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Дискогезивная карцинома желудка: периоперационная химиотерапия или хирургия на первом этапе? Ретроспективное исследование
Дискогезивная карцинома желудка: периоперационная химиотерапия или хирургия на первом этапе? Ретроспективное исследование
Неред С.Н., Торосян Р.О., Козлов Н.А., Авдюхин И.Г., Стилиди И.С., Абу-Хайдар О.Б. Дискогезивная карцинома желудка: периоперационная химиотерапия или хирургия на первом этапе? Ретроспективное исследование. Современная Онкология. 2026;28(1):46–52. DOI: 10.26442/18151434.2026.1.203641
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Аннотация
Обоснование. Интерес к вопросу комбинированного лечения перстневидноклеточного рака и других подтипов дискогезивной карциномы усиливается с каждым годом.
Цель. Изучить и сравнить эффективность двух подходов к лечению дискогезивной карциномы: периоперационной химиотерапии (ХТ) и хирургического лечения на I этапе.
Материалы и методы. В исследование включены 112 пациентов с дискогезивным раком желудка, из которых 40 пациентов в 2018–2023 гг. получили периоперационную ХТ по схеме FLOT или mFOLFIRINOX, а у 72 в период 2015–2018 гг. на I этапе проведено хирургическое лечение (историческая группа контроля) с последующей адъювантной ХТ XELOX в случаях pТ≥2 и pN+. В обеих группах дискогезивный тип рака желудка подтвержден пересмотром гистологических препаратов операционного материала.
Результаты. Пятилетняя общая выживаемость (ОВ) в группе периоперационной ХТ составила 56,8%, в группе хирургического лечения – 50,8%. Показатели выживаемости имеют тенденцию к достоверным различиям в пользу периоперационного лечения (Log-Rank test; p=0,073). Медиана ОВ в группе хирургического лечения составила 67 мес, в группе периоперационной ХТ не достигнута. Пациенты в группе хирургического лечения имели более распространенную стадию опухолевого процесса, что может быть причиной более высоких показателей ОВ в группе периоперационной ХТ. Постадийный анализ не выявил различий в ОВ между группами ни при одной стадии. При однофакторном анализе с применением регрессии Кокса вид лечения имел тенденцию к влиянию на ОВ с пограничным значением достоверности (p=0,081). Многофакторный регрессионный анализ показал, что только TNM-стадия является значимым фактором прогноза ОВ. Периоперационная ХТ не является независимым прогностическим фактором. Различия в 3-летней ОВ при градации пациентов в зависимости от режима периоперационной ХТ не выявлены. В группах FLOT и FOLFIRINOX 3-летняя ОВ составила 77,7 и 80,5% соответственно (Log-Rank test; p=0,44). Медиана ОВ в группе FOLFIRINOX – 49,7 мес, в группе FLOT не достигнута.
Заключение. Отсутствие достоверных различий в выживаемости не позволяет сделать однозначный вывод о преимуществе периоперационной ХТ по сравнению с хирургическим лечением на I этапе у больных дискогезивной карциномой желудка. Требуется дальнейшее изучение данного вопроса в рамках рандомизированного исследования.
Ключевые слова: дискогезивная карцинома желудка, перстневидноклеточный рак желудка, диффузный рак, комбинированное лечение, предоперационная химиотерапия, FLOT, FOLFIRINOX, прогноз
Objective. To study and compare the effectiveness of two approaches to the treatment of poorly cohesive carcinoma: perioperative chemotherapy (CT) and surgery at the initial stage.
Materials and methods. A total of 112 patients with poorly cohesive gastric carcinoma were included. Of these, 40 patients treated between 2018 and 2023 received perioperative chemotherapy with FLOT or mFOLFIRINOX. The historical control group comprised 72 patients treated between 2015 and 2018 who underwent initial surgery, followed by adjuvant XELOX chemotherapy in cases of pT≥2 and pN+. In both groups, the diagnosis of poorly cohesive gastric carcinoma was confirmed by histological slide review of surgical specimens.
Results. The five-year overall survival (OS) rate was 56.8% in the perioperative chemotherapy group and 50.8% in the surgical treatment group. Although survival rates favored perioperative treatment, the difference was not statistically significant (Log-Rank test; p=0.073). The median OS in the surgery group was 67 months, while it was not reached in the perioperative chemotherapy group. Patients in the surgical treatment group presented with more advanced tumor stages, which may have contributed to the observed OS differences. Stage-specific analysis revealed no significant differences in OS between groups at any stage. Univariate Cox regression analysis indicated a trend toward treatment affecting OS (p=0.081), but multivariate regression identified TNM stage as the only significant predictor of OS. Perioperative chemotherapy was not an independent prognostic factor. No differences in three-year OS were observed among patients with different tumor grades, regardless of perioperative chemotherapy regimen. In the FLOT and FOLFIRINOX groups, the three-year OS rates were 77.7% and 80.5%, respectively (Log-Rank test; p=0.44). The median OS in the FOLFIRINOX group was 49.7 months, while it was not reached in the FLOT group.
Conclusion. The lack of significant differences in survival prevents a definitive conclusion regarding the superiority of perioperative chemotherapy compared to initial surgery in patients with poorly cohesive gastric carcinoma. Further investigation in randomized controlled trials is warranted.
