000554

    Article  CAS  PubMed  Google Scholar 

  34. Popat S, Hubner R, Houlston RS (2005) Systematic review of microsatellite instability and colorectal cancer prognosis. J Clin Oncol 23 (3):609-618. doi:https://doi.org/10.1200/JCO.2005.01.086

    Article  CAS  PubMed  Google Scholar 

  35. Zaanan A, Flejou JF, Emile JF, Des GG, Cuilliere-Dartigues P, Malka D, Lecaille C, Validire P, Louvet C, Rougier P, de Gramont A, Bonnetain F, Praz F, Taieb J (2011) Defective mismatch repair status as a prognostic biomarker of disease-free survival in stage III colon cancer patients treated with adjuvant FOLFOX chemotherapy. Clin Cancer Res 17 (23):7470-7478. doi:https://doi.org/10.1158/1078-0432.CCR-11-1048

    Article  CAS  PubMed  Google Scholar 

  36. Zaanan A, Shi Q, Taieb J, Alberts SR, Meyers JP, Smyrk TC, Julie C, Zawadi A, Tabernero J, Mini E, Goldberg RM, Folprecht G, Van Laethem JL, Le Malicot K, Sargent DJ, Laurent-Puig P, Sinicrope FA (2018) Role of Deficient DNA Mismatch Repair Status in Patients With Stage III Colon Cancer Treated With FOLFOX Adjuvant Chemotherapy: A Pooled Analysis From 2 Randomized Clinical Trials. JAMA Oncol 4 (3):379-383. doi:https://doi.org/10.1001/jamaoncol.2017.2899

    Article  PubMed  Google Scholar 

  37. Tohme S, Simmons RL, Tsung A (2017) Surgery for Cancer: A Trigger for Metastases. Cancer Res 77 (7):1548-1552. doi:https://doi.org/10.1158/0008-5472.CAN-16-1536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Foxtrot Collaborative G (2012) Feasibility of preoperative chemotherapy for locally advanced, operable colon cancer: the pilot phase of a randomised controlled trial. Lancet Oncol 13 (11):1152-1160. doi:https://doi.org/10.1016/S1470-2045(12)70348-0

    Article  CAS  Google Scholar 

  39. Jakobsen A, Andersen F, Fischer A, Jensen LH, Jorgensen JC, Larsen O, Lindebjerg J, Ploen J, Rafaelsen SR, Vilandt J (2015) Neoadjuvant chemotherapy in locally advanced colon cancer. A phase II trial. Acta Oncol 54 (10):1747-1753. doi:https://doi.org/10.3109/0284186X.2015.1037007

    Article  CAS  PubMed  Google Scholar 

  40. Dehal AN, Graff-Baker AN, Vuong B, Nelson D, Chang SC, Lee DY, Goldfarb M, Bilchik AJ (2018) Correlation Between Clinical and Pathologic Staging in Colon Cancer: Implications for Neoadjuvant Treatment. J Gastrointest Surg 22 (10):1764-1771. doi:https://doi.org/10.1007/s11605-018-3777-y

    Article  PubMed  Google Scholar 

  41. Dighe S, Swift I, Magill L, Handley K, Gray R, Quirke P, Morton D, Seymour M, Warren B, Brown G (2012) Accuracy of radiological staging in identifying high-risk colon cancer patients suitable for neoadjuvant chemotherapy: a multicentre experience. Colorectal Dis 14 (4):438-444. doi:https://doi.org/10.1111/j.1463-1318.2011.02638.x

    Article  CAS  PubMed  Google Scholar 

  42. Jakobsen A Neoadjuvant chemotherapy versus standard treatment in patients with locally advanced colon cancer. https://clinicaltrials.gov/ct2/show/NCT01918527. 11/8/2022

  43. Karoui M, Rullier A, Piessen G, Legoux JL, Barbier E, De Chaisemartin C, Lecaille C, Bouche O, Ammarguellat H, Brunetti F, Prudhomme M, Regimbeau JM, Glehen O, Lievre A, Portier G, Hartwig J, Goujon G, Romain B, Lepage C, Taieb J, for Pic (2020) Perioperative FOLFOX 4 Versus FOLFOX 4 Plus Cetuximab Versus Immediate Surgery for High-Risk Stage II and III Colon Cancers: A Phase II Multicenter Randomized Controlled Trial (PRODIGE 22). Annals of surgery 271 (4):637-645. doi:https://doi.org/10.1097/SLA.0000000000003454

