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Erschienen in: European Surgery 4/2018

28.03.2018 | original article

Should surgical ex vivo lymphadenectomy be a standard procedure in the management of patients with gastric cancer?

Our personal experience, systematic literature review, and meta-analysis

verfasst von: Mihai Dan Boşcaiu, Mihnea Dragomir, Bogdan Trandafir, Vlad Herlea, Cătălin Vasilescu

Erschienen in: European Surgery | Ausgabe 4/2018

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Summary

Background

The total number of retrieved and analyzed lymph nodes is known to impact on survival of patients with gastric cancer. Multiple factors are responsible for the high variability of total lymph node yields. Among these factors, the use of surgical ex vivo lymphodissection may be significant for optimizing the lymph node count.

Methods

This article includes our personal experience regarding ex vivo lymphodissection and a meta-analysis which included all the articles related to this topic. We compared two groups of patients with gastric adenocarcinoma who underwent gastrectomy with at least D2 lymphodissection. In the first group, the lymph node count was performed by the pathologist. As for the second, the surgeon performed an ex vivo lymphodissection of the resected specimens before submitting these to the pathologist for further analysis. For the systematic literature review and the meta-analysis, the PubMed database was thoroughly searched, and in order to assess the inter-study heterogeneity, we used I2 and chi2 tests.

Results

The total lymph node yield proved to be significantly higher in the ex vivo lymphodissection group than in the non-ex vivo lymphodissection group (37.4 versus 23.2, p < 0.001). The meta-analysis confirmed our results: the cumulative mean difference between ex vivo lymphodissection and non-ex vivo lymphodissection group is 11.52 (p < 0.00001); inter-study heterogeneity was statistically significant (I2 > 58%, chi2 = 9.63, df = 4, p = 0.05).

