Anonymous User
Login / Registration

Gastroenterologie
a hepatologie

Gastroenterology and Hepatology

Gastroent Hepatol 2021; 75(5): 390–398. doi: 10.48095/ccgh2021390.

Pancreatic cancer screening: ready for prime time?

Peter Slodička1, Tomáš Tichý1, Jana Tesaříková2, Hana Švébišová3, Radim Kovář4, Daniela Kurfürstová5, Mária Janíková6, Veroniko Woitková6, Martin Procházka6, Přemysl Falt Orcid.org  1,7, Vincent Zoundjiekpon Orcid.org  1, Ondřej Urban1

+ Affiliation

Summary

Early detection of pancreatic cancer is considered to be the most effective way to improve survival. Individuals with familial occurrence or genetic susceptibility syndromes have an increased risk of developing pancreatic cancer. Current guidelines are based on evidence of the benefits of systematic surveillance in high-risk individuals and emphasize the potential of screening programs to affect overall survival. This type of screening has not yet been introduced in the Czech Republic even though such programs are already being established in other countries. With this review we aim to summarize knowledge about hereditary and familial pancreatic cancer and issue a call for collaboration on a pilot screening program.


Keywords

pancreatic carcinoma, hereditární karcinom pankreatu, onkologický screening

To read this article in full, please register for free on this website.