    Article  CAS  PubMed  Google Scholar 

  44. Chalabi M, Fanchi LF, Dijkstra KK, Van den Berg JG, Aalbers AG, Sikorska K, Lopez-Yurda M, Grootscholten C, Beets GL, Snaebjornsson P, Maas M, Mertz M, Veninga V, Bounova G, Broeks A, Beets-Tan RG, de Wijkerslooth TR, van Lent AU, Marsman HA, Nuijten E, Kok NF, Kuiper M, Verbeek WH, Kok M, Van Leerdam ME, Schumacher TN, Voest EE, Haanen JB (2020) Neoadjuvant immunotherapy leads to pathological responses in MMR-proficient and MMR-deficient early-stage colon cancers. Nat Med 26 (4):566-576. doi:https://doi.org/10.1038/s41591-020-0805-8

    Article  CAS  PubMed  Google Scholar 

  45. van den Berg I, van de Weerd S, Roodhart JML, Vink GR, van den Braak R, Jimenez CR, Elias SG, van Vliet D, Koelink M, Hong E, van Grevenstein WMU, van Oijen MGH, Beets-Tan RGH, van Krieken J, JNM IJ, Medema JP, Koopman M, group CO-s (2020) Improving clinical management of colon cancer through CONNECTION, a nation-wide colon cancer registry and stratification effort (CONNECTION II trial): rationale and protocol of a single arm intervention study. BMC Cancer 20 (1):776. doi:https://doi.org/10.1186/s12885-020-07236-y

    Article  PubMed  PubMed Central  Google Scholar 

  46. Riva F, Bidard FC, Houy A, Saliou A, Madic J, Rampanou A, Hego C, Milder M, Cottu P, Sablin MP, Vincent-Salomon A, Lantz O, Stern MH, Proudhon C, Pierga JY (2017) Patient-Specific Circulating Tumor DNA Detection during Neoadjuvant Chemotherapy in Triple-Negative Breast Cancer. Clin Chem 63 (3):691-699. doi:https://doi.org/10.1373/clinchem.2016.262337

    Article  CAS  PubMed  Google Scholar 

  47. Bahadoer RR, Dijkstra EA, van Etten B, Marijnen CAM, Putter H, Kranenbarg EM, Roodvoets AGH, Nagtegaal ID, Beets-Tan RGH, Blomqvist LK, Fokstuen T, Ten Tije AJ, Capdevila J, Hendriks MP, Edhemovic I, Cervantes A, Nilsson PJ, Glimelius B, van de Velde CJH, Hospers GAP, investigators Rc (2021) Short-course radiotherapy followed by chemotherapy before total mesorectal excision (TME) versus preoperative chemoradiotherapy, TME, and optional adjuvant chemotherapy in locally advanced rectal cancer (RAPIDO): a randomised, open-label, phase 3 trial. Lancet Oncol 22 (1):29-42. doi:https://doi.org/10.1016/S1470-2045(20)30555-6

    Article  CAS  PubMed  Google Scholar 

  48. Acunas B, Rozanes I, Acunas G, Celik L, Sayi I, Gokmen E (1990) Preoperative CT staging of colon carcinoma (excluding the recto-sigmoid region). Eur J Radiol 11 (2):150-153. doi:https://doi.org/10.1016/0720-048x(90)90166-9

    Article  CAS  PubMed  Google Scholar 

  49. Balthazar EJ, Megibow AJ, Hulnick D, Naidich DP (1988) Carcinoma of the colon: detection and preoperative staging by CT. AJR Am J Roentgenol 150 (2):301-306. doi:https://doi.org/10.2214/ajr.150.2.301

    Article  CAS  PubMed  Google Scholar 

  50. Keeney G, Jafri SZ, Mezwa DG (1989) Computed tomographic evaluation and staging of cecal carcinoma. Gastrointest Radiol 14 (1):65-69. doi:https://doi.org/10.1007/BF01889158

    Article  CAS  PubMed  Google Scholar 

  51. Dighe S, Blake H, Koh MD, Swift I, Arnaout A, Temple L, Barbachano Y, Brown G (2010) Accuracy of multidetector computed tomography in identifying poor prognostic factors in colonic cancer. Br J Surg 97 (9):1407-1415. doi:https://doi.org/10.1002/bjs.7096

