Macroscopic type is implicated in the prognostic impact of initial chemotherapy on peritoneal lavage cytology-positive gastric cancer with no other noncurative factors.

Gastric cancer Initial chemotherapy Initial surgery Macroscopic type Peritoneal lavage cytology

Journal

International journal of clinical oncology
ISSN: 1437-7772
Titre abrégé: Int J Clin Oncol
Pays: Japan
ID NLM: 9616295

Informations de publication

Date de publication:
21 Mar 2024
Historique:
received: 21 10 2023
accepted: 19 02 2024
medline: 21 3 2024
pubmed: 21 3 2024
entrez: 21 3 2024
Statut: aheadofprint

Résumé

Initial chemotherapy (Initial-C) followed by surgery is a promising treatment strategy for peritoneal lavage cytology-positive gastric cancer (CY1 GC) with no other noncurative factors. The aim of this study was to investigate the survival advantage of Initial-C compared to initial surgery (Initial-S) for this disease according to the macroscopic type, which was associated with prognosis and the efficacy of chemotherapy in GC. One hundred eighty-nine patients who were diagnosed with CY1 GC with no other noncurative factors at four institutions from January 2007 to December 2018 were enrolled. The patients were divided into a macroscopic type 4 group (N = 48) and a non-type 4 group (N = 141). The influence of initial treatment on overall survival (OS) in each group was evaluated. In the type 4 group, the 5-year OS rates of Initial-C (N = 35) and Initial-S (N = 13) were 11.6% and 0%, respectively (P = 0.801). The multivariate analysis could not show the survival advantage of Initial-C. In the non-type 4 group, the 5-year OS rates of Initial-C (N = 41) and Initial-S (N = 100) were 48.4% and 29.0%, respectively (P = 0.020). The multivariate analysis revealed that Initial-C was independently associated with prolonged OS (hazard ratio, 0.591; 95% confidence interval, 0.375-0.933: P = 0.023). Initial-C improves the prognosis of non-type 4 CY1 GC with no other noncurative factors. On the other hand, further development of effective chemotherapeutic regimens and innovative treatment strategies are required for type 4 CY1 GC.

Sections du résumé

BACKGROUND BACKGROUND
Initial chemotherapy (Initial-C) followed by surgery is a promising treatment strategy for peritoneal lavage cytology-positive gastric cancer (CY1 GC) with no other noncurative factors. The aim of this study was to investigate the survival advantage of Initial-C compared to initial surgery (Initial-S) for this disease according to the macroscopic type, which was associated with prognosis and the efficacy of chemotherapy in GC.
METHODS METHODS
One hundred eighty-nine patients who were diagnosed with CY1 GC with no other noncurative factors at four institutions from January 2007 to December 2018 were enrolled. The patients were divided into a macroscopic type 4 group (N = 48) and a non-type 4 group (N = 141). The influence of initial treatment on overall survival (OS) in each group was evaluated.
RESULTS RESULTS
In the type 4 group, the 5-year OS rates of Initial-C (N = 35) and Initial-S (N = 13) were 11.6% and 0%, respectively (P = 0.801). The multivariate analysis could not show the survival advantage of Initial-C. In the non-type 4 group, the 5-year OS rates of Initial-C (N = 41) and Initial-S (N = 100) were 48.4% and 29.0%, respectively (P = 0.020). The multivariate analysis revealed that Initial-C was independently associated with prolonged OS (hazard ratio, 0.591; 95% confidence interval, 0.375-0.933: P = 0.023).
CONCLUSIONS CONCLUSIONS
Initial-C improves the prognosis of non-type 4 CY1 GC with no other noncurative factors. On the other hand, further development of effective chemotherapeutic regimens and innovative treatment strategies are required for type 4 CY1 GC.

Identifiants

pubmed: 38512543
doi: 10.1007/s10147-024-02496-1
pii: 10.1007/s10147-024-02496-1
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : KAKENHI
ID : JP22K16483

Informations de copyright

© 2024. The Author(s) under exclusive licence to Japan Society of Clinical Oncology.

