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MRI-detected extramural vascular invasion potentiates the risk for pathological metastasis to the lateral lymph nodes in rectal cancer

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Abstract

Purpose

Multidisciplinary treatment for locally advanced rectal cancer requires an accurate assessment of the risk of metastasis to the lateral lymph nodes (LNs). We herein aimed to stratify the risk of pathological metastasis to lateral LNs based on the preoperatively detected malignant features.

Methods

All patients with rectal cancer who underwent surgery from January 2016 to July 2020 were identified. We recorded the TNM factors; perirectal and lateral LN sizes; and MRI findings, including mesorectal fascia involvement, extramural vascular invasion (EMVI), tumor site, and tumor distance from the anal verge.

Results

101 patients underwent rectal resection with lateral lymph node dissection, of whom 16 (15.8%) exhibited pathological metastases to the lateral LNs. Univariate analyses demonstrated that lateral LN metastasis was significantly correlated with mrEMVI positivity (p = 0.0023) and a baseline lateral LN short-axis length of ≥ 5 mm (p < 0.0001). These significant associations were confirmed by a multivariate analysis (p = 0.0254 and 0.0027, respectively). The lateral LN metastasis rate was as high as 44% in cases bearing both risk factors, compared to 0% in cases lacking both risk factors.

Conclusion

The results elucidated in this study may contribute to risk stratification, which can be used when determining the indications for lateral lymph node dissection.

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References

  1. Heald RJ, Ryall RD. Recurrence and survival after total mesorectal excision for rectal cancer. Lancet. 1986;1:1479–82.

    Article  CAS  PubMed  Google Scholar 

  2. Adam IJ, Mohamdee MO, Martin IG, Scott N, Finan PJ, Johnston D, et al. Role of circumferential margin involvement in the local recurrence of rectal cancer. Lancet. 1994;344:707–11.

    Article  CAS  PubMed  Google Scholar 

  3. Bosset JF, Collette L, Calais G, Mineur L, Maingon P, Radosevic-Jelic L, et al. Chemotherapy with preoperative radiotherapy in rectal cancer. N Engl J Med. 2006;355:1114–23.

    Article  CAS  PubMed  Google Scholar 

  4. Kapiteijn EMC, Nagtegaal ID, Putter H, Steup WH, Wiggers T, Rutten HJ, et al. Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med. 2001;345:638–46.

    Article  CAS  PubMed  Google Scholar 

  5. Gerard JP, Conroy T, Bonnetain F, Bouche O, Chapet O, Closon-Dejardin MT, et al. Preoperative radiotherapy with or without concurrent fluorouracil and leucovorin in T3–4 rectal cancers: results of FFCD 9203. J Clin Oncol. 2006;24:4620–5.

    Article  PubMed  Google Scholar 

  6. Sauer R, Liersch T, Merkel S, Fietkau R, Hohenberger W, Hess C, et al. Preoperative versus postoperative chemoradiotherapy for locally advanced rectal cancer: results of the German CAO/ARO/AIO-94 randomized phase III trial after a median follow-up of 11 years. J Clin Oncol. 2012;30:1926–33.

    Article  CAS  PubMed  Google Scholar 

  7. Moriya Y, Sugihara K, Akasu T, Fujita S. Nerve-sparing surgery with lateral node dissection for advanced lower rectal cancer. Eur J Cancer. 1995;31A:1229–32.

    Article  CAS  PubMed  Google Scholar 

  8. Sugihara K, Kobayashi H, Kato T, Mori T, Mochizuki H, Kameoka S, et al. Indication and benefit of pelvic sidewall dissection for rectal cancer. Dis Colon Rectum. 2006;49:1663–72.

    Article  PubMed  Google Scholar 

  9. Hashiguchi Y, Muro K, Saito Y, Ito Y, Ajioka Y, Hamaguchi T, et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2019 for the treatment of colorectal cancer. Int J Clin Oncol. 2020;25:1–42.

    Article  PubMed  Google Scholar 

  10. Fujita S, Mizusawa J, Kanemitsu Y, Ito M, Kinugasa Y, Komori K, et al. Mesorectal excision with or without lateral lymph node dissection for clinical stage II/III lower rectal cancer (JCOG0212): a multicenter, randomized controlled, Noninferiority Trial. Ann Surg. 2017;266:201–7.

