The yield of first-time endoscopic ultrasonography in screening individuals at a high risk of developing pancreatic cancer
Abstract
OBJECTIVES: Approximately 10-15% of all pancreatic cancers (PCs) may be hereditary in origin. We investigated the use of endoscopic ultrasonography (EUS) for the screening of individuals at high risk for developing PC. In this paper the results of first-time screening with EUS are presented. METHODS: Those eligible for screening in this study were first-degree family members of affected individuals from familial pancreatic cancer (FPC) families, mutation carriers of PC-prone hereditary syndromes, individuals with Peutz-Jeghers syndrome, and mutation carriers of other PC-prone hereditary syndromes with clustering (> or =2 cases per family) of PC. All individuals were asymptomatic and had not undergone EUS before. RESULTS: Forty-four individuals (M/F 18/26), aged 32-75 years underwent screening with EUS. Thirteen were from families with familial atypical multiple-mole melanoma (FAMMM), 21 with FPC, 3 individuals were diagnosed with hereditary pancreatitis, 2 were Peutz-Jeghers patients, 3 were BRCA1 and 2 were BRCA2 mutation carriers with familial clustering of PC, and 1 individual had a p53 mutation. Three (6.8%) patients had an asymptomatic mass lesion (12, 27, and 50 mm) in the body (n=2) or tail of the pancreas. All lesions were completely resected. Pathology showed moderately differentiated adenocarcinomas with N1 disease in the two patients with the largest lesions. EUS showed branch-type intraductal papillary mucinous neoplasia (IPMN) in seven individuals. CONCLUSIONS: Screening of individuals at a high risk for PC with EUS is feasible and safe. The incidence of clinically relevant findings at first screening is high with asymptomatic cancer in 7% and premalignant IPMN-like lesions in 16% in our series. Whether screening improves survival remains to be determined, as does the optimal screening interval with EUS.
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Medical imaging has been shown to detect precancerous tissue changes in the pancreas among individuals at high risk.
“The ability to detect precancerous tissue changes in the pancreas using medical imaging among individuals at high risk has also been shown.110,122–125”
From Early detection of pancreatic cancer (2020) · cites this paper as [124]
Cites
Jemal, A., Siegel, R., Ward, E., Murray, T., Xu, J., & Thun, M. J. (2007) · CA: A Cancer Journal for Clinicians · doi:10.3322/canjclin.57.1.43 · Cited by 7,439 · see citing works
Six Hundred Fifty Consecutive Pancreaticoduodenectomies in the 1990s
Yeo, C. J., Cameron, J. L., Riall, T. S., Lillemoe, K. D., Pitt, H. A., Talamini, M. A., Hruban, R. H., Ord, S. E., Sauter, P. K., Coleman, J., et al. (1997) · Annals of Surgery · doi:10.1097/00000658-199709000-00004 · Cited by 1,781 · see citing works
Very high risk of cancer in familial Peutz–Jeghers syndrome
Giardiello, F. M., Brensinger, J. D., Tersmette, A. C., Goodman, S. N., Petersen, G. M., Booker, S. V., Cruz–Correa, M., & Offerhaus, G. J. A. (2000) · Gastroenterology · doi:10.1053/gast.2000.20228 · Cited by 1,435 · see citing works
Edwards, B. K., Brown, M. L., Wingo, P. A., Howe, H. L., Ward, E., Ries, L. A. G., Schrag, D., Jamison, P. M., Jemal, A., Wu, X. C., et al. (2005) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/dji289 · Cited by 952 · see citing works
[Principles and practice of mass screening for disease].