Références

Brierley JD, Gospodarowicz MK, Wittekind C (2017) International union against cancer (UICC) TNM classification of malignant tumours, 8th edn. John Wiley & Sons, Hoboken
Amin MB, Edge SB, Greene FL et al (2017) AJCC cancer staging manual, 8th edn. Springer, New York
Japanese Gastric Cancer Association (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14:101–12
doi: 10.1007/s10120-011-0041-5
Jamel S, Markar SR, Malietzis G et al (2018) Prognostic significance of peritoneal lavage cytology in staging gastric cancer: systematic review and meta-analysis. Gastric Cancer 21:10–18
doi: 10.1007/s10120-017-0749-y pubmed: 28779261
Ajani JA, D’Amico TA, Bentrem DJ et al (2022) Gastric cancer, version 2.2022, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 20:167–92
doi: 10.6004/jnccn.2022.0008 pubmed: 35130500
Lordick F, Carneiro F, Cascinu S et al (2022) ESMO clinical practice guideline for diagnosis, treatment and follow-up. Ann Oncol 33:1005–1020
doi: 10.1016/j.annonc.2022.07.004 pubmed: 35914639
Kodera Y, Ito S, Mochizuki Y et al (2012) Long term follow up of patients who were positive for peritoneal lavage cytology:fnal report from the CCOG0301 study. Gastric Cancer 15:335–337
doi: 10.1007/s10120-012-0156-3 pubmed: 22527184
Kano Y, Ichikawa H, Hanyu T et al (2022) Conversion surgery for stage IV gastric cancer: a multicenter retrospective study. BMC Surg 14(22):428
doi: 10.1186/s12893-022-01874-8
Solaini L, Ministrini S, Bencivenga M et al (2019) Conversion gastrectomy for stage IV unresectable gastric cancer: a IRCG retrospective cohort study. Gastric Cancer 22:1285–1293
doi: 10.1007/s10120-019-00968-2 pubmed: 31065878
Yoshida K, Yasufuku I, Terashima M et al (2021) CONVO-GC-1 study group, federation of Asian clinical oncology (FACO). International retrospective cohort study of conversion therapy for stage IV gastric cancer 1 (CONVO-GC-1). Ann Gastroenterol Surg 6:227–40
doi: 10.1002/ags3.12515 pubmed: 35261948 pmcid: 8889854
Yamaguchi K, Yoshida K, Tanahashi T et al (2018) The long-term survival of stage IV gastric cancer patients with conversion therapy. Gastric Cancer 21:315–323
doi: 10.1007/s10120-017-0738-1 pubmed: 28616743
Yasufuku I, Nunobe S, Ida S et al (2020) Conversion therapy for peritoneal lavage cytology-positive type 4 and large type 3 gastric cancer patients selected as candidates for R0 resection by diagnostic staging laparoscopy. Gastric Cancer 23:319–327
doi: 10.1007/s10120-019-00994-0 pubmed: 31350702
Aizawa M, Nashimoto A, Yabusaki H et al (2015) The clinical significance of potentially curative resection for gastric cancer following the clearance of free cancer cells in the peritoneal cavity by induction chemotherapy. Surg Today 45:611–617
doi: 10.1007/s00595-014-0979-0 pubmed: 25027056
Nakamura M, Ojima T, Nakamori M et al (2019) Conversion surgery for gastric cancer with peritoneal metastasis based on the diagnosis of second-look staging laparoscopy. J Gastrointest Surg 23:1758–1766
doi: 10.1007/s11605-018-3983-7 pubmed: 30264385
Yamaguchi T, Takashima A, Nagashima K et al (2021) Impact of preoperative chemotherapy as initial treatment for advanced gastric cancer with peritoneal metastasis limited to positive peritoneal lavage cytology (CY1) or localized peritoneal metastasis (P1a): a multi-institutional retrospective study. Gastric Cancer 24:701–709
doi: 10.1007/s10120-020-01137-6 pubmed: 33179192
Bollschweiler E, Boettcher K, Hoelscher AH et al (1993) Is the prognosis for Japanese and German patients with gastric cancer really different? Cancer 71:2918–2925
doi: 10.1002/1097-0142(19930515)71:10<2918::AID-CNCR2820711006>3.0.CO;2-V pubmed: 8490819
Blackham AU, Swords DS, Levine EA et al (2016) Is linitis plastica a contraindication for surgical resection: a multi-institution study of the U.S. Gastric cancer collaborative. Ann Surg Oncol 23:1203–11
doi: 10.1245/s10434-015-4947-8 pubmed: 26530447
An JY, Kang TH, Choi MG et al (2008) Borrmann type IV: an independent prognostic factor for survival in gastric cancer. J Gastrointest Surg 12:1364–1369
doi: 10.1007/s11605-008-0516-9 pubmed: 18516653
Song XH, Zhang WH, Kai Liu et al (2020) Prognostic impact of Borrmann classification on advanced gastric cancer: a retrospective cohort from a single institution in western China. World J Surg Oncol 18:204
