Prognostic Relevance of the Proximal Resection Margin Distance in Distal Gastrectomy for Gastric Adenocarcinoma.

Distal gastrectomy Gastric cancer Gastric neoplasm Margin distance Resection margin Surgery

Journal

Annals of surgical oncology
ISSN: 1534-4681
Titre abrégé: Ann Surg Oncol
Pays: United States
ID NLM: 9420840

Informations de publication

Date de publication:
05 Jul 2024
Historique:
received: 21 03 2024
accepted: 16 06 2024
medline: 6 7 2024
pubmed: 6 7 2024
entrez: 5 7 2024
Statut: aheadofprint

Résumé

The risk for recurrence in patients with distal gastric cancer can be reduced by surgical radicality. However, dispute exists about the value of the proposed minimum proximal margin distance (PMD). Here, we assess the prognostic value of the safety distance between the proximal resection margin and the tumor. This is a single-center cohort study of patients undergoing distal gastrectomy for gastric adenocarcinoma (2001-2021). Cohorts were defined by adequacy of the PMD according to the European Society for Medical Oncology (ESMO) guidelines (≥ 5 cm for intestinal and ≥ 8 cm for diffuse Laurén's subtypes). Overall survival (OS) and time to progression (TTP) were assessed by log-rank and multivariable Cox-regression analyses. Of 176 patients, 70 (39.8%) had a sufficient PMD. An adequate PMD was associated with cancer of the intestinal subtype (67% vs. 45%, p = 0.010). Estimated 5-year survival was 63% [95% confidence interval (CI) 51-78] and 62% (95% CI 53-73) for adequate and inadequate PMD, respectively. Overall, an adequate PMD was not prognostic for OS (HR 0.81, 95% CI 0.48-1.38) in the multivariable analysis. However, in patients with diffuse subtype, an adequate PMD was associated with improved oncological outcomes (median OS not reached versus 131 months, p = 0.038, median TTP not reached versus 88.0 months, p = 0.003). Patients with diffuse gastric cancer are at greater risk to undergo resection with an inadequate PMD, which in those patients is associated with worse oncological outcomes. For the intestinal subtype, there was no prognostic association with PMD, indicating that a distal gastrectomy with partial preservation of the gastric function may also be feasible in the setting where an extensive PMD is not achievable.

Sections du résumé

BACKGROUND BACKGROUND
The risk for recurrence in patients with distal gastric cancer can be reduced by surgical radicality. However, dispute exists about the value of the proposed minimum proximal margin distance (PMD). Here, we assess the prognostic value of the safety distance between the proximal resection margin and the tumor.
PATIENTS AND METHODS METHODS
This is a single-center cohort study of patients undergoing distal gastrectomy for gastric adenocarcinoma (2001-2021). Cohorts were defined by adequacy of the PMD according to the European Society for Medical Oncology (ESMO) guidelines (≥ 5 cm for intestinal and ≥ 8 cm for diffuse Laurén's subtypes). Overall survival (OS) and time to progression (TTP) were assessed by log-rank and multivariable Cox-regression analyses.
RESULTS RESULTS
Of 176 patients, 70 (39.8%) had a sufficient PMD. An adequate PMD was associated with cancer of the intestinal subtype (67% vs. 45%, p = 0.010). Estimated 5-year survival was 63% [95% confidence interval (CI) 51-78] and 62% (95% CI 53-73) for adequate and inadequate PMD, respectively. Overall, an adequate PMD was not prognostic for OS (HR 0.81, 95% CI 0.48-1.38) in the multivariable analysis. However, in patients with diffuse subtype, an adequate PMD was associated with improved oncological outcomes (median OS not reached versus 131 months, p = 0.038, median TTP not reached versus 88.0 months, p = 0.003).
CONCLUSION CONCLUSIONS
Patients with diffuse gastric cancer are at greater risk to undergo resection with an inadequate PMD, which in those patients is associated with worse oncological outcomes. For the intestinal subtype, there was no prognostic association with PMD, indicating that a distal gastrectomy with partial preservation of the gastric function may also be feasible in the setting where an extensive PMD is not achievable.

