A Multiscale Model Evaluates Screening for Neoplasia in Barrett’s Esophagus

PLoS Computational Biology

Volumn 11, Issue 5, 2015, Pages

  Curtius, Kit ^a   Hazelton, William D ^b   Jeon, Jihyoun ^b   Luebeck, E Georg ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPSY; CELL CULTURE; CELL PROLIFERATION; CLONE CELLS; COMPUTATIONAL METHODS; DISEASES; PATIENT TREATMENT;

CLONAL EXPANSION; DISEASE BURDENS; ESOPHAGEAL TISSUES; HIGH GRADES; HISTOLOGICAL ANALYSIS; IN-SILICO; MULTI-STAGES; MULTISCALE MODELING; SCREENING MODELS; TISSUE SAMPLES;

TISSUE;

ABLATION THERAPY; ARTICLE; BARRETT ESOPHAGUS; CANCER INCIDENCE; CANCER SCREENING; CANCER THERAPY; CELL POPULATION; COMPUTER ASSISTED TOMOGRAPHY; COMPUTER MODEL; ESOPHAGUS BIOPSY; ESOPHAGUS CANCER; ESOPHAGUS DYSPLASIA; MULTISCALE CLONAL EXPANSION; PREDICTION; PROBABILITY; SENSITIVITY ANALYSIS; SPATIOTEMPORAL ANALYSIS; TUMOR CELL; ADENOCARCINOMA; ALGORITHM; BIOPSY; CALIBRATION; COMPUTER SIMULATION; ESOPHAGEAL NEOPLASMS; GASTROESOPHAGEAL REFLUX; HUMAN; INCIDENCE; MARKOV CHAIN; MASS SCREENING; PATHOPHYSIOLOGY; PREVALENCE; REPRODUCIBILITY; THEORETICAL MODEL;

ADENOCARCINOMA; ALGORITHMS; BARRETT ESOPHAGUS; BIOPSY; CALIBRATION; COMPUTER SIMULATION; ESOPHAGEAL NEOPLASMS; GASTROESOPHAGEAL REFLUX; HUMANS; INCIDENCE; MASS SCREENING; MODELS, THEORETICAL; PREVALENCE; PROBABILITY; REPRODUCIBILITY OF RESULTS; STOCHASTIC PROCESSES;

EID: 84930599391     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004272     Document Type: Article

References (43)