Benefits for subscribers

Benefits for logged users

Literature

1. ÚZIS ČR. Novotvary 2018 ČR. 2021 [online]. Dostupné z: https: //www.uzis.cz/res/f/008352/novotvary2018.pdf.
2. Loveček M, Skalický P, Ryska M et al. Aktuální stav chirurgické léčby karcinomu pankreatu v České republice. Rozhl Chir 2016; 95(4): 151–155.
3. Huang L, Jansen L, Balavarca Y et al. Resection of pancreatic cancer in Europe and USA: an international large-scale study highlighting large variations. Gut 2019; 68(1): 130–139. doi: 10.1136/gutjnl-2017-314828.
4. National Cancer Institute. Cancer stat facts: pancreatic cancer. 2021 [online]. Available from: https: //seer.cancer.gov/statfacts/html/pancreas.html.
5. Ryska M. Karcinom pankreatu – současný efektivní dia­gnostický a terapeutický postup. Čas Lék Čes 2016; 155(1): 38–43.
6. Aslanian HR, Lee JH, Canto MI. AGA clinical practice update on pancreas cancer screening in high-risk individuals: expert review. Gastroenterology 2020; 159(1): 358–362. doi: 10.1053/j.gastro.2020.03.088.
7. Owens DK, Davidson KW, Krist AH et al. Screening for pancreatic cancer: US preventive services task force reaffirmation recommendation statement. JAMA 2019; 322(5): 438–444. doi: 10.1001/jama.2019.10232.
8. Goggins M, Overbeek KA, Brand R et al. Management of patients with increased risk for familial pancreatic cancer: updated recommendations from the International Cancer of the Pancreas Screening (CAPS) Consortium. Gut 2020; 69(1): 7–17. doi: 10.1136/gutjnl-2019-319352.
9. Syngal S, Brand RE, Church JM et al. ACG clinical guideline: genetic testing and management of hereditary gastrointestinal cancer syndromes. Am J Gastroenterol 2015; 110(2): 223–263. doi: 10.1038/ajg.2014.435.10. Henrikson NB, Aiello Bowles EJ, Blasi PR et al. Screening for pancreatic cancer: updated evidence report and systematic review for the US preventive services task force. JAMA 2019; 322(5): 445–454. doi: 10.1001/jama.2019.6190.
11. Canto MI, Harinck F, Hruban RH et al. International Cancer of the Pancreas Screening (CAPS) Consortium summit on the management of patients with increased risk for familial pancreatic cancer. Gut 2013; 62(3): 339–347. doi: 10.1136/gutjnl-2012-303108.
12. Klein AP, Brune KA, Petersen GM et al. Prospective risk of pancreatic cancer in familial pancreatic cancer kindreds. Cancer Res 2004; 64(7): 2634–2638. doi: 10.1158/0008-5472.can-03-3823.
13. Schneider R, Slater EP, Sina M et al. German national case collection for familial pancreatic cancer (FaPaCa): ten years experience. Fam Cancer 2011; 10(2): 323–330. doi: 10.1007/s10689-010-9414-x.
14. Lowenfels AB, Maisonneuve P, Whitcomb DC. Risk factors for cancer in hereditary pancreatitis. International Hereditary Pancreatitis Study Group. Med Clin North Am 2000; 84(3): 565–573. doi: 10.1016/s0025-7125(05)70240-6.
15. Yeo TP, Hruban RH, Brody J et al. Assessment of „gene-environment“ interaction in cases of familial and sporadic pancreatic cancer. J Gastrointest Surg 2009; 13(8): 1487–1494. doi: 10.1007/s11605-009-0923-6.
16. Giardiello FM, Welsh SB, Hamilton SR et al. Increased risk of cancer in the Peutz-Jeghers syndrome. N Engl J Med 1987; 316(24): 1511–1514. doi: 10.1056/NEJM198706113162404.
17. Giardiello FM, Brensinger JD, Tersmette AC et al. Very high risk of cancer in familial Peutz-Jeghers syndrome. Gastroenterology 2000; 119(6): 1447–1453. doi: 10.1053/gast.2000.20228.
18. van Lier MG, Wagner A, Mathus-Vliegen EM et al. High cancer risk in Peutz-Jeghers syndrome: a systematic review and surveillance recommendations. Am J Gastroenterol 2010; 105(6): 1258–1264. doi: 10.1038/ajg.2009.725.
19. DaVee T, Coronel E, Papafragkakis C et al. Pancreatic cancer screening in high-risk individuals with germline genetic mutations. Gastrointest Endosc 2018; 87(6): 1443–1450. doi: 10.1016/j.gie.2017.12.019.
20. Vasen HF, Gruis NA, Frants RR et al. Risk of developing pancreatic cancer in families with familial atypical multiple mole melanoma associated with a specific 19 deletion of p16 (p16-Leiden). Int J Cancer 2000; 87(6): 809–811.