    Article  CAS  PubMed  Google Scholar 

  52. Malmstrom ML, Brisling S, Klausen TW, Saftoiu A, Perner T, Vilmann P, Gogenur I (2018) Staging with computed tomography of patients with colon cancer. Int J Colorectal Dis 33 (1):9-17. doi:https://doi.org/10.1007/s00384-017-2932-3

    Article  CAS  PubMed  Google Scholar 

  53. Norgaard A, Dam C, Jakobsen A, Ploen J, Lindebjerg J, Rafaelsen SR (2014) Selection of colon cancer patients for neoadjuvant chemotherapy by preoperative CT scan. Scand J Gastroenterol 49 (2):202-208. doi:https://doi.org/10.3109/00365521.2013.862294

    Article  CAS  PubMed  Google Scholar 

  54. Olsen ASF, Gundestrup AK, Kleif J, Thanon T, Bertelsen CA (2021) Accuracy of preoperative staging with multidetector computed tomography in colon cancer. Colorectal Dis 23 (3):680-688. doi:https://doi.org/10.1111/codi.15415

    Article  CAS  PubMed  Google Scholar 

  55. Park H, Cho SH, Kim JE, Moon SK, Park BG, Seo AN, Kim SH, Kim GC, Ryeom H, Choi GS (2020) Potential image-based criteria of neoadjuvant chemotherapy for colon cancer: multireaders' diagnostic performance. Abdominal radiology (New York) 45 (10):2997-3006. doi:https://doi.org/10.1007/s00261-019-02243-5

    Article  PubMed  Google Scholar 

  56. Smith NJ, Bees N, Barbachano Y, Norman AR, Swift RI, Brown G (2007) Preoperative computed tomography staging of nonmetastatic colon cancer predicts outcome: implications for clinical trials. Br J Cancer 96 (7):1030-1036. doi:https://doi.org/10.1038/sj.bjc.6603646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Nerad E, Lahaye MJ, Maas M, Nelemans P, Bakers FC, Beets GL, Beets-Tan RG (2016) Diagnostic Accuracy of CT for Local Staging of Colon Cancer: A Systematic Review and Meta-Analysis. AJR Am J Roentgenol 207 (5):984-995. doi:https://doi.org/10.2214/AJR.15.15785

    Article  PubMed  Google Scholar 

  58. Horvat N, Raj A, Liu S, Matkowskyj KA, Knezevic A, Capanu M, Shia J, Pickhardt PJ, Gollub MJ (2019) CT Colonography in Preoperative Staging of Colon Cancer: Evaluation of FOxTROT Inclusion Criteria for Neoadjuvant Therapy. AJR Am J Roentgenol 212 (1):94-102. doi:https://doi.org/10.2214/AJR.18.19928

    Article  PubMed  Google Scholar 

  59. Chung DJ, Huh KC, Choi WJ, Kim JK (2005) CT colonography using 16-MDCT in the evaluation of colorectal cancer. AJR Am J Roentgenol 184 (1):98-103. doi:https://doi.org/10.2214/ajr.184.1.01840098

    Article  PubMed  Google Scholar 

  60. da Fonte AC, Chojniak R, de Oliveira Ferreira F, Pinto PN, dos Santos Neto PJ, Bitencourt AG (2012) Inclusion of computed tomographic colonography on pre-operative CT for patients with colorectal cancer. Eur J Radiol 81 (3):e298-303. doi:https://doi.org/10.1016/j.ejrad.2011.10.017

    Article  PubMed  Google Scholar 

  61. Filippone A, Ambrosini R, Fuschi M, Marinelli T, Genovesi D, Bonomo L (2004) Preoperative T and N staging of colorectal cancer: accuracy of contrast-enhanced multi-detector row CT colonography--initial experience. Radiology 231 (1):83-90. doi:https://doi.org/10.1148/radiol.2311021152

    Article  PubMed  Google Scholar 

  62. Flor N, Mezzanzanica M, Rigamonti P, Rocco EG, Bosari S, Ceretti AP, Soldi S, Peri M, Sardanelli F, Cornalba GP (2013) Contrast-enhanced computed tomography colonography in preoperative distinction between T1-T2 and T3-T4 staging of colon cancer. Acad Radiol 20 (5):590-595. doi:https://doi.org/10.1016/j.acra.2013.01.008

