Laparoscopic Staging in Patients with Newly Diagnosed Pancreatic Cancer

  • Timothy Gilbert
  • Ryan Baron
  • Paula Ghaneh
  • Christopher Halloran
Reference work entry

Abstract

Prompt accurate staging is paramount in managing patients with newly diagnosed pancreatic cancer. Initially, diagnosis and staging are undertaken using contrast-enhanced multidetector computerized tomography (CE-MDCT) or magnetic resonance imaging (MRI), supplemented with endoscopic ultrasound in selected cases. Staging laparoscopy (SL) with or without laparoscopic ultrasound (L-LUS) has been found to detect occult disease in 13–28% of patients with pancreatic cancer who are considered potentially resectable on imaging; however, between 1% and 30% of patients thought to be resectable on SL/L-LUS have subsequently been found to have unresectable disease. The clinical utility of SL/L-LUS can be enhanced by adopting a selective approach, only undertaking SL/L-LUS when one or more criteria are present, including (1) presumed pancreatic primary >3 cm diameter, (2) lesions in the body and tail of the pancreas, (3) CA 19–9>150 kU/L (>300 when total bilirubin >35 micromol/L), and (4) platelet/lymphocyte ratio >150. The judicious use of SL/L-LUS and cross-sectional imaging are complementary; however, the advent of PET-CT may lead to improvements in the detection of small previously radiologically occult metastases and may reduce the future role of SL/L-LUS.

Keywords

Pancreas Pancreatic cancer Laparoscopy Laparoscopic ultrasound Diagnosis Staging 

References

  1. 1.
    Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ. Cancer statistics, 2007. CA Cancer J Clin. 2007;57:43–66.CrossRefGoogle Scholar
  2. 2.
    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;74:2913–21.CrossRefGoogle Scholar
  3. 3.
    Ghaneh P, Costello E, Neoptolemos JP. Biology and management of pancreatic cancer. Gut. 2007;56:1134–52.CrossRefGoogle Scholar
  4. 4.
    Takaori K, Bassi C, Biankin A, Brunner TB, Cataldo I, Campbell F, et al. International Association of Pancreatology (IAP)/European Pancreatic Club (EPC) consensus review of guidelines for the treatment of pancreatic cancer. Pancreatology. 2016;16:14–27.CrossRefGoogle Scholar
  5. 5.
    Bipat S, Phoa SSKS, van Delden OM, Bossuyt PMM, Gouma DJ, Lameris JS, et al. Ultrasonography, computed tomography and magnetic resonance imaging for diagnosis and determining resectability of pancreatic adenocarcinoma: a meta-analysis. J Comput Assist Tomogr. 2005;29:438–45.CrossRefGoogle Scholar
  6. 6.
    Miller FH, Rini NJ, Keppke AL. MRI of adenocarcinoma of the pancreas. AJR Am J Roentgenol. 2006;187:W365–74.CrossRefGoogle Scholar
  7. 7.
    Rafique A, Freeman S, Carroll N. A clinical algorithm for the assessment of pancreatic lesions: utilization of 16- and 64-section multidetector CT and endoscopic ultrasound. Clin Radiol. 2007;62:1142–53.CrossRefGoogle Scholar
  8. 8.
    Schima W, Ba-Ssalamah A, Goetzinger P, Scharitzer M, Koelblinger C. State-of-the-art magnetic resonance imaging of pancreatic cancer. Top Magn Reson Imaging: TMRI. 2007;18:421–9.CrossRefGoogle Scholar
  9. 9.
    Agarwal B, Krishna NB, Labundy JL, Safdar R, Akduman EI. EUS and/or EUS-guided FNA in patients with CT and/or magnetic resonance imaging findings of enlarged pancreatic head or dilated pancreatic duct with or without a dilated common bile duct. Gastrointest Endosc. 2008;68:237–42; quiz 334–5.CrossRefGoogle Scholar
  10. 10.
    Farma JM, Santillan AA, Melis M, Walters J, Belinc D, Chen D-T, et al. PET/CT fusion scan enhances CT staging in patients with pancreatic neoplasms. Ann Surg Oncol. 2008;15:2465–71.CrossRefGoogle Scholar
  11. 11.
