Prognostic impact of positive peritoneal cytology (POPEC) in gastric cancer: Multi-centre European retrospective cohort study

Richard Owen; Swathikan Chidambaram; Khalid Shamiyah; Jessie A. Elliott; Jakob Hedberg; Sivesh Kamarajah; Frederik Klevebro; Marcel Andre Schneider; Lana Fourie; Christian Gutschow; Magnus Nilsson; Ewen Griffiths; Ricardo Rosati; Javed Sultan; Manuel Pera; Peter Grimminger; Guillaume Piessen; Clarisse Eveno; Jelle Ruurda; Richard van Hillegersberg; John V. Reynolds; Mark van Berge Henegouwen; Suzanne Gisbertz; Jimmy B.Y. So; Nick Maynard; Sheraz Markar; on behalf of the POPEC study group; Vanessa Peronace; Ellen A. Boyle; Aileen Pang; Candy Yap; Daryl Chia; Guowei Kim; Asim Shabbir; Amina Youcef; Khalid Bhatti; Kammy Keywani; Ricardo Calef; Eren Uzun; Mariagiulia Dal Cero; James Halle-Smith; Tim Bagnell; Lianne Triemstra; Matthias Josef; Kerstin Neuschütz; Andrea Cossu; John Saunders

doi:10.1016/j.soi.2025.100145

Prognostic impact of positive peritoneal cytology (POPEC) in gastric cancer: Multi-centre European retrospective cohort study

Richard Owen
, Swathikan Chidambaram
, Khalid Shamiyah
, Jessie A. Elliott
, Jakob Hedberg
, Sivesh Kamarajah
, Frederik Klevebro
, Marcel Andre Schneider
, Lana Fourie
, Christian Gutschow
, Magnus Nilsson
, Ewen Griffiths
, Ricardo Rosati
, Javed Sultan
, Manuel Pera
, Peter Grimminger
, Guillaume Piessen
, Clarisse Eveno
, Jelle Ruurda
, Richard van Hillegersberg

John V. Reynolds, Mark van Berge Henegouwen, Suzanne Gisbertz, Jimmy B.Y. So, Nick Maynard, Sheraz Markar^*, on behalf of the POPEC study group, Vanessa Peronace, Ellen A. Boyle, Aileen Pang, Candy Yap, Daryl Chia, Guowei Kim, Asim Shabbir, Amina Youcef, Khalid Bhatti, Kammy Keywani, Ricardo Calef, Eren Uzun, Mariagiulia Dal Cero, James Halle-Smith, Tim Bagnell, Lianne Triemstra, Matthias Josef, Kerstin Neuschütz, Andrea Cossu, John Saunders

^*Corresponding author for this work

Applied Health Sciences

Research output: Contribution to journal › Article › peer-review

Abstract

Objective: Positive peritoneal cytology is traditionally viewed as representative of metastatic disease and a poor prognostic factor. The objective of this multi-center study was to define the prognostic role of peritoneal cytology in curative gastrectomy, evaluate international variation in cytology sampling, and assess the impact on positive peritoneal cytology yields.

Methods: This was a multi-center international retrospective cohort study of 16 tertiary gastric cancer centers. Adult patients who underwent peritoneal lavage cytology at staging laparoscopy and subsequent gastrectomy between 2009 and 2023 were included. The primary outcome measure was overall survival at five years. Multivariable Cox regression provided hazard ratios (HRs) with 95 % CIs, adjusted for relevant confounding factors.

Results: 837 patients with no radiological or macroscopic M1 disease were included, with a mean age of 66 (IQR 58–73) and 71 % were male. Non-distal gastric cancer was most common (47 %), with 59 % and 43 % of tumors staged pT3/4 and pN2/3, respectively. 66 patients (7.9 %) had positive cytology. Positive cytology was not associated with overall survival in multivariable analysis, controlled for stage and neoadjuvant treatment (HR=1.0; 95 %CI 0.51–2.0). Higher T and N stages were associated with positive cytology (p < 0.001). The proportion of patients with positive cytology was variable, depending on how many quadrants were sampled.

Conclusion: Positive peritoneal cytology with otherwise M0 disease was not associated with decreased survival after curative intent gastrectomy in this study, meaning prospective study is needed. The technique of performing peritoneal washings influenced cytology yield and thus must be standardized in a much-needed prospective evaluation of peritoneal cytology.

