Role of gastrointestinal endoscopy in the screening of digestive tract cancers in Europe: European Society of Gastrointestinal Endoscopy (ESGE) Position Statement

Summary of statements

In Europe at present, but also in 2040, 1 in 3 cancer-related deaths are expected to be caused by digestive cancers. Endoscopic technologies enable diagnosis, with relatively low invasiveness, of precancerous conditions and early cancers, thereby improving patient survival. Overall, endoscopy capacity must be adjusted to facilitate both effective screening programs and rigorous control of the quality assurance and surveillance systems required.

1 For average-risk populations, ESGE recommends the implementation of organized population-based screening programs for colorectal cancer, based on fecal immunochemical testing (FIT), targeting individuals, irrespective of gender, aged between 50 and 75 years. Depending on local factors, namely the adherence of the target population and availability of endoscopy services, primary screening by colonoscopy or sigmoidoscopy may also be recommendable.

2 In high-risk populations, endoscopic screening for gastric cancer should be considered for individuals aged more than 40 years. Its use in countries/regions with intermediate risk may be considered on the basis of local settings and availability of endoscopic resources.

3 For esophageal and pancreatic cancer, endoscopic screening may be considered only in high-risk individuals:

– For squamous cell carcinoma, in those with a personal history of head/neck cancer, achalasia, or previous caustic injury;

– For Barrett’s esophagus (BE)-associated adenocarcinoma, in those with long-standing gastroesophageal reflux disease symptoms (i. e., > 5 years) and multiple risk factors (age ≥ 50 years, white race, male sex, obesity, first-degree relative with BE or esophageal adenocarcinoma [EAC]).

– For pancreatic cancer screening, endoscopic ultrasound may be used in selected high-risk patients such as those with a strong family history and/or genetic susceptibility.