Conclusion

Surgical ex vivo lymphodissection increases the total lymph node yield and may lead not only to a more accurate staging of gastric cancer, but also to an improved clinical outcome.
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Literatur
1.
Zurück zum Zitat Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. Ca Cancer J Clin. 2015;65(2):87–108.CrossRefPubMed Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. Ca Cancer J Clin. 2015;65(2):87–108.CrossRefPubMed
2.
Zurück zum Zitat Orditura M, Galizia G, Sforza V, Gambardella V, Fabozzi A, Laterza MM, et al. Treatment of gastric cancer. World J Gastroenterol. 2014;20(7):1635–49.CrossRefPubMedPubMedCentral Orditura M, Galizia G, Sforza V, Gambardella V, Fabozzi A, Laterza MM, et al. Treatment of gastric cancer. World J Gastroenterol. 2014;20(7):1635–49.CrossRefPubMedPubMedCentral
3.
Zurück zum Zitat 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(suppl 5):v38–v49.CrossRefPubMed 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(suppl 5):v38–v49.CrossRefPubMed
4.
Zurück zum Zitat Japanese Gastric Cancer Association.. Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer. 2011;14(2):113–23.CrossRef Japanese Gastric Cancer Association.. Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer. 2011;14(2):113–23.CrossRef
5.
Zurück zum Zitat Edge SB, Compton CC. Cancer staging manual. 7th ed. New York: Springer; 2010. Edge SB, Compton CC. Cancer staging manual. 7th ed. New York: Springer; 2010.
6.
Zurück zum Zitat Woo Y, Goldner B, Ituarte P, Lee B, Melstrom L, Son T, et al. Lymphadenectomy with optimum of 29 lymph nodes retrieved associated with improved survival in advanced gastric cancer: a 25,000-patient international database study. J Am Coll Surg. 2017;224(4):546–55.CrossRefPubMed Woo Y, Goldner B, Ituarte P, Lee B, Melstrom L, Son T, et al. Lymphadenectomy with optimum of 29 lymph nodes retrieved associated with improved survival in advanced gastric cancer: a 25,000-patient international database study. J Am Coll Surg. 2017;224(4):546–55.CrossRefPubMed
7.
Zurück zum Zitat Chen HN, Chen XZ, Zhang WH, Chen XL, Yang K, Liu JP, et al. Necessity of harvesting at least 25 lymph nodes in patients with stage N2–N3 resectable gastric cancer: a 10-year, single-institution cohort study. Medicine (Baltimore). 2015;94(10):e620.CrossRef Chen HN, Chen XZ, Zhang WH, Chen XL, Yang K, Liu JP, et al. Necessity of harvesting at least 25 lymph nodes in patients with stage N2–N3 resectable gastric cancer: a 10-year, single-institution cohort study. Medicine (Baltimore). 2015;94(10):e620.CrossRef
8.
Zurück zum Zitat Zheng G, Feng F, Guo M, Xu G, Liu S, Liu Z, et al. Harvest of at least 23 lymph nodes is indispensable for stage N3 gastric cancer patients. Ann Surg Oncol. 2017;24(4):998–1002.CrossRefPubMed Zheng G, Feng F, Guo M, Xu G, Liu S, Liu Z, et al. Harvest of at least 23 lymph nodes is indispensable for stage N3 gastric cancer patients. Ann Surg Oncol. 2017;24(4):998–1002.CrossRefPubMed
10.
Zurück zum Zitat Szczepanik AM, Paszko A, Szura M, Scully-Horner T, Kulig J. Alternative staging of regional lymph nodes in gastric cancer. Prz Gastroenterol. 2016;11(3):145–9.PubMedPubMedCentral Szczepanik AM, Paszko A, Szura M, Scully-Horner T, Kulig J. Alternative staging of regional lymph nodes in gastric cancer. Prz Gastroenterol. 2016;11(3):145–9.PubMedPubMedCentral
11.
Zurück zum Zitat Sun Z, Xu Y, de Li M, Wang ZN, Zhu GL, Huang BJ, et al. Log odds of positive lymph nodes: a novel prognostic indicator superior to the number-based and the ratio-based N category for gastric cancer patients with R0 resection. Cancer. 2010;116(11):2571–80.CrossRefPubMed Sun Z, Xu Y, de Li M, Wang ZN, Zhu GL, Huang BJ, et al. Log odds of positive lymph nodes: a novel prognostic indicator superior to the number-based and the ratio-based N category for gastric cancer patients with R0 resection. Cancer. 2010;116(11):2571–80.CrossRefPubMed