21. Goldstein AM, Fraser MC, Struewing JP et al. Increased risk of pancreatic cancer in melanoma-prone kindreds with p16INK4 mutations. N Engl J Med 1995; 333(15): 970–974. doi: 10.1056/NEJM199510123331504.
22. Yang X, Leslie G, Doroszuk A et al. Cancer risks associated with germline PALB2 pathogenic variants: an international study of 524 families. J Clin Oncol 2020; 38(7): 674–685. doi: 10.1200/JCO.19.01907.
23. Kastrinos F, Mukherjee B, Tayob N et al. Risk of pancreatic cancer in families with Lynch syndrome. JAMA 2009; 302(16): 1790–1795. doi: 10.1001/jama.2009.1529.
24. Dítě P, Hermanová M, Trna J et al. The role of chronic inflammation: chronic pancreatitis as a risk factor of pancreatic cancer. Dig Dis 2012; 30(3): 277–283. doi: 10.1159/000336991.
25. Lowenfels AB, Maisonneuve P, DiMagno EP et al. Hereditary pancreatitis and the risk of pancreatic cancer. International Hereditary Pancreatitis Study Group. J Natl Cancer Inst 1997; 89(6): 442–446. doi: 10.1093/jnci/89.6.442.
26. Rebours V, Boutron-Ruault MC, Schnee M et al. Risk of pancreatic adenocarcinoma in patients with hereditary pancreatitis: a national exhaustive series. Am J Gastroenterol 2008; 103(1): 111–119. doi: 10.1111/j.1572-0241.2007.01597.x.
27. Klein AP, Beaty TH, Bailey-Wilson JE et al. Evidence for a major gene influencing risk of pancreatic cancer. Genet Epidemiol 2002; 23(2): 133–149. doi: 10.1002/gepi.1102.
28. Stoffel EM, McKernin SE, Brand R et al. Evaluating susceptibility to pancreatic cancer: ASCO provisional clinical opinion. J Clin Oncol 2019; 37(2): 153–164. doi: 10.1200/JCO.18.01489.
29. National Comprehensive Cancer Network. NCCN Guidelines – Pancreatic Adenocarcinoma. 2021 [online]. Available from: https: //www.nccn.org/guidelines/guidelines-detail?category=1&id=1455.
30. Lowery MA, Wong W, Jordan EJ et al. Prospective evaluation of germline alterations in patients with exocrine pancreatic neoplasms. J Natl Cancer Inst 2018; 110(10): 1067–1074. doi: 10.1093/jnci/djy024.
31. Grant RC, Selander I, Connor AA et al. Prevalence of germline mutations in cancer predisposition genes in patients with pancreatic cancer. Gastroenterology 2015; 148(3): 556–564. doi: 10.1053/j.gastro.2014.11.042.
32. Salo-Mullen EE, O’Reilly EM, Kelsen DP et al. Identification of germline genetic mutations in patients with pancreatic cancer. Cancer 2015; 121(24): 4382–4388. doi: 10.1002/cncr.29664.
33. Yurgelun MB, Chittenden AB, Morales-Oyarvide V et al. Germline cancer susceptibility gene variants, somatic second hits, and survival outcomes in patients with resected pancreatic cancer. Genet Med 2019; 21(1): 213–223. doi: 10.1038/s41436-018-0009-5.
34. Brand R, Borazanci E, Speare V et al. Prospective study of germline genetic testing in incident cases of pancreatic adenocarcinoma. Cancer 2018; 124(17): 3520–3527. doi: 10.1002/cncr.31628.
35. Dudley B, Karloski E, Monzon FA et al. Germline mutation prevalence in individuals with pancreatic cancer and a history of previous malignancy. Cancer 2018; 124(8): 1691–1700. doi: 10.1002/cncr.31242.
36. Shindo K, Yu J, Suenaga M et al. Deleterious germline mutations in patients with apparently sporadic pancreatic adenocarcinoma. J Clin Oncol 2017; 35(30): 3382–3390. doi: 10.1200/JCO.2017.72.3502.
37. Zemanek T, Melichar B, Lovecek M et al. Biomarkers and pathways of chemoresistance and chemosensitivity for personalized treatment of pancreatic adenocarcinoma. Pharmacogenomics 2019; 20(2): 113–127. doi: 10.2217/pgs- 2018-0073.
38. Canto MI, Hruban RH, Fishman EK et al. Frequent detection of pancreatic lesions in asymptomatic high-risk individuals. Gastroenterology 2012; 142(4): 796–804. doi: 10.1053/j.gastro.2012.01.005.
39. Overbeek KA, Levink IJ, Koopmann BD et al. Long-term yield of pancreatic cancer surveillance in high-risk individuals. Gut 2021; 70(Suppl). doi: 10.1136/gutjnl-2020-323611.