Publikationsverlauf

Artikel online veröffentlicht:
12. Februar 2020

• References

• 1 Survival of Cancer Patients in Europe. Eurocare 5 database. Accessed: 16 Sept 2019, Available at: https://w3.iss.it/site/EU5Results/
• 2 van Leerdam ME, Roos VH, van Hooft JE. et al. Endoscopic management of Lynch syndrome and of familial risk of colorectal cancer: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2019; 51: 1082-1093
• 3 Pimentel-Nunes P, Libânio D, Marcos-Pinto R. et al. Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter and Microbiota Study Group (EHMSG), European Society of Pathology (ESP), and Sociedade Portuguesa de Endoscopia Digestiva (SPED) guideline update 2019. Endoscopy 2019; 51: 365-388
• 4 ECIS. ECIS - European Cancer Information System. Accessed: 15 Sept 2019, Available from: https://ecis.jrc.ec.europa.eu
• 5 RARECARENet Information Network on Rare Cancers. Accessed: 16 Sept 2019, Available from: http://rarecarenet.eu/index.php
• 6 IARC. Available at: https://gco.iarc.fr/today/data/factsheets/cancers/10_8_9-Colorectum-fact-sheet.pdf
• 7 Vuik FE, Nieuwenburg SA, Bardou M. et al. Increasing incidence of colorectal cancer in young adults in Europe over the last 25 years. Gut 2019; 68: 1820-1826
• 8 Brenner H, Stock C, Hoffmeister M. Effect of screening sigmoidoscopy and screening colonoscopy on colorectal cancer incidence and mortality: systematic review and meta-analysis of randomised controlled trials and observational studies. BMJ 2014; 348: g2467
• 9 Holme Ø, Bretthauer M, Fretheim A. et al. Flexible sigmoidoscopy versus faecal occult blood testing for colorectal cancer screening in asymptomatic individuals. Cochrane Database Syst Rev 2013; CD009259
• 10 Hassan C, Giorgi Rossi P, Camilloni L. et al. Meta-analysis: adherence to colorectal cancer screening and the detection rate for advanced neoplasia, according to the type of screening test. Aliment Pharmacol Ther 2012; 36: 929-940
• 11 Atkin WS, Edwards R, Kralj-Hans I. et al. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet 2010; 375: 1624-1633
• 12 Segnan N, Armaroli P, Bonelli L. et al. Once-only sigmoidoscopy in colorectal cancer screening: follow-up findings of the Italian Randomized Controlled Trial--SCORE. J Natl Cancer Inst 2011; 103: 1310-1322
• 13 Brenner H, Arndt V, Stürmer T. et al. Long-lasting reduction of risk of colorectal cancer following screening endoscopy. Br J Cancer 2001; 85: 972-976
• 14 Singal AG, Gupta S, Skinner CS. et al. Effect of colonoscopy outreach vs fecal immunochemical test outreach on colorectal cancer screening completion: A randomized clinical trial. JAMA 2017; 318: 806-815
• 15 Lauby-Secretan B, Vilahur N, Bianchini F. et al. International Agency for Research on Cancer Handbook Working Group. The IARC perspective on colorectal cancer screening. N Engl J Med 2018; 378: 1734-1740
• 16 Kaminski MF, Thomas-Gibson S, Bugajski M. et al. Performance measures for lower gastrointestinal endoscopy: a European Society of Gastrointestinal Endoscopy (ESGE) Quality Improvement Initiative. Endoscopy 2017; 49: 378-397
• 17 Chen C, Läcke E, Stock C. et al. Colonoscopy and sigmoidoscopy use among older adults in different countries: A systematic review. Prev Med 2017; 103: 33-42
• 18 Senore C, Inadomi J, Segnan N. et al. Optimising colorectal cancer screening acceptance: a review. Gut 2015; 64: 1158-1177
• 19 Basu P, Ponti A, Anttila A. et al. Status of implementation and organization of cancer screening in The European Union Member States - Summary results from the second European screening report. Int J Cancer 2018; 142: 44-56
• 20 Eisinger F, Cals L, Calazel-Benque A. et al. Impact of organised programs on colorectal cancer screening. BMC Cancer 2008; 8: 104
• 21 van Turenhout ST, Terhaar sive Droste JS, Meijer GA. et al. Anticipating implementation of colorectal cancer screening in The Netherlands: a nationwide survey on endoscopic supply and demand. BMC Cancer 2012; 12: 46
• 22 Parente F, Marino B, Ardizzoia A. et al. Impact of a population-based colorectal cancer screening program on local health services demand in Italy: a 7-year survey in a northern province. Am J Gastroenterol 2011; 106: 1986-1993
