Clinical impact of high-quality testing for peritoneal lavage cytology in pancreatic cancer.
Liquid biopsy
Occult metastasis
Pancreatic cancer
Peritoneal lavage cytology
Peritoneal recurrence
Staging laparoscopy
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
03 May 2024
03 May 2024
Historique:
received:
29
11
2023
accepted:
29
04
2024
medline:
4
5
2024
pubmed:
4
5
2024
entrez:
3
5
2024
Statut:
epublish
Résumé
In pancreatic ductal adenocarcinoma (PDAC) patients, the importance of peritoneal lavage cytology, which indicates unresectability, remains controversial. This study sought to determine whether positive peritoneal lavage cytology (CY+) precludes pancreatectomy. Furthermore, we propose a novel liquid biopsy using peritoneal lavage fluid to detect viable peritoneal tumor cells (v-PTCs) with TelomeScan F35, a telomerase-specific replication-selective adenovirus engineered to express green fluorescent protein. Resectable cytologically or histologically proven PDAC patients (n = 53) were enrolled. CY was conducted immediately following laparotomy. The resulting fluid was examined by conventional cytology (conv-CY; Papanicolaou staining and MOC-31 immunostaining) and by the novel technique (Telo-CY; using TelomeScan F35). Of them, 5 and 12 were conv-CY+ and Telo-CY+, respectively. All underwent pancreatectomy. The two double-CY+ (conv-CY+ and Telo-CY+) patients showed early peritoneal recurrence (P-rec) postoperatively, despite adjuvant chemotherapy. None of the three conv-CY+ Telo-CY- patients exhibited P-rec. Six of the 10 Telo-CY+ conv-CY- patients (60%) relapsed with P-rec. Of the remaining 38 double-CY- [conv-CY-, Telo-CY-, conv-CY± (Class III)] patients, 3 (8.3%) exhibited P-rec. Although conv-CY+ status predicted poor prognosis and a higher risk of P-rec, Telo-CY was more sensitive for detecting v-PTC. Staging laparoscopy and performing conv-CY and Telo-CY are needed to confirm the indication for pancreatectomy.
Identifiants
pubmed: 38702437
doi: 10.1038/s41598-024-60936-4
pii: 10.1038/s41598-024-60936-4
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
10199Subventions
Organisme : Ministry of Education, Sports and Culture of Japan
ID : 22K08799
Informations de copyright
© 2024. The Author(s).
Références
Siegel, R. L., Miller, K. D., Wagle, N. S. & Jemal, A. Cancer statistics, 2023. CA Cancer J. Clin. 73, 17–48 (2023).
pubmed: 36633525
doi: 10.3322/caac.21763
Cancer Registry and Statistics. Cancer Information Service. https://ganjoho.jp/reg_stat/statistics/stat/summary.html
Rahib, L. et al. Projecting cancer incidence and deaths to 2030: The unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res. 74, 2913–2921 (2014).
pubmed: 24840647
doi: 10.1158/0008-5472.CAN-14-0155
Neoptolemos, J. P. et al. Comparison of adjuvant gemcitabine and capecitabine with gemcitabine monotherapy in patients with resected pancreatic cancer (ESPAC-4): A multicentre, open-label, randomised, phase 3 trial. Lancet 389, 1011–1024 (2017).
pubmed: 28129987
doi: 10.1016/S0140-6736(16)32409-6
Oettle, H. et al. Adjuvant chemotherapy with gemcitabine and long-term outcomes among patients with resected pancreatic cancer: The CONKO-001 randomized trial. JAMA 310, 1473–1481 (2013).
pubmed: 24104372
doi: 10.1001/jama.2013.279201
Uesaka, K. et al. Adjuvant chemotherapy of S-1 versus gemcitabine for resected pancreatic cancer: A phase 3, open-label, randomised, non-inferiority trial (JASPAC 01). Lancet 388, 248–257 (2016).
pubmed: 27265347
doi: 10.1016/S0140-6736(16)30583-9
Motoi, F. & Unno, M. Adjuvant and neoadjuvant treatment for pancreatic adenocarcinoma. Jpn. J. Clin. Oncol. 50, 483–489 (2020).
pubmed: 32083290
doi: 10.1093/jjco/hyaa018
Jang, J. Y. et al. Oncological benefits of neoadjuvant chemoradiation with gemcitabine versus upfront surgery in patients with borderline resectable pancreatic cancer: A prospective, randomized, open-label, multicenter phase 2/3 trial. Ann. Surg. 268, 215–222 (2018).