    Klauss M, Mohr A, Tengg-Kobligk von H, Friess H, Singer R, Seidensticker P, et al. A new invasion score for determining the resectability of pancreatic carcinomas with contrast-enhanced multidetector computed tomography. Pancreatology. 2008;8:204–10.CrossRefGoogle Scholar
  12. 12.
    Safi MW, Cornfield D, Modarresifar H, Ojha B. 18F-FDG positron emission tomography CT (FDG PET-CT) in the management of pancreatic cancer: initial experience in 12 patients. J Gastrointest Liver Dis: JGLD. 2008;17:173–8.Google Scholar
  13. 13.
    Schick V, Franzius C, Beyna T, Oei ML, Schnekenburger J, Weckesser M, et al. Diagnostic impact of 18F-FDG PET-CT evaluating solid pancreatic lesions versus endosonography, endoscopic retrograde cholangio-pancreatography with intraductal ultrasonography and abdominal ultrasound. Eur J Nucl Med Mol Imaging. 2008;35:1775–85.CrossRefGoogle Scholar
  14. 14.
    Singh AK, Sahani DV, Blake MA, Joshi MC, Wargo JA, Fernandez-del CC. Assessment of pancreatic tumor resectability with multidetector computed tomography: semiautomated console-generated images versus dedicated workstation-generated images. Acad Radiol. 2008;15:1058–68.CrossRefGoogle Scholar
  15. 15.
    Takeuchi M, Matsuzaki K, Kubo H, Nishitani H. High-b-value diffusion-weighted magnetic resonance imaging of pancreatic cancer and mass-forming chronic pancreatitis: preliminary results. Acta Radiol. 2008;49:383–6.CrossRefGoogle Scholar
  16. 16.
    Yamaguchi K, Okusaka T, Shimizu K, Furuse J, Ito Y, Hanada K, et al. EBM-based Clinical Guidelines for Pancreatic Cancer (2013) issued by the Japan Pancreas Society: a synopsis. Jpn J Clin Oncol. 2014;44:883–8.CrossRefGoogle Scholar
  17. 17.
    Ducreux M, Cuhna AS, Caramella C, Hollebecque A, Burtin P, Goere D, et al. Cancer of the pancreas: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2015;26(Suppl 5):v56–68.CrossRefGoogle Scholar
  18. 18.
    Ma X, Setty B, Uppot RN, Sahani DV. Multiple-detector computed tomographic angiography of pancreatic neoplasm for presurgical planning: comparison of low- and high-concentration nonionic contrast media. J Comput Assist Tomogr. 2008;32:511–7.CrossRefGoogle Scholar
  19. 19.
    Asbun HJ, Conlon K, Fernandez-Cruz L, Friess H, Shrikhande SV, Adham M, et al. When to perform a pancreatoduodenectomy in the absence of positive histology? A consensus statement by the International Study Group of Pancreatic Surgery. Surgery. 2014;155:887–92.CrossRefGoogle Scholar
  20. 20.
    Kauhanen SP, Komar G, Seppanen MP, Dean KI, Minn HR, Kajander SA, et al. A prospective diagnostic accuracy study of 18F-fluorodeoxyglucose positron emission tomography/computed tomography, multidetector row computed tomography, and magnetic resonance imaging in primary diagnosis and staging of pancreatic cancer. Ann Surg. 2009;250:957–63.CrossRefGoogle Scholar
  21. 21.
    Wang X-Y, Yang F, Jin C, Fu D-L. Utility of PET/CT in diagnosis, staging, assessment of resectability and metabolic response of pancreatic cancer. World J Gastroenterol WJG. 2014;20:15580–9.CrossRefGoogle Scholar
  22. 22.
    Tang S, Huang G, Liu J, Liu T, Traven L, Song S, et al. Usefulness of 18F-FDG PET, combined FDG-PET/CT and EUS in diagnosing primary pancreatic carcinoma: a meta-analysis. Euro J Radial. 2011;78:142–50.CrossRefGoogle Scholar
  23. 23.