Keywords: poorly cohesive gastric carcinoma, signet ring cancer, diffuse cancer, combined treatment, preoperative chemotherapy, FLOT, FOLFIRINOX, prognosis
Цель. Изучить и сравнить эффективность двух подходов к лечению дискогезивной карциномы: периоперационной химиотерапии (ХТ) и хирургического лечения на I этапе.
Материалы и методы. В исследование включены 112 пациентов с дискогезивным раком желудка, из которых 40 пациентов в 2018–2023 гг. получили периоперационную ХТ по схеме FLOT или mFOLFIRINOX, а у 72 в период 2015–2018 гг. на I этапе проведено хирургическое лечение (историческая группа контроля) с последующей адъювантной ХТ XELOX в случаях pТ≥2 и pN+. В обеих группах дискогезивный тип рака желудка подтвержден пересмотром гистологических препаратов операционного материала.
Результаты. Пятилетняя общая выживаемость (ОВ) в группе периоперационной ХТ составила 56,8%, в группе хирургического лечения – 50,8%. Показатели выживаемости имеют тенденцию к достоверным различиям в пользу периоперационного лечения (Log-Rank test; p=0,073). Медиана ОВ в группе хирургического лечения составила 67 мес, в группе периоперационной ХТ не достигнута. Пациенты в группе хирургического лечения имели более распространенную стадию опухолевого процесса, что может быть причиной более высоких показателей ОВ в группе периоперационной ХТ. Постадийный анализ не выявил различий в ОВ между группами ни при одной стадии. При однофакторном анализе с применением регрессии Кокса вид лечения имел тенденцию к влиянию на ОВ с пограничным значением достоверности (p=0,081). Многофакторный регрессионный анализ показал, что только TNM-стадия является значимым фактором прогноза ОВ. Периоперационная ХТ не является независимым прогностическим фактором. Различия в 3-летней ОВ при градации пациентов в зависимости от режима периоперационной ХТ не выявлены. В группах FLOT и FOLFIRINOX 3-летняя ОВ составила 77,7 и 80,5% соответственно (Log-Rank test; p=0,44). Медиана ОВ в группе FOLFIRINOX – 49,7 мес, в группе FLOT не достигнута.
Заключение. Отсутствие достоверных различий в выживаемости не позволяет сделать однозначный вывод о преимуществе периоперационной ХТ по сравнению с хирургическим лечением на I этапе у больных дискогезивной карциномой желудка. Требуется дальнейшее изучение данного вопроса в рамках рандомизированного исследования.
Ключевые слова: дискогезивная карцинома желудка, перстневидноклеточный рак желудка, диффузный рак, комбинированное лечение, предоперационная химиотерапия, FLOT, FOLFIRINOX, прогноз
________________________________________________
Objective. To study and compare the effectiveness of two approaches to the treatment of poorly cohesive carcinoma: perioperative chemotherapy (CT) and surgery at the initial stage.
Materials and methods. A total of 112 patients with poorly cohesive gastric carcinoma were included. Of these, 40 patients treated between 2018 and 2023 received perioperative chemotherapy with FLOT or mFOLFIRINOX. The historical control group comprised 72 patients treated between 2015 and 2018 who underwent initial surgery, followed by adjuvant XELOX chemotherapy in cases of pT≥2 and pN+. In both groups, the diagnosis of poorly cohesive gastric carcinoma was confirmed by histological slide review of surgical specimens.
Results. The five-year overall survival (OS) rate was 56.8% in the perioperative chemotherapy group and 50.8% in the surgical treatment group. Although survival rates favored perioperative treatment, the difference was not statistically significant (Log-Rank test; p=0.073). The median OS in the surgery group was 67 months, while it was not reached in the perioperative chemotherapy group. Patients in the surgical treatment group presented with more advanced tumor stages, which may have contributed to the observed OS differences. Stage-specific analysis revealed no significant differences in OS between groups at any stage. Univariate Cox regression analysis indicated a trend toward treatment affecting OS (p=0.081), but multivariate regression identified TNM stage as the only significant predictor of OS. Perioperative chemotherapy was not an independent prognostic factor. No differences in three-year OS were observed among patients with different tumor grades, regardless of perioperative chemotherapy regimen. In the FLOT and FOLFIRINOX groups, the three-year OS rates were 77.7% and 80.5%, respectively (Log-Rank test; p=0.44). The median OS in the FOLFIRINOX group was 49.7 months, while it was not reached in the FLOT group.
Conclusion. The lack of significant differences in survival prevents a definitive conclusion regarding the superiority of perioperative chemotherapy compared to initial surgery in patients with poorly cohesive gastric carcinoma. Further investigation in randomized controlled trials is warranted.
Keywords: poorly cohesive gastric carcinoma, signet ring cancer, diffuse cancer, combined treatment, preoperative chemotherapy, FLOT, FOLFIRINOX, prognosis
Полный текст
Список литературы
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2. Chen YC, Fang WL, Wang RF, et al. Clinicopathological Variation of Lauren Classification in Gastric Cancer. Pathol Oncol Res. 2016;22:197-202. DOI:10.1007/s12253-015-9996-6
3. Lee JH, Chang KK, Yoon C, et al. Lauren histologic type is the most important factor associated with pattern of recurrence following resection of gastric adenocarcinoma. Ann Surg. 2018;267(1):105-13. DOI:10.1097/SLA.0000000000002040
4. Nered SN, Klimenkov AA, Stilidi IS, et al. Perstnevidnokletochnyi rak zheludka: kliniko-morfologicheskie aspekty, rezultaty khirurgicheskogo lecheniia i prognoz. Voprosy onkologii. 2006;52(3):294-300 (in Russian).