doi: 10.1186/s12957-020-01987-5 pubmed: 32792016 pmcid: 7427284
Eba J, Nakamura K (2022) Overview of the ethical guidelines for medical and biological research involving human subjects in Japan. Jpn J Clin Oncol 52:539–544
doi: 10.1093/jjco/hyac034 pubmed: 35349681 pmcid: 9157286
Japanese Gastric Cancer Association (2021) Japanese gastric cancer treatment guidelines 2018. Gastric Cancer 24:1–21
doi: 10.1007/s10120-020-01042-y
Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213
doi: 10.1097/01.sla.0000133083.54934.ae pubmed: 15273542 pmcid: 1360123
Smyth EC, Nilsson M, Grabsch HI et al (2020) Gastric cancer. Lancet 396:635–648
doi: 10.1016/S0140-6736(20)31288-5 pubmed: 32861308
Piessen G, Messager M, Leteurtre E et al (2009) Signet ring cell histology is an independent predictor of poor prognosis in gastric adenocarcinoma regardless of tumoral clinical presentation. Ann Surg 250:878–887
doi: 10.1097/SLA.0b013e3181b21c7b pubmed: 19855261
Heger U, Blank S, Wiecha C et al (2014) Is preoperative chemotherapy followed by surgery the appropriate treatment for signet ring cell containing adenocarcinomas of the esophagogastric junction and stomach? Ann Surg Oncol 21:1739–1748
doi: 10.1245/s10434-013-3462-z pubmed: 24419755
Koseki Y, Hatakeyama K, Terashima M et al (2023) Molecular profile of poorly cohesive gastric carcinoma with special reference to survival. Gastric Cancer 26:553–64
doi: 10.1007/s10120-023-01390-5 pubmed: 37036539
Fukagawa T, Katai H, Saka M et al (2010) Significance of lavage cytology in advanced gastric cancer patients. World J Surg 34:563–568
doi: 10.1007/s00268-009-0355-1 pubmed: 20054543
Endo S, Ikenaga M, Ohta K et al (2019) Prognostic factors for cytology-positive gastric cancer. Surg Today 49:56–64
doi: 10.1007/s00595-018-1704-1 pubmed: 30167924
Kano K, Aoyama T, Maezawa Y et al (2017) The survival and prognosticators of peritoneal cytology-positive gastric cancer patients who received upfront gastrectomy and subsequent S-1 chemotherapy. Int J Clin Oncol 22:887–896
doi: 10.1007/s10147-017-1128-8 pubmed: 28456896
Yago A, Haruta S, Ueno M et al (2022) Clinical significance of initial treatment for peritoneal lavage cytology-positive gastric cancer: outcomes according to treatment strategy. World J Surg Oncol 20:35
doi: 10.1186/s12957-022-02512-6 pubmed: 35168610 pmcid: 8848799
Kuramoto M, Shimada S, Ikeshima S et al (2009) Extensive intraoperative peritoneal lavage as a standard prophylactic strategy for peritoneal recurrence in patients with gastric carcinoma. Ann Surg 250:242–246
doi: 10.1097/SLA.0b013e3181b0c80e pubmed: 19638909
Yamaguchi T, Takashima A, Nagashima K et al (2020) Efficacy of postoperative chemotherapy after resection that leaves no macroscopically visible disease of gastric cancer with positive peritoneal lavage cytology (CY1) or localized peritoneum metastasis (P1a): a multicenter retrospective study. Ann Surg Oncol 27:284–292
doi: 10.1245/s10434-019-07697-x pubmed: 31535301
Iwasaki Y, Terashima M, Mizusawa J et al (2021) Gastrectomy with or without neoadjuvant S-1 plus cisplatin for type 4 or large type 3 gastric cancer (JCOG0501): an open-label, phase 3, randomized controlled trial. Gastric Cancer 24:492–502
doi: 10.1007/s10120-020-01136-7 pubmed: 33200303
Chen GM, Yuan SQ, Nie RC et al (2020) Surgical outcome and long-term survival of conversion surgery for advanced gastric cancer. Ann Surg Oncol 27:4250–4260
doi: 10.1245/s10434-020-08559-7 pubmed: 32506192
Lee JH, Son SY, Lee CM et al (2014) Factors predicting peritoneal recurrence in advanced gastric cancer: implication for adjuvant intraperitoneal chemotherapy. Gastric Cancer 17:529–536
doi: 10.1007/s10120-013-0306-2 pubmed: 24101155
Ishigami H, Fujiwara Y, Fukushima R et al (2018) Phase III trial comparing intraperitoneal and intravenous paclitaxel plus S-1 versus cisplatin plus S-1 in patients with gastric cancer with peritoneal metastasis: PHOENIX-GC trial. J Clin Oncol 36:1922–1929
doi: 10.1200/JCO.2018.77.8613 pubmed: 29746229
Ishigami H, Tsuji Y, Shinohara H et al (2021) Intraperitoneal chemotherapy as adjuvant or perioperative chemotherapy for patients with type 4 scirrhous gastric cancer: PHOENIX-GC2 trial. J Clin Med 10:5666
doi: 10.3390/jcm10235666 pubmed: 34884367 pmcid: 8658657