12.
Zurück zum Zitat Jian-Hui C, Shi-Rong C, Hui W, Si-le C, Jian-Bo X, Er-Tao Z, et al. Prognostic value of three different lymph node staging systems in the survival of patients with gastric cancer following D2 lymphadenectomy. Tumour Biol. 2016;37(8):11105–13.CrossRefPubMedPubMedCentral Jian-Hui C, Shi-Rong C, Hui W, Si-le C, Jian-Bo X, Er-Tao Z, et al. Prognostic value of three different lymph node staging systems in the survival of patients with gastric cancer following D2 lymphadenectomy. Tumour Biol. 2016;37(8):11105–13.CrossRefPubMedPubMedCentral
13.
Zurück zum Zitat Xu J, Bian YH, Jin X, Cao H. Prognostic assessment of different metastatic lymph node staging methods for gastric cancer after D2 resection. World J Gastroenterol. 2013;19(12):1975–83.CrossRefPubMedPubMedCentral Xu J, Bian YH, Jin X, Cao H. Prognostic assessment of different metastatic lymph node staging methods for gastric cancer after D2 resection. World J Gastroenterol. 2013;19(12):1975–83.CrossRefPubMedPubMedCentral
14.
Zurück zum Zitat Schoenleber SJ, Schnelldorfer T, Wood CM, Qin R, Sarr MG, Donohue JH. Factors influencing lymph node recovery from the operative specimen after gastrectomy for gastric adenocarcinoma. J Gastrointest Surg. 2009;13(7):1233–7.CrossRefPubMed Schoenleber SJ, Schnelldorfer T, Wood CM, Qin R, Sarr MG, Donohue JH. Factors influencing lymph node recovery from the operative specimen after gastrectomy for gastric adenocarcinoma. J Gastrointest Surg. 2009;13(7):1233–7.CrossRefPubMed
15.
Zurück zum Zitat Parkash V, Bifulco C, Feinn R, Concato J, Jain D. To count and how to count, that is the question: interobserver and intraobserver variability among pathologists in lymph node counting. Am J Clin Pathol. 2010;134(1):42–9.CrossRefPubMed Parkash V, Bifulco C, Feinn R, Concato J, Jain D. To count and how to count, that is the question: interobserver and intraobserver variability among pathologists in lymph node counting. Am J Clin Pathol. 2010;134(1):42–9.CrossRefPubMed
16.
Zurück zum Zitat Abbassi-Ghadi N, Boshier PR, Goldin R, Hanna GB. Techniques to increase lymph node harvest from gastrointestinal cancer specimens: a systematic review and meta-analysis. Histopathology. 2012;61(4):531–42.CrossRefPubMed Abbassi-Ghadi N, Boshier PR, Goldin R, Hanna GB. Techniques to increase lymph node harvest from gastrointestinal cancer specimens: a systematic review and meta-analysis. Histopathology. 2012;61(4):531–42.CrossRefPubMed
17.
Zurück zum Zitat Hanna GB, Amygdalos I, Ni M, Boshier PR, Mikhail S, Lloyd J, et al. Improving the standard of lymph node retrieval after gastric cancer surgery. Histopathology. 2013;63(3):316–24.CrossRefPubMed Hanna GB, Amygdalos I, Ni M, Boshier PR, Mikhail S, Lloyd J, et al. Improving the standard of lymph node retrieval after gastric cancer surgery. Histopathology. 2013;63(3):316–24.CrossRefPubMed
18.
Zurück zum Zitat Cook DA, Reed DA. Appraising the quality of medical education research methods: the Medical Education Research Study Quality Instrument and the Newcastle-Ottawa Scale-Education. Acad Med. 2015;90(8):1067–76.CrossRefPubMed Cook DA, Reed DA. Appraising the quality of medical education research methods: the Medical Education Research Study Quality Instrument and the Newcastle-Ottawa Scale-Education. Acad Med. 2015;90(8):1067–76.CrossRefPubMed
19.