pubmed: 29462005
doi: 10.1097/SLA.0000000000002705
Ryan, D. P., Hong, T. S. & Bardeesy, N. Pancreatic adenocarcinoma. N. Engl. J. Med. 371, 1039–1049 (2014).
pubmed: 25207767
doi: 10.1056/NEJMra1404198
Rall, C. J. et al. Peritoneal exfoliative cytology and Ki-ras mutational analysis in patients with pancreatic adenocarcinoma. Cancer Lett. 97, 203–211 (1995).
pubmed: 7497464
doi: 10.1016/0304-3835(95)03978-6
Van den Broeck, A. et al. Patterns of recurrence after curative resection of pancreatic ductal adenocarcinoma. Eur. J. Surg. Oncol. 35, 600–604 (2009).
pubmed: 19131205
doi: 10.1016/j.ejso.2008.12.006
Hoshimoto, S. et al. Prognostic significance of intraoperative peritoneal washing cytology for patients with potentially resectable pancreatic ductal adenocarcinoma. Pancreatology 17, 109–114 (2017).
pubmed: 27840175
doi: 10.1016/j.pan.2016.11.001
Yoshioka, R. et al. The implications of positive peritoneal lavage cytology in potentially resectable pancreatic cancer. World J. Surg. 36, 2187–2191 (2012).
pubmed: 22555286
doi: 10.1007/s00268-012-1622-0
Satoi, S. et al. Reappraisal of peritoneal washing cytology in 984 patients with pancreatic ductal adenocarcinoma who underwent margin-negative resection. J. Gastrointest. Surg. 19, 6–14 (2015).
pubmed: 25316482
doi: 10.1007/s11605-014-2637-7
National Comprehensive Cancer Network, Clinical Practice Guidelines in Oncology. Pancreatic Adenocarcinoma ver. 2 2023. https://www.nccn.org/professionals/physician_gls/pdf/pancreatic.pdf
Tsuchida, H. et al. 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 166, 997–1003 (2019).
pubmed: 31445763
doi: 10.1016/j.surg.2019.06.023
Amin, M. B. et al. The Eighth Edition AJCC Cancer Staging Manual: Continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J. Clin. 67, 93–99 (2017).
pubmed: 28094848
doi: 10.3322/caac.21388
Ferrone, C. R. et al. The influence of positive peritoneal cytology on survival in patients with pancreatic adenocarcinoma. J. Gastrointest. Surg. 10, 1347–1353 (2006).
pubmed: 17175453
doi: 10.1016/j.gassur.2006.07.013
Katsuragi, K. et al. Prognostic impact of PCR-based identification of isolated tumour cells in the peritoneal lavage fluid of gastric cancer patients who underwent a curative R0 resection. Br. J. Cancer. 97, 550–556 (2007).
pubmed: 17667927
pmcid: 2360343
doi: 10.1038/sj.bjc.6603909
Uen, Y. H. et al. Prognostic significance of multiple molecular markers for patients with stage II colorectal cancer undergoing curative resection. Ann. Surg. 246, 1040–1046 (2007).
pubmed: 18043108
doi: 10.1097/SLA.0b013e318142d918
Takahashi, H. et al. Subclinical cancer cell dissemination in peritoneal lavage fluid detected by reverse-transcription polymerase chain reaction identifies patients at high risk for peritoneal recurrence and consequent impaired survival in the setting of preoperative chemoradiation therapy for pancreatic cancer. Surgery 164, 1168–1177 (2018).
pubmed: 30146098
doi: 10.1016/j.surg.2018.06.047
Kanetaka, K. et al. Clinical significance of carcinoembryonic antigen in peritoneal lavage from patients with gastric cancer. Surgery 154, 563–572 (2013).
pubmed: 23806263
doi: 10.1016/j.surg.2013.03.005
Yamamoto, M., Yoshinaga, K., Matsuyama, A., Tsutsui, S. & Ishida, T. CEA/CA72-4 levels in peritoneal lavage fluid are predictive factors in patients with gastric carcinoma. J. Cancer Res. Clin. Oncol. 140, 607–612 (2014).
pubmed: 24509654
doi: 10.1007/s00432-014-1601-y
Tan, Y. et al. Diagnostic value of tumor markers in peritoneal lavage fluid for peritoneal metastasis from colorectal cancer. Ann. Clin. Lab. Sci. 52, 95–100 (2022).
pubmed: 35181622
Hata, T. et al. Levels of tumor markers CEA/CA 19–9 in serum and peritoneal lavage predict postoperative recurrence in patients with pancreatic cancer. Ann. Gastroenterol. Surg. 6, 862–872 (2022).