Synopsis: The POPEC multicenter international retrospective cohort study included 837 patients receiving curative gastrectomy. This study showed the technique of performing peritoneal washings influenced cytology yield, however positive peritoneal cytology was not associated with decreased survival. Therefore, positive peritoneal cytology should not be considered an absolute contradiction to curatively intended gastrectomy.

Original language	English
Article number	100145
Number of pages	6
Journal	Surgical Oncology Insight
Volume	2
Issue number	3
Early online date	8 May 2025
DOIs	https://doi.org/10.1016/j.soi.2025.100145
Publication status	Published - Sept 2025

Bibliographical note

Publisher Copyright:
© 2025

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Keywords

Gastric cancer
HIPEC
Hyperthermic Intraperitoneal Chemotherapy
Peritoneal carcinomatosis
Peritoneal cytology
PIPAC
Pressurised IntraPeritoneal Aerosolised Chemotherapy
Surgical oncology

ASJC Scopus subject areas

Oncology

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Cite this

Owen, R., Chidambaram, S., Shamiyah, K., Elliott, J. A., Hedberg, J., Kamarajah, S., Klevebro, F., Schneider, M. A., Fourie, L., Gutschow, C., Nilsson, M., Griffiths, E., Rosati, R., Sultan, J., Pera, M., Grimminger, P., Piessen, G., Eveno, C., Ruurda, J., ... Saunders, J. (2025). Prognostic impact of positive peritoneal cytology (POPEC) in gastric cancer: Multi-centre European retrospective cohort study. Surgical Oncology Insight, 2(3), Article 100145. https://doi.org/10.1016/j.soi.2025.100145

@article{63ae0fb6d9414af497fbaebb401911be,

title = "Prognostic impact of positive peritoneal cytology (POPEC) in gastric cancer: Multi-centre European retrospective cohort study",

abstract = "Objective: Positive peritoneal cytology is traditionally viewed as representative of metastatic disease and a poor prognostic factor. The objective of this multi-center study was to define the prognostic role of peritoneal cytology in curative gastrectomy, evaluate international variation in cytology sampling, and assess the impact on positive peritoneal cytology yields. Methods: This was a multi-center international retrospective cohort study of 16 tertiary gastric cancer centers. Adult patients who underwent peritoneal lavage cytology at staging laparoscopy and subsequent gastrectomy between 2009 and 2023 were included. The primary outcome measure was overall survival at five years. Multivariable Cox regression provided hazard ratios (HRs) with 95 \% CIs, adjusted for relevant confounding factors. Results: 837 patients with no radiological or macroscopic M1 disease were included, with a mean age of 66 (IQR 58–73) and 71 \% were male. Non-distal gastric cancer was most common (47 \%), with 59 \% and 43 \% of tumors staged pT3/4 and pN2/3, respectively. 66 patients (7.9 \%) had positive cytology. Positive cytology was not associated with overall survival in multivariable analysis, controlled for stage and neoadjuvant treatment (HR=1.0; 95 \%CI 0.51–2.0). Higher T and N stages were associated with positive cytology (p < 0.001). The proportion of patients with positive cytology was variable, depending on how many quadrants were sampled. Conclusion: Positive peritoneal cytology with otherwise M0 disease was not associated with decreased survival after curative intent gastrectomy in this study, meaning prospective study is needed. The technique of performing peritoneal washings influenced cytology yield and thus must be standardized in a much-needed prospective evaluation of peritoneal cytology. Synopsis: The POPEC multicenter international retrospective cohort study included 837 patients receiving curative gastrectomy. This study showed the technique of performing peritoneal washings influenced cytology yield, however positive peritoneal cytology was not associated with decreased survival. Therefore, positive peritoneal cytology should not be considered an absolute contradiction to curatively intended gastrectomy.",

keywords = "Gastric cancer, HIPEC, Hyperthermic Intraperitoneal Chemotherapy, Peritoneal carcinomatosis, Peritoneal cytology, PIPAC, Pressurised IntraPeritoneal Aerosolised Chemotherapy, Surgical oncology",