Zurück zum Zitat Partlett C, Riley RD. Random effects meta-analysis: coverage performance of 95% confidence and prediction intervals following REML estimation. Stat Med. 2017;36(2):301–17.CrossRefPubMed Partlett C, Riley RD. Random effects meta-analysis: coverage performance of 95% confidence and prediction intervals following REML estimation. Stat Med. 2017;36(2):301–17.CrossRefPubMed
22.
Zurück zum Zitat Afaneh C, Levy A, Selby L, Ku G, Tang L, Yoon SS, et al. Ex vivo lymphadenectomy during gastrectomy for adenocarcinoma optimizes lymph node yield. J Gastrointest Surg. 2016;20(1):165–71. discussion 71.CrossRefPubMed Afaneh C, Levy A, Selby L, Ku G, Tang L, Yoon SS, et al. Ex vivo lymphadenectomy during gastrectomy for adenocarcinoma optimizes lymph node yield. J Gastrointest Surg. 2016;20(1):165–71. discussion 71.CrossRefPubMed
23.
Zurück zum Zitat Bunt AM, Hermans J, van de Velde CJ, Sasako M, Hoefsloot FA, Fleuren G, et al. Lymph node retrieval in a randomized trial on western-type versus Japanese-type surgery in gastric cancer. J Clin Oncol. 1996;14(8):2289–94.CrossRefPubMed Bunt AM, Hermans J, van de Velde CJ, Sasako M, Hoefsloot FA, Fleuren G, et al. Lymph node retrieval in a randomized trial on western-type versus Japanese-type surgery in gastric cancer. J Clin Oncol. 1996;14(8):2289–94.CrossRefPubMed
24.
Zurück zum Zitat Jiang L, Yao Z, Zhang Y, Hu J, Zhao D, Zhai H, et al. Comparison of lymph node number and prognosis in gastric cancer patients with perigastric lymph nodes retrieved by surgeons and pathologists. Chin J Cancer Res. 2016;28(5):511–8.CrossRefPubMedPubMedCentral Jiang L, Yao Z, Zhang Y, Hu J, Zhao D, Zhai H, et al. Comparison of lymph node number and prognosis in gastric cancer patients with perigastric lymph nodes retrieved by surgeons and pathologists. Chin J Cancer Res. 2016;28(5):511–8.CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Schmidt B, Chang KK, Maduekwe UN, Look-Hong N, Rattner DW, Lauwers GY, et al. D2 lymphadenectomy with surgical ex vivo dissection into node stations for gastric adenocarcinoma can be performed safely in Western patients and ensures optimal staging. Ann Surg Oncol. 2013;20(9):2991–9.CrossRefPubMed Schmidt B, Chang KK, Maduekwe UN, Look-Hong N, Rattner DW, Lauwers GY, et al. D2 lymphadenectomy with surgical ex vivo dissection into node stations for gastric adenocarcinoma can be performed safely in Western patients and ensures optimal staging. Ann Surg Oncol. 2013;20(9):2991–9.CrossRefPubMed
26.
Zurück zum Zitat Gholami S, Janson L, Worhunsky DJ, Tran TB, Squires MH 3rd, Jin LX, et al. Number of lymph nodes removed and survival after gastric cancer resection: an analysis from the US gastric cancer collaborative. J Am Coll Surg. 2015;221(2):291–9.CrossRefPubMedPubMedCentral Gholami S, Janson L, Worhunsky DJ, Tran TB, Squires MH 3rd, Jin LX, et al. Number of lymph nodes removed and survival after gastric cancer resection: an analysis from the US gastric cancer collaborative. J Am Coll Surg. 2015;221(2):291–9.CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat Lavy R, Hershkovitz Y, Kapiev A, Chikman B, Shapira Z, Poluksht N, et al. A comparative study on two different pathological methods to retrieve lymph nodes following gastrectomy. Int J Surg. 2014;12(7):725–8.CrossRefPubMed Lavy R, Hershkovitz Y, Kapiev A, Chikman B, Shapira Z, Poluksht N, et al. A comparative study on two different pathological methods to retrieve lymph nodes following gastrectomy. Int J Surg. 2014;12(7):725–8.CrossRefPubMed
28.
Zurück zum Zitat Okajima W, Komatsu S, Ichikawa D, Kosuga T, Kubota T, Okamoto K, et al. Prognostic impact of the number of retrieved lymph nodes in patients with gastric cancer. J Gastroenterol Hepatol. 2016;31(9):1566–71.CrossRefPubMed Okajima W, Komatsu S, Ichikawa D, Kosuga T, Kubota T, Okamoto K, et al. Prognostic impact of the number of retrieved lymph nodes in patients with gastric cancer. J Gastroenterol Hepatol. 2016;31(9):1566–71.CrossRefPubMed