    Article  PubMed  Google Scholar 

  11. Kusters M, Beets GL, van de Velde CJ, Beets-Tan RG, Marijnen CA, Rutten HJ, et al. A comparison between the treatment of low rectal cancer in Japan and the Netherlands, focusing on the patterns of local recurrence. Ann Surg. 2009;249:229–35.

    Article  PubMed  Google Scholar 

  12. Kim MJ, Kim TH, Kim DY, Kim SY, Baek JY, Chang HJ, et al. Can chemoradiation allow for omission of lateral pelvic node dissection for locally advanced rectal cancer? J Surg Oncol. 2015;111:459–64.

    Article  PubMed  Google Scholar 

  13. Kim TG, Park W, Choi DH, Park HC, Kim SH, Cho YB, et al. Factors associated with lateral pelvic recurrence after curative resection following neoadjuvant chemoradiotherapy in rectal cancer patients. Int J Colorectal Dis. 2014;29:193–200.

    Article  PubMed  Google Scholar 

  14. Kim TH, Jeong SY, Choi DH, Kim DY, Jung KH, Moon SH, et al. Lateral lymph node metastasis is a major cause of locoregional recurrence in rectal cancer treated with preoperative chemoradiotherapy and curative resection. Ann Surg Oncol. 2008;15:729–37.

    Article  PubMed  Google Scholar 

  15. Kusters M, Slater A, Muirhead R, Hompes R, Guy RJ, Jones OM, et al. What to do with lateral nodal disease in low locally advanced rectal cancer? a call for further reflection and research. Dis Colon Rectum. 2017;60:577–85.

    Article  PubMed  Google Scholar 

  16. Ogura A, Konishi T, Cunningham C, Garcia-Aguilar J, Iversen H, Toda S, et al. Neoadjuvant (Chemo)radiotherapy with total mesorectal excision only is not sufficient to prevent lateral local recurrence in enlarged nodes: results of the multicenter lateral node study of patients with low cT3/4 rectal cancer. J Clin Oncol. 2019;37:33–43.

    Article  CAS  PubMed  Google Scholar 

  17. Akiyoshi T, Matsueda K, Hiratsuka M, Unno T, Nagata J, Nagasaki T, et al. Indications for lateral pelvic lymph node dissection based on magnetic resonance imaging before and after preoperative chemoradiotherapy in patients with advanced low-rectal cancer. Ann Surg Oncol. 2015;22:S614–20.

    Article  PubMed  Google Scholar 

  18. Matsuda T, Sumi Y, Yamashita K, Hasegawa H, Yamamoto M, Matsuda Y, et al. Outcomes and prognostic factors of selective lateral pelvic lymph node dissection with preoperative chemoradiotherapy for locally advanced rectal cancer. Int J Colorectal Dis. 2018;33:367–74.

    Article  PubMed  Google Scholar 

  19. Nakanishi R, Yamaguchi T, Akiyoshi T, Nagasaki T, Nagayama S, Mukai T, et al. Laparoscopic and robotic lateral lymph node dissection for rectal cancer. Surg Today. 2020;50:209–16.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Fujita S, Akasu T, Mizusawa J, Saito N, Kinugasa Y, Kanemitsu Y, et al. Postoperative morbidity and mortality after mesorectal excision with and without lateral lymph node dissection for clinical stage II or stage III lower rectal cancer (JCOG0212): results from a multicentre, randomised controlled, non-inferiority trial. Lancet Oncol. 2012;13:616–21.

    Article  PubMed  Google Scholar 

  21. Komori K, Fujita S, Mizusawa J, Kanemitsu Y, Ito M, Shiomi A, et al. Predictive factors of pathological lateral pelvic lymph node metastasis in patients without clinical lateral pelvic lymph node metastasis (clinical stage II/III): the analysis of data from the clinical trial (JCOG0212). Eur J Surg Oncol. 2019;45:336–40.

    Article  PubMed  Google Scholar 

  22. Glynne-Jones R, Wyrwicz L, Tiret E, Brown G, Rödel C, Cervantes A, et al. Rectal cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2017;28:iv22–40.

    Article  CAS  PubMed  Google Scholar 

  23. Benson AB, Venook AP, Al-Hawary MM, Cederquist L, Chen YJ, Ciombor KK, et al. Rectal cancer, version 2.2018, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2018;16:874–901.