Wilson, J. M., & Jungner, Y. G. (1968) · PubMed · Cited by 785 · see citing works
Prognostic indicators for survival after resection of pancreatic adenocarcinoma
Geer, R. J., & Brennan, M. F. (1993) · The American Journal of Surgery · doi:10.1016/s0002-9610(05)80406-4 · Cited by 758 · see citing works
Screening for early pancreatic neoplasia in high-risk individuals: a prospective controlled study
Canto, M. I., Goggins, M., Hruban, R. H., Petersen, G. M., Giardiello, F. M., Yeo, C., Fishman, E. K., Brune, K., Axilbund, J., Griffin, C., et al. (2006) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2006.02.005 · Cited by 524 · see citing works
Screening for pancreatic neoplasia in high-risk individuals: an EUS-based approach
Canto, M. I., Goggins, M., Yeo, C. J., Griffin, C., Axilbund, J. E., Brune, K., Ali, S. Z., Jagannath, S., Petersen, G. M., Fishman, E. K., et al. (2004) · Clinical Gastroenterology and Hepatology · doi:10.1016/s1542-3565(04)00244-7 · Cited by 448 · see citing works
Validation of the 6 th edition AJCC pancreatic cancer staging system
Bilimoria, K. Y., Bentrem, D. J., Ko, C. Y., Ritchey, J. D., Stewart, A. K., Winchester, D. P., & Talamonti, M. S. (2007) · Cancer · doi:10.1002/cncr.22852 · Cited by 424 · see citing works
Brentnall, T. A., Bronner, M. P., Byrd, D. R., Haggitt, R. C., & Kimmey, M. B. (1999) · Annals of Internal Medicine · doi:10.7326/0003-4819-131-4-199908170-00003 · Cited by 391 · see citing works
Patient age, histologic features, and length of survival in patients with glioblastoma multiforme
Burger, P. C., & Green, S. B. (1987) · Cancer · doi:10.1002/1097-0142(19870501)59:9 · Cited by 391 · see citing works
Precursors to Invasive Pancreatic Cancer
Maitra, A., Fukushima, N., Takaori, K., & Hruban, R. H. (2005) · Advances in Anatomic Pathology · doi:10.1097/01.pap.0000155055.14238.25 · Cited by 290 · see citing works
Sato, N., Rosty, C., Jansen, M., Fukushima, N., Ueki, T., Yeo, C. J., Cameron, J. L., Iacobuzio–Donahue, C. A., Hruban, R. H., & Goggins, M. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63053-2 · Cited by 268 · see citing works
Rebours, V., Boutron‐Ruault, M., Schnee, M., Férec, C., Maire, F., Hammel, P. R., Ruszniewski, P. B., & Lévy, P. (2008) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2007.01597.x · Cited by 264 · see citing works
Lévy, P., Jouannaud, V., O'Toole, D., Couvelard, A., Vullierme, M., Palazzo, L., Aubert, A., Ponsot, P., Sauvanet, A., Maire, F., et al. (2006) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2006.01.018 · Cited by 244 · see citing works
Familial pancreatic cancer: a review.
Lynch, H. T., Smyrk, T. C., Kern, S. E., Hruban, R. H., Lightdale, C. J., Lemon, S. J., Lynch, J. F., Fusaro, L., Fusaro, R. M., & Ghadirian, P. (1996) · PubMed · Cited by 239 · see citing works
ASGE guideline: complications of EUS
Jacobson, B. C., Adler, D. G., Davila, R. E., et al. (2005) · Gastrointestinal Endoscopy · doi:10.1016/s0016-5107(04)02393-4 · Cited by 238 · see citing works
Tanno, S., Nakano, Y., Nishikawa, T., Nakamura, K., Sasajima, J., Minoguchi, M., Mizukami, Y., Yanagawa, N., FUJII, T., Obara, T., et al. (2007) · Gut · doi:10.1136/gut.2007.129684 · Cited by 222 · see citing works
Manfredi, R. M., Costamagna, G., Brizi, M. G., et al. (2000) · Radiology · doi:10.1148/radiology.214.3.r00mr24849 · Cited by 207 · see citing works
Ghadirian, P., Boyle, P., Simard, A., Baillargeon, J., Maisonneuve, P., & Perret, C. (1991) · International Journal of Pancreatology · doi:10.1007/bf02924156 · Cited by 192 · see citing works
Sugiyama, M., & Atomi, Y. (1999) · American Journal of Gastroenterology · doi:10.1111/j.1572-0241.1999.879_h.x · Cited by 188 · see citing works
Hunt, G. C., & Faigel, D. O. (2002) · Gastrointestinal Endoscopy · doi:10.1067/mge.2002.121342 · Cited by 178 · see citing works
