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Published in: World Journal of Surgery 5/2021

01-05-2021 | Rectal Cancer | Scientific Review

Prevalence of Metastatic Lateral Lymph Nodes in Asian Patients with Lateral Lymph Node Dissection for Rectal Cancer: A Meta-analysis

Authors: Niki Christou, Jeremy Meyer, Christophe Combescure, Alexandre Balaphas, Joan Robert-Yap, Nicolas C. Buchs, Frédéric Ris

Published in: World Journal of Surgery | Issue 5/2021

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Abstract

Importance

Rectal cancers occupy the eighth position worldwide for new cases and deaths for both men and women. These cancers have a high tendency to form metastases in the mesorectum but also in the lateral lymph nodes. The therapeutic approach for the involved lateral lymph nodes remains controversial.

Objective

We performed a systematic review and meta-analysis to assess the prevalence of metastatic lateral lymph nodes in patients with lateral lymph node dissection (LLND) for rectal cancer, which seems to be a fundamental and necessary criterion to discuss any possible indications for LLND.

Methods

Data sources–study selection–data extraction and synthesis–main outcome and measures. We searched MEDLINE, EMBASE and COCHRANE from November 1, 2018, to November 19, 2018, for studies reporting the presence of metastatic lateral lymph nodes (iliac, obturator and middle sacral nodes) among patients undergoing rectal surgery with LLND. Pooled prevalence values were obtained by random effects models, and the robustness was tested by leave-one-out sensitivity analyses. Heterogeneity was assessed using the Q-test, quantified based on the I2 value and explored by subgroup analyses.

Results

Our final analysis included 31 studies from Asian countries, comprising 7599 patients. The pooled prevalence of metastatic lateral lymph nodes was 17.3% (95% CI: 14.6–20.5). The inter-study variability (heterogeneity) was high (I2 = 89%). The pooled prevalence was, however, robust and varied between 16.6% and 17.9% according to leave-one-out sensitivity analysis. The pooled prevalence of metastatic lymph nodes was not significantly different when pooling only studies including patients who received neoadjuvant treatment or those without neoadjuvant treatment (p = 0.44). Meta-regression showed that the pooled prevalence was associated with the sample size of studies (p < 0.05), as the prevalence decreased when the sample size increased.