    Article  PubMed  Google Scholar 

  24. Battersby NJ, How P, Moran B, Stelzner S, West NP, Branagan G, et al. Prospective validation of a low rectal cancer magnetic resonance imaging staging system and development of a local recurrence risk stratification model: the MERCURY II study. Ann Surg. 2016;263:751–60.

    Article  PubMed  Google Scholar 

  25. Beets-Tan RGH, Lambregts DMJ, Maas M, Bipat S, Barbaro B, Curvo-Semedo L, et al. Magnetic resonance imaging for clinical management of rectal cancer: updated recommendations from the 2016 European Society of Gastrointestinal and Abdominal Radiology (ESGAR) consensus meeting. Eur Radiol. 2018;28:1465–75.

    Article  PubMed  Google Scholar 

  26. Taylor FG, Quirke P, Heald RJ, Moran BJ, Blomqvist L, Swift IR, et al. Preoperative magnetic resonance imaging assessment of circumferential resection margin predicts disease-free survival and local recurrence: 5-year follow-up results of the MERCURY study. J Clin Oncol. 2014;32:34–43.

    Article  PubMed  Google Scholar 

  27. Smith NJ, Barbachano Y, Norman AR, Swift RI, Abulafi AM, Brown G. Prognostic significance of magnetic resonance imaging-detected extramural vascular invasion in rectal cancer. Br J Surg. 2008;95:229–36.

    Article  CAS  PubMed  Google Scholar 

  28. Zhang XY, Wang S, Li XT, Wang YP, Shi YJ, Wang L, et al. MRI of extramural venous invasion in locally advanced rectal cancer: relationship to tumor recurrence and overall survival. Radiology. 2018;289:677–85.

    Article  PubMed  Google Scholar 

  29. Hatakenaka M. Spatial resolution of CT. Eur J Surg Oncol. 2019;45(9):1748.

    Article  PubMed  Google Scholar 

  30. Hasegawa J, Nishimura J, Mizushima T, Miyake Y, Kim HM, Takemoto H, et al. Neoadjuvant capecitabine and oxaliplatin (XELOX) combined with bevacizumab for high-risk localized rectal cancer. Cancer Chemother Pharmacol. 2014;73:1079–87.

    Article  CAS  PubMed  Google Scholar 

  31. Hata T, Takahashi H, Sakai D, Haraguchi N, Nishimura J, Kudo T, et al. Neoadjuvant CapeOx therapy followed by sphincter-preserving surgery for lower rectal cancer. Surg Today. 2017;47:1372–7.

    Article  CAS  PubMed  Google Scholar 

  32. Kamiya T, Uehara K, Nakayama G, Ishigure K, Kobayashi S, Hiramatsu K, et al. Early results of multicenter phase II trial of perioperative oxaliplatin and capecitabine without radiotherapy for high-risk rectal cancer: CORONA I study. Eur J Surg Oncol. 2016;42:829–35.

    Article  CAS  PubMed  Google Scholar 

  33. Kudo T, Takemasa I, Hata T, Sakai D, Takahashi H, Haraguchi N, et al. A phase I study of neoadjuvant capecitabine, oxaliplatin, and irinotecan (XELOXIRI) in patients with locally advanced rectal cancer. Oncology. 2019;97:211–6.

    Article  CAS  PubMed  Google Scholar 

  34. Schrag D, Weiser MR, Goodman KA, Gonen M, Hollywood E, Cercek A, et al. Neoadjuvant chemotherapy without routine use of radiation therapy for patients with locally advanced rectal cancer: a pilot trial. J Clin Oncol. 2014;32:513–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Uehara K, Hiramatsu K, Maeda A, Sakamoto E, Inoue M, Kobayashi S, et al. Neoadjuvant oxaliplatin and capecitabine and bevacizumab without radiotherapy for poor-risk rectal cancer: N-SOG 03 Phase II trial. Jpn J Clin Oncol. 2013;43:964–71.

    Article  PubMed  Google Scholar 

  36. Fujita S, Yamamoto S, Akasu T, Moriya Y. Risk factors of lateral pelvic lymph node metastasis in advanced rectal cancer. Int J Colorectal Dis. 2009;24:1085–90.