• 23 Zorzi M, Senore C, Turrin A. et al. Appropriateness of endoscopic surveillance recommendations in organised colorectal cancer screening programmes based on the faecal immunochemical test. Gut 2016; 65: 1822-1828
• 24 Schreuders EH, Ruco A, Rabeneck L. et al. Colorectal cancer screening: a global overview of existing programmes. Gut 2015; 64: 1637-1649
• 25 Senore C, Basu P, Anttila A. et al. Performance of colorectal cancer screening in the European Union Member States: data from the second European screening report. Gut 2019; 68: 1232-1244
• 26 Lansdorp-Vogelaar I, Knudsen A, Brenner H. Cost-effectiveness of colorectal cancer screening – an overview. Best Pract Res Clin Gastroenterol 2010; 24: 439-449
• 27 Torre LA, Bray F, Siegel RL. et al. Global cancer statistics, 2012. CA Cancer J Clin 2015; 65: 87-108
• 28 Zhang X, Li M, Chen S. et al. Endoscopic screening in Asian countries is associated with reduced gastric cancer mortality: A meta-analysis and systematic review. Gastroenterology 2018; 155: 347-354.e9
• 29 Correa P. Human gastric carcinogenesis: a multistep and multifactorial process -- First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 1992; 52: 6735-6740
• 30 Hamashima C. Systematic Review Group and Guideline Development Group for Gastric Cancer Screening Guidelines. Update version of the Japanese Guidelines for Gastric Cancer Screening. Jpn J Clin Oncol 2018; 48: 673-683
• 31 Kim BJ, Heo C, Kim BK. et al. Effectiveness of gastric cancer screening programs in South Korea: organized vs opportunistic models. World J Gastroenterol 2013; 19: 736-741
• 32 Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T. et al. Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2015; 47: 829-854
• 33 Ono H, Yao K, Fujishiro M. et al. Guidelines for endoscopic submucosal dissection and endoscopic mucosal resection for early gastric cancer. Dig Endosc 2016; 28: 3-15
• 34 Dinis-Ribeiro M, Yamaki G, Miki K. et al. Meta-analysis on the validity of pepsinogen test for gastric carcinoma, dysplasia or chronic atrophic gastritis screening. J Med Screen 2004; 11: 141-147
• 35 Lomba-Viana R, Dinis-Ribeiro M, Fonseca F. et al. Serum pepsinogen test for early detection of gastric cancer in a European country. Eur J Gastroenterol Hepatol 2012; 24: 37-41
• 36 Huang Y, Yu J, Kang W. et al. Significance of serum pepsinogens as a biomarker for gastric cancer and atrophic gastritis screening: A systematic review and meta-analysis. PLoS One 2015; 10: e0142080 Accessed: 24 Oct 2019, Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4640555
• 37 Kim GH, Liang PS, Bang SJ. et al. Screening and surveillance for gastric cancer in the United States: Is it needed?. Gastrointest Endosc 2016; 84: 18-28
• 38 Areia M, Spaander MC, Kuipers EJ. et al. Endoscopic screening for gastric cancer: A cost-utility analysis for countries with an intermediate gastric cancer risk. United Eur Gastroenterol J 2018; 6: 192-202
• 39 Tashiro A, Sano M, Kinameri K. et al. Comparing mass screening techniques for gastric cancer in Japan. World J Gastroenterol 2006; 12: 4873-4874
• 40 Zhou L, Guan P, Sun L. et al. Health economic assessment for screening of gastric cancer in a high risk population in northeastern China. Chin J Cancer Res 2011; 23: 21-24
• 41 Lee H-Y, Park E-C, Jun J-K. et al. Comparing upper gastrointestinal X-ray and endoscopy for gastric cancer diagnosis in Korea. World J Gastroenterol 2010; 16: 245-250
• 42 Chang H-S, Park E-C, Chung W. et al. Comparing endoscopy and upper gastrointestinal X-ray for gastric cancer screening in South Korea: a cost-utility analysis. Asian Pac J Cancer Prev 2012; 13: 2721-2728
• 43 Areia M, Carvalho R, Cadime AT. et al. Screening for gastric cancer and surveillance of premalignant lesions: a systematic review of cost-effectiveness studies. Helicobacter 2013; 18: 325-337
• 44 Cho E, Kang MH, Choi KS. et al. Cost-effectiveness outcomes of the national gastric cancer screening program in South Korea. Asian Pac J Cancer Prev 2013; 14: 2533-2540