pubmed: 36338582
pmcid: 9628216
doi: 10.1002/ags3.12597
Chiba, K. et al. impact of tumor-derived DNA testing in peritoneal lavage of pancreatic cancer patients with and without occult intra-abdominal metastases. Ann. Surg. Oncol. 29, 2685–2697 (2022).
pubmed: 34739641
doi: 10.1245/s10434-021-10997-w
Diaz, L. A. Jr. & Bardelli, A. Liquid biopsies: Genotyping circulating tumor DNA. J. Clin. Oncol. 32, 579–586 (2014).
pubmed: 24449238
pmcid: 4820760
doi: 10.1200/JCO.2012.45.2011
Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: The next generation. Cell 144, 646–674 (2011).
pubmed: 21376230
doi: 10.1016/j.cell.2011.02.013
Cong, Y. S., Wright, W. E. & Shay, J. W. Human telomerase and its regulation. Microbiol. Mol. Biol. Rev. 66, 407–425 (2002).
pubmed: 12208997
pmcid: 120798
doi: 10.1128/MMBR.66.3.407-425.2002
Sakurai, F. et al. Efficient detection of human circulating tumor cells without significant production of false-positive cells by a novel conditionally replicating adenovirus. Mol. Ther. Methods Clin. Dev. 3, 16001. https://doi.org/10.1038/mtm.2016.1 (2016).
doi: 10.1038/mtm.2016.1
pubmed: 26966699
pmcid: 4774621
Yamashita, S. et al. Impact of endoscopic stent insertion on detection of viable circulating tumor cells from obstructive colorectal cancer. Oncol. Lett. 15, 400–406 (2018).
pubmed: 29391884
Pitman, M. B. & Layfield, L. J. Guidelines for pancreaticobiliary cytology from the Papanicolaou Society of Cytopathology: A review. Cancer Cytopathol. 122, 399–411 (2014).
pubmed: 24777782
doi: 10.1002/cncy.21427
Patriarca, C., Macchi, R. M., Marschner, A. K. & Mellstedt, H. Epithelial cell adhesion molecule expression (CD326) in cancer: A short review. Cancer Treat. Rev. 38, 68–75 (2012).
pubmed: 21576002
doi: 10.1016/j.ctrv.2011.04.002
Asare, E. A. et al. Neoadjuvant treatment sequencing adds value to the care of patients with operable pancreatic cancer. J. Surg. Oncol. 114, 291–295 (2016).
pubmed: 27264017
doi: 10.1002/jso.24316
Tang, K., Lu, W., Qin, W. & Wu, Y. Neoadjuvant therapy for patients with borderline resectable pancreatic cancer: A systematic review and meta-analysis of response and resection percentages. Pancreatology 16, 28–37 (2016).
pubmed: 26687001
doi: 10.1016/j.pan.2015.11.007
Katz, M. H. et al. Preoperative modified FOLFIRINOX treatment followed by capecitabine-based chemoradiation for borderline resectable pancreatic cancer: Alliance for Clinical Trials in Oncology Trial A021101. JAMA Surg. 151, e161137. https://doi.org/10.1001/jamasurg.2016.1137 (2016).
doi: 10.1001/jamasurg.2016.1137
pubmed: 27275632
pmcid: 5210022
Takahashi, H. et al. Preoperative gemcitabine-based chemoradiation therapy for resectable and borderline resectable pancreatic cancer. Ann. Surg. 258, 1040–1050 (2013).
pubmed: 23799421
doi: 10.1097/SLA.0b013e31829b3ce4
Katz, M. H. et al. Serum CA 19–9 as a marker of resectability and survival in patients with potentially resectable pancreatic cancer treated with neoadjuvant chemoradiation. Ann. Surg. Oncol. 17, 1794–1801 (2010).
pubmed: 20162463
pmcid: 2889288
doi: 10.1245/s10434-010-0943-1
Wu, C. C. et al. Optimal surgical strategy for potentially curable serosa-involved gastric carcinoma with intraperitoneal free cancer cells. J. Am. Coll. Surg. 184, 611–617 (1997).
pubmed: 9179118
Li, B. Q. et al. Should Positive cytology revealed by intraoperative lavage preclude radical resection in resectable pancreatic cancer? A systematic review and meta-analysis. Pancreas 51, 1263–1276 (2022).
pubmed: 37099766
doi: 10.1097/MPA.0000000000002163
Tanaka, M. et al. Meta-analysis of effect of routine enteral nutrition on postoperative outcomes after pancreatoduodenectomy. Br. J. Surg. 106, 1138–1146 (2019).
pubmed: 31241185
doi: 10.1002/bjs.11217
Nomoto, S. et al. Peritoneal washing cytology combined with immunocytochemical staining and detecting mutant K-ras in pancreatic cancer: Comparison of the sensitivity and availability of various methods. Pancreas 14, 126–132 (1997).