Conclusion

The pooled prevalence of metastatic lateral lymph nodes was 17.3% among patients who underwent rectal surgery with LLND in Asian countries. Further studies are necessary to determine whether this finding could impact the therapeutic strategy (total mesorectal excision with LLND versus total mesorectal excision with neoadjuvant radiochemotherapy).
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Literature
1.
go back to reference Funahashi K, Koike J, Shimada M, Okamoto K, Goto T, Teramoto T (2006) A preliminary study of the draining lymph node basin in advanced lower rectal cancer using a radioactive tracer. Dis Colon Rectum 49(10 Suppl):S53-58CrossRef Funahashi K, Koike J, Shimada M, Okamoto K, Goto T, Teramoto T (2006) A preliminary study of the draining lymph node basin in advanced lower rectal cancer using a radioactive tracer. Dis Colon Rectum 49(10 Suppl):S53-58CrossRef
2.
go back to reference Manfredi S, Benhamiche AM, Meny B, Cheynel N, Rat P, Faivre J (2001) Population-based study of factors influencing occurrence and prognosis of local recurrence after surgery for rectal cancer. Br J Surg 88(9):1221–1227CrossRef Manfredi S, Benhamiche AM, Meny B, Cheynel N, Rat P, Faivre J (2001) Population-based study of factors influencing occurrence and prognosis of local recurrence after surgery for rectal cancer. Br J Surg 88(9):1221–1227CrossRef
3.
go back to reference van de Velde CJ, Boelens PG, Borras JM et al (2014) EURECCA colorectal: multidisciplinary management: European consensus conference colon and rectum. Eur J Cancer 50(1):1-e1PubMed van de Velde CJ, Boelens PG, Borras JM et al (2014) EURECCA colorectal: multidisciplinary management: European consensus conference colon and rectum. Eur J Cancer 50(1):1-e1PubMed
4.
go back to reference Watanabe T, Muro K, Ajioka Y et al (2018) Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2016 for the treatment of colorectal cancer. Int J Clin Oncol 23(1):1–34CrossRef Watanabe T, Muro K, Ajioka Y et al (2018) Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2016 for the treatment of colorectal cancer. Int J Clin Oncol 23(1):1–34CrossRef
5.
go back to reference Fujita S, Akasu T, Mizusawa J et al (2012) 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 13(6):616–621CrossRef Fujita S, Akasu T, Mizusawa J et al (2012) 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 13(6):616–621CrossRef
6.
go back to reference Masaki T, Matsuoka H, Kobayashi T et al (2010) Quality assurance of pelvic autonomic nerve-preserving surgery for advanced lower rectal cancer–preliminary results of a randomized controlled trial. Langenbecks Arch Surg 395(6):607–613CrossRef Masaki T, Matsuoka H, Kobayashi T et al (2010) Quality assurance of pelvic autonomic nerve-preserving surgery for advanced lower rectal cancer–preliminary results of a randomized controlled trial. Langenbecks Arch Surg 395(6):607–613CrossRef
7.
go back to reference DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188CrossRef DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188CrossRef
8.
go back to reference Viechtbauer W, Lopez-Lopez JA, Sanchez-Meca J, Marin-Martinez F (2015) A comparison of procedures to test for moderators in mixed-effects meta-regression models. Psychol Methods 20(3):360–374CrossRef Viechtbauer W, Lopez-Lopez JA, Sanchez-Meca J, Marin-Martinez F (2015) A comparison of procedures to test for moderators in mixed-effects meta-regression models. Psychol Methods 20(3):360–374CrossRef
9.
go back to reference Hara M, Hirai T, Nakanishi H et al (2007) Isolated tumor cell in lateral lymph node has no influences on the prognosis of rectal cancer patients. Int J Colorectal Dis 22(8):911–917CrossRef Hara M, Hirai T, Nakanishi H et al (2007) Isolated tumor cell in lateral lymph node has no influences on the prognosis of rectal cancer patients. Int J Colorectal Dis 22(8):911–917CrossRef