• 45 Zhou HJ, Dan YY, Naidoo N. et al. A cost-effectiveness analysis evaluating endoscopic surveillance for gastric cancer for populations with low to intermediate risk. PloS One 2013; 8: e83959
• 46 Wu JT, Zhou J, Naidoo N. et al. Determining the cost-effectiveness of endoscopic surveillance for gastric cancer in patients with precancerous lesions. Asia Pac J Clin Oncol 2016; 12: 359-368
• 47 Gupta N, Bansal A, Wani SB. et al. Endoscopy for upper GI cancer screening in the general population: a cost-utility analysis. Gastrointest Endosc 2011; 74: 610-624.e2
• 48 Yeh JM, Hur C, Ward Z. et al. Gastric adenocarcinoma screening and prevention in the era of new biomarker and endoscopic technologies: a cost-effectiveness analysis. Gut 2016; 65: 563-574
• 49 Oesophageal cancer statistics. World Cancer Research Fund 2018. Accessed: 24 Oct 2019, Available at: https://www.wcrf.org/dietandcancer/cancer-trends/oesophageal-cancer-statistics
• 50 Rossini AR, Hashimoto CL, Iriya K. et al. Dietary habits, ethanol and tobacco consumption as predictive factors in the development of esophageal carcinoma in patients with head and neck neoplasms. Dis Esophagus 2008; 21: 316-321
• 51 Muto M, Hironaka S, Nakane M. et al. Association of multiple Lugol-voiding lesions with synchronous and metachronous esophageal squamous cell carcinoma in patients with head and neck cancer. Gastrointest Endosc 2002; 56: 517-521
• 52 Zendehdel K, Nyrén O, Edberg A. et al. Risk of esophageal adenocarcinoma in achalasia patients, a retrospective cohort study in Sweden. Am J Gastroenterol 2011; 106: 57-61
• 53 Blaydon DC, Etheridge SL, Risk JM. et al. RHBDF2 mutations are associated with tylosis, a familial esophageal cancer syndrome. Am J Hum Genet 2012; 90: 340-346
• 54 Ravi K, Geno DM, Katzka DA. Esophageal cancer screening in achalasia: is there a consensus?. Dis Esophagus 2015; 28: 299-304
• 55 Smyth EC, Lagergren J, Fitzgerald RC. et al. Oesophageal cancer. Nat Rev Dis Primer 2017; 3: 17048
• 56 Pan Q-J, Roth MJ, Guo H-Q. et al. Cytologic detection of esophageal squamous cell carcinoma and its precursor lesions using balloon samplers and liquid-based cytology in asymptomatic adults in Llinxian, China. Acta Cytol 2008; 52: 14-23
• 57 Yang J, Wei W-Q, Niu J. et al. Cost-benefit analysis of esophageal cancer endoscopic screening in high-risk areas of China. World J Gastroenterol 2012; 18: 2493-2501
• 58 Hur C, Choi SE, Kong CY. et al. High-resolution microendoscopy for esophageal cancer screening in China: A cost-effectiveness analysis. World J Gastroenterol 2015; 21: 5513-5523
• 59 Herszényi L, Tulassay Z. Epidemiology of gastrointestinal and liver tumors. Eur Rev Med Pharmacol Sci 2010; 14: 249-258
• 60 Blot WJ, Devesa SS, Kneller RW. et al. Rising incidence of adenocarcinoma of the esophagus and gastric cardia. JAMA 1991; 265: 1287-1289
• 61 Edgren G, Adami H-O, Weiderpass E. et al. A global assessment of the oesophageal adenocarcinoma epidemic. Gut 2013; 62: 1406-1414
• 62 Thrift AP. The epidemic of oesophageal carcinoma: Where are we now?. Cancer Epidemiol 2016; 41: 88-95
• 63 Fitzgerald RC, di Pietro M, Ragunath K. et al. British Society of Gastroenterology guidelines on the diagnosis and management of Barrett’s oesophagus. Gut 2014; 63: 7-42
• 64 Bennett C, Moayyedi P, Corley DA. et al. BOB CAT: A large-scale review and Delphi consensus for management of Barrett’s esophagus with no dysplasia, indefinite for, or low-grade dysplasia. Am J Gastroenterol 2015; 110: 662-682
• 65 Ronkainen J, Aro P, Storskrubb T. et al. Prevalence of Barrett’s esophagus in the general population: an endoscopic study. Gastroenterology 2005; 129: 1825-1831
• 66 di Pietro M, Chan D, Fitzgerald RC. et al. Screening for Barrett’s esophagus. Gastroenterology 2015; 148: 912-923
• 67 Hvid-Jensen F, Pedersen L, Drewes AM. et al. Incidence of adenocarcinoma among patients with Barrett’s esophagus. N Engl J Med 2011; 365: 1375-1383
• 68 Sharma P, Falk GW, Weston AP. et al. Dysplasia and cancer in a large multicenter cohort of patients with Barrett’s esophagus. Clin Gastroenterol Hepatol 2006; 4: 566-572