Familial Risk of Pancreatic Cancer
Schenk, M., Schwartz, A. G., O'Neal, E., Kinnard, M. F., Greenson, J. K., Fryzek, J. P., Ying, G., & Garabrant, D. H. (2001) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/93.8.640 · Cited by 157 · see citing works
Accuracy of Staging Node-Negative Pancreas Cancer
Tomlinson, J. S. (2007) · Archives of Surgery · doi:10.1001/archsurg.142.8.767 · Cited by 129 · see citing works
Familial and second primary pancreatic cancers: A nationwide epidemiologic study from Sweden
Hemminki, K., & Li, X. (2002) · International Journal of Cancer · doi:10.1002/ijc.10863 · Cited by 128 · see citing works
Pylorus-Preserving Pancreatoduodenectomy
Tsao, J. I. (1994) · Archives of Surgery · doi:10.1001/archsurg.1994.01420280081010 · Cited by 126 · see citing works
Intraductal Papillary-Mucinous Tumors of the Pancreas
Bernard, P., Scoazec, J., Joubert, M., et al. (2002) · Archives of Surgery · doi:10.1001/archsurg.137.11.1274 · Cited by 123 · see citing works
Gan, S. I., Rajan, E., Adler, D. G., et al. (2007) · Gastrointestinal Endoscopy · doi:10.1016/j.gie.2007.05.026 · Cited by 117 · see citing works
Natural History of Pancreatic Intraductal Papillary Mucinous Tumor of Branch Duct Type
Irié, H., Yoshimitsu, K., Aibe, H., et al. (2004) · Journal of Computer Assisted Tomography · doi:10.1097/00004728-200401000-00020 · Cited by 114 · see citing works
Risk of pancreatic cancer among individuals with a family history of cancer of the pancreas
Ghadirian, P., Liu, G., Gallinger, S., Schmocker, B., Paradis, A., Lal, G., Brunet, J., Foulkes, W. D., & Narod, S. A. (2001) · International Journal of Cancer · doi:10.1002/ijc.10123 · Cited by 72 · see citing works
Prevention of Pancreatic Cancer and Strategies for Management of Familial Pancreatic Cancer
Hruban, R. H., Canto, M. I., & Yeo, C. J. (2001) · Digestive Diseases · doi:10.1159/000050656 · Cited by 61 · see citing works
Familial Pancreatic Cancer Syndromes
Habbe, N., Langer, P., Sina‐Frey, M., & Bartsch, D. K. (2006) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2006.02.016 · Cited by 53 · see citing works
Pancreatic Carcinoma in Brothers
DAT, N. M., & SONTAG, S. J. (1982) · Annals of Internal Medicine · doi:10.7326/0003-4819-97-2-282_1 · Cited by 42 · see citing works
Pylorus-preserving pancreatoduodenectomy
Farnell, M. B. (2001) · Operative Techniques in General Surgery · doi:10.1053/otgn.2001.21543 · Cited by 39 · see citing works
Staging and treatment for patients with pancreatic cancer. How small is an early pancreatic cancer?
Tsunoda, T., Yamamoto, Y., Kimoto, M., et al. (1998) · Journal of Hepato-Biliary-Pancreatic Surgery · doi:10.1007/s005340050022 · Cited by 35 · see citing works
Familial carcinoma of the pancreas*
Friedman, J. M., & Fialkow, P. J. (1976) · Clinical Genetics · doi:10.1111/j.1399-0004.1976.tb01598.x · Cited by 34 · see citing works
Reproduction of MINIMAL STANDARD TERMINOLOGY IN GASTROINTESTINAL ENDOSONOGRAPHY
(1998) · Digestive Endoscopy · doi:10.1111/j.1443-1661.1998.tb00555.x · Cited by 20 · see citing works
A family history of pancreatic cancer
Keswani, R. N., Noffsinger, A. E., & Waxman, I. (2006) · Nature Clinical Practice Gastroenterology & Hepatology · doi:10.1038/ncpgasthep0604 · Cited by 2 · see citing works
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Sorted by citations
Syngal, S., Brand, R. E., Church, J. M., Giardiello, F. M., Hampel, H. L., & Burt, R. W. (2015) · American Journal of Gastroenterology · doi:10.1038/ajg.2014.435 · Cited by 1,662 · see citing works
Lin, J. S., Bowles, E. J. A., Williams, S. B., & Morrison, C. C. (2017) · JAMA · doi:10.1001/jama.2017.0562 · Cited by 1,082 · see citing works