10.
go back to reference Ishibe A, Ota M, Watanabe J et al (2016) Prediction of lateral pelvic lymph-node metastasis in low rectal cancer by magnetic resonance imaging. World J Surg 40(4):995–1001CrossRef Ishibe A, Ota M, Watanabe J et al (2016) Prediction of lateral pelvic lymph-node metastasis in low rectal cancer by magnetic resonance imaging. World J Surg 40(4):995–1001CrossRef
11.
go back to reference Kanemitsu Y, Komori K, Shida D et al (2017) Potential impact of lateral lymph node dissection (LLND) for low rectal cancer on prognoses and local control: a comparison of 2 high-volume centers in Japan that employ different policies concerning LLND. Surgery 162(2):303–314CrossRef Kanemitsu Y, Komori K, Shida D et al (2017) Potential impact of lateral lymph node dissection (LLND) for low rectal cancer on prognoses and local control: a comparison of 2 high-volume centers in Japan that employ different policies concerning LLND. Surgery 162(2):303–314CrossRef
12.
go back to reference Ishida H, Hatano S, Ishiguro T, Kumamoto K, Ishibashi K, Haga N (2012) Prediction of lateral lymph node metastasis in lower rectal cancer: analysis of paraffin-embedded sections. Jpn J Clin Oncol 42(6):485–490CrossRef Ishida H, Hatano S, Ishiguro T, Kumamoto K, Ishibashi K, Haga N (2012) Prediction of lateral lymph node metastasis in lower rectal cancer: analysis of paraffin-embedded sections. Jpn J Clin Oncol 42(6):485–490CrossRef
13.
go back to reference Kagawa H, Kinugasa Y, Shiomi A et al (2015) Robotic-assisted lateral lymph node dissection for lower rectal cancer: short-term outcomes in 50 consecutive patients. Surg Endosc 29(4):995–1000CrossRef Kagawa H, Kinugasa Y, Shiomi A et al (2015) Robotic-assisted lateral lymph node dissection for lower rectal cancer: short-term outcomes in 50 consecutive patients. Surg Endosc 29(4):995–1000CrossRef
14.
go back to reference Matsuoka H, Nakamura A, Masaki T et al (2007) Optimal diagnostic criteria for lateral pelvic lymph node metastasis in rectal carcinoma. Anticancer Res 27(5B):3529–3533PubMed Matsuoka H, Nakamura A, Masaki T et al (2007) Optimal diagnostic criteria for lateral pelvic lymph node metastasis in rectal carcinoma. Anticancer Res 27(5B):3529–3533PubMed
15.
go back to reference Miyake Y, Mizushima T, Hata T et al (2017) Inspection of perirectal lymph nodes by one-step nucleic acid amplification predicts lateral lymph node metastasis in advanced rectal cancer. Ann Surg Oncol 24(13):3850–3856CrossRef Miyake Y, Mizushima T, Hata T et al (2017) Inspection of perirectal lymph nodes by one-step nucleic acid amplification predicts lateral lymph node metastasis in advanced rectal cancer. Ann Surg Oncol 24(13):3850–3856CrossRef
16.
go back to reference Min BS, Kim JS, Kim NK et al (2009) Extended lymph node dissection for rectal cancer with radiologically diagnosed extramesenteric lymph node metastasis. Ann Surg Oncol 16(12):3271–3278CrossRef Min BS, Kim JS, Kim NK et al (2009) Extended lymph node dissection for rectal cancer with radiologically diagnosed extramesenteric lymph node metastasis. Ann Surg Oncol 16(12):3271–3278CrossRef
17.
go back to reference Sato T, Ozawa H, Hatate K et al (2011) A Phase II trial of neoadjuvant preoperative chemoradiotherapy with S-1 plus irinotecan and radiation in patients with locally advanced rectal cancer: clinical feasibility and response rate. Int J Radiat Oncol Biol Phys 79(3):677–683CrossRef Sato T, Ozawa H, Hatate K et al (2011) A Phase II trial of neoadjuvant preoperative chemoradiotherapy with S-1 plus irinotecan and radiation in patients with locally advanced rectal cancer: clinical feasibility and response rate. Int J Radiat Oncol Biol Phys 79(3):677–683CrossRef
18.