Identifiants

pubmed: 38969858
doi: 10.1245/s10434-024-15721-y
pii: 10.1245/s10434-024-15721-y
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Siegel RL, Miller KD, Wagle NS, Jemal A. Cancer statistics, 2023. CA Cancer J Clin. 2023;73(1):17–48. https://doi.org/10.3322/caac.21763 .
doi: 10.3322/caac.21763 pubmed: 36633525
Etemadi A, Safiri S, Sepanlou SG, et al. The global, regional, and national burden of stomach cancer in 195 countries, 1990–2017: a systematic analysis for the Global Burden of Disease study 2017. Lancet Gastroenterol Hepatol. 2020;5(1):42–54. https://doi.org/10.1016/s2468-1253(19)30328-0 .
doi: 10.1016/s2468-1253(19)30328-0
Japanese gastric cancer treatment guidelines 2018 (5th edition). Gastric Cancer. 2021;24(1):1–21. https://doi.org/10.1007/s10120-020-01042-y
Wang FH, Zhang XT, Li YF, et al. The Chinese Society of Clinical Oncology (CSCO): clinical guidelines for the diagnosis and treatment of gastric cancer, 2021. Cancer Commun (Lond). 2021;41(8):747–95. https://doi.org/10.1002/cac2.12193 .
doi: 10.1002/cac2.12193 pubmed: 34197702
Smyth EC, Verheij M, Allum W, Cunningham D, Cervantes A, Arnold D. Gastric cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up†. Ann Oncol. 2016;27:v38–49. https://doi.org/10.1093/annonc/mdw350 .
doi: 10.1093/annonc/mdw350 pubmed: 27664260
Smyth EC, Nilsson M, Grabsch HI, van Grieken NCT, Lordick F. Gastric cancer. Lancet. 2020;396(10251):635–48. https://doi.org/10.1016/S0140-6736(20)31288-5 .
doi: 10.1016/S0140-6736(20)31288-5 pubmed: 32861308
Hess T, Maj C, Gehlen J, et al. Dissecting the genetic heterogeneity of gastric cancer. EBioMedicine. 2023;92:104616. https://doi.org/10.1016/j.ebiom.2023.104616 .
doi: 10.1016/j.ebiom.2023.104616 pubmed: 37209533 pmcid: 10212786
Takahashi M, Terashima M, Kawahira H, et al. Quality of life after total vs distal gastrectomy with Roux-en-Y reconstruction: use of the postgastrectomy syndrome assessment scale-45. World J Gastroenterol. 2017;23(11):2068–76. https://doi.org/10.3748/wjg.v23.i11.2068 .
doi: 10.3748/wjg.v23.i11.2068 pubmed: 28373774 pmcid: 5360649
Spolverato G, Ejaz A, Kim Y, et al. Rates and patterns of recurrence after curative intent resection for gastric cancer: a United States multi-institutional analysis. J Am Coll Surg. 2014;219(4):664–75. https://doi.org/10.1016/j.jamcollsurg.2014.03.062 .
doi: 10.1016/j.jamcollsurg.2014.03.062 pubmed: 25154671
Toriumi T, Terashima M, Mizusawa J, et al. Recurrence patterns after curative gastrectomy for pStage II/III gastric cancer: Exploratory analysis of the randomized controlled JCOG1001 trial. Eur J Surg Oncol. 2023;49(4):838–44. https://doi.org/10.1016/j.ejso.2022.11.093 .
doi: 10.1016/j.ejso.2022.11.093 pubmed: 36424261
Jung JO, Crnovrsanin N, Wirsik NM, et al. Machine learning for optimized individual survival prediction in resectable upper gastrointestinal cancer. J Cancer Res Clin Oncol. 2023;149(5):1691–702. https://doi.org/10.1007/s00432-022-04063-5 .
doi: 10.1007/s00432-022-04063-5 pubmed: 35616729
Nienhüser H, Crnovrsanin N, Nerz D, et al. Expression of angiogenic proteins in tumor and stroma affects survival in patients with gastric cancer. J Surg Res. 2020;255:172–80. https://doi.org/10.1016/j.jss.2020.05.045 .
doi: 10.1016/j.jss.2020.05.045 pubmed: 32563757
Randle RW, Swords DS, Levine EA, et al. Optimal extent of lymphadenectomy for gastric adenocarcinoma: a 7-institution study of the U.S. gastric cancer collaborative. J Surg Oncol. 2016;113(7):750–5. https://doi.org/10.1002/jso.24227 .
doi: 10.1002/jso.24227 pubmed: 26996496 pmcid: 4874863
Liang Y, Ding X, Wang X, Wang B, Deng J, Zhang L, Liang H. Prognostic value of surgical margin status in gastric cancer patients. ANZ J Surg. 2015;85(9):678–84. https://doi.org/10.1111/ans.12515 .