author = "Richard Owen and Swathikan Chidambaram and Khalid Shamiyah and Elliott, \{Jessie A.\} and Jakob Hedberg and Sivesh Kamarajah and Frederik Klevebro and Schneider, \{Marcel Andre\} and Lana Fourie and Christian Gutschow and Magnus Nilsson and Ewen Griffiths and Ricardo Rosati and Javed Sultan and Manuel Pera and Peter Grimminger and Guillaume Piessen and Clarisse Eveno and Jelle Ruurda and \{van Hillegersberg\}, Richard and Reynolds, \{John V.\} and \{van Berge Henegouwen\}, Mark and Suzanne Gisbertz and So, \{Jimmy B.Y.\} and Nick Maynard and Sheraz Markar and \{on behalf of the POPEC study group\} and Vanessa Peronace and Boyle, \{Ellen A.\} and Aileen Pang and Candy Yap and Daryl Chia and Guowei Kim and Asim Shabbir and Amina Youcef and Khalid Bhatti and Kammy Keywani and Ricardo Calef and Eren Uzun and Cero, \{Mariagiulia Dal\} and James Halle-Smith and Tim Bagnell and Lianne Triemstra and Matthias Josef and Kerstin Neusch{\"u}tz and Andrea Cossu and John Saunders",

note = "Publisher Copyright: {\textcopyright} 2025",

year = "2025",

month = sep,

doi = "10.1016/j.soi.2025.100145",

language = "English",

volume = "2",

journal = "Surgical Oncology Insight",

issn = "2950-2470",

publisher = "Elsevier",

number = "3",

}

Owen, R, Chidambaram, S, Shamiyah, K, Elliott, JA, Hedberg, J, Kamarajah, S, Klevebro, F, Schneider, MA, Fourie, L, Gutschow, C, Nilsson, M, Griffiths, E, Rosati, R, Sultan, J, Pera, M, Grimminger, P, Piessen, G, Eveno, C, Ruurda, J, van Hillegersberg, R, Reynolds, JV, van Berge Henegouwen, M, Gisbertz, S, So, JBY, Maynard, N, Markar, S, on behalf of the POPEC study group, Peronace, V, Boyle, EA, Pang, A, Yap, C, Chia, D, Kim, G, Shabbir, A, Youcef, A, Bhatti, K, Keywani, K, Calef, R, Uzun, E, Cero, MD, Halle-Smith, J, Bagnell, T, Triemstra, L, Josef, M, Neuschütz, K, Cossu, A & Saunders, J 2025, 'Prognostic impact of positive peritoneal cytology (POPEC) in gastric cancer: Multi-centre European retrospective cohort study', Surgical Oncology Insight, vol. 2, no. 3, 100145. https://doi.org/10.1016/j.soi.2025.100145

TY - JOUR

T1 - Prognostic impact of positive peritoneal cytology (POPEC) in gastric cancer

T2 - Multi-centre European retrospective cohort study

AU - Owen, Richard

AU - Chidambaram, Swathikan

AU - Shamiyah, Khalid

AU - Elliott, Jessie A.

AU - Hedberg, Jakob

AU - Kamarajah, Sivesh

AU - Klevebro, Frederik

AU - Schneider, Marcel Andre

AU - Fourie, Lana

AU - Gutschow, Christian

AU - Nilsson, Magnus

AU - Griffiths, Ewen

AU - Rosati, Ricardo

AU - Sultan, Javed

AU - Pera, Manuel

AU - Grimminger, Peter

AU - Piessen, Guillaume

AU - Eveno, Clarisse

AU - Ruurda, Jelle

AU - van Hillegersberg, Richard

AU - Reynolds, John V.

AU - van Berge Henegouwen, Mark

AU - Gisbertz, Suzanne

AU - So, Jimmy B.Y.

AU - Maynard, Nick

AU - Markar, Sheraz

AU - on behalf of the POPEC study group

AU - Peronace, Vanessa

AU - Boyle, Ellen A.