    Article  PubMed  Google Scholar 

  37. Ogawa S, Hida J, Ike H, Kinugasa T, Ota M, Shinto E, et al. The important risk factor for lateral pelvic lymph node metastasis of lower rectal cancer is node-positive status on magnetic resonance imaging: study of the Lymph Node Committee of Japanese Society for Cancer of the Colon and Rectum. Int J Colorectal Dis. 2016;31:1719–28.

    Article  PubMed  Google Scholar 

  38. Akiyoshi T, Watanabe T, Miyata S, Kotake K, Muto T, Sugihara K, et al. Results of a Japanese nationwide multi-institutional study on lateral pelvic lymph node metastasis in low rectal cancer: is it regional or distant disease? Ann Surg. 2012;255:1129–34.

    Article  PubMed  Google Scholar 

  39. Brown G, Richards CJ, Bourne MW, Newcombe RG, Radcliffe AG, Dallimore NS, et al. Morphologic predictors of lymph node status in rectal cancer with use of high-spatial-resolution MR imaging with histopathologic comparison. Radiology. 2003;227:371–7.

    Article  PubMed  Google Scholar 

  40. Liu Y, Wang R, Ding Y, Tu S, Liu Y, Qian Y, et al. A predictive nomogram improved diagnostic accuracy and interobserver agreement of perirectal lymph nodes metastases in rectal cancer. Oncotarget. 2016;7:14755–64.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Chand M, Evans J, Swift RI, Tekkis PP, West NP, Stamp G, et al. The prognostic significance of postchemoradiotherapy high-resolution MRI and histopathology detected extramural venous invasion in rectal cancer. Ann Surg. 2015;261:473–9.

    Article  PubMed  Google Scholar 

  42. Siddiqui MRS, Simillis C, Hunter C, Chand M, Bhoday J, Garant A, et al. A meta-analysis comparing the risk of metastases in patients with rectal cancer and MRI-detected extramural vascular invasion (mrEMVI) vs mrEMVI-negative cases. Br J Cancer. 2017;116:1513–9.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Deng Y, Chi P, Lan P, Wang L, Chen W, Cui L, et al. Neoadjuvant modified FOLFOX6 with or without radiation versus fluorouracil plus radiation for locally advanced rectal cancer: final results of the Chinese FOWARC trial. J Clin Oncol. 2019;37:3223–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Brouquet A, Bachet JB, Huguet F, Karoui M, Artru P, Sabbagh C, et al. NORAD01-GRECCAR16 multicenter phase III non-inferiority randomized trial comparing preoperative modified FOLFIRINOX without irradiation to radiochemotherapy for resectable locally advanced rectal cancer (intergroup FRENCH-GRECCAR-PRODIGE trial). BMC Cancer. 2020;20:485.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Achilli P, Grass F, Larson DW. Robotic surgery for rectal cancer as a platform to build on: review of current evidence. Surg Today. 2021;51:44–51.

    Article  PubMed  Google Scholar 

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Acknowledgements

None to be declared.

Funding

This study received no funding.

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Authors and Affiliations

Authors

Contributions

Study concept and design (AH, MI, KO, MH, IT); acquisition of data (AH, MI, KO, KO, TN, KO, EA, RM, TK); analysis and interpretation of data (AH, MI, KO, KO, TN, KO, MH, IT); statistical analysis (AH, MI, KO); drafting of the manuscript (AH, MI, KO, MH, IT).

Corresponding author

Correspondence to Ichiro Takemasa.

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Supplementary Information

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595_2021_2250_MOESM1_ESM.eps

Supplementary Fig 1 Receiver-operating characteristic curve used to analyze the prognostic efficacy of lateral lymph node short-axis length for the risk of pathological metastasis to lateral lymph nodes. The white circle indicates the point at which the cutoff value is 5 mm. The area under the receiver-operating characteristic curve is 0.874 (EPS 141 KB)

595_2021_2250_MOESM2_ESM.tiff

Supplementary Fig. 2 Relapse-free survival rate of patients who had a follow-up period of over three years according to mrEMVI positivity (TIFF 7047 KB)

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Hamabe, A., Ishii, M., Onodera, K. et al. MRI-detected extramural vascular invasion potentiates the risk for pathological metastasis to the lateral lymph nodes in rectal cancer. Surg Today 51, 1583–1593 (2021). https://doi.org/10.1007/s00595-021-02250-4

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  • DOI: https://doi.org/10.1007/s00595-021-02250-4

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