doi: 10.1111/ans.12515 pubmed: 24438078
Rompen IF, Crnovrsanin N, Nienhüser H, et al. Age dependent benefit of neoadjuvant treatment in adenocarcinoma of the esophagus and gastroesophageal junction—a multicenter retrospective observational study of young versus old patients. Int J Surg. 2023. https://doi.org/10.1097/js9.0000000000000713 .
doi: 10.1097/js9.0000000000000713 pubmed: 37720939 pmcid: 10720874
Squires MH III, Kooby DA, Poultsides GA, et al. Is it time to abandon the 5-cm margin rule during resection of distal gastric adenocarcinoma? A multi-institution study of the U.S. Gastric Cancer Collaborative. Ann Surg Oncol. 2015;22(4):1243–51. https://doi.org/10.1245/s10434-014-4138-z .
doi: 10.1245/s10434-014-4138-z pubmed: 25316491
Eom SS, Choi W, Eom BW, et al. A comprehensive and comparative review of global gastric cancer treatment guidelines. J Gastric Cancer. 2022;22(1):3–23. https://doi.org/10.5230/jgc.2022.22.e10 .
doi: 10.5230/jgc.2022.22.e10 pubmed: 35425651 pmcid: 8980601
von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP, Initiative S. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Int J Surg. 2014;12(12):1495–9. https://doi.org/10.1016/j.ijsu.2014.07.013 .
doi: 10.1016/j.ijsu.2014.07.013
Rompen IF, Nienhüser H, Crnovrsanin N, et al. Clinical characteristics and oncological outcomes of surgically treated early-onset gastric adenocarcinoma - a retrospective cohort study, Research paper. J Cancer. 2023;14(9):1470–8. https://doi.org/10.7150/jca.82876 .
doi: 10.7150/jca.82876 pubmed: 37325055 pmcid: 10266247
Stelmach R, Apostolidis L, Kahle S, et al. Pattern and time point of relapse in locally advanced esophagogastric adenocarcinoma after multimodal treatment: implications for a useful structured follow-up. J Cancer Res Clin Oncol. 2023;149(16):14785–96. https://doi.org/10.1007/s00432-023-05254-4 .
doi: 10.1007/s00432-023-05254-4 pubmed: 37589924 pmcid: 10602954
Sisic L, Strowitzki MJ, Blank S, et al. Postoperative follow-up programs improve survival in curatively resected gastric and junctional cancer patients: a propensity score matched analysis. Gastric Cancer. 2018;21(3):552–68. https://doi.org/10.1007/s10120-017-0751-4 .
doi: 10.1007/s10120-017-0751-4 pubmed: 28741059
Rice TW, Patil DT, Blackstone EH. 8th edition AJCC/UICC staging of cancers of the esophagus and esophagogastric junction: application to clinical practice. Ann Cardiothorac Surg. 2017;6(2):119–30. https://doi.org/10.21037/acs.2017.03.14 .
doi: 10.21037/acs.2017.03.14 pubmed: 28447000 pmcid: 5387145
Becker K, Mueller JD, Schulmacher C, et al. Histomorphology and grading of regression in gastric carcinoma treated with neoadjuvant chemotherapy. Cancer. 2003;98(7):1521–30. https://doi.org/10.1002/cncr.11660 .
doi: 10.1002/cncr.11660 pubmed: 14508841
Mariette C, Carneiro F, Grabsch HI, et al. Consensus on the pathological definition and classification of poorly cohesive gastric carcinoma. Gastric Cancer. 2019;22(1):1–9. https://doi.org/10.1007/s10120-018-0868-0 .
doi: 10.1007/s10120-018-0868-0 pubmed: 30167905
Laurén PA, Nevalainen TJ. Epidemiology of intestinal and diffuse types of gastric carcinoma. A time-trend study in Finland with comparison between studies from high- and low-risk areas. Cancer. 1993;71(10):2926–2933. https://doi.org/10.1002/1097-0142(19930515)71:10<2926::aid-cncr2820711007>3.0.co;2-x
Huang C, Liu H, Hu Y, et al. Laparoscopic vs open distal gastrectomy for locally advanced gastric cancer: five-year outcomes from the CLASS-01 randomized clinical trial. JAMA Surg. 2022;157(1):9–17. https://doi.org/10.1001/jamasurg.2021.5104 .