5. Nered SN, Klimenkov AA. Khirurgicheskoe lechenie raka zheludka s vysokim riskom implantatsionnogo metastazirovaniia. Voprosy onkologii. 2005;51(1):75-80 (in Russian).
6. Lemoine N, Adenis A, Bouche O, et al. Signet Ring Cells and Efficacy of First-line Chemotherapy in Advanced Gastric or Oesogastric Junction Adenocarcinoma. Anticancer Res. 2016;36:5543-50. DOI:10.21873/anticanres.11138
7. Schirren R, Novotny A, Oesterlin Е, et al. Significance of Lauren Classification in Patients Undergoing Neoadjuvant/Perioperative Chemotherapy for Locally Advanced Gastric or Gastroesophageal Junction Cancers - Analysis from a Large Single Center Cohort in Germany. Cancers. 2021;13:290. DOI:10.3390/cancers13020290
8. Schiefer S, Crnovrsanin N, Kalkum E, et al. Is neoadjuvant chemotherapy followed by surgery the appropriate treatment for esophagogastric signet ring cell carcinomas? A systematic review and meta-analysis. Front Surg. 2024;11:1382039. DOI:10.3389/fsurg.2024.1382039
9. Al-Batran SE, Hofheinz RD, Pauligk C, et al. Histopathological regression after neoadjuvant docetaxel, oxaliplatin, fluorouracil, and leucovorin versus epirubicin, cisplatin, and fluorouracil or capecita bine in patients with resectable gastric or gastro-oesophageal junction adenocarcinoma (FLOT4-AIO): results from the phase 2 part of a multicentre, open-label, randomised phase 2/3 trial. Lancet Oncol. 2016;17(12):1697-708. DOI:10.1016/S1470-2045(16)30531-9
10. Wang K, Li E, Busuttil RA, et al. A cohort study and meta-analysis of the evidence for consideration of Lauren subtype when prescribing adjuvant or palliative chemotherapy for gastric cancer. Ther Adv Med Oncol. 2020;12:1-22. DOI:10.1177/1758835920930359
11. Messager M, Lefevre JH, Pichot-Delahaye V, et al. The Impact of Perioperative Chemotherapy on Survival in Patients With Gastric Signet Ring Cell Adenocarcinoma. A Multicenter Comparative Study. Ann Surg. 2011;254(5):684-93. DOI:10.1097/SLA.0b013e3182352647
12. Machlowska J, Pucułek M, Sitarz M, et al. State of the art for gastric signet ring cell: from classification, prognosis, and genomic characteristics to specified treatments. Cancer Management Res. 2019;11:2151-61.
13. Voron T, Messager M, Duhamel A, et al. Is signet-ring cell carcinoma a specific entity among gastric cancers? Gastric Cancer. 2016;19:1027-40. DOI:10.1007/s10120-015-0564-2
14. Heger U, Sisic L, Nienhüser H, Blank S, at al. Neoadjuvant Therapy Improves Outcomes in Locally Advanced Signet-Ring-Cell Containing Esophagogastric Adenocarcinomas. Ann Surg Oncol. 2018;25:2418-27. DOI:10.1245/s10434-018-6541-3
15. Gertsen EC, van der Veen A, Brenkman HJF, et al. Multimodal Therapy Versus Primary Surgery for Gastric and Gastroesophageal Junction Diffuse Type Carcinoma, with a Focus on Signet Ring Cell Carcinoma: A Nationwide Study. Ann Surg Oncol. 2024;31(3):1760-72. DOI:10.1245/s10434-023-14690-y
16. Smyth EC, Verheij M, Allum W, et al. Arnold on behalf of the ESMO Guidelines Committee. Gastric cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2016;27 (Suppl.5):v38-49. DOI:10.1093/annonc/mdw350
17. Besova NS, Bolotina LV, Gamayunov SV, et al. Gastric cancer. RUSSCO practical recommendations, part 1.1. Malignant Tumours. 2024;14(3s2):241-62 (in Russian). DOI:10.18027/2224-5057-2024-14-3s2-1.1-13
18. Borch K, Jönsson B, Tarpila E, et al. Changing pattern of histological type, location, stage and outcome of surgical treatment of gastric carcinoma. Br J Surg. 2000;87(5):618-26. DOI:10.1046/j.1365-2168.2000.01425.x.
19. Henson DE, Dittus C, Younes M, et al. Differential trends in the intestinal and diffuse types of gastric carcinoma in the United States, 1973-2000: increase in the signet ring cell type. Arch Pathol Lab Med. 2004;128:765-70. DOI:10.5858/2004-128-765-DTITIA.
20. Pernot S, Voron T, Perkins G, et al. Signet-ring cell carcinoma of the stomach: Impact on prognosis and specific therapeutic challenge. World J Gastroenterol 2015;21(40):11428-38. DOI:10.3748/wjg.v21.i40.11428
21. Lauren P. The two histological main types of gastric carcinoma: dif fuse and so-called intestinal-type carcinoma. An attempt at a his to-clinical classification. Acta Pathol Microbiol Scand. 1965:64:31-49. DOI:10.1111/apm.1965.64.1.31
22. Zheng H, Li X, Hara T, et al. Mixed-type gastric carcinomas exhibit more aggressive features and indicate the histogenesis of carcinomas. Virchows Arch. 2008;452:525-34. DOI:10.1007/s00428-007-0572-7
23. Nered SN, Kozlov NA, Torosyan RO, Stilidi IS. Prognosis of poorly cohesive gastric carcinoma depending on the depth of tumor invasion and the amount of signet ring cells in tumor. Russian Journal of Archive of Pathology. 2025;87(6):20‑7 (in Russian).