29.
Zurück zum Zitat Baxter NN, Tuttle TM. Inadequacy of lymph node staging in gastric cancer patients: a population-based study. Ann Surg Oncol. 2005;12(12):981–7.CrossRefPubMed Baxter NN, Tuttle TM. Inadequacy of lymph node staging in gastric cancer patients: a population-based study. Ann Surg Oncol. 2005;12(12):981–7.CrossRefPubMed
30.
Zurück zum Zitat Mullaney PJ, Wadley MS, Hyde C, Wyatt J, Lawrence G, Hallissey MT, et al. Appraisal of compliance with the UICC/AJCC staging system in the staging of gastric cancer. Union Internacional Contra la Cancrum/American Joint Committee on Cancer. Br J Surg. 2002;89(11):1405–8.CrossRefPubMed Mullaney PJ, Wadley MS, Hyde C, Wyatt J, Lawrence G, Hallissey MT, et al. Appraisal of compliance with the UICC/AJCC staging system in the staging of gastric cancer. Union Internacional Contra la Cancrum/American Joint Committee on Cancer. Br J Surg. 2002;89(11):1405–8.CrossRefPubMed
31.
Zurück zum Zitat Kong SH, Lee HJ, Ahn HS, Kim JW, Kim WH, Lee KU, et al. Stage migration effect on survival in gastric cancer surgery with extended lymphadenectomy: the reappraisal of positive lymph node ratio as a proper N‑staging. Ann Surg. 2012;255(1):50–8.CrossRefPubMed Kong SH, Lee HJ, Ahn HS, Kim JW, Kim WH, Lee KU, et al. Stage migration effect on survival in gastric cancer surgery with extended lymphadenectomy: the reappraisal of positive lymph node ratio as a proper N‑staging. Ann Surg. 2012;255(1):50–8.CrossRefPubMed
32.
Zurück zum Zitat Liu YY, Fang WL, Wang F, Hsu JT, Tsai CY, Liu KH, et al. Does a higher cutoff value of lymph node retrieval substantially improve survival in patients with advanced gastric cancer?—time to embrace a new digit. Oncologist. 2017;22(1):97–106.CrossRefPubMed Liu YY, Fang WL, Wang F, Hsu JT, Tsai CY, Liu KH, et al. Does a higher cutoff value of lymph node retrieval substantially improve survival in patients with advanced gastric cancer?—time to embrace a new digit. Oncologist. 2017;22(1):97–106.CrossRefPubMed
33.
Zurück zum Zitat Vasilescu C, Herlea V, Tidor S, Ivanov B, Stanciulea O, Manuc M, et al. D2 lymph node dissection in gastric cancer surgery: long term results—analysis of an experience with 227 patients. Chirurgia. 2006;101(4):375–84.PubMed Vasilescu C, Herlea V, Tidor S, Ivanov B, Stanciulea O, Manuc M, et al. D2 lymph node dissection in gastric cancer surgery: long term results—analysis of an experience with 227 patients. Chirurgia. 2006;101(4):375–84.PubMed
34.
Zurück zum Zitat Vasilescu C, Trandafir B. Current problems in surgical oncology 2. A lesson from Japan. D2 lymphadenectomy in gastric cancer. Chirurgia (Bucur). 2011;106(2):163–70. Vasilescu C, Trandafir B. Current problems in surgical oncology 2. A lesson from Japan. D2 lymphadenectomy in gastric cancer. Chirurgia (Bucur). 2011;106(2):163–70.
35.
Zurück zum Zitat Wu CW, Hsiung CA, Lo SS, Hsieh MC, Chen JH, Li AF, et al. Nodal dissection for patients with gastric cancer: a randomised controlled trial. Lancet Oncol. 2006;7(4):309–15.CrossRefPubMed Wu CW, Hsiung CA, Lo SS, Hsieh MC, Chen JH, Li AF, et al. Nodal dissection for patients with gastric cancer: a randomised controlled trial. Lancet Oncol. 2006;7(4):309–15.CrossRefPubMed
36.
Zurück zum Zitat Wagner PK, Ramaswamy A, Ruschoff J, Schmitz-Moormann P, Rothmund M. Lymph node counts in the upper abdomen: anatomical basis for lymphadenectomy in gastric cancer. Br J Surg. 1991;78(7):825–7.CrossRefPubMed Wagner PK, Ramaswamy A, Ruschoff J, Schmitz-Moormann P, Rothmund M. Lymph node counts in the upper abdomen: anatomical basis for lymphadenectomy in gastric cancer. Br J Surg. 1991;78(7):825–7.CrossRefPubMed