• 69 di Pietro M, Canto MI, Fitzgerald RC. Endoscopic management of early adenocarcinoma and squamous cell carcinoma of the esophagus: Screening, diagnosis, and therapy. Gastroenterology 2018; 154: 421-436
• 70 Lagergren J, Bergström R, Lindgren A. et al. Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma. N Engl J Med 1999; 340: 825-831
• 71 Rubenstein JH, Scheiman JM, Sadeghi S. et al. Esophageal adenocarcinoma incidence in individuals with gastroesophageal reflux: synthesis and estimates from population studies. Am J Gastroenterol 2011; 106: 254-260
• 72 Weusten B, Bisschops R, Coron E. et al. Endoscopic management of Barrett’s esophagus: European Society of Gastrointestinal Endoscopy (ESGE) Position Statement. Endoscopy 2017; 49: 191-198
• 73 Sharma P, Dent J, Armstrong D. et al. The development and validation of an endoscopic grading system for Barrett’s esophagus: the Prague C & M criteria. Gastroenterology 2006; 131: 1392-1399
• 74 Kadri S, Lao-Sirieix P, Fitzgerald RC. Developing a nonendoscopic screening test for Barrett’s esophagus. Biomark Med 2011; 5: 397-404
• 75 Trevisani L, Cifalà V, Sartori S. et al. Unsedated ultrathin upper endoscopy is better than conventional endoscopy in routine outpatient gastroenterology practice: a randomized trial. World J Gastroenterol 2007; 13: 906-911
• 76 Shariff MK, Bird-Lieberman EL, O’Donovan M. et al. Randomized crossover study comparing efficacy of transnasal endoscopy with that of standard endoscopy to detect Barrett’s esophagus. Gastrointest Endosc 2012; 75: 954-961
• 77 Ross-Innes CS, Debiram-Beecham I, O’Donovan M. et al. Evaluation of a minimally invasive cell sampling device coupled with assessment of trefoil factor 3 expression for diagnosing Barrett’s esophagus: a multi-center case-control study. PLoS Med 2015; 12: e1001780
• 78 Sharma P. Clinical practice. Barrett’s esophagus. N Engl J Med 2009; 361: 2548-2556
• 79 Kastelein F, van Olphen S, Steyerberg EW. et al. Surveillance in patients with long-segment Barrett’s oesophagus: a cost-effectiveness analysis. Gut 2015; 64: 864-871
• 80 Benaglia T, Sharples LD, Fitzgerald RC. et al. Health benefits and cost effectiveness of endoscopic and nonendoscopic cytosponge screening for Barrett’s esophagus. Gastroenterology 2013; 144: 62-73.e6
• 81 Xiao AY, Tan MLY, Wu LM. et al. Global incidence and mortality of pancreatic diseases: a systematic review, meta-analysis, and meta-regression of population-based cohort studies. Lancet Gastroenterol Hepatol 2016; 1: 45-55
• 82 Zhang Q, Zeng L, Chen Y. et al. Pancreatic cancer epidemiology, detection, and management. Gastroenterol Res Pract 2016; 2016: 8962321
• 83 Oberstein PE, Olive KP. Pancreatic cancer: why is it so hard to treat?. Ther Adv Gastroenterol 2013; 6: 321-337
• 84 McAllister F, Montiel MF, Uberoi GS. et al. Current status and future directions for screening patients at high risk for pancreatic cancer. Gastroenterol Hepatol 2017; 13: 268-375
• 85 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: 339-347
• 86 Goggins M, Overbeek KA, Brand R. et al. International Cancer of the Pancreas Screening (CAPS) consortium. 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: 7-17
• 87 Ogawa Y, Tanaka M, Inoue K. et al. A prospective pancreatographic study of the prevalence of pancreatic carcinoma in patients with diabetes mellitus. Cancer 2002; 94: 2344-2349
• 88 Illés D, Terzin V, Holzinger G. et al. New-onset type 2 diabetes mellitus – A high-risk group suitable for the screening of pancreatic cancer?. Pancreatology 2016; 16: 266-271
• 89 Molina-Montes E, Gómez-Rubio P, Malats N. Type 2 diabetes mellitus and pancreatic cancer risk. An independent etiological relation?. Pancreatology 2018; 18: S7
• 90 Bhutani MS, Koduru P, Joshi V. et al. The role of endoscopic ultrasound in pancreatic cancer screening. Endosc Ultrasound 2016; 5: 8-16
• 91 DaVee T, Coronel E, Papafragkakis C. et al. Pancreatic cancer screening in high-risk individuals with germline genetic mutations. Gastrointest Endosc 2018; 87: 1443-1450