1. Thrift AP, Whiteman DC, (2012) The incidence of esophageal adenocarcinoma continues to rise: analysis of period and birth cohort effects on recent trends. Ann Oncol 23: 3155–3162. 22847812
2. Hur C, Miller M, Kong CY, Dowling EC, Nattinger KJ, et al. (2013) Trends in esophageal adenocarcinoma incidence and mortality. Cancer 119: 1149–1158. doi: 10.1002/cncr.27834 23303625
3. Prasad G, Bansal A, Sharma P, Wang K, (2010) Predictors of progression in Barrett’s esophagus: current knowledge and future directions. Am J Gastroenterol 105: 1490–1502. doi: 10.1038/ajg.2010.2 20104216
4. Reid BJ, Li X, Galipeau PC, Vaughan TL, (2010) Barrett’s oesophagus and oesophageal adenocarcinoma: time for a new synthesis. Nat Rev Cancer 10: 87–101. doi: 10.1038/nrc2773 20094044
5. Barrett M, Sanchez C, Prevo L, Wong D, Galipeau P, et al. (1999) Evolution of neoplastic cell lineages in Barrett oesophagus. Nat Genet 22: 106–109. doi: 10.1038/8816 10319873
6. Maley C, (2007) Multistage carcinogenesis in Barrett’s esophagus. Cancer Lett 245: 22–32. doi: 10.1016/j.canlet.2006.03.018 16713672
7. Neshat K, Sanchez C, Galipeau P, Cowan D, Ramel S, et al. (1994) Barrett’s esophagus: A model of human neoplastic progression. Cold Spring Harb Symp Quant Biol 59: 577–583. doi: 10.1101/SQB.1994.059.01.065 7587115
8. Paulson T, Maley C, Xiaohong L, (2009) Chromosomal instability and copy number alterations in Barrett’s esophagus and esophageal adenocarcinoma. Clin Cancer Res 15: 3305–3314. doi: 10.1158/1078-0432.CCR-08-2494 19417022
9. Ronkainen J, Aro P, Storskrubb T, Johansson S, Lind T, et al. (2005) Prevalence of Barrett’s esophagus in the general population: an endoscopic study. Gastroenterology 129: 1825–1831. doi: 10.1053/j.gastro.2005.08.053 16344051
10. Cameron A, Zinsmeister A, Ballard D, Carney J, (1990) Prevalence of columnar-lined (Barrett’s) esophagus. comparison of population-based clinical and autopsy findings. Gastroenterology 99: 918–922. 2394347
11. Surveillance, Epidemiology, and End Results (SEER) Program (www.seer.cancer.gov) SEER*Stat Database: Incidence—SEER 9 Regs Research Data, Nov 2013 Sub (1973–2011) Katrina/Rita Population Adjustment—Linked To County Attributes—Total U.S., 1969–2012 Counties, National Cancer Institute, DCCPS, Surveillance Research Program, Surveillance Systems Branch, released April 2014, based on the November 2013 submission.
12. Kong CY, Kroep S, Curtius K, Hazelton WD, Jeon J, et al. (2014) Exploring the recent trend in esophageal adenocarcinoma incidence and mortality using comparative simulation modeling. Cancer Epidemiol Biomarkers Prev 23: 997–1006. doi: 10.1158/1055-9965.EPI-13-1233 24692500
13. Taylor J, Rubenstein J, (2010) Meta-analyses of the effect of symptoms of gastroesophageal reflux on the risk of Barrett’s esophagus. Am J Gastroenterol 105: 1730–1737. doi: 10.1038/ajg.2010.194
14. Falk GW, Jacobson BC, Riddell RH, Rubenstein JH, El-Zimaity H, et al. (2011) Barrett’s esophagus: prevalence-incidence and etiology-origins. Ann NY Acad Sci 1232: 1–17. doi: 10.1111/j.1749-6632.2011.06042.x 21950804
15. Thrift A, Kramer J, Qureshi Z, Richardson P, El-Serag H, (2013) Age at onset of gerd symptoms predicts risk of Barrett’s esophagus. Am J Gastroenterol 108: 915–922. doi: 10.1038/ajg.2013.72 23567358
16. Jeon J, Luebeck E, Moolgavkar S, (2006) Age effects and temporal trends in adenocarcinoma of the esophagus and gastric cardia (united states). Cancer Cause Control 17: 971–981. doi: 10.1007/s10552-006-0037-3
17. Luebeck E, Curtius K, Jeon J, Hazelton W, (2013) Impact of tumor progression on cancer incidence curves. Cancer Res 73: 1086–1096. doi: 10.1158/0008-5472.CAN-12-2198 23054397
18. Gillespie D, (1977) Exact stochastic simulation of coupled chemical reactions. J Phys Chem 81: 2340–2361. doi: 10.1021/j100540a008
19. Reya T, Clevers H, (2005) Wnt signaling in stem cells and cancer. Nature 434: 843–850. doi: 10.1038/nature03319 15829953
20. Humphries A, Wright N, (2008) Colonic crypt organization and tumorigenesis. Nature 8: 415–424.
21. Kostadinov RL, Kuhner MK, Li X, Sanchez CA, Galipeau PC, et al. (2013) Nsaids modulate clonal evolution in barrett’s esophagus. PLoS Genet 9: e1003553. doi: 10.1371/journal.pgen.1003553 23785299
22. Nicolas P, Kim K, Shibata D, Tavare S, (2007) The stem cell population of the human colon crypt: Analysis via methylation patterns. PLoS Comput Biol 3: e28. doi: 10.1371/journal.pcbi.0030028 17335343
23. Yatabe Y, Tavaré S, Shibata D, (2001) Investigating stem cells in human colon by using methylation patterns. Proc Natl Acad Sci U S A 98: 10839–10844. doi: 10.1073/pnas.191225998 11517339
24. Baker AM, Cereser B, Melton S, Fletcher AG, Rodriguez-Justo M, et al. (2014) Quantification of Crypt and Stem Cell Evolution in the Normal and Neoplastic Human Colon. Cell Rep 8: 940–947. doi: 10.1016/j.celrep.2014.07.019 25127143
25. Miros M, Kerlin P, Walker N, (1991) Only patients with dysplasia progress to adenocarcinoma in Barrett’s oesophagus. Gut 32: 1441–1446. doi: 10.1136/gut.32.12.1441 1773946
26. Abela J, Going J, Mackenzie J, McKernan M, O’Mahoney M, et al. (2008) Systematic four-quadrant biopsy detects Barrett’s dysplasia in more patients than nonsystematic biopsy. Am J Gastroenterol 103: 850–855. doi: 10.1111/j.1572-0241.2007.01746.x 18371135
27. Peters F, Curvers W, Rosmolen W, de Vries C, Ten Kate F, et al. (2008) Surveillance history of endoscopically treated patients with early Barrett’s neoplasia: nonadherence to the Seattle biopsy protocol leads to sampling error. Dis Esophagus 21: 475–479. doi: 10.1111/j.1442-2050.2008.00813.x 18430186
28. Reid B, Weinstein W, Lewin K, Haggit R, VanDeventer G, et al. (1988) Endoscopic biopsy can detect high-grade dysplasia or early adenocarcinoma in Barrett’s esophagus without grossly recognizable neoplastic lesions. Gastroenterology 94: 81–90. 3335302
29. Abrams JA, Kapel RC, Lindberg