doi: 10.1001/jamasurg.2021.5104 pubmed: 34668963
de Jongh C, van der Veen A, Brosens LAA, Nieuwenhuijzen GAP, Stoot J, Ruurda JP, van Hillegersberg R. Distal versus total D2-gastrectomy for gastric cancer: a secondary analysis of surgical and oncological outcomes including quality of life in the multicenter randomized LOGICA-Trial. J Gastrointest Surg. 2023;27(9):1812–24. https://doi.org/10.1007/s11605-023-05683-z .
doi: 10.1007/s11605-023-05683-z pubmed: 37340107 pmcid: 10511620
Bozzetti F, Bonfanti G, Bufalino R, et al. Adequacy of margins of resection in gastrectomy for cancer. Ann Surg. 1982;196(6):685–90. https://doi.org/10.1097/00000658-198212001-00012 .
doi: 10.1097/00000658-198212001-00012 pubmed: 7149820 pmcid: 1352985
Papachristou DN, Agnanti N, D’Agostino H, Fortner JG. Histologically positive esophageal margin in the surgical treatment of gastric cancer. Am J Surg. 1980;139(5):711–3. https://doi.org/10.1016/0002-9610(80)90369-4 .
doi: 10.1016/0002-9610(80)90369-4 pubmed: 7468923
Jang YJ, Park MS, Kim JH, et al. Advanced gastric cancer in the middle one-third of the stomach: should surgeons perform total gastrectomy? J Surg Oncol. 2010;101(6):451–6. https://doi.org/10.1002/jso.21431 .
doi: 10.1002/jso.21431 pubmed: 19924722
Lee CM, Jee YS, Lee JH, Son SY, Ahn SH, Park DJ, Kim HH. Length of negative resection margin does not affect local recurrence and survival in the patients with gastric cancer. World J Gastroenterol. 2014;20(30):10518–24. https://doi.org/10.3748/wjg.v20.i30.10518 .
doi: 10.3748/wjg.v20.i30.10518 pubmed: 25132770 pmcid: 4130861
Lee JH, Kim YI. Which is the optimal extent of resection in middle third gastric cancer between total gastrectomy and subtotal gastrectomy? J Gastric Cancer. 2010;10(4):226–33. https://doi.org/10.5230/jgc.2010.10.4.226 .
doi: 10.5230/jgc.2010.10.4.226 pubmed: 22076190 pmcid: 3204494
Postlewait LM, Squires MH III, Kooby DA, et al. The importance of the proximal resection margin distance for proximal gastric adenocarcinoma: a multi-institutional study of the US Gastric Cancer Collaborative. J Surg Oncol. 2015;112(2):203–7. https://doi.org/10.1002/jso.23971 .
doi: 10.1002/jso.23971 pubmed: 26272801
Berlth F, Kim WH, Choi JH, Park SH, Kong SH, Lee HJ, Yang HK. Prognostic impact of frozen section investigation and extent of proximal safety margin in gastric cancer resection. Ann Surg. 2020;272(5):871–8. https://doi.org/10.1097/sla.0000000000004266 .
doi: 10.1097/sla.0000000000004266 pubmed: 32833759
Lee J-H, Lee H-J, Kong S-H, et al. Analysis of the lymphatic stream to predict sentinel nodes in gastric cancer patients. Ann Surg Oncol. 2014;21(4):1090–8. https://doi.org/10.1245/s10434-013-3392-9 .
doi: 10.1245/s10434-013-3392-9 pubmed: 24276637
Tokunaga M, Ohyama S, Hiki N, Fukunaga T, Yamada K, Sano T, Yamaguchi T. Investigation of the lymphatic stream of the stomach in gastric cancer with solitary lymph node metastasis. World J Surg. 2009;33(6):1208. https://doi.org/10.1007/s00268-009-9985-6 .
doi: 10.1007/s00268-009-9985-6
Jeong SH, Seo KW, Min JS. Intraoperative tumor localization of early gastric cancers. J Gastric Cancer. 2021;21(1):4–15. https://doi.org/10.5230/jgc.2021.21.e4 .
doi: 10.5230/jgc.2021.21.e4 pubmed: 33854809 pmcid: 8020001
Symeonidis D, Zacharoulis D, Petsa E, Samara AA, Kissa L, Tepetes K. Extent of surgical resection for gastric cancer: the safety distance between the tumor and the proximal resection margin. Cancer Diagn Progn. 2022;2(5):520–4. https://doi.org/10.21873/cdp.10136 .
doi: 10.21873/cdp.10136 pubmed: 36060018 pmcid: 9425586
Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86. https://doi.org/10.1002/ijc.29210 .
doi: 10.1002/ijc.29210 pubmed: 25220842