24. Mariette C, Carneiro F, Grabsch HI, et al. Consensus on the pathological definition and classification of poorly cohesive gastric carcinoma. European Chapter of International Gastric Cancer Association. Gastric Cancer. 2019;22(1):1-9. DOI:10.1007/s10120-018-0868-0
25. Park SH, Sohn TS, Lee J, et al. Phase III Trial to Compare Adjuvant Chemotherapy With Capecitabine and Cisplatin Versus Concurrent Chemoradiotherapy in Gastric Cancer: Final Report of the Adjuvant Chemoradiotherapy in Stomach Tumors Trial, Including Survival and Subset Analyses. J Clin Oncol. 2015;33(28):3130-6. DOI:10.1200/JCO.2014.58.3930
26. Li Y, Ma FH, Xue LY, Tian YT. Neoadjuvant chemotherapy vs upfront surgery for gastric signet ring cell carcinoma: A retrospective, propensity score-matched study. World J Gastroenterol. 2020;26(8):818-27. DOI:10.3748/wjg.v26.i8.818
27. Piessen G, Messager M, Le Malicot K, et al. Phase II/III multicentre randomised controlled trial evaluating a strategy of primary surgery and adjuvant chemotherapy versus peri-operative chemotherapy for resectable gastric signet ring cell adenocarcinomas – PRODIGE 19 – FFCD1103 – ADCI002. BMC Cancer. 2013;13:281. DOI:10.1186/1471-2407-13-281
28. Al-Batran S-E, Homann N, Pauligk C, et al. Perioperative chemotherapy with fluorouracil plus leucovorin, oxaliplatin, and docetaxel versus fluorouracil or capecitabine plus cisplatin and epirubicin for locally advanced, resectable gastric or gastro-oesophageal junction adenocarcinoma (FLOT4): a randomised, phase 2/3 trial. Lancet. 2019;393(10184):1948-57. DOI:10.1016/S0140-6736(18)32557-1
29. Giampieri R, Baleani MG, Bittoni A, et al. Impact of Signet-Ring Cell Histology in the Management of Patients with Non-Metastatic Gastric Cancer: Results from a Retrospective Multicenter Analysis Comparing FLOT Perioperative Chemotherapy vs. Surgery Followed by Adjuvant Chemotherapy. Cancers. 2023;15:3342. DOI:10.3390/ cancers15133342
30. Li Z-F, Li Z, Zhang X-J, et al. Perioperative chemotherapy improves survival of patients with locally advanced diffuse gastric cancer. World J Gastrointest Surg. 2024;16(9):2878-92. DOI:10.4240/wjgs.v16.i9.2878
31. Chen L, Shi Y, Yuan J, et al. Evaluation of docetaxel- and oxaliplatin-based adjuvant chemotherapy in postgastrectomy gastric cancer patients reveals obvious survival benefits in docetaxel-treated mixed signet ring cell carcinoma patients. Med Oncol. 2014;31:159 DOI:10.1007/s12032-014-0159-5
32. Fonseca PJ, Carmona-Bayonas A, Hernandez R, et al. Lauren subtypes of advanced gastric cancer influence survival and response to chemotherapy: real-world data from the AGAMENON National Cancer Registry. Br J Cancer. 2017;117:775-82. DOI:10.1038/bjc.2017.245
33. Homann N, Pauligk C, Luley K, et al. Pathological complete remission in patients with oesophagogastric cancer receiving preoperative 5-fluorouracil, oxaliplatin and docetaxel. Int J Cancer. 2012;130(7):1706-13. DOI:10.1002/ijc.26180
34. Schulz C, Kullmann F, Kunzmann V, et al. NeoFLOT: Multicenter phase II study of perioperative chemotherapy in resectable adenocarcinoma of the gastroesophageal junction or gastric adenocarcinoma-Very good response predominantly in patients with intestinal type tumors. Int J Cancer. 2015;137(3):678-85. DOI:10.1002/ijc.29403
35. Kalinin AE, Avdyukhin IG, Nered SN, et al. Efficacy of perioperative FOLFIRINOX chemotherapy versus FLOT chemotherapy in patients with resectable adenocarcinoma of the stomach or gastroesophageal junction (SIEWERT types II–III, cT4aN0M0, T1–4cN+ cM0): preliminary results of the study. Malignant Tumours. 2023;13(4):7-17 (in Russian). DOI:10.18027 / 2224-5057-2023-13-4-7-17
36. Nered SN, Torosyan RO, Kozlov NA, et al. Frequency of MSI, PD-L1 (CPS), HER2 in poorly cohesive gastric carcinomas. Arkh Patol. 2025;87(2):11-7 (in Russian). DOI:10.17116/patol20258702111
2. Chen YC, Fang WL, Wang RF, et al. Clinicopathological Variation of Lauren Classification in Gastric Cancer. Pathol Oncol Res. 2016;22:197-202. DOI:10.1007/s12253-015-9996-6
3. Lee JH, Chang KK, Yoon C, et al. Lauren histologic type is the most important factor associated with pattern of recurrence following resection of gastric adenocarcinoma. Ann Surg. 2018;267(1):105-13. DOI:10.1097/SLA.0000000000002040
4. Неред С.Н., Клименков А.А., Стилиди И.С., и др. Перстневидноклеточный рак желудка: клинико-морфологические аспекты, результаты хирургического лечения и прогноз. Вопросы онкологии. 2006;52(3):294-300 [Nered SN, Klimenkov AA, Stilidi IS, et al. Perstnevidnokletochnyi rak zheludka: kliniko-morfologicheskie aspekty, rezultaty khirurgicheskogo lecheniia i prognoz. Voprosy onkologii. 2006;52(3):294-300 (in Russian)].