go back to reference Sato H, Maeda K, Maruta M (2011) Prognostic significance of lateral lymph node dissection in node positive low rectal carcinoma. Int J Colorectal Dis 26(7):881–889CrossRef Sato H, Maeda K, Maruta M (2011) Prognostic significance of lateral lymph node dissection in node positive low rectal carcinoma. Int J Colorectal Dis 26(7):881–889CrossRef
19.
go back to reference Shimoyama M, Yamazaki T, Suda T, Hatakeyama K (2003) Prognostic significance of lateral lymph node micrometastases in lower rectal cancer: an immunohistochemical study with CAM5.2. Dis Colon Rectum 46(3):333–339CrossRef Shimoyama M, Yamazaki T, Suda T, Hatakeyama K (2003) Prognostic significance of lateral lymph node micrometastases in lower rectal cancer: an immunohistochemical study with CAM5.2. Dis Colon Rectum 46(3):333–339CrossRef
20.
go back to reference Yokoyama S, Takifuji K, Hotta T et al (2014) Survival benefit of lateral lymph node dissection according to the region of involvement and the number of lateral lymph nodes involved. Surg Today 44(6):1097–1103CrossRef Yokoyama S, Takifuji K, Hotta T et al (2014) Survival benefit of lateral lymph node dissection according to the region of involvement and the number of lateral lymph nodes involved. Surg Today 44(6):1097–1103CrossRef
21.
go back to reference Komori K, Kanemitsu Y, Kimura K et al (2013) Detailed stratification of TNM stage III rectal cancer based on the presence/absence of extracapsular invasion of the metastatic lymph nodes. Dis Colon Rectum 56(6):726–732CrossRef Komori K, Kanemitsu Y, Kimura K et al (2013) Detailed stratification of TNM stage III rectal cancer based on the presence/absence of extracapsular invasion of the metastatic lymph nodes. Dis Colon Rectum 56(6):726–732CrossRef
22.
go back to reference Masaki T, Takayama M, Matsuoka H et al (2008) Intraoperative radiotherapy for oncological and function-preserving surgery in patients with advanced lower rectal cancer. Langenbecks Arch Surg 393(2):173–180CrossRef Masaki T, Takayama M, Matsuoka H et al (2008) Intraoperative radiotherapy for oncological and function-preserving surgery in patients with advanced lower rectal cancer. Langenbecks Arch Surg 393(2):173–180CrossRef
23.
go back to reference Wu ZY, Wan J, Li JH et al (2007) Prognostic value of lateral lymph node metastasis for advanced low rectal cancer. World J Gastroenterol 13(45):6048–6052CrossRef Wu ZY, Wan J, Li JH et al (2007) Prognostic value of lateral lymph node metastasis for advanced low rectal cancer. World J Gastroenterol 13(45):6048–6052CrossRef
24.
go back to reference Hida J, Yasutomi M, Fujimoto K, Maruyama T, Okuno K, Shindo K (1997) Does lateral lymph node dissection improve survival in rectal carcinoma? examination of node metastases by the clearing method. J Am Coll Surg 184(5):475–480PubMed Hida J, Yasutomi M, Fujimoto K, Maruyama T, Okuno K, Shindo K (1997) Does lateral lymph node dissection improve survival in rectal carcinoma? examination of node metastases by the clearing method. J Am Coll Surg 184(5):475–480PubMed
25.
go back to reference Ueno M, Oya M, Azekura K, Yamaguchi T, Muto T (2005) Incidence and prognostic significance of lateral lymph node metastasis in patients with advanced low rectal cancer. Br J Surg 92(6):756–763CrossRef Ueno M, Oya M, Azekura K, Yamaguchi T, Muto T (2005) Incidence and prognostic significance of lateral lymph node metastasis in patients with advanced low rectal cancer. Br J Surg 92(6):756–763CrossRef
26.
go back to reference Ueno H, Mochizuki H, Hashiguchi Y et al (2007) Potential prognostic benefit of lateral pelvic node dissection for rectal cancer located below the peritoneal reflection. Ann Surg 245(1):80–87CrossRef Ueno H, Mochizuki H, Hashiguchi Y et al (2007) Potential prognostic benefit of lateral pelvic node dissection for rectal cancer located below the peritoneal reflection. Ann Surg 245(1):80–87CrossRef