AU - Pang, Aileen

AU - Yap, Candy

AU - Chia, Daryl

AU - Kim, Guowei

AU - Shabbir, Asim

AU - Youcef, Amina

AU - Bhatti, Khalid

AU - Keywani, Kammy

AU - Calef, Ricardo

AU - Uzun, Eren

AU - Cero, Mariagiulia Dal

AU - Halle-Smith, James

AU - Bagnell, Tim

AU - Triemstra, Lianne

AU - Josef, Matthias

AU - Neuschütz, Kerstin

AU - Cossu, Andrea

AU - Saunders, John

PY - 2025/9

Y1 - 2025/9

N2 - Objective: Positive peritoneal cytology is traditionally viewed as representative of metastatic disease and a poor prognostic factor. The objective of this multi-center study was to define the prognostic role of peritoneal cytology in curative gastrectomy, evaluate international variation in cytology sampling, and assess the impact on positive peritoneal cytology yields. Methods: This was a multi-center international retrospective cohort study of 16 tertiary gastric cancer centers. Adult patients who underwent peritoneal lavage cytology at staging laparoscopy and subsequent gastrectomy between 2009 and 2023 were included. The primary outcome measure was overall survival at five years. Multivariable Cox regression provided hazard ratios (HRs) with 95 % CIs, adjusted for relevant confounding factors. Results: 837 patients with no radiological or macroscopic M1 disease were included, with a mean age of 66 (IQR 58–73) and 71 % were male. Non-distal gastric cancer was most common (47 %), with 59 % and 43 % of tumors staged pT3/4 and pN2/3, respectively. 66 patients (7.9 %) had positive cytology. Positive cytology was not associated with overall survival in multivariable analysis, controlled for stage and neoadjuvant treatment (HR=1.0; 95 %CI 0.51–2.0). Higher T and N stages were associated with positive cytology (p < 0.001). The proportion of patients with positive cytology was variable, depending on how many quadrants were sampled. Conclusion: Positive peritoneal cytology with otherwise M0 disease was not associated with decreased survival after curative intent gastrectomy in this study, meaning prospective study is needed. The technique of performing peritoneal washings influenced cytology yield and thus must be standardized in a much-needed prospective evaluation of peritoneal cytology. Synopsis: The POPEC multicenter international retrospective cohort study included 837 patients receiving curative gastrectomy. This study showed the technique of performing peritoneal washings influenced cytology yield, however positive peritoneal cytology was not associated with decreased survival. Therefore, positive peritoneal cytology should not be considered an absolute contradiction to curatively intended gastrectomy.

AB - Objective: Positive peritoneal cytology is traditionally viewed as representative of metastatic disease and a poor prognostic factor. The objective of this multi-center study was to define the prognostic role of peritoneal cytology in curative gastrectomy, evaluate international variation in cytology sampling, and assess the impact on positive peritoneal cytology yields. Methods: This was a multi-center international retrospective cohort study of 16 tertiary gastric cancer centers. Adult patients who underwent peritoneal lavage cytology at staging laparoscopy and subsequent gastrectomy between 2009 and 2023 were included. The primary outcome measure was overall survival at five years. Multivariable Cox regression provided hazard ratios (HRs) with 95 % CIs, adjusted for relevant confounding factors. Results: 837 patients with no radiological or macroscopic M1 disease were included, with a mean age of 66 (IQR 58–73) and 71 % were male. Non-distal gastric cancer was most common (47 %), with 59 % and 43 % of tumors staged pT3/4 and pN2/3, respectively. 66 patients (7.9 %) had positive cytology. Positive cytology was not associated with overall survival in multivariable analysis, controlled for stage and neoadjuvant treatment (HR=1.0; 95 %CI 0.51–2.0). Higher T and N stages were associated with positive cytology (p < 0.001). The proportion of patients with positive cytology was variable, depending on how many quadrants were sampled. Conclusion: Positive peritoneal cytology with otherwise M0 disease was not associated with decreased survival after curative intent gastrectomy in this study, meaning prospective study is needed. The technique of performing peritoneal washings influenced cytology yield and thus must be standardized in a much-needed prospective evaluation of peritoneal cytology. Synopsis: The POPEC multicenter international retrospective cohort study included 837 patients receiving curative gastrectomy. This study showed the technique of performing peritoneal washings influenced cytology yield, however positive peritoneal cytology was not associated with decreased survival. Therefore, positive peritoneal cytology should not be considered an absolute contradiction to curatively intended gastrectomy.

KW - Gastric cancer

KW - HIPEC

KW - Hyperthermic Intraperitoneal Chemotherapy

KW - Peritoneal carcinomatosis

KW - Peritoneal cytology

KW - PIPAC

KW - Pressurised IntraPeritoneal Aerosolised Chemotherapy

KW - Surgical oncology

UR - https://www.scopus.com/pages/publications/105010958232

U2 - 10.1016/j.soi.2025.100145

DO - 10.1016/j.soi.2025.100145

M3 - Article

AN - SCOPUS:105010958232

SN - 2950-2470

VL - 2

JO - Surgical Oncology Insight

JF - Surgical Oncology Insight

IS - 3

M1 - 100145

ER -

Prognostic impact of positive peritoneal cytology (POPEC) in gastric cancer: Multi-centre European retrospective cohort study

Abstract

Bibliographical note

UN SDGs

Keywords

ASJC Scopus subject areas

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