• 92 Brentnall TA, Bronner MP, Byrd DR. et al. Early diagnosis and treatment of pancreatic dysplasia in patients with a family history of pancreatic cancer. Ann Intern Med 1999; 131: 247-255
• 93 Poley JW, Kluijt I, Gouma DJ. et al. The yield of first-time endoscopic ultrasound in screening individuals at a high risk of developing pancreatic cancer. Am J Gastroenterol 2009; 104: 2175-2181
• 94 Langer P, Kann PH, Fendrich V. et al. Five years of prospective screening of high-risk individuals from families with familial pancreatic cancer. Gut 2009; 58: 1410-1418
• 95 Sud A, Wham D, Catalano M. et al. Promising outcomes of screening for pancreatic cancer by genetic testing and endoscopic ultrasound. Pancreas 2014; 43: 458-461
• 96 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: 87-95
• 97 Ludwig E, Olson SH, Bayuga S. et al. Feasibility and yield of screening in relatives from familial pancreatic cancer families. Am J Gastroenterol 2011; 106: 946-954
• 98 Verna EC, Hwang C, Stevens PD. et al. Pancreatic cancer screening in a prospective cohort of high-risk patients: a comprehensive strategy of imaging and genetics. Clin Cancer Res 2010; 16: 5028-5037
• 99 Mocci E, Guillen-Ponce C, Earl J. et al. PanGen-Fam: Spanish registry of hereditary pancreatic cancer. Eur J Cancer 2015; 51: 1911-1917
• 100 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: 771-783
• 101 Lucas AL, Frado LE, Hwang C. et al. BRCA1 and BRCA2 germline mutations are frequently demonstrated in both high-risk pancreatic cancer screening and pancreatic cancer cohorts. Cancer 2014; 120: 1960-1967
• 102 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: 766-781 ; quiz 665
• 103 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: 606-621
• 104 Canto MI, Hruban RH, Fishman EK. et al. Frequent detection of pancreatic lesions in asymptomatic high-risk individuals. Gastroenterology 2012; 142: 796-804 ; quiz e14–15
• 105 Shin EJ, Topazian M, Goggins MG. et al. Linear-array EUS improves detection of pancreatic lesions in high-risk individuals: a randomized tandem study. Gastrointest Endosc 2015; 82: 812-818
• 106 Gangi A, Malafa M, Klapman J. Endoscopic ultrasound-based pancreatic cancer screening of high-risk individuals: A prospective observational trial. Pancreas 2018; 47: 586-591
• 107 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: 1505-1513
• 108 Corral JE, Mareth KF, Riegert-Johnson DL. et al. Diagnostic yield from screening asymptomatic individuals at high risk for pancreatic cancer: A meta-analysis of cohort studies. Clin Gastroenterol Hepatol 2019; 17: 41-53
• 109 Topazian M, Enders F, Kimmey M. et al. Interobserver agreement for EUS findings in familial pancreatic-cancer kindreds. Gastrointest Endosc 2007; 66: 62-67
• 110 Cazacu IM, Luzuriaga Chavez AA, Saftoiu A. et al. A quarter century of EUS-FNA: Progress, milestones, and future directions. Endosc Ultrasound 2018; 7: 141-160
• 111 Brugge WR, Lewandrowski K, Lee-Lewandrowski E. et al. Diagnosis of pancreatic cystic neoplasms: a report of the cooperative pancreatic cyst study. Gastroenterology 2004; 126: 1330-1336
• 112 Yeo CJ, Cameron JL, Sohn TA. et al. Six hundred fifty consecutive pancreaticoduodenectomies in the 1990s: pathology, complications, and outcomes. Ann Surg 1997; 226: 248-257 ; discussion 257–260
• 113 Balcom JH, Rattner DW, Warshaw AL. et al. Ten-year experience with 733 pancreatic resections: changing indications, older patients, and decreasing length of hospitalization. Arch Surg 2001; 136: 391-398
• 114 Stauffer JA, Onkendi EO, Wallace MB. et al. Standardization and streamlining of a pancreas surgery practice improves outcomes and resource utilization: A single institution’s 20-year experience. Am J Surg 2017; 214: 450-455
• 115 Cazacu IM, Luzuriaga Chavez AA. et al. Psychological impact of pancreatic cancer screening by EUS or magnetic resonance imaging in high-risk individuals: A systematic review. Endosc Ultrasound 2019; 8: 17-24
• 116 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: 740-751