pubmed: 9057184
doi: 10.1097/00006676-199703000-00004
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 8, 15004–15013 (2017).
pubmed: 28122342
pmcid: 5362462
doi: 10.18632/oncotarget.14745
Hirabayashi, K. et al. Positive intraoperative peritoneal lavage cytology is a negative prognostic factor in pancreatic ductal adenocarcinoma: a retrospective single-center study. Front. Oncol. 5, 182. https://doi.org/10.3389/fonc.2015.00182 (2015).
doi: 10.3389/fonc.2015.00182
pubmed: 26301205
pmcid: 4528174
Steen, W. et al. 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. 114, 743–751 (2016).
pubmed: 27642007
doi: 10.1002/jso.24402
Kubo, H. et al. Clinical significance of immunocytochemical staining for peritoneal lavage cytology in pancreatic cancer. Surgery 172, 1776–1781 (2022).
pubmed: 36371356
doi: 10.1016/j.surg.2022.09.025
Nakao, A. et al. Peritoneal washings cytology combined with immunocytochemical staining in pancreatic cancer. Hepatogastroenterology 46, 2974–2977 (1999).
pubmed: 10576385
Vogel, I. et al. Disseminated tumor cells in pancreatic cancer patients detected by immunocytology: A new prognostic factor. Clin. Cancer Res. 5, 593–599 (1999).
pubmed: 10100711
Cristofanilli, M. et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N. Engl. J. Med. 351, 781–791 (2004).
pubmed: 15317891
doi: 10.1056/NEJMoa040766
Danila, D. C., Fleisher, M. & Scher, H. I. Circulating tumor cells as biomarkers in prostate cancer. Clin. Cancer Res. 17, 3903–3912 (2011).
pubmed: 21680546
pmcid: 3743247
doi: 10.1158/1078-0432.CCR-10-2650
Vasseur, A., Kiavue, N., Bidard, F. C., Pierga, J. Y. & Cabel, L. Clinical utility of circulating tumor cells: An update. Mol. Oncol. 15, 1647–1666 (2021).
pubmed: 33289351
doi: 10.1002/1878-0261.12869
Nagrath, S. et al. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 450, 1235–1239 (2007).
pubmed: 18097410
pmcid: 3090667
doi: 10.1038/nature06385
Androulakis, N. et al. Clinical relevance of circulating CK-19mRNA-positive tumour cells before front-line treatment in patients with metastatic breast cancer. Br. J. Cancer 106, 1917–1925 (2012).
pubmed: 22669159
pmcid: 3388568
doi: 10.1038/bjc.2012.202
Hayes, D. F. et al. Circulating tumor cells at each follow-up time point during therapy of metastatic breast cancer patients predict progression-free and overall survival. Clin. Cancer Res. 12, 4218–4224 (2006).
pubmed: 16857794
doi: 10.1158/1078-0432.CCR-05-2821
Moll, R. et al. Cytokeratins in normal and malignant transitional epithelium. Maintenance of expression of urothelial differentiation features in transitional cell carcinomas and bladder carcinoma cell culture lines. Am. J. Pathol. 132, 123–144 (1988).
pubmed: 2456018
pmcid: 1880621
Castle, J., Morris, K., Pritchard, S. & Kirwan, C. C. Challenges in enumeration of CTCs in breast cancer using techniques independent of cytokeratin expression. PLoS ONE 12, e0175647. https://doi.org/10.1371/journal.pone.0175647 (2017).
doi: 10.1371/journal.pone.0175647
pubmed: 28422972
pmcid: 5397021
Kojima, T. et al. A simple biological imaging system for detecting viable human circulating tumor cells. J. Clin. Invest. 119, 3172–3181 (2009).
pubmed: 19729837
pmcid: 2752068
doi: 10.1172/JCI38609
Satoi, S. et al. Multicenter phase II study of intravenous and intraperitoneal paclitaxel with S-1 for pancreatic ductal adenocarcinoma patients with peritoneal metastasis. Ann. Surg. 265, 397–401 (2009).
doi: 10.1097/SLA.0000000000001705
Eguchi, H. et al. Prolonged neoadjuvant therapy for locally advanced pancreatic cancer. Dig. Surg. 35, 70–76 (2018).
pubmed: 28482348
doi: 10.1159/000475477
Liu, X. L. et al. Differentiation of genetically modified canine bone mesenchymal stem cells labeled with superparamagnetic iron oxide into neural-like cells. Mol. Med. Rep. 17, 7902–7910 (2018).
pubmed: 29620288