40. Harinck F, Konings IC, Kluijt I et al. A multicentre comparative prospective blinded analysis of EUS and MRI for screening of pancreatic cancer in high-risk individuals. Gut 2016; 65(9): 1505–1513. doi: 10.1136/gutjnl-2014-308008.
41. Canto MI, Almario JA, Schulick RD et al. Risk of neoplastic progression in individuals at high risk for pancreatic cancer undergoing long-term surveillance. Gastroenterology 2018; 155(3): 740–751. doi: 10.1053/j.gastro.2018.05.035.
42. Psar R, Urban O, Cerna M et al. Improvement of the dia­gnosis of isoattenuating pancreatic carcinomas by defining their characteristics on contrast enhanced computed tomography and endosonography with Fine-Needle Aspiration (EUS-FNA). Dia­gnostics 2021; 11(5): 776. doi: 10.3390/dia­gnostics11050776.
43. Danai LV, Babic A, Rosenthal MH et al. Altered exocrine function can drive adipose wasting in early pancreatic cancer. Nature 2018; 558(7711): 600–604. doi: 10.1038/s41586-018-0235-7.
44. Sah RP, Sharma A, Nagpal S et al. Phases of metabolic and soft tissue changes in months preceding a dia­gnosis of pancreatic ductal adenocarcinoma. Gastroenterology 2019; 156(6): 1742–1752. doi: 10.1053/j.gastro.2019.01.039.
45. Canto MI, Goggins M, Hruban RH et al. Screening for early pancreatic neoplasia in high-risk individuals: a prospective controlled study. Clin Gastroenterol Hepatol 2006; 4(6): 766–781. doi: 10.1016/j.cgh.2006.02.005.
46. Hanada K, Minami T, Shimizu A et al. Roles of ERCP in the early dia­gnosis of pancreatic cancer. Dia­gnostics 2019; 9(1): 30. doi: 10.3390/dia­gnostics9010030.
47. Kanno Y, Koshita S, Ogawa T et al. Predictive value of localized stenosis of the main pancreatic duct for early detection of pancreatic cancer. Clin Endosc 2019; 52(6): 588–597. doi: 10.5946/ce.2019.018.
48. Wu J, Matthaei H, Maitra A et al. Recurrent GNAS mutations define an unexpected pathway for pancreatic cyst development. Sci Transl Med 2011; 3(92): 92ra66. doi: 10.1126/scitranslmed.3002543.
49. Kanda M, Knight S, Topazian M et al. Mutant GNAS detected in duodenal collections of secretin-stimulated pancreatic juice indicates the presence or emergence of pancreatic cysts. Gut 2013; 62(7): 1024–1033. doi: 10.1136/gutjnl-2012-302823.
50. Kanda M, Sadakari Y, Borges M et al. Mutant TP53 in duodenal samples of pancreatic juice from patients with pancreatic cancer or high-grade dysplasia. Clin Gastroenterol Hepatol 2013; 11(6): 719–730. doi: 10.1016/j.cgh.2012.11.016.
51. Zubarik R, Gordon SR, Lidofsky SD et al. Screening for pancreatic cancer in a high-risk population with serum CA 19-9 and targeted EUS: a feasibility study. Gastrointest Endosc 2011; 74(1): 87–95. doi: 10.1016/j.gie.2011.03.1235.
52. Cohen JD, Li L, Wang Y et al. Detection and localization of surgically resectable cancers with a multi-analyte blood test. Science 2018; 359(6378): 926–930. doi: 10.1126/science.aar3247.
53. Liu J, Gao J, Du Y et al. Combination of plasma microRNAs with serum CA19-9 for early detection of pancreatic cancer. Int J Cancer 2012; 131(3): 683–691. doi: 10.1002/ijc.26422.
54. Sharma A, Kandlakunta H, Nagpal SJ et al. Model to determine risk of pancreatic cancer in patients with new-onset diabetes. Gastroenterology 2018; 155(3): 730–739. doi: 10.1053/j.gastro.2018.05.023.
55. Sharma A, Smyrk TC, Levy MJ et al. Fasting blood glucose levels provide estimate of duration and progression of pancreatic cancer before dia­gnosis. Gastroenterology 2018; 155(2): 490–500. doi: 10.1053/j.gastro.2018.04.025.
56. Khan S, Safarudin RF, Kupec JT. Validation of the ENDPAC model: identifying new-onset diabetics at risk of pancreatic cancer. Pancreatology 2021; 21(3): 550–555. doi: 10.1016/j.pan.2021.02.001.
57. Chen W, Butler RK, Lustigova E et al. Validation of the enriching new-onset diabetes for pancreatic cancer model in a diverse and integrated healthcare setting. Dig Dis Sci 2021; 66(1): 78–87. doi: 10.1007/s10620-020-06139-z.
58. Frič P, Šedo A, Škrha J et al. Časná detekce sporadického karcinomu pankreatu. Čas Lék Čes 2016; 155(1): 44–47.