5. Неред С.Н., Клименков А.А. Хирургическое лечение рака желудка с высоким риском имплантационного метастазирования. Вопросы онкологии. 2005;51(1):75-80 [Nered SN, Klimenkov AA. Khirurgicheskoe lechenie raka zheludka s vysokim riskom implantatsionnogo metastazirovaniia. Voprosy onkologii. 2005;51(1):75-80 (in Russian)].
6. Lemoine N, Adenis A, Bouche O, et al. Signet Ring Cells and Efficacy of First-line Chemotherapy in Advanced Gastric or Oesogastric Junction Adenocarcinoma. Anticancer Res. 2016;36:5543-50. DOI:10.21873/anticanres.11138
7. Schirren R, Novotny A, Oesterlin Е, et al. Significance of Lauren Classification in Patients Undergoing Neoadjuvant/Perioperative Chemotherapy for Locally Advanced Gastric or Gastroesophageal Junction Cancers - Analysis from a Large Single Center Cohort in Germany. Cancers. 2021;13:290. DOI:10.3390/cancers13020290
8. Schiefer S, Crnovrsanin N, Kalkum E, et al. Is neoadjuvant chemotherapy followed by surgery the appropriate treatment for esophagogastric signet ring cell carcinomas? A systematic review and meta-analysis. Front Surg. 2024;11:1382039. DOI:10.3389/fsurg.2024.1382039
9. Al-Batran SE, Hofheinz RD, Pauligk C, et al. Histopathological regression after neoadjuvant docetaxel, oxaliplatin, fluorouracil, and leucovorin versus epirubicin, cisplatin, and fluorouracil or capecita bine in patients with resectable gastric or gastro-oesophageal junction adenocarcinoma (FLOT4-AIO): results from the phase 2 part of a multicentre, open-label, randomised phase 2/3 trial. Lancet Oncol. 2016;17(12):1697-708. DOI:10.1016/S1470-2045(16)30531-9
10. Wang K, Li E, Busuttil RA, et al. A cohort study and meta-analysis of the evidence for consideration of Lauren subtype when prescribing adjuvant or palliative chemotherapy for gastric cancer. Ther Adv Med Oncol. 2020;12:1-22. DOI:10.1177/1758835920930359
11. Messager M, Lefevre JH, Pichot-Delahaye V, et al. The Impact of Perioperative Chemotherapy on Survival in Patients With Gastric Signet Ring Cell Adenocarcinoma. A Multicenter Comparative Study. Ann Surg. 2011;254(5):684-93. DOI:10.1097/SLA.0b013e3182352647
12. Machlowska J, Pucułek M, Sitarz M, et al. State of the art for gastric signet ring cell: from classification, prognosis, and genomic characteristics to specified treatments. Cancer Management Res. 2019;11:2151-61.
13. Voron T, Messager M, Duhamel A, et al. Is signet-ring cell carcinoma a specific entity among gastric cancers? Gastric Cancer. 2016;19:1027-40. DOI:10.1007/s10120-015-0564-2
14. Heger U, Sisic L, Nienhüser H, Blank S, at al. Neoadjuvant Therapy Improves Outcomes in Locally Advanced Signet-Ring-Cell Containing Esophagogastric Adenocarcinomas. Ann Surg Oncol. 2018;25:2418-27. DOI:10.1245/s10434-018-6541-3
15. Gertsen EC, van der Veen A, Brenkman HJF, et al. Multimodal Therapy Versus Primary Surgery for Gastric and Gastroesophageal Junction Diffuse Type Carcinoma, with a Focus on Signet Ring Cell Carcinoma: A Nationwide Study. Ann Surg Oncol. 2024;31(3):1760-72. DOI:10.1245/s10434-023-14690-y
16. Smyth EC, Verheij M, Allum W, et al. Arnold on behalf of the ESMO Guidelines Committee. Gastric cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2016;27 (Suppl.5):v38-49. DOI:10.1093/annonc/mdw350
17. Бесова Н.С., Болотина Л.В., Гамаюнов С.В., и др. Рак желудка. Практические рекомендации RUSSCO, часть 1.1. Злокачественные опухоли. 2024;14(3s2):241-62 [Besova NS, Bolotina LV, Gamayunov SV, et al. Gastric cancer. RUSSCO practical recommendations, part 1.1. Malignant Tumours. 2024;14(3s2):241-62 (in Russian)]. DOI:10.18027/2224-5057-2024-14-3s2-1.1-13
18. Borch K, Jönsson B, Tarpila E, et al. Changing pattern of histological type, location, stage and outcome of surgical treatment of gastric carcinoma. Br J Surg. 2000;87(5):618-26. DOI:10.1046/j.1365-2168.2000.01425.x.