Auteurs

Yosuke Kano (Y)

Division of Digestive and General Surgery, Niigata University Graduate School of Medical and Dental Sciences, 1-757 Asahimachi-dori, Chuo-ku, Niigata, 951-8510, Japan.

Hiroshi Ichikawa (H)

Division of Digestive and General Surgery, Niigata University Graduate School of Medical and Dental Sciences, 1-757 Asahimachi-dori, Chuo-ku, Niigata, 951-8510, Japan. hichikawa-nii@med.niigata-u.ac.jp.

Masaki Aizawa (M)

Department of Gastroenterological Surgery, Niigata Cancer Center Hospital, 2‑15‑3 Kawagishi‑cho, Chuo‑ku, Niigata, 951‑8566, Japan.

Yusuke Muneoka (Y)

Division of Digestive and General Surgery, Niigata University Graduate School of Medical and Dental Sciences, 1-757 Asahimachi-dori, Chuo-ku, Niigata, 951-8510, Japan.

Kenji Usui (K)

Division of Digestive and General Surgery, Niigata University Graduate School of Medical and Dental Sciences, 1-757 Asahimachi-dori, Chuo-ku, Niigata, 951-8510, Japan.

Takaaki Hanyu (T)

Division of Digestive and General Surgery, Niigata University Graduate School of Medical and Dental Sciences, 1-757 Asahimachi-dori, Chuo-ku, Niigata, 951-8510, Japan.

Takashi Ishikawa (T)

Division of Digestive and General Surgery, Niigata University Graduate School of Medical and Dental Sciences, 1-757 Asahimachi-dori, Chuo-ku, Niigata, 951-8510, Japan.

Hiroshi Yabusaki (H)

Department of Gastroenterological Surgery, Niigata Cancer Center Hospital, 2‑15‑3 Kawagishi‑cho, Chuo‑ku, Niigata, 951‑8566, Japan.

Kazuaki Kobayashi (K)

Department of Digestive Surgery, Niigata City General Hospital, 463‑7 Shumoku, Chuo‑ku, Niigata, 950‑1197, Japan.

Shirou Kuwabara (S)

Department of Digestive Surgery, Niigata City General Hospital, 463‑7 Shumoku, Chuo‑ku, Niigata, 950‑1197, Japan.

Shigeto Makino (S)

Department of Surgery, Nagaoka Chuo General Hospital, 2041 Kawasaki‑cho, Nagaoka, Niigata, 940‑0861, Japan.

Yasuyuki Kawachi (Y)

Department of Surgery, Nagaoka Chuo General Hospital, 2041 Kawasaki‑cho, Nagaoka, Niigata, 940‑0861, Japan.

Kohei Miura (K)

Division of Digestive and General Surgery, Niigata University Graduate School of Medical and Dental Sciences, 1-757 Asahimachi-dori, Chuo-ku, Niigata, 951-8510, Japan.

Yosuke Tajima (Y)

Division of Digestive and General Surgery, Niigata University Graduate School of Medical and Dental Sciences, 1-757 Asahimachi-dori, Chuo-ku, Niigata, 951-8510, Japan.

Yoshifumi Shimada (Y)

Division of Digestive and General Surgery, Niigata University Graduate School of Medical and Dental Sciences, 1-757 Asahimachi-dori, Chuo-ku, Niigata, 951-8510, Japan.

Jun Sakata (J)

Division of Digestive and General Surgery, Niigata University Graduate School of Medical and Dental Sciences, 1-757 Asahimachi-dori, Chuo-ku, Niigata, 951-8510, Japan.

Toshifumi Wakai (T)

Division of Digestive and General Surgery, Niigata University Graduate School of Medical and Dental Sciences, 1-757 Asahimachi-dori, Chuo-ku, Niigata, 951-8510, Japan.

Classifications MeSH