Canto, M. I., Harinck, F., Hruban, R. H., Offerhaus, G. J., Poley, J.-W., Kamel, I., Nio, Y., Schulick, R. S., Bassi, C., Kluijt, I., et al. (2013) · Gut · doi:10.1136/gutjnl-2012-303108 · Cited by 784 · see citing works
Self-citationGoggins, M., Overbeek, K. A., Brand, R., Syngal, S., Del Chiaro, M., Bartsch, D. K., Bassi, C., Carrato, A., Farrell, J., Fishman, E. K., et al. (2020) · Gut · doi:10.1136/gutjnl-2019-319352 · Cited by 659 · see citing works
Self-citationFrequent detection of pancreatic lesions in asymptomatic high-risk individuals
Canto, M. I., Hruban, R. H., Fishman, E. K., Kamel, I. R., Schulick, R., Zhang, Z., Topazian, M., Takahashi, N., Fletcher, J., Petersen, G., et al. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.01.005 · Cited by 648 · see citing works
European experts consensus statement on cystic tumours of the pancreas
Del Chiaro, M., Verbeke, C., Salvia, R., Klöppel, G., Werner, J., McKay, C., Friess, H., Manfredi, R., Van Cutsem, E., Löhr, M., et al. (2013) · Digestive and Liver Disease · doi:10.1016/j.dld.2013.01.010 · Cited by 498 · see citing works
Self-citationEarly detection of pancreatic cancer
Pereira, S. P., Oldfield, L., Ney, A., Hart, P. A., Keane, M. G., Pandol, S. J., Li, D., Greenhalf, W., Jeon, C. Y., Koay, E. J., et al. (2020) · The Lancet Gastroenterology & Hepatology · doi:10.1016/s2468-1253(19)30416-9 · Cited by 482 · see citing works
Canto, M. I., Almario, J. A., Schulick, R. D., Yeo, C. J., Klein, A., Blackford, A., Shin, E. J., Sanyal, A., Yenokyan, G., Lennon, A. M., et al. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.05.035 · Cited by 414 · see citing works
Vasen, H., Ibrahim, I., Ponce, C. G., Slater, E. P., Matthäi, E., Carrato, A., Earl, J., Robbers, K., van Mil, A. M., Potjer, T., et al. (2016) · Journal of Clinical Oncology · doi:10.1200/jco.2015.64.0730 · Cited by 344 · see citing works
Screening for Pancreatic Cancer: Why, How, and Who?
Poruk, K. E., Firpo, M. A., Adler, D. G., & Mulvihill, S. J. (2013) · Annals of Surgery · doi:10.1097/sla.0b013e31825ffbfb · Cited by 249 · see citing works
Pancreatic Cancer Prediction Through an Artificial Neural Network
Muhammad, W., Hart, G. R., Nartowt, B., Farrell, J. J., Johung, K., Liang, Y., & Deng, J. (2019) · Frontiers in Artificial Intelligence · doi:10.3389/frai.2019.00002 · Cited by 159 · see citing works
Vasen, H. F. A., Wasser, M., van Mil, A., Tollenaar, R. A., Konstantinovski, M., Gruis, N. A., Bergman, W., Hes, F. J., Hommes, D. W., Offerhaus, G. J. A., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2010.11.048 · Cited by 152 · see citing works
Klein, A. P., Lindström, S., Mendelsohn, J. B., Steplowski, E., Arslan, A. A., Bueno-de-Mesquita, H. B., Fuchs, C. S., Gallinger, S., Gross, M., Helzlsouer, K., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072311 · Cited by 148 · see citing works
Henrikson, N. B., Aiello Bowles, E. J., Blasi, P. R., Morrison, C. C., Nguyen, M., Pillarisetty, V. G., & Lin, J. S. (2019) · JAMA · doi:10.1001/jama.2019.6190 · Cited by 140 · see citing works
Corral, J. E., Mareth, K. F., Riegert-Johnson, D. L., Das, A., & Wallace, M. B. (2019) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2018.04.065 · Cited by 113 · see citing works
Early Diagnosis of Pancreatic Cancer: The Key for Survival
Gheorghe, G., Bungau, S., Ilie, M., Behl, T., Vesa, C. M., Brisc, C., Bacalbasa, N., Turi, V., Costache, R. S., & Diaconu, C. C. (2020) · Diagnostics · doi:10.3390/diagnostics10110869 · Cited by 100 · see citing works
Suenaga, M., Yu, J., Shindo, K., Tamura, K., Almario, J. A., Zaykoski, C., Witmer, P. D., Fesharakizadeh, S., Borges, M., Lennon, A.-M., et al. (2018) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-2463 · Cited by 81 · see citing works
Anderson, M. A., Zolotarevsky, E., Cooper, K. L., Sherman, S., Shats, O., Whitcomb, D. C., Lynch, H. T., Ghiorzo, P., Rubinstein, W. S., Vogel, K. J., et al. (2012) · American Journal of Gastroenterology · doi:10.1038/ajg.2012.288 · Cited by 73 · see citing works