    Kim M-J, Lee KH, Lee KT, Lee JK, Ku B-H, Oh C-R, et al. The value of positron emission tomography/computed tomography for evaluating metastatic disease in patients with pancreatic cancer. Pancreas. 2012;41:897–903.CrossRefGoogle Scholar
  24. 24.
    Yao J, Gan G, Farlow D, Laurence JM, Hollands M, Richardson A, et al. Impact of F18-fluorodeoxyglycose positron emission tomography/computed tomography on the management of resectable pancreatic tumours. ANZ J Surg. 2012;82:140–4.CrossRefGoogle Scholar
  25. 25.
    Sultana A, Jackson R, Tim G, Bostock E, Psarelli EE, Cox TF, et al. What is the best way to identify malignant transformation within pancreatic IPMN: a systematic review and meta-analyses. Clin Transl Gastroenterol. 2015;6:e130.CrossRefGoogle Scholar
  26. 26.
    Ghaneh P, Wong WL, Titman A, Plumpton C, Vinjamuri S, Johnson C, et al. PET-PANC: multi-centre prospective diagnostic accuracy and clinical value trial of FDG PET/CT in the diagnosis and management of suspected pancreatic cancer. ASCO Meet Abstr. 2016;34:4008.Google Scholar
  27. 27.
    Johnson CD. Guidelines for the management of patients with pancreatic cancer periampullary and ampullary carcinomas. Gut. 2005;54 Suppl 5:v1–16.Google Scholar
  28. 28.
    Halloran CM, Ghaneh P, Connor S, Sutton R, Neoptolemos JP, Raraty MG. Carbohydrate antigen 19.9 accurately selects patients for laparoscopic assessment to determine resectability of pancreatic malignancy. Br J Surg. 2008;95:453–9.CrossRefGoogle Scholar
  29. 29.
    Satoi S, Yanagimoto H, Toyokawa H, Inoue K, Wada K, Yamamoto T, et al. Selective use of staging laparoscopy based on carbohydrate antigen 19-9 level and tumor size in patients with radiographically defined potentially or borderline resectable pancreatic cancer. Pancreas. 2011;40:426–32.CrossRefGoogle Scholar
  30. 30.
    Garcea G, Cairns V, Berry DP, Neal CP, Metcalfe MS, Dennison AR. Improving the diagnostic yield from staging laparoscopy for periampullary malignancies: the value of preoperative inflammatory markers and radiological tumor size. Pancreas. 2012;41:233–7.CrossRefGoogle Scholar
  31. 31.
    Vollmer CM, Drebin JA, Middleton WD, Teefey SA, Linehan DC, Soper NJ, et al. Utility of staging laparoscopy in subsets of peripancreatic and biliary malignancies. Ann Surg. 2002;235:1–7.CrossRefGoogle Scholar
  32. 32.
    Enestvedt CK, Mayo SC, Diggs BS, Mori M, Austin DA, Shipley DK, et al. Diagnostic laparoscopy for patients with potentially resectable pancreatic adenocarcinoma: is it cost-effective in the current era? J Gastrointest Surg. 2008;12:1177–84.CrossRefGoogle Scholar
  33. 33.
    Hariharan D, Constantinides VA, Froeling FEM, Tekkis PP, Kocher HM. The role of laparoscopy and laparoscopic ultrasound in the preoperative staging of pancreatico-biliary cancers – a meta-analysis. Eur J Surg Oncol. 2010;36:941–8.CrossRefGoogle Scholar
  34. 34.
    Allen VB, Gurusamy KS, Takwoingi Y, Kalia A, Davidson BR. Diagnostic accuracy of laparoscopy following computed tomography (CT) scanning for assessing the resectability with curative intent in pancreatic and periampullary cancer. Cochrane Database Syst Rev. 2013;25(11):CD009323.Google Scholar
  35. 35.
    Taylor AM, Roberts SA, Manson JM. Experience with laparoscopic ultrasonography for defining tumour resectability in carcinoma of the pancreatic head and periampullary region. Br J Surg. 2001;88:1077–83.CrossRefGoogle Scholar
  36. 36.
    Menack MJ, Spitz JD, Arregui ME. Staging of pancreatic and ampullary cancers for resectability using laparoscopy with laparoscopic ultrasound. Surg Endosc. 2001;15:1129–34.CrossRefGoogle Scholar
  37. 37.