59. Trna J, Kala Z, Kunovský L et al (eds). Klinická pankreatologie. 2. přepracované a doplněné vydání. Praha: Maxdorf 2021.
60. Vasen H, Ibrahim I, Ponce CG et al. Benefit of surveillance for pancreatic cancer in high-risk individuals: outcome of long-term prospective follow-up studies from three European expert centers. J Clin Oncol 2016; 34(17): 2010–2019. doi: 10.1200/JCO.2015.64.0730.
61. Roberts NJ, Norris AL, Petersen GM et al. Whole genome sequencing defines the genetic heterogeneity of familial pancreatic cancer. Cancer Discov 2016; 6(2): 166–175. doi: 10.1158/2159-8290.CD-15-0402.
62. Bartsch DK, Dietzel K, Bargello M et al. Multiple small „imaging“ branch-duct type intraductal papillary mucinous neoplasms (IPMNs) in familial pancreatic cancer: indicator for concomitant high grade pancreatic intraepithelial neoplasia? Fam Cancer 2013; 12(1): 89–96. doi: 10.1007/s10689-012-9582-y.
63. Brune K, Abe T, Canto M et al. Multifocal neoplastic precursor lesions associated with lobular atrophy of the pancreas in patients having a strong family history of pancreatic cancer. Am J Surg Pathol 2006; 30(9): 1067–1076.
64. Canto MI, Goggins M, Yeo CJ et al. Screening for pancreatic neoplasia in high-risk individuals: an EUS-based approach. Clin Gastroenterol Hepatol 2004; 2(7): 606–621. doi: 10.1016/s1542-3565 (04) 00244-7.
65. Lang J, Kunovský L, Kala Z et al. Risk factors of pancreatic cancer and their possible uses in dia­gnostics. Neoplasma 2021; 68(2): 227–239. doi: 10.4149/neo_2020_200706N699.
66. Vasen HF, Wasser M, van Mil A et al. Magnetic resonance imaging surveillance detects early-stage pancreatic cancer in carriers of a p16-Leiden mutation. Gastroenterology 2011; 140(3): 850–856. doi: 10.1053/j.gastro.2010.11.048.
67. Konings IC, Sidharta GN, Harinck F et al. Repeated participation in pancreatic cancer surveillance by high-risk individuals imposes low psychological burden. Psychooncology 2016; 25(8): 971–978. doi: 10.1002/pon.4047.
68. Al-Sukhni W, Borgida A, Rothenmund H et al. Screening for pancreatic cancer in a high-risk cohort: an eight-year experience. J Gastrointest Surg 2012; 16(4): 771–783. doi: 10.1007/s11605-011-1781-6.
69. Yu J, Sadakari Y, Shindo K et al. Digital next-generation sequencing identifies low-abundance mutations in pancreatic juice samples collected from the duodenum of patients with pancreatic cancer and intraductal papillary mucinous neoplasms. Gut 2017; 66(9): 1677–1687. doi: 10.1136/gutjnl-2015-311166.
70. Suenaga M, Yu J, Shindo K et al. Pancreatic juice mutation concentrations can help predict the grade of dysplasia in patients undergoing pancreatic surveillance. Clin Cancer Res 2018; 24(12): 2963–2974. doi: 10.1158/1078-0432.CCR-17-2463.
71. Pea A, Yu J, Marchionni L et al. Genetic analysis of small well-differentiated pancreatic neuroendocrine tumors identifies subgroups with differing risks of liver metastases. Ann Surg 2020; 271(3): 566–573. doi: 10.1097/SLA.0000000000003022.
72. Falconi M, Eriksson B, Kaltsas G et al. ENETS consensus guidelines update for the management of patients with functional pancreatic neuroendocrine tumors and non-functional pancreatic neuroendocrine tumors. Neuroendocrinology 2016; 103(2): 153–171. doi: 10.1159/000443171.
73. Matthaei H, Hong SM, Mayo SC et al. Presence of pancreatic intraepithelial neoplasia in the pancreatic transection margin does not influence outcome in patients with R0 resected pancreatic cancer. Ann Surg Oncol 2011; 18(12): 3493–3499. doi: 10.1245/s10434-011-1745-9.
74. Basturk O, Hong SM, Wood LD et al. A revised classification system and recommendations from the Baltimore consensus meeting for neoplastic precursor lesions in the pancreas. Am J Surg Pathol 2015; 39(12): 1730–1741. doi: 10.1097/PAS.0000000000000533.
75. Canto MI, Kerdsirichairat T, Yeo CJ et al. Surgical outcomes after pancreatic resection of screening-detected lesions in individuals at high risk for developing pancreatic cancer. J Gastrointest Surg 2020; 24(5): 1101–1110. doi: 10.1007/s11605-019-04230-z.

Credited self-teaching test