Auteurs

Ingmar F Rompen (IF)

Department of General, Visceral and Transplantat Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Isabel Schütte (I)

Department of General, Visceral and Transplantat Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Nerma Crnovrsanin (N)

Department of General, Visceral and Transplantat Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Sabine Schiefer (S)

Department of General, Visceral and Transplantat Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Adrian T Billeter (AT)

Department of General, Visceral and Transplantat Surgery, Heidelberg University Hospital, Heidelberg, Germany.
Department of Surgery, Clarunis-University Digestive Health Care Center, St. Clara Hospital and University Hospital Basel, Basel, Switzerland.

Georg Martin Haag (GM)

Department of Medical Oncology, National Center for Tumor Diseases (NCT), Heidelberg University Hospital, Heidelberg, Germany.

Thomas Longerich (T)

Institute of Pathology Heidelberg, Heidelberg University Hospital, Heidelberg, Germany.

Zoltan Czigany (Z)

Department of General, Visceral and Transplantat Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Thomas Schmidt (T)

Department of General, Visceral and Transplantat Surgery, Heidelberg University Hospital, Heidelberg, Germany.
Department of General, Visceral, Cancer and Transplant Surgery, University Hospital of Cologne, Cologne, Germany.

Franck Billmann (F)

Department of General, Visceral and Transplantat Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Leila Sisic (L)

Department of General, Visceral and Transplantat Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Henrik Nienhüser (H)

Department of General, Visceral and Transplantat Surgery, Heidelberg University Hospital, Heidelberg, Germany. henrik.nienhueser@med.uni-heidelberg.de.

Classifications MeSH