    Nieveen van Dijkum EJM, Romijn MG, Terwee CB, de Wit LT, van der Meulen JHP, Lameris HS, et al. Laparoscopic staging and subsequent palliation in patients with peripancreatic carcinoma. Ann Surg. 2003;237:66–73.CrossRefGoogle Scholar
  38. 38.
    Doran HE, Bosonnet L, Connor S, Jones L, Garvey C, Hughes M, et al. Laparoscopy and laparoscopic ultrasound in the evaluation of pancreatic and periampullary tumours. Dig Surg. 2004;21:305–13.CrossRefGoogle Scholar
  39. 39.
    Thomson BNJ, Parks RW, Redhead DN, Welsh FKS, Madhavan KK, Wigmore SJ, et al. Refining the role of laparoscopy and laparoscopic ultrasound in the staging of presumed pancreatic head and ampullary tumours. Br J Cancer. 2006;94:213–7.CrossRefGoogle Scholar
  40. 40.
    Doucas H, Sutton CD, Zimmerman A, Dennison AR, Berry DP. Assessment of pancreatic malignancy with laparoscopy and intraoperative ultrasound. Surg Endosc. 2007;21:1147–52.CrossRefGoogle Scholar
  41. 41.
    Ahmed SI, Bochkarev V, Oleynikov D, Sasson AR. Patients with pancreatic adenocarcinoma benefit from staging laparoscopy. J Laparoendosc Adv Surg Tech A. 2006;16:458–63.CrossRefGoogle Scholar
  42. 42.
    White R, Winston C, Gonen M, D’Angelica M, Jarnagin W, Fong Y, et al. Current utility of staging laparoscopy for pancreatic and peripancreatic neoplasms. J Am Coll Surg. 2008;206:445–50.CrossRefGoogle Scholar
  43. 43.
    Contreras CM, Stanelle EJ, Mansour J, Hinshaw JL, Rikkers LF, Rettammel R, et al. Staging laparoscopy enhances the detection of occult metastases in patients with pancreatic adenocarcinoma. J Surg Oncol. 2009;100:663–9.CrossRefGoogle Scholar
  44. 44.
    Lavy R, Gatot I, Markon I, Shapira Z, Chikman B, Copel L, et al. The role of diagnostic laparoscopy in detecting minimal peritoneal metastatic deposits in patients with pancreatic cancer scheduled for curative resection. Surg Laparosc Endosc Percutaneous Tech. 2012;22:358–60.CrossRefGoogle Scholar
  45. 45.
    Schnelldorfer T, Gagnon AI, Birkett RT, Reynolds G, Murphy KM, Jenkins RL. Staging laparoscopy in pancreatic cancer: a potential role for advanced laparoscopic techniques. J Am Coll Surg. 2014;218:1201–6.CrossRefGoogle Scholar
  46. 46.
    Connor S, Bosonnet L, Alexakis N, Raraty M, Ghaneh P, Sutton R, et al. Serum CA19-9 measurement increases the effectiveness of staging laparoscopy in patients with suspected pancreatic malignancy. Dig Surg. 2005;22:80–5.CrossRefGoogle Scholar
  47. 47.
    Smith RA, Bosonnet L, Ghaneh P, Sutton R, Evans J, Healey P, et al. The platelet-lymphocyte ratio improves the predictive value of serum CA19-9 levels in determining patient selection for staging laparoscopy in suspected periampullary cancer. Surgery. 2008;143:658–66.CrossRefGoogle Scholar
  48. 48.
    Allen VB, Gurusamy KS, Takwoingi Y, Kalia A, Davidson BR. Diagnostic accuracy of laparoscopy following computed tomography (CT) scanning for assessing the resectability with curative intent in pancreatic and periampullary cancer. Cochrane Database Syst Rev. 2016;7:CD009323.PubMedPubMedCentralGoogle Scholar
  49. 49.
    Levy J, Tahiri M, Vanounou T, Maimon G, Bergman S. Diagnostic laparoscopy with ultrasound still has a role in the staging of pancreatic cancer: a systematic review of the literature. HPB Surg: World J Hepatic Pancreat Biliary Surg. 2016;2016:8092109.CrossRefGoogle Scholar
  50. 50.
