Abstract
Background
The prognostic value of peritoneal lavage cytology (CY) for pancreatic ductal adenocarcinoma (PDAC) remains controversial. We assessed the prognostic impact of CY status stratified by resectability in PDAC patients treated with surgical resection.
Methods
Clinical data from 440 patients with PDAC who underwent surgical resection were retrospectively analyzed to examine the association of CY status with clinicopathological factors and survival.
Results
Positive CY status (CY+) was found in 30 patients (7%). These patients had significantly worse overall survival in both the resectable (R) (P = 0.002) and borderline resectable (BR) (P < 0.001) groups. The median survival time of CY+ patients in the R and BR groups was 25.6 and 6.7 months, respectively. Multivariate analysis revealed that CY+ was an independent prognostic factor in the BR group (P < 0.001) but not in the R group (P = 0.08). In the R group, CY+ patients who received adjuvant chemotherapy had significantly longer overall survival than those without adjuvant chemotherapy (34.3 vs. 9.8 months, respectively; P < 0.001).
Conclusions
The prognosis of CY+ patients in the BR group was extremely poor. In the R group, surgical resection combined with adjuvant chemotherapy may improve the prognosis of CY+ patients.
Similar content being viewed by others
References
Rahib L, Smith BD, Aizenberg R, Rosenzweig AB, Fleshman JM, Matrisian LM. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res. 2014;74:2913-2921.
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin. 2020;70:7-30.
Amin M, Edge S, Greene F, Byrd D, Brookland R, Washington M, Gershenwald J, Compton C, Hess K, Sullivan D, Jessup J, Brierley J, Gaspar L, Schilsky R, Balch C, Winchester D, Asare E, Madera M, Gress D, Meyer L. The AJCC TNM Cancer Staging Manual. 8th ed. New York: Springer, 2017.
National Comprehensive Cancer Network. NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines). Pancreatic Adenocarcinoma. Version 1.2020 https://www.nccn.org/professionals/physician_gls/default.aspx [Accessed 18 September 2020]
Brierley JD, Gospodarowicz MK, Wittekind C. TNM Classification of Malignant Tumours. 8th ed. Oxford: Wiley-Blackwell, 2017.
Japan Pancreas Society. General Rules for the Study of Pancreatic Cancer. 7th ed. Tokyo: Kanehara & Co, 2016.
Satoi S, Murakami Y, Motoi F, Uemura K, Kawai M, Kurata M, Sho M, Matsumoto I, Yanagimoto H, Yamamoto T, Mizuma M, Unno M, Hashimoto Y, Hirono S, Yamaue H, Honda G, Nagai M, Nakajima Y, Shinzeki M, Fukumoto T, Kwon AH. Reappraisal of peritoneal washing cytology in 984 patients with pancreatic ductal adenocarcinoma who underwent margin-negative resection. J Gastrointest Surg. 2015;19:6-14.
Tsuchida H, Fujii T, Mizuma M, Satoi S, Igarashi H, Eguchi H, Kuroki T, Shimizu Y, Tani M, Tanno S, Tsuji Y, Hirooka Y, Masamune A, Mizumoto K, Itoi T, Egawa S, Kodama Y, Hamada S, Unno M, Yamaue H, Okazaki K. Prognostic importance of peritoneal washing cytology in patients with otherwise resectable pancreatic ductal adenocarcinoma who underwent pancreatectomy: A nationwide, cancer registry-based study from the Japan Pancreas Society. Surgery. 2019;166:997-1003.
Ferrone CR, Haas B, Tang L, Coit DG, Fong Y, Brennan MF, Allen PJ. The influence of positive peritoneal cytology on survival in patients with pancreatic adenocarcinoma. J Gastrointest Surg. 2006;10:1347-1353.
Yamada S, Fujii T, Kanda M, Sugimoto H, Nomoto S, Takeda S, Nakao A, Kodera Y. Value of peritoneal cytology in potentially resectable pancreatic cancer. Br J Surg. 2013;100:1791-1796.
Hirabayashi K, Imoto A, Yamada M, Hadano A, Kato N, Miyajima Y, Ito H, Kawaguchi Y, Nakagohri T, Mine T, Nakamura N. Positive Intraoperative Peritoneal Lavage Cytology is a Negative Prognostic Factor in Pancreatic Ductal Adenocarcinoma: A Retrospective Single-Center Study. Front Oncol. 2015;5:182.
Meszoely IM, Lee JS, Watson JC, Meyers M, Wang H, Hoffman JP. Peritoneal cytology in patients with potentially resectable adenocarcinoma of the pancreas. Am Surg. 2004;70:208-213.
Konishi M, Kinoshita T, Nakagohri T, Inoue K, Oda T, Takahashi S. Prognostic value of cytologic examination of peritoneal washings in pancreatic cancer. Arch Surg. 2002;137:475-480.
Yachida S, Fukushima N, Sakamoto M, Matsuno Y, Kosuge T, Hirohashi S. Implications of peritoneal washing cytology in patients with potentially resectable pancreatic cancer. Br J Surg. 2002;89:573-578.
Yoshioka R, Saiura A, Koga R, Arita J, Takemura N, Ono Y, Yamamoto J, Yamaguchi T. The implications of positive peritoneal lavage cytology in potentially resectable pancreatic cancer. World J Surg. 2012;36:2187-2191.