    Article  PubMed  Google Scholar 

  63. Jin KN, Lee JM, Kim SH, Shin KS, Lee JY, Han JK, Choi BI (2006) The diagnostic value of multiplanar reconstruction on MDCT colonography for the preoperative staging of colorectal cancer. Eur Radiol 16 (10):2284-2291. doi:https://doi.org/10.1007/s00330-006-0316-0

    Article  PubMed  Google Scholar 

  64. Komono A, Kajitani R, Matsumoto Y, Nagano H, Yoshimatsu G, Aisu N, Urakawa H, Hasegawa S (2021) Preoperative T staging of advanced colorectal cancer by computed tomography colonography. International Journal of Colorectal Disease 36 (11):2489-2496. doi:https://doi.org/10.1007/s00384-021-03971-1

    Article  PubMed  Google Scholar 

  65. Komono A, Shida D, Iinuma G, Tsukamoto S, Sakamoto R, Moritani K, Miyake M, Kanemitsu Y (2019) Preoperative T staging of colon cancer using CT colonography with multiplanar reconstruction: new diagnostic criteria based on "bordering vessels". International Journal of Colorectal Disease 34 (4):641-648. doi:https://doi.org/10.1007/s00384-019-03236-y

    Article  PubMed  Google Scholar 

  66. Laghi A, Iannaccone R, Trenna S, Mangiapane F, Sinibaldi G, Piacentini F, Sammartino P, Stipa V, Passariello R (2002) Multislice spiral CT colonography in the evaluation of colorectal neoplasms. La Radiologia medica 104 (5-6):394-403

    PubMed  Google Scholar 

  67. Mainenti PP, Cirillo LC, Camera L, Persico F, Cantalupo T, Pace L, De Palma GD, Persico G, Salvatore M (2006) Accuracy of single phase contrast enhanced multidetector CT colonography in the preoperative staging of colo-rectal cancer. Eur J Radiol 60 (3):453-459. doi:https://doi.org/10.1016/j.ejrad.2006.08.001

    Article  PubMed  Google Scholar 

  68. Maupoey Ibanez J, Pamies Guilabert J, Frasson M, Bosca Robledo A, Giner Segura F, Garcia-Granero Ximenez E (2019) Accuracy of CT colonography in the preoperative staging of colon cancer: a prospective study of 217 patients. Colorectal Disease 21 (10):1151-1163. doi:https://doi.org/10.1111/codi.14724

    Article  CAS  PubMed  Google Scholar 

  69. Nagata K, Endo S, Kudo SE, Kitanosono T, Kushihashi T (2004) CT air-contrast enema as a preoperative examination for colorectal cancer. Dig Surg 21 (5-6):352-358. doi:https://doi.org/10.1159/000081543

    Article  PubMed  Google Scholar 

  70. Narayanan S, Kalra N, Bhatia A, Wig J, Rana S, Bhasin D, Vaiphei K, Khandelwal N (2014) Staging of colorectal cancer using contrast-enhanced multidetector computed tomographic colonography. Singapore Med J 55 (12):660-666. doi:https://doi.org/10.11622/smedj.2014182

    Article  PubMed  PubMed Central  Google Scholar 

  71. Sato K, Tanaka T, Sato J, Shibata E, Nagai Y, Murono K, Yasuda K, Otani K, Nishikawa T, Tanaka J, Kiyomatsu T, Hata K, Kawai K, Nozawa H, Kazama S, Yamaguchi H, Ishihara S, Sunami E, Kitayama J, Ohtomo K, Watanabe T (2017) Usefulness of preoperative CT colonography for colon cancer. Asian J Surg 40 (6):438-443. doi:https://doi.org/10.1016/j.asjsur.2016.04.002

    Article  PubMed  Google Scholar 

  72. Stabile Ianora AA, Moschetta M, Pedote P, Scardapane A, Angelelli G (2012) Preoperative local staging of colosigmoideal cancer: air versus water multidetector-row CT colonography. La Radiologia medica 117 (2):254-267. doi:https://doi.org/10.1007/s11547-011-0782-6