27.
go back to reference Steup WH, Hojo K, Moriya Y et al (1994) An analysis on the effect of blood transfusion on recurrence and survival in patients undergoing extended lymphadenectomy for colorectal cancer. Hepatogastroenterology 41(3):253–259PubMed Steup WH, Hojo K, Moriya Y et al (1994) An analysis on the effect of blood transfusion on recurrence and survival in patients undergoing extended lymphadenectomy for colorectal cancer. Hepatogastroenterology 41(3):253–259PubMed
28.
go back to reference Mori T, Takahashi K, Yasuno M (1998) Radical resection with autonomic nerve preservation and lymph node dissection techniques in lower rectal cancer surgery and its results: the impact of lateral lymph node dissection. Langenbecks Arch Surg 383(6):409–415CrossRef Mori T, Takahashi K, Yasuno M (1998) Radical resection with autonomic nerve preservation and lymph node dissection techniques in lower rectal cancer surgery and its results: the impact of lateral lymph node dissection. Langenbecks Arch Surg 383(6):409–415CrossRef
29.
go back to reference Tan KY, Yamamoto S, Fujita S, Akasu T, Moriya Y (2010) Improving prediction of lateral node spread in low rectal cancers–multivariate analysis of clinicopathological factors in 1046 cases. Langenbecks Arch Surg 395(5):545–549CrossRef Tan KY, Yamamoto S, Fujita S, Akasu T, Moriya Y (2010) Improving prediction of lateral node spread in low rectal cancers–multivariate analysis of clinicopathological factors in 1046 cases. Langenbecks Arch Surg 395(5):545–549CrossRef
30.
go back to reference Nagasaki T, Akiyoshi T, Fujimoto Y et al (2017) Preoperative chemoradiotherapy might improve the prognosis of patients with locally advanced low rectal cancer and lateral pelvic lymph node metastases. World J Surg 41(3):876–883CrossRef Nagasaki T, Akiyoshi T, Fujimoto Y et al (2017) Preoperative chemoradiotherapy might improve the prognosis of patients with locally advanced low rectal cancer and lateral pelvic lymph node metastases. World J Surg 41(3):876–883CrossRef
31.
go back to reference Yamaoka Y, Kinugasa Y, Shiomi A et al (2017) Preoperative chemoradiotherapy changes the size criterion for predicting lateral lymph node metastasis in lower rectal cancer. Int J Colorectal Dis 32(11):1631–1637CrossRef Yamaoka Y, Kinugasa Y, Shiomi A et al (2017) Preoperative chemoradiotherapy changes the size criterion for predicting lateral lymph node metastasis in lower rectal cancer. Int J Colorectal Dis 32(11):1631–1637CrossRef
32.
go back to reference Numata M, Yamaguchi T, Kinugasa Y et al (2017) Index of estimated benefit from lateral lymph node dissection for middle and lower rectal cancer. Anticancer Res 37(5):2549–2555CrossRef Numata M, Yamaguchi T, Kinugasa Y et al (2017) Index of estimated benefit from lateral lymph node dissection for middle and lower rectal cancer. Anticancer Res 37(5):2549–2555CrossRef
33.
go back to reference Yamaguchi T, Kinugasa Y, Shiomi A, Tomioka H, Kagawa H, Yamakawa Y (2016) Robotic-assisted vs. conventional laparoscopic surgery for rectal cancer: short-term outcomes at a single center. Surg Today 46(8):957–962CrossRef Yamaguchi T, Kinugasa Y, Shiomi A, Tomioka H, Kagawa H, Yamakawa Y (2016) Robotic-assisted vs. conventional laparoscopic surgery for rectal cancer: short-term outcomes at a single center. Surg Today 46(8):957–962CrossRef
34.
go back to reference Yu YY, Wang C, Xu D, Shen XG, Ding SQ, Zhou ZG (2011) Mesorectal and lateral node metastasis and micrometastasis in lower rectal cancer. Hepatogastroenterology 58(107–108):745–748PubMed Yu YY, Wang C, Xu D, Shen XG, Ding SQ, Zhou ZG (2011) Mesorectal and lateral node metastasis and micrometastasis in lower rectal cancer. Hepatogastroenterology 58(107–108):745–748PubMed
35.