Lucas, A. L., Frado, L. E., Hwang, C., Kumar, S., Khanna, L. G., Levinson, E. J., Chabot, J. A., Chung, W. K., & Frucht, H. (2014) · Cancer · doi:10.1002/cncr.28662 · Cited by 68 · see citing works
Cost-effectiveness of Pancreatic Cancer Surveillance in High-Risk Individuals: An Economic Analysis
Corral, J. E., Das, A., Bruno, M. J., & Wallace, M. B. (2019) · Pancreas · doi:10.1097/mpa.0000000000001268 · Cited by 66 · see citing works
Self-citationThe role of endoscopic ultrasound in pancreatic cancer screening
Bhutani, M., Koduru, P., Joshi, V., Saxena, P., Suzuki, R., Irisawa, A., & Yamao, K. (2016) · Endoscopic Ultrasound · doi:10.4103/2303-9027.175876 · Cited by 55 · see citing works
Konings, I. C. A. W., Harinck, F., Poley, J.-W., Aalfs, C. M., van Rens, A., Krak, N. C., Wagner, A., Nio, C. Y., Sijmons, R. H., van Dullemen, H. M., et al. (2017) · Pancreas · doi:10.1097/mpa.0000000000000725 · Cited by 41 · see citing works
Self-citationSheel, A. R. G., Harrison, S., Sarantitis, I., Nicholson, J. A., Hanna, T., Grocock, C., Raraty, M., Ramesh, J., Farooq, A., Costello, E., et al. (2019) · American Journal of Gastroenterology · doi:10.1038/s41395-018-0395-y · Cited by 36 · see citing works
Surveillance for neoplasia in the pancreas
Overbeek, K. A., Cahen, D. L., Canto, M. I., & Bruno, M. J. (2016) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2016.10.013 · Cited by 28 · see citing works
Self-citationRisk of Pancreatic Cancer in Patients With Pancreatic Cysts and Family History of Pancreatic Cancer
Mukewar, S. S., Sharma, A., Phillip, N., Gupta, R., Aryal-Khanal, A., de Pretis, N., Anani, V., Enders, F. T., Larson, J. J., Takahashi, N., et al. (2018) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2018.01.049 · Cited by 26 · see citing works
Prediction of Pancreatic Cancer Based on Imaging Features in Patients With Duct Abnormalities
Chen, W., Butler, R. K., Zhou, Y., Parker, R. A., Jeon, C. Y., & Wu, B. U. (2020) · Pancreas · doi:10.1097/mpa.0000000000001499 · Cited by 27 · see citing works
- Authors
- Poley, J. W., Kluijt, I., Gouma, D. J., Harinck, F., Wagner, A., Aalfs, C., van Eijck, C. H. J., Cats, A., Kuipers, E. J., Nio, Y., Fockens, P., & Bruno, M. J.
- Affiliations
- Erasmus MC (NL)
- The Netherlands Cancer Institute (NL)
- Amsterdam UMC Location University of Amsterdam (NL)
- Corresponding author
- Poley, J W
- Venue
- The American Journal of Gastroenterology
- Published
- 2009-06-02
- Volume
- 104
- Issue
- 9
- Pages
- 2175-2181
- ISSN
- 0002-9270 (ISSN-L)
- 1572-0241
- OpenAlex
- W2028828517
- Cited by
- 257
- References
- 38
- Citations by year
- 2026: 3 · 2024: 7 · 2023: 12 · 2022: 9 · 2021: 4 · 2020: 8 · 2019: 11 · 2018: 23 · 2017: 18 · 2016: 18 · 2015: 23 · 2014: 25 · 2013: 15 · 2012: 25
- FWCI
- 13.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The American Journal of Gastroenterology (publishedVersion)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion)
- Topics
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Health Sciences › Medicine › Surgery › Pancreatitis Pathology and Treatment
- Health Sciences › Medicine › Epidemiology › Neuroendocrine Tumor Research Advances
- Keywords
- pancreatic cancer screening, endoscopic ultrasound, hereditary pancreatic cancer, familial pancreatic cancer, Peutz-Jeghers syndrome, hereditary pancreatitis, BRCA1, BRCA2, TP53 mutation, intraductal papillary mucinous neoplasm, pancreatic ductal adenocarcinoma, premalignant pancreatic lesions, high-risk individuals
- MeSH terms
- Adult, Aged, Female, Humans, Male, Mass Screening, Middle Aged, Pancreatic Neoplasms, Endosonography, Genetic Predisposition to Disease
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