    Bemelman WA, de Wit LT, van Deaden OM, Smits NJ, Overtop H, Rauws EJ, et al. Diagnostic laparoscopy combined with laparoscopic ultrasonography in staging of cancer of the pancreatic head region. Br J Surg. 1995;82:820–4.CrossRefGoogle Scholar
  51. 51.
    Fristrup CW, Mortensen MB, Pless T, Durup J, Ainsworth A, Hovendal C, et al. Combined endoscopic and laparoscopic ultrasound as preoperative assessment of patients with pancreatic cancer. HPB: Off J Int Hepato Pancreato Biliary Assoc. 2006;8:57–60.CrossRefGoogle Scholar
  52. 52.
    Norton JA. Intraoperative methods to stage and localize pancreatic and duodenal tumors. Ann Oncol. 1999;10:S182–4.CrossRefGoogle Scholar
  53. 53.
    Friess H, Kleeff J, Silva JC, Sadowski C, Baer HU, Buchler MW. The role of diagnostic laparoscopy in pancreatic and periampullary malignancies. J Am Coll Surg. 1998;186:675–82.CrossRefGoogle Scholar
  54. 54.
    Barabino M, Santambrogio R, Pisani Ceretti A, Scalzone R, Montorsi M, Opocher E. Is there still a role for laparoscopy combined with laparoscopic ultrasonography in the staging of pancreatic cancer? Surg Endosc. 2011;25:160–5.CrossRefGoogle Scholar
  55. 55.
    Pisters PW, Lee JE, Vauthey JN, Charnsangavej C, Evans DB. Laparoscopy in the staging of pancreatic cancer. Br J Surg. 2001;88:325–37.CrossRefGoogle Scholar
  56. 56.
    Maithel SK, Maloney S, Winston C, Gonen M, D’Angelica MI, Dematteo RP, et al. Preoperative CA 19-9 and the yield of staging laparoscopy in patients with radiographically resectable pancreatic adenocarcinoma. Ann Surg Oncol. 2008;15:3512–20.CrossRefGoogle Scholar
  57. 57.
    Yoshida T, Matsumoto T, Morii Y, Ishio T, Kitano S, Yamada Y, et al. Staging with helical computed tomography and laparoscopy in pancreatic head cancer. Hepato-Gastroenterology. 2002;49:1428–31.PubMedGoogle Scholar
  58. 58.
    Morganti AG, Brizi MG, Macchia G, Sallustio G, Costamagna G, Alfieri S, et al. The prognostic effect of clinical staging in pancreatic adenocarcinoma. Ann Surg Oncol. 2005;12:145–51.CrossRefGoogle Scholar
  59. 59.
    Schlieman MG, Ho HS, Bold RJ. Utility of tumor markers in determining resectability of pancreatic cancer. Arch Surg. 2003;138:951–5; discussion 955–6.CrossRefGoogle Scholar
  60. 60.
    Warshaw AL, Tepper JE, Shipley WU. Laparoscopy in the staging and planning of therapy for pancreatic cancer. Am J Surg. 1986;151:76–80.CrossRefGoogle Scholar
  61. 61.
    Warshaw AL, Gu ZY, Wittenberg J, Waltman AC. Preoperative staging and assessment of resectability of pancreatic cancer. Arch Surg. 1990;125:230–3.CrossRefGoogle Scholar
  62. 62.
    Jimenez RE, Warshaw AL, Rattner DW, Willett CG, McGrath D, Fernandez-del Castillo C. Impact of laparoscopic staging in the treatment of pancreatic cancer. Arch Surg. 2000;135:409–14; discussion 414–5.CrossRefGoogle Scholar
  63. 63.
    Liu RC, Traverso LW. Diagnostic laparoscopy improves staging of pancreatic cancer deemed locally unresectable by computed tomography. Surg Endosc. 2005;19:638–42.CrossRefGoogle Scholar
  64. 64.
    Warshaw AL. Implications of peritoneal cytology for staging of early pancreatic cancer. Am J Surg. 1991;161:26–9; discussion 29–30.CrossRefGoogle Scholar
  65. 65.