19. Henson DE, Dittus C, Younes M, et al. Differential trends in the intestinal and diffuse types of gastric carcinoma in the United States, 1973-2000: increase in the signet ring cell type. Arch Pathol Lab Med. 2004;128:765-70. DOI:10.5858/2004-128-765-DTITIA.
20. Pernot S, Voron T, Perkins G, et al. Signet-ring cell carcinoma of the stomach: Impact on prognosis and specific therapeutic challenge. World J Gastroenterol 2015;21(40):11428-38. DOI:10.3748/wjg.v21.i40.11428
21. Lauren P. The two histological main types of gastric carcinoma: dif fuse and so-called intestinal-type carcinoma. An attempt at a his to-clinical classification. Acta Pathol Microbiol Scand. 1965:64:31-49. DOI:10.1111/apm.1965.64.1.31
22. Zheng H, Li X, Hara T, et al. Mixed-type gastric carcinomas exhibit more aggressive features and indicate the histogenesis of carcinomas. Virchows Arch. 2008;452:525-34. DOI:10.1007/s00428-007-0572-7
23. Неред С.Н., Козлов Н.А., Торосян Р.О., Стилиди И.С. Прогноз при дискогезивной карциноме желудка в зависимости от глубины инвазии опухоли и количества перстневидных клеток. Архив патологии. 2025;87(6):20-7 [Nered SN, Kozlov NA, Torosyan RO, Stilidi IS. Prognosis of poorly cohesive gastric carcinoma depending on the depth of tumor invasion and the amount of signet ring cells in tumor. Russian Journal of Archive of Pathology. 2025;87(6):20‑7 (in Russian)].
24. Mariette C, Carneiro F, Grabsch HI, et al. Consensus on the pathological definition and classification of poorly cohesive gastric carcinoma. European Chapter of International Gastric Cancer Association. Gastric Cancer. 2019;22(1):1-9. DOI:10.1007/s10120-018-0868-0
25. Park SH, Sohn TS, Lee J, et al. Phase III Trial to Compare Adjuvant Chemotherapy With Capecitabine and Cisplatin Versus Concurrent Chemoradiotherapy in Gastric Cancer: Final Report of the Adjuvant Chemoradiotherapy in Stomach Tumors Trial, Including Survival and Subset Analyses. J Clin Oncol. 2015;33(28):3130-6. DOI:10.1200/JCO.2014.58.3930
26. Li Y, Ma FH, Xue LY, Tian YT. Neoadjuvant chemotherapy vs upfront surgery for gastric signet ring cell carcinoma: A retrospective, propensity score-matched study. World J Gastroenterol. 2020;26(8):818-27. DOI:10.3748/wjg.v26.i8.818
27. Piessen G, Messager M, Le Malicot K, et al. Phase II/III multicentre randomised controlled trial evaluating a strategy of primary surgery and adjuvant chemotherapy versus peri-operative chemotherapy for resectable gastric signet ring cell adenocarcinomas – PRODIGE 19 – FFCD1103 – ADCI002. BMC Cancer. 2013;13:281. DOI:10.1186/1471-2407-13-281
28. Al-Batran S-E, Homann N, Pauligk C, et al. Perioperative chemotherapy with fluorouracil plus leucovorin, oxaliplatin, and docetaxel versus fluorouracil or capecitabine plus cisplatin and epirubicin for locally advanced, resectable gastric or gastro-oesophageal junction adenocarcinoma (FLOT4): a randomised, phase 2/3 trial. Lancet. 2019;393(10184):1948-57. DOI:10.1016/S0140-6736(18)32557-1
29. Giampieri R, Baleani MG, Bittoni A, et al. Impact of Signet-Ring Cell Histology in the Management of Patients with Non-Metastatic Gastric Cancer: Results from a Retrospective Multicenter Analysis Comparing FLOT Perioperative Chemotherapy vs. Surgery Followed by Adjuvant Chemotherapy. Cancers. 2023;15:3342. DOI:10.3390/ cancers15133342
30. Li Z-F, Li Z, Zhang X-J, et al. Perioperative chemotherapy improves survival of patients with locally advanced diffuse gastric cancer. World J Gastrointest Surg. 2024;16(9):2878-92. DOI:10.4240/wjgs.v16.i9.2878
31. Chen L, Shi Y, Yuan J, et al. Evaluation of docetaxel- and oxaliplatin-based adjuvant chemotherapy in postgastrectomy gastric cancer patients reveals obvious survival benefits in docetaxel-treated mixed signet ring cell carcinoma patients. Med Oncol. 2014;31:159 DOI:10.1007/s12032-014-0159-5
32. Fonseca PJ, Carmona-Bayonas A, Hernandez R, et al. Lauren subtypes of advanced gastric cancer influence survival and response to chemotherapy: real-world data from the AGAMENON National Cancer Registry. Br J Cancer. 2017;117:775-82. DOI:10.1038/bjc.2017.245
33. Homann N, Pauligk C, Luley K, et al. Pathological complete remission in patients with oesophagogastric cancer receiving preoperative 5-fluorouracil, oxaliplatin and docetaxel. Int J Cancer. 2012;130(7):1706-13. DOI:10.1002/ijc.26180