37.
Zurück zum Zitat Candela FC, Urmacher C, Brennan MF. Comparison of the conventional method of lymph node staging with a comprehensive fat-clearing method for gastric adenocarcinoma. Cancer. 1990;66(8):1828–32.CrossRefPubMed Candela FC, Urmacher C, Brennan MF. Comparison of the conventional method of lymph node staging with a comprehensive fat-clearing method for gastric adenocarcinoma. Cancer. 1990;66(8):1828–32.CrossRefPubMed
38.
Zurück zum Zitat Dias AR, Pereira MA, Mello ES, Zilberstein B, Cecconello I, Ribeiro JU. Carnoy’s solution increases the number of examined lymph nodes following gastrectomy for adenocarcinoma: a randomized trial. Gastric Cancer. 2016;19(1):136–42.CrossRefPubMed Dias AR, Pereira MA, Mello ES, Zilberstein B, Cecconello I, Ribeiro JU. Carnoy’s solution increases the number of examined lymph nodes following gastrectomy for adenocarcinoma: a randomized trial. Gastric Cancer. 2016;19(1):136–42.CrossRefPubMed
39.
Zurück zum Zitat Koren R, Paz A, Konichezsky M, Sadikov E, Klein B, Livne P, et al. Lymph node revealing solution: a rapid method for the fixation of cystectomy specimens. Pathol Res Pract. 1999;195(2):77–80.CrossRefPubMed Koren R, Paz A, Konichezsky M, Sadikov E, Klein B, Livne P, et al. Lymph node revealing solution: a rapid method for the fixation of cystectomy specimens. Pathol Res Pract. 1999;195(2):77–80.CrossRefPubMed
40.
Zurück zum Zitat Noda N, Sasako M, Yamaguchi N, Nakanishi Y. Ignoring small lymph nodes can be a major cause of staging error in gastric cancer. Br J Surg. 1998;85(6):831–4.CrossRefPubMed Noda N, Sasako M, Yamaguchi N, Nakanishi Y. Ignoring small lymph nodes can be a major cause of staging error in gastric cancer. Br J Surg. 1998;85(6):831–4.CrossRefPubMed
41.
Zurück zum Zitat Sayegh ME. Those who can do; those who can teach’ Management of Gastric Cancer in Japan. Jpn J Clin Oncol. 2004;34(8):489–90.CrossRefPubMed Sayegh ME. Those who can do; those who can teach’ Management of Gastric Cancer in Japan. Jpn J Clin Oncol. 2004;34(8):489–90.CrossRefPubMed
42.
Zurück zum Zitat Lehnert T, Erlandson RA, Decosse JJ. Lymph and blood capillaries of the human gastric mucosa. A morphologic basis for metastasis in early gastric carcinoma. Gastroenterology. 1985;89(5):939–50.CrossRefPubMed Lehnert T, Erlandson RA, Decosse JJ. Lymph and blood capillaries of the human gastric mucosa. A morphologic basis for metastasis in early gastric carcinoma. Gastroenterology. 1985;89(5):939–50.CrossRefPubMed
43.
Zurück zum Zitat Listrom MB, Fenoglio-Preiser CM. Lymphatic distribution of the stomach in normal, inflammatory, hyperplastic, and neoplastic tissue. Gastroenterology. 1987;93(3):506–14.CrossRefPubMed Listrom MB, Fenoglio-Preiser CM. Lymphatic distribution of the stomach in normal, inflammatory, hyperplastic, and neoplastic tissue. Gastroenterology. 1987;93(3):506–14.CrossRefPubMed
44.
Zurück zum Zitat Tokunaga M, Ohyama S, Hiki N, Fukunaga T, Yamada K, Sano T, et al. Investigation of the lymphatic stream of the stomach in gastric cancer with solitary lymph node metastasis. World J Surg. 2009;33(6):1235–9.CrossRefPubMed Tokunaga M, Ohyama S, Hiki N, Fukunaga T, Yamada K, Sano T, et al. Investigation of the lymphatic stream of the stomach in gastric cancer with solitary lymph node metastasis. World J Surg. 2009;33(6):1235–9.CrossRefPubMed
45.