    Article  CAS  PubMed  Google Scholar 

  73. Sun CH, Li ZP, Meng QF, Yu SP, Xu DS (2005) Assessment of spiral CT pneumocolon in preoperative colorectal carcinoma. World J Gastroenterol 11 (25):3866-3870. doi:https://doi.org/10.3748/wjg.v11.i25.3866

    Article  PubMed  PubMed Central  Google Scholar 

  74. Tsurumaru D, Takatsu N, Kai S, Oki E, Ishigami K (2021) Measurement of circumferential tumor extent of colorectal cancer on CT colonography: relation to clinicopathological features and patient prognosis after surgery. Japanese Journal of Radiology 39 (10):966-972. doi:https://doi.org/10.1007/s11604-021-01141-5

    Article  PubMed  Google Scholar 

  75. Utano K, Endo K, Togashi K, Sasaki J, Kawamura HJ, Horie H, Nakamura Y, Konishi F, Sugimoto H (2008) Preoperative T staging of colorectal cancer by CT colonography. Dis Colon Rectum 51 (6):875-881. doi:https://doi.org/10.1007/s10350-008-9261-0

    Article  PubMed  Google Scholar 

  76. Pickhardt PJ (2006) Incidence of colonic perforation at CT colonography: review of existing data and implications for screening of asymptomatic adults. Radiology 239 (2):313-316

    Article  PubMed  Google Scholar 

  77. Bates DDB, Homsi ME, Chang KJ, Lalwani N, Horvat N, Sheedy SP (2022) MRI for Rectal Cancer: Staging, mrCRM, EMVI, Lymph Node Staging and Post-Treatment Response. Clin Colorectal Cancer 21 (1):10-18. doi:https://doi.org/10.1016/j.clcc.2021.10.007

    Article  PubMed  Google Scholar 

  78. Feng Q, Yan YQ, Zhu J, Xu JR (2014) T staging of rectal cancer: accuracy of diffusion-weighted imaging compared with T2-weighted imaging on 3.0 tesla MRI. J Dig Dis 15 (4):188-194. doi:https://doi.org/10.1111/1751-2980.12124

    Article  PubMed  Google Scholar 

  79. Kassam Z, Lang R, Arya S, Bates DDB, Chang KJ, Fraum TJ, Friedman KA, Golia Pernicka JS, Gollub MJ, Harisinghani M, Khatri G, Korngold E, Lall C, Lee S, Magnetta M, Moreno C, Nougaret S, Paroder V, Paspulati RM, Petkovska I, Pickhardt PJ, Shaish H, Sheedy S, Weiser MR, Xuan L, Kim DH (2022) Update to the structured MRI report for primary staging of rectal cancer : Perspective from the SAR Disease Focused Panel on Rectal and Anal Cancer. Abdominal radiology (New York) 47 (10):3364-3374. doi:https://doi.org/10.1007/s00261-022-03612-3

    Article  PubMed  Google Scholar 

  80. Maas M, Lambregts DM, Lahaye MJ, Beets GL, Backes W, Vliegen RF, Osinga-de Jong M, Wildberger JE, Beets-Tan RG (2012) T-staging of rectal cancer: accuracy of 3.0 Tesla MRI compared with 1.5 Tesla. Abdom Imaging 37 (3):475-481. doi:https://doi.org/10.1007/s00261-011-9770-5

    Article  PubMed  Google Scholar 

  81. Mulla M, Deb R, Singh R (2010) MRI in T staging of rectal cancer: How effective is it? Indian J Radiol Imaging 20 (2):118-121. doi:https://doi.org/10.4103/0971-3026.63055

    Article  PubMed  PubMed Central  Google Scholar 

  82. Rao SX, Zeng MS, Xu JM, Qin XY, Chen CZ, Li RC, Hou YY (2007) Assessment of T staging and mesorectal fascia status using high-resolution MRI in rectal cancer with rectal distention. World J Gastroenterol 13 (30):4141-4146. doi:https://doi.org/10.3748/wjg.v13.i30.4141

    Article  PubMed  PubMed Central  Google Scholar 

  83. Jayaprakasam VS, Javed-Tayyab S, Gangai N, Zheng J, Capanu M, Bates DDB, Fuqua JL, 3rd, Paroder V, Golia-Pernicka J, Gollub MJ, Petkovska I (2021) Does microenema administration improve the quality of DWI sequences in rectal MRI? Abdominal radiology (New York) 46 (3):858-866. doi:https://doi.org/10.1007/s00261-020-02718-w