34. Schulz C, Kullmann F, Kunzmann V, et al. NeoFLOT: Multicenter phase II study of perioperative chemotherapy in resectable adenocarcinoma of the gastroesophageal junction or gastric adenocarcinoma-Very good response predominantly in patients with intestinal type tumors. Int J Cancer. 2015;137(3):678-85. DOI:10.1002/ijc.29403
35. Калинин А.Е., Авдюхин И.Г., Неред С.Н., и др. Предварительные результаты исследования по оценке эффективности периоперационной химиотерапии в режиме FOLFIRINOX в сравнении с режимом FLOT у больных операбельной аденокарциномой желудка или кардиоэзофагеального перехода (II–III тип по классификации SIEWERT) cT4aN0M0, T1–4cN+cM0. Злокачественные опухоли. 2023;13(4):7-17 [Kalinin AE, Avdyukhin IG, Nered SN, et al. Efficacy of perioperative FOLFIRINOX chemotherapy versus FLOT chemotherapy in patients with resectable adenocarcinoma of the stomach or gastroesophageal junction (SIEWERT types II–III, cT4aN0M0, T1–4cN+ cM0): preliminary results of the study. Malignant Tumours. 2023;13(4):7-17 (in Russian)]. DOI:10.18027 / 2224-5057-2023-13-4-7-17
36. Неред С.Н., Торосян Р.О., Козлов Н.А., и др. Частота встречаемости MSI, PD-L1 (CPS), HER2 при дискогезивных карциномах желудка. Архив патологии. 2025;87(2):11-7 [Nered SN, Torosyan RO, Kozlov NA, et al. Frequency of MSI, PD-L1 (CPS), HER2 in poorly cohesive gastric carcinomas. Arkh Patol. 2025;87(2):11-7 (in Russian)]. DOI:10.17116/patol20258702111
________________________________________________
2. Chen YC, Fang WL, Wang RF, et al. Clinicopathological Variation of Lauren Classification in Gastric Cancer. Pathol Oncol Res. 2016;22:197-202. DOI:10.1007/s12253-015-9996-6
3. Lee JH, Chang KK, Yoon C, et al. Lauren histologic type is the most important factor associated with pattern of recurrence following resection of gastric adenocarcinoma. Ann Surg. 2018;267(1):105-13. DOI:10.1097/SLA.0000000000002040
4. Nered SN, Klimenkov AA, Stilidi IS, et al. Perstnevidnokletochnyi rak zheludka: kliniko-morfologicheskie aspekty, rezultaty khirurgicheskogo lecheniia i prognoz. Voprosy onkologii. 2006;52(3):294-300 (in Russian).
5. Nered SN, Klimenkov AA. Khirurgicheskoe lechenie raka zheludka s vysokim riskom implantatsionnogo metastazirovaniia. Voprosy onkologii. 2005;51(1):75-80 (in Russian).
6. Lemoine N, Adenis A, Bouche O, et al. Signet Ring Cells and Efficacy of First-line Chemotherapy in Advanced Gastric or Oesogastric Junction Adenocarcinoma. Anticancer Res. 2016;36:5543-50. DOI:10.21873/anticanres.11138
7. Schirren R, Novotny A, Oesterlin Е, et al. Significance of Lauren Classification in Patients Undergoing Neoadjuvant/Perioperative Chemotherapy for Locally Advanced Gastric or Gastroesophageal Junction Cancers - Analysis from a Large Single Center Cohort in Germany. Cancers. 2021;13:290. DOI:10.3390/cancers13020290
8. Schiefer S, Crnovrsanin N, Kalkum E, et al. Is neoadjuvant chemotherapy followed by surgery the appropriate treatment for esophagogastric signet ring cell carcinomas? A systematic review and meta-analysis. Front Surg. 2024;11:1382039. DOI:10.3389/fsurg.2024.1382039
9. Al-Batran SE, Hofheinz RD, Pauligk C, et al. Histopathological regression after neoadjuvant docetaxel, oxaliplatin, fluorouracil, and leucovorin versus epirubicin, cisplatin, and fluorouracil or capecita bine in patients with resectable gastric or gastro-oesophageal junction adenocarcinoma (FLOT4-AIO): results from the phase 2 part of a multicentre, open-label, randomised phase 2/3 trial. Lancet Oncol. 2016;17(12):1697-708. DOI:10.1016/S1470-2045(16)30531-9
10. Wang K, Li E, Busuttil RA, et al. A cohort study and meta-analysis of the evidence for consideration of Lauren subtype when prescribing adjuvant or palliative chemotherapy for gastric cancer. Ther Adv Med Oncol. 2020;12:1-22. DOI:10.1177/1758835920930359
11. Messager M, Lefevre JH, Pichot-Delahaye V, et al. The Impact of Perioperative Chemotherapy on Survival in Patients With Gastric Signet Ring Cell Adenocarcinoma. A Multicenter Comparative Study. Ann Surg. 2011;254(5):684-93. DOI:10.1097/SLA.0b013e3182352647
12. Machlowska J, Pucułek M, Sitarz M, et al. State of the art for gastric signet ring cell: from classification, prognosis, and genomic characteristics to specified treatments. Cancer Management Res. 2019;11:2151-61.