go back to reference Kobayashi H, Mochizuki H, Kato T et al (2009) Outcomes of surgery alone for lower rectal cancer with and without pelvic sidewall dissection. Dis Colon Rectum 52(4):567–576CrossRef Kobayashi H, Mochizuki H, Kato T et al (2009) Outcomes of surgery alone for lower rectal cancer with and without pelvic sidewall dissection. Dis Colon Rectum 52(4):567–576CrossRef
36.
go back to reference Yano H, Saito Y, Takeshita E, Miyake O, Ishizuka N (2007) Prediction of lateral pelvic node involvement in low rectal cancer by conventional computed tomography. Br J Surg 94(8):1014–1019CrossRef Yano H, Saito Y, Takeshita E, Miyake O, Ishizuka N (2007) Prediction of lateral pelvic node involvement in low rectal cancer by conventional computed tomography. Br J Surg 94(8):1014–1019CrossRef
37.
go back to reference Kinugasa T, Akagi Y, Ochi T et al (2013) Lateral lymph-node dissection for rectal cancer: meta-analysis of all 944 cases undergoing surgery during 1975–2004. Anticancer Res 33(7):2921–2927PubMed Kinugasa T, Akagi Y, Ochi T et al (2013) Lateral lymph-node dissection for rectal cancer: meta-analysis of all 944 cases undergoing surgery during 1975–2004. Anticancer Res 33(7):2921–2927PubMed
38.
go back to reference Yamaguchi T, Kinugasa Y, Shiomi A, Tomioka H, Kagawa H (2016) Robotic-assisted laparoscopic versus open lateral lymph node dissection for advanced lower rectal cancer. Surg Endosc 30(2):721–728CrossRef Yamaguchi T, Kinugasa Y, Shiomi A, Tomioka H, Kagawa H (2016) Robotic-assisted laparoscopic versus open lateral lymph node dissection for advanced lower rectal cancer. Surg Endosc 30(2):721–728CrossRef
39.
go back to reference Steup WH, Moriya Y, van de Velde CJ (2002) Patterns of lymphatic spread in rectal cancer. a topographical analysis on lymph node metastases. Eur J Cancer. 38(7):911–918CrossRef Steup WH, Moriya Y, van de Velde CJ (2002) Patterns of lymphatic spread in rectal cancer. a topographical analysis on lymph node metastases. Eur J Cancer. 38(7):911–918CrossRef
41.
go back to reference Yang X, Yang S, Hu T, Gu C, Wei M, Deng X et al (2020) What is the role of lateral lymph node dissection in rectal cancer patients with clinically suspected lateral lymph node metastasis after preoperative chemoradiotherapy? a meta-analysis and systematic review. Cancer Med 9(13):4477–4489CrossRef Yang X, Yang S, Hu T, Gu C, Wei M, Deng X et al (2020) What is the role of lateral lymph node dissection in rectal cancer patients with clinically suspected lateral lymph node metastasis after preoperative chemoradiotherapy? a meta-analysis and systematic review. Cancer Med 9(13):4477–4489CrossRef
42.
go back to reference Gao X, Wang C, Yu Y, Yang L, Zhou Z (2020) Lateral lymph node dissection reduces local recurrence of locally advanced lower rectal cancer in the absence of preoperative neoadjuvant chemoradiotherapy: a systematic review and meta-analysis. Disponible sur: https://europepmc.org/article/ppr/ppr216100 Gao X, Wang C, Yu Y, Yang L, Zhou Z (2020) Lateral lymph node dissection reduces local recurrence of locally advanced lower rectal cancer in the absence of preoperative neoadjuvant chemoradiotherapy: a systematic review and meta-analysis. Disponible sur: https://​europepmc.​org/​article/​ppr/​ppr216100
Metadata
Title
Prevalence of Metastatic Lateral Lymph Nodes in Asian Patients with Lateral Lymph Node Dissection for Rectal Cancer: A Meta-analysis
Authors
Niki Christou
Jeremy Meyer
Christophe Combescure
Alexandre Balaphas
Joan Robert-Yap
Nicolas C. Buchs
Frédéric Ris
Publication date
01-05-2021
Publisher
Springer International Publishing
Published in
World Journal of Surgery / Issue 5/2021
Print ISSN: 0364-2313
Electronic ISSN: 1432-2323
DOI
https://doi.org/10.1007/s00268-021-05956-1

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