    Makary MA, Warshaw AL, Centeno BA, Willet CG, Rattner DW, Fernandez-del CC. Implications of peritoneal cytology for pancreatic cancer management. Arch Surg. 1998;133:361–5.CrossRefGoogle Scholar
  66. 66.
    Jimenez RE, Warshaw AL, Fernandez-del CC. Laparoscopy and peritoneal cytology in the staging of pancreatic cancer. J Hepato-Biliary-Pancreat Surg. 2000;7:15–20.CrossRefGoogle Scholar
  67. 67.
    Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 2010;17:1471–4.CrossRefGoogle Scholar
  68. 68.
    Merchant NB, Conlon KC, Saigo P, Dougherty E, Brennan MF. Positive peritoneal cytology predicts unresectability of pancreatic adenocarcinoma. J Am Coll Surg. 1999;188:421–6.CrossRefGoogle Scholar
  69. 69.
    Ferrone CR, Haas B, Tang L, Coit DG, Fong Y, Brennan MF, et al. The influence of positive peritoneal cytology on survival in patients with pancreatic adenocarcinoma. J Gastrointest Surg. 2006;10:1347–53.CrossRefGoogle Scholar
  70. 70.
    Yamada S, Fujii T, Kanda M, Sugimoto H, Nomoto S, Takeda S, et al. Value of peritoneal cytology in potentially resectable pancreatic cancer. Br J Surg. 2013;100:1791–6.CrossRefGoogle Scholar
  71. 71.
    Winner M, Allendorf JD, Saif MW. An update on surgical staging of patients with pancreatic cancer. JOP: J Pancreas. 2012;13:143–6.Google Scholar
  72. 72.
    Fernandez-del Castillo C, Rattner DW, Warshaw AL. Further experience with laparoscopy and peritoneal cytology in the staging of pancreatic cancer. Br J Surg. 1995;82:1127–9.CrossRefGoogle Scholar
  73. 73.
    Shoup M, Winston C, Brennan MF, Bassman D, Conlon KC. Is there a role for staging laparoscopy in patients with locally advanced, unresectable pancreatic adenocarcinoma? J Gastrointest Surg. 2004;8:1068–71.CrossRefGoogle Scholar
  74. 74.
    White RR, Paulson EK, Freed KS, Keogan MT, Hurwitz HI, Lee C, et al. Staging of pancreatic cancer before and after neoadjuvant chemoradiation. J Gastrointest Surg. 2001;5:626–33.CrossRefGoogle Scholar
  75. 75.
    Morris S, Gurusamy KS, Sheringham J, Davidson BR. Cost-effectiveness of diagnostic laparoscopy for assessing resectability in pancreatic and periampullary cancer. BMC Gastroenterol. 2015;15:44.CrossRefGoogle Scholar
  76. 76.
    Jayakrishnan TT, Nadeem H, Groeschl RT, George B, Thomas JP, Ritch PS, et al. Diagnostic laparoscopy should be performed before definitive resection for pancreatic cancer: a financial argument. HPB: Off J Int Hepato Pancreato Biliary Assoc. 2015;17:131–9.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Timothy Gilbert
    • 1
  • Ryan Baron
    • 1
  • Paula Ghaneh
    • 2
    • 1
  • Christopher Halloran
    • 1
  1. 1.Department of Molecular and Clinical Cancer MedicineInstitute of Translational Medicine, University of LiverpoolLiverpoolUK
  2. 2.Department of SurgeryThe Royal Liverpool and Broadgreen University Hospitals NHS TrustLiverpoolUK

Section editors and affiliations

  • James L. Abbruzzese
    • 1
  • Raul A. Urrutia
    • 2
  • John Neoptolemos
    • 3
  • Markus W. Büchler
    • 4
  1. 1.Duke University Medical CenterDurhamUSA
  2. 2.Mayo Clinic Cancer CenterMayo ClinicRochesterUSA
  3. 3.Division of Surgery and OncologyUniversity of LiverpoolLiverpoolUK
  4. 4.Department of General, Visceral and Transplantation SurgeryUniversity of HeidelbergHeidelbergGermany

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