Zurück zum Zitat Bara T Jr., Gurzu S, Jung I, Kadar Z, Sugimura H, Bara T. Single skip metastasis in sentinel lymph node: in an early gastric cancer. World J Gastroenterol. 2015;21(33):9803–7.CrossRefPubMedPubMedCentral Bara T Jr., Gurzu S, Jung I, Kadar Z, Sugimura H, Bara T. Single skip metastasis in sentinel lymph node: in an early gastric cancer. World J Gastroenterol. 2015;21(33):9803–7.CrossRefPubMedPubMedCentral
46.
Zurück zum Zitat Peeters KC, Hundahl SA, Kranenbarg EK, Hartgrink H, van de Velde CJ. Low Maruyama index surgery for gastric cancer: blinded reanalysis of the Dutch D1–D2 trial. World J Surg. 2005;29(12):1576–84.CrossRefPubMed Peeters KC, Hundahl SA, Kranenbarg EK, Hartgrink H, van de Velde CJ. Low Maruyama index surgery for gastric cancer: blinded reanalysis of the Dutch D1–D2 trial. World J Surg. 2005;29(12):1576–84.CrossRefPubMed
47.
48.
Zurück zum Zitat Bollschweiler EH, Monig SP, Hensler K, Baldus SE, Maruyama K, Holscher AH. Artificial neural network for prediction of lymph node metastases in gastric cancer: a phase II diagnostic study. Ann Surg Oncol. 2004;11(5):506–11.CrossRefPubMed Bollschweiler EH, Monig SP, Hensler K, Baldus SE, Maruyama K, Holscher AH. Artificial neural network for prediction of lymph node metastases in gastric cancer: a phase II diagnostic study. Ann Surg Oncol. 2004;11(5):506–11.CrossRefPubMed
49.
Zurück zum Zitat Zulfikaroglu B, Koc M, Ozmen MM, Kucuk NO, Ozalp N, Aras G. Intraoperative lymphatic mapping and sentinel lymph node biopsy using radioactive tracer in gastric cancer. Surgery. 2005;138(5):899–904.CrossRefPubMed Zulfikaroglu B, Koc M, Ozmen MM, Kucuk NO, Ozalp N, Aras G. Intraoperative lymphatic mapping and sentinel lymph node biopsy using radioactive tracer in gastric cancer. Surgery. 2005;138(5):899–904.CrossRefPubMed
51.
Zurück zum Zitat Senol S, Aydin A, Kosemetin D, Ece D, Akalin I, Abuoglu H, et al. Gastric adenocarcinoma biomarker expression profiles and their prognostic value. J Environ Pathol Toxicol Oncol. 2016;35(3):207–22.CrossRefPubMed Senol S, Aydin A, Kosemetin D, Ece D, Akalin I, Abuoglu H, et al. Gastric adenocarcinoma biomarker expression profiles and their prognostic value. J Environ Pathol Toxicol Oncol. 2016;35(3):207–22.CrossRefPubMed
52.
Zurück zum Zitat Ren C, Chen H, Han C, Fu D, Wang D, Shen M. High expression of miR-16 and miR-451 predicating better prognosis in patients with gastric cancer. J Cancer Res Clin Oncol. 2016;142(12):2489–96.CrossRefPubMed Ren C, Chen H, Han C, Fu D, Wang D, Shen M. High expression of miR-16 and miR-451 predicating better prognosis in patients with gastric cancer. J Cancer Res Clin Oncol. 2016;142(12):2489–96.CrossRefPubMed
53.
Zurück zum Zitat Kattan MW, Hess KR, Amin MB, Lu Y, Moons KG, Gershenwald JE, et al. American Joint Committee on Cancer acceptance criteria for inclusion of risk models for individualized prognosis in the practice of precision medicine. CA Cancer J Clin. 2016;66(5):370–4.CrossRefPubMedPubMedCentral Kattan MW, Hess KR, Amin MB, Lu Y, Moons KG, Gershenwald JE, et al. American Joint Committee on Cancer acceptance criteria for inclusion of risk models for individualized prognosis in the practice of precision medicine. CA Cancer J Clin. 2016;66(5):370–4.CrossRefPubMedPubMedCentral
Metadaten
Titel
Should surgical ex vivo lymphadenectomy be a standard procedure in the management of patients with gastric cancer?
Our personal experience, systematic literature review, and meta-analysis
verfasst von
Mihai Dan Boşcaiu
Mihnea Dragomir
Bogdan Trandafir
Vlad Herlea
Cătălin Vasilescu
Publikationsdatum
28.03.2018
Verlag
Springer Vienna
Erschienen in
European Surgery / Ausgabe 4/2018
Print ISSN: 1682-8631
Elektronische ISSN: 1682-4016
DOI
https://doi.org/10.1007/s10353-018-0519-z

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