    Article  PubMed  Google Scholar 

  84. Dam C, Lindebjerg J, Jakobsen A, Jensen LH, Rahr H, Rafaelsen SR (2017) Local staging of sigmoid colon cancer using MRI. Acta Radiol Open 6 (7):2058460117720957. doi:https://doi.org/10.1177/2058460117720957

    Article  PubMed  PubMed Central  Google Scholar 

  85. Nerad E, Lambregts DM, Kersten EL, Maas M, Bakers FC, van den Bosch HC, Grabsch HI, Beets-Tan RG, Lahaye MJ (2017) MRI for Local Staging of Colon Cancer: Can MRI Become the Optimal Staging Modality for Patients With Colon Cancer? Dis Colon Rectum 60 (4):385-392. doi:https://doi.org/10.1097/DCR.0000000000000794

    Article  PubMed  Google Scholar 

  86. Liu LH, Lv H, Wang ZC, Rao SX, Zeng MS (2019) Performance comparison between MRI and CT for local staging of sigmoid and descending colon cancer. Eur J Radiol 121:108741. doi:https://doi.org/10.1016/j.ejrad.2019.108741

    Article  PubMed  Google Scholar 

  87. Rafaelsen SR, Dam C, Vagn-Hansen C, Moller J, Rahr HB, Sjostrom M, Lindebjerg J, Hansen TF, Pedersen MRV (2022) CT and 3 Tesla MRI in the TN Staging of Colon Cancer: A Prospective, Blind Study. Curr Oncol 29 (2):1069-1079. doi:https://doi.org/10.3390/curroncol29020091

    Article  PubMed  Google Scholar 

  88. Zhao Z, Zhou Y, Jiang M, Dang L (2022) Application Value of MRI Combined with MSCT in Diagnosis and Staging of Colon Carcinoma. Comput Math Methods Med 2022:2593844. doi:https://doi.org/10.1155/2022/2593844

    Article  PubMed  PubMed Central  Google Scholar 

  89. Furukawa H, Ikuma H, Seki A, Yokoe K, Yuen S, Aramaki T, Yamagushi S (2006) Positron emission tomography scanning is not superior to whole body multidetector helical computed tomography in the preoperative staging of colorectal cancer. Gut 55 (7):1007-1011. doi:https://doi.org/10.1136/gut.2005.076273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Nahas CS, Akhurst T, Yeung H, Leibold T, Riedel E, Markowitz AJ, Minsky BD, Paty PB, Weiser MR, Temple LK, Wong WD, Larson SM, Guillem JG (2008) Positron emission tomography detection of distant metastatic or synchronous disease in patients with locally advanced rectal cancer receiving preoperative chemoradiation. Ann Surg Oncol 15 (3):704-711. doi:https://doi.org/10.1245/s10434-007-9626-y

    Article  PubMed  Google Scholar 

  91. Vogel JD, Felder SI, Bhama AR, Hawkins AT, Langenfeld SJ, Shaffer VO, Thorsen AJ, Weiser MR, Chang GJ, Lightner AL, Feingold DL, Paquette IM (2022) The American Society of Colon and Rectal Surgeons Clinical Practice Guidelines for the Management of Colon Cancer. Dis Colon Rectum 65 (2):148-177. doi:https://doi.org/10.1097/DCR.0000000000002323

    Article  PubMed  Google Scholar 

  92. Veit-Haibach P, Kuehle CA, Beyer T, Stergar H, Kuehl H, Schmidt J, Borsch G, Dahmen G, Barkhausen J, Bockisch A, Antoch G (2006) Diagnostic accuracy of colorectal cancer staging with whole-body PET/CT colonography. JAMA 296 (21):2590-2600. doi:https://doi.org/10.1001/jama.296.21.2590

    Article  CAS  PubMed  Google Scholar 

  93. Mainenti PP, Iodice D, Segreto S, Storto G, Magliulo M, De Palma GD, Salvatore M, Pace L (2011) Colorectal cancer and 18FDG-PET/CT: what about adding the T to the N parameter in loco-regional staging? World J Gastroenterol 17 (11):1427-1433. doi:https://doi.org/10.3748/wjg.v17.i11.1427