Kondo N, Murakami Y, Uemura K, Nakagawa N, Okada K, Takahashi S, Sueda T. Prognostic impact of postoperative complication after pancreatoduodenectomy for pancreatic adenocarcinoma stratified by the resectability status. J Surg Oncol. 2018;118:1105-1114.
Murakami Y, Uemura K, Sudo T, Hayashidani Y, Hashimoto Y, Nakagawa N, Ohge H, Sueda T. Adjuvant gemcitabine plus S-1 chemotherapy after surgical resection for pancreatic adenocarcinoma. Am J Surg. 2008;195:757-762.
Cao F, Li J, Li A, Li F. Prognostic significance of positive peritoneal cytology in resectable pancreatic cancer: a systemic review and meta-analysis. Oncotarget. 2017;8:15004-15013.
Yin Z, Ma T, Chen S. Intraoperative Peritoneal Washing Cytology on Survival in Pancreatic Ductal Adenocarcinoma With Resectable, Locally Advanced, and Metastatic Disease. Pancreas. 2019;48:519-525.
Steen W, Blom R, Busch O, Gerhards M, Besselink M, Dijk F, Festen S. Prognostic value of occult tumor cells obtained by peritoneal lavage in patients with resectable pancreatic cancer and no ascites: A systematic review. J Surg Oncol. 2016;114:743-751.
Burris HA 3rd, Moore MJ, Andersen J, Green MR, Rothenberg ML, Modiano MR, Cripps MC, Portenoy RK, Storniolo AM, Tarassoff P, Nelson R, Dorr FA, Stephens CD, Von Hoff DD. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J Clin Oncol. 1997;15:2403-2413.
Moore MJ, Goldstein D, Hamm J, Figer A, Hecht JR, Gallinger S, Au HJ, Murawa P, Walde D, Wolff RA, Campos D, Lim R, Ding K, Clark G, Voskoglou-Nomikos T, Ptasynski M, Parulekar W. Erlotinib plus gemcitabine compared with gemcitabine alone in patients with advanced pancreatic cancer: a phase III trial of the National Cancer Institute of Canada Clinical Trials Group. J Clin Oncol. 2007;25:1960-1966.
Ueno H, Ioka T, Ikeda M, Ohkawa S, Yanagimoto H, Boku N, Fukutomi A, Sugimori K, Baba H, Yamao K, Shimamura T, Sho M, Kitano M, Cheng AL, Mizumoto K, Chen JS, Furuse J, Funakoshi A, Hatori T, Yamaguchi T, Egawa S, Sato A, Ohashi Y, Okusaka T, Tanaka M. Randomized phase III study of gemcitabine plus S-1, S-1 alone, or gemcitabine alone in patients with locally advanced and metastatic pancreatic cancer in Japan and Taiwan: GEST study. J Clin Oncol. 2013;31:1640-1648.
Conroy T, Desseigne F, Ychou M, Bouché O, Guimbaud R, Bécouarn Y, Adenis A, Raoul JL, Gourgou-Bourgade S, de la Fouchardière C, Bennouna J, Bachet JB, Khemissa-Akouz F, Péré-Vergé D, Delbaldo C, Assenat E, Chauffert B, Michel P, Montoto-Grillot C, Ducreux M. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med. 2011;364:1817-1825.
Goldstein D, El-Maraghi RH, Hammel P, Heinemann V, Kunzmann V, Sastre J, Scheithauer W, Siena S, Tabernero J, Teixeira L, Tortora G, Van Laethem JL, Young R, Penenberg DN, Lu B, Romano A, Von Hoff DD. nab-Paclitaxel plus gemcitabine for metastatic pancreatic cancer: long-term survival from a phase III trial. J Natl Cancer Inst. 2015;107:dju413.
Motoi F, Kosuge T, Ueno H, Yamaue H, Satoi S, Sho M, Honda G, Matsumoto I, Wada K, Furuse J, Matsuyama Y, Unno M. Randomized phase II/III trial of neoadjuvant chemotherapy with gemcitabine and S-1 versus upfront surgery for resectable pancreatic cancer (Prep-02/JSAP05). Jpn J Clin Oncol. 2019;49:190-194.
Acknowledgments
The authors would like to thank Enago (www.enago.jp) for the English language review.
Author information
Authors and Affiliations
Contributions
T Sakoda: conception, design, acquisition, analysis and interpretation of data, drafting the work; KU: design, interpretation of data, critical revision of the work; NK: conception, design, acquisition, interpretation of data, critical revision of the work; T Sumiyoshi: design, interpretation of data, critical revision of the work; KO: design, interpretation of data, critical revision of the work; SS: design, interpretation of data, critical revision of the work; HO: design, interpretation of data, critical revision of the work; YM: design, interpretation of data, critical revision of the work; ST: conception, design, interpretation of data, critical revision of the work. All authors approved the final manuscript and agree to be accountable for all aspects of the work.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Sakoda, T., Uemura, K., Kondo, N. et al. Prognostic Value of Peritoneal Lavage Cytology in Patients with Pancreatic Ductal Adenocarcinoma Stratified by the Resectability Status. J Gastrointest Surg 25, 2871–2880 (2021). https://doi.org/10.1007/s11605-021-04978-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11605-021-04978-3