13. Voron T, Messager M, Duhamel A, et al. Is signet-ring cell carcinoma a specific entity among gastric cancers? Gastric Cancer. 2016;19:1027-40. DOI:10.1007/s10120-015-0564-2
14. Heger U, Sisic L, Nienhüser H, Blank S, at al. Neoadjuvant Therapy Improves Outcomes in Locally Advanced Signet-Ring-Cell Containing Esophagogastric Adenocarcinomas. Ann Surg Oncol. 2018;25:2418-27. DOI:10.1245/s10434-018-6541-3
15. Gertsen EC, van der Veen A, Brenkman HJF, et al. Multimodal Therapy Versus Primary Surgery for Gastric and Gastroesophageal Junction Diffuse Type Carcinoma, with a Focus on Signet Ring Cell Carcinoma: A Nationwide Study. Ann Surg Oncol. 2024;31(3):1760-72. DOI:10.1245/s10434-023-14690-y
16. Smyth EC, Verheij M, Allum W, et al. Arnold on behalf of the ESMO Guidelines Committee. Gastric cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2016;27 (Suppl.5):v38-49. DOI:10.1093/annonc/mdw350
17. Besova NS, Bolotina LV, Gamayunov SV, et al. Gastric cancer. RUSSCO practical recommendations, part 1.1. Malignant Tumours. 2024;14(3s2):241-62 (in Russian). DOI:10.18027/2224-5057-2024-14-3s2-1.1-13
18. Borch K, Jönsson B, Tarpila E, et al. Changing pattern of histological type, location, stage and outcome of surgical treatment of gastric carcinoma. Br J Surg. 2000;87(5):618-26. DOI:10.1046/j.1365-2168.2000.01425.x.
19. Henson DE, Dittus C, Younes M, et al. Differential trends in the intestinal and diffuse types of gastric carcinoma in the United States, 1973-2000: increase in the signet ring cell type. Arch Pathol Lab Med. 2004;128:765-70. DOI:10.5858/2004-128-765-DTITIA.
20. Pernot S, Voron T, Perkins G, et al. Signet-ring cell carcinoma of the stomach: Impact on prognosis and specific therapeutic challenge. World J Gastroenterol 2015;21(40):11428-38. DOI:10.3748/wjg.v21.i40.11428
21. Lauren P. The two histological main types of gastric carcinoma: dif fuse and so-called intestinal-type carcinoma. An attempt at a his to-clinical classification. Acta Pathol Microbiol Scand. 1965:64:31-49. DOI:10.1111/apm.1965.64.1.31
22. Zheng H, Li X, Hara T, et al. Mixed-type gastric carcinomas exhibit more aggressive features and indicate the histogenesis of carcinomas. Virchows Arch. 2008;452:525-34. DOI:10.1007/s00428-007-0572-7
23. Nered SN, Kozlov NA, Torosyan RO, Stilidi IS. Prognosis of poorly cohesive gastric carcinoma depending on the depth of tumor invasion and the amount of signet ring cells in tumor. Russian Journal of Archive of Pathology. 2025;87(6):20‑7 (in Russian).
24. Mariette C, Carneiro F, Grabsch HI, et al. Consensus on the pathological definition and classification of poorly cohesive gastric carcinoma. European Chapter of International Gastric Cancer Association. Gastric Cancer. 2019;22(1):1-9. DOI:10.1007/s10120-018-0868-0
25. Park SH, Sohn TS, Lee J, et al. Phase III Trial to Compare Adjuvant Chemotherapy With Capecitabine and Cisplatin Versus Concurrent Chemoradiotherapy in Gastric Cancer: Final Report of the Adjuvant Chemoradiotherapy in Stomach Tumors Trial, Including Survival and Subset Analyses. J Clin Oncol. 2015;33(28):3130-6. DOI:10.1200/JCO.2014.58.3930
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Авторы
С.Н. Неред*1,2, Р.О. Торосян1, Н.А. Козлов1, И.Г. Авдюхин1, И.С. Стилиди1,3, О.Б. Абу-Хайдар1
1ФГБУ «Национальный медицинский исследовательский центр онкологии им. Н.Н. Блохина» Минздрава России, Москва, Российская Федерация
2ФГБОУ ДПО «Российская медицинская академия непрерывного профессионального образования» Минздрава России, Москва, Российская Федерация
3ФГАОУ ВО «Российский национальный исследовательский медицинский университет им. Н.И. Пирогова» Минздрава России (Пироговский Университет), Москва, Российская Федерация
*nered@mail.ru
1Blokhin National Medical Research Center of Oncology, Moscow, Russian Federation
2Russian Medical Academy of Continuous Professional Education, Moscow, Russian Federation
3Pirogov Russian National Research Medical University (Pirogov University), Moscow, Russian Federation
*nered@mail.ru
1ФГБУ «Национальный медицинский исследовательский центр онкологии им. Н.Н. Блохина» Минздрава России, Москва, Российская Федерация
2ФГБОУ ДПО «Российская медицинская академия непрерывного профессионального образования» Минздрава России, Москва, Российская Федерация
3ФГАОУ ВО «Российский национальный исследовательский медицинский университет им. Н.И. Пирогова» Минздрава России (Пироговский Университет), Москва, Российская Федерация
*nered@mail.ru
________________________________________________
1Blokhin National Medical Research Center of Oncology, Moscow, Russian Federation
2Russian Medical Academy of Continuous Professional Education, Moscow, Russian Federation
3Pirogov Russian National Research Medical University (Pirogov University), Moscow, Russian Federation
*nered@mail.ru
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