    Article  PubMed  PubMed Central  Google Scholar 

  94. Liao CY, Chen SW, Wu YC, Chen WT, Yen KY, Hsieh TC, Chen PJ, Kao CH (2014) Correlations between 18F-FDG PET/CT parameters and pathological findings in patients with rectal cancer. Clin Nucl Med 39 (1):e40-45. doi:https://doi.org/10.1097/RLU.0b013e318292f0f6

    Article  PubMed  Google Scholar 

  95. Chen SW, Chen WT, Wu YC, Yen KY, Hsieh TC, Lin TY, Kao CH (2013) Which FDG/PET parameters of the primary tumors in colon or sigmoid cancer provide the best correlation with the pathological findings? Eur J Radiol 82 (9):e405-410. doi:https://doi.org/10.1016/j.ejrad.2013.04.022

    Article  PubMed  Google Scholar 

  96. Suzuki Y, Okabayashi K, Hasegawa H, Tsuruta M, Shigeta K, Murakami K, Kitagawa Y (2016) Metabolic Tumor Volume and Total Lesion Glycolysis in PET/CT Correlate With the Pathological Findings of Colorectal Cancer and Allow Its Accurate Staging. Clin Nucl Med 41 (10):761-765. doi:https://doi.org/10.1097/RLU.0000000000001332

    Article  PubMed  Google Scholar 

  97. Rollven E, Abraham-Nordling M, Holm T, Blomqvist L (2017) Assessment and diagnostic accuracy of lymph node status to predict stage III colon cancer using computed tomography. Cancer Imaging 17 (1):3. doi:https://doi.org/10.1186/s40644-016-0104-2

    Article  PubMed  PubMed Central  Google Scholar 

  98. Sjovall A, Blomqvist L, Egenvall M, Johansson H, Martling A (2016) Accuracy of preoperative T and N staging in colon cancer--a national population-based study. Colorectal Dis 18 (1):73-79. doi:https://doi.org/10.1111/codi.13091

    Article  CAS  PubMed  Google Scholar 

  99. Hong EK, Landolfi F, Castagnoli F, Park SJ, Boot J, Van den Berg J, Lee JM, Beets-Tan R (2021) CT for lymph node staging of Colon cancer: not only size but also location and number of lymph node count. Abdominal radiology (New York) 46 (9):4096-4105. doi:https://doi.org/10.1007/s00261-021-03057-0

    Article  PubMed  Google Scholar 

  100. van de Weerd S, Hong E, van den Berg I, Wijlemans JW, van Vooren J, Prins MW, Wessels FJ, Heeres BC, Roberti S, Nederend J, van Krieken J, Roodhart JML, Beets-Tan RGH, Medema JP (2022) Accurate staging of non-metastatic colon cancer with CT: the importance of training and practice for experienced radiologists and analysis of incorrectly staged cases. Abdominal radiology (New York) 47 (10):3375-3385. doi:https://doi.org/10.1007/s00261-022-03573-7

    Article  PubMed  Google Scholar 

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  1. Department of Radiology, Boston University Medical Center, Radiology- FGH 4001, 820 Harrison Ave, Boston, MA, 02118, USA

    Kevin J. Chang

  2. Department of Radiology, University of Wisconsin School of Medicine and Public Health, Madison, WI, USA

    David H. Kim & Perry J. Pickhardt

  3. Diagnostic Radiology, University of Massachusetts Medical School, Worcester, MA, USA

    Tasneem K. Lalani

  4. Department of Radiology, Memorial Sloan Kettering Cancer Center, New York, NY, USA

    Viktoriya Paroder & David D. B. Bates

  5. Department of Radiology, Columbia University Medical Center, New York, NY, USA

    Hiram Shaish

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KJC, TKL, VP, HS, and DDBB have no relevant conflicts of interest. DHK is Co-founder of VirtuoCTC, Consultant for Viatronix, Medical Advisory Board Digitalartforms, Shareholder Cellectar, and Shareholder Elucent. PJP is a paid consultant for Zebra and Bracco; Shareholder in SHINE and Elucent.

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Chang, K.J., Kim, D.H., Lalani, T.K. et al. Radiologic T staging of colon cancer: renewed interest for clinical practice. Abdom Radiol 48, 2874–2887 (2023). https://doi.org/10.1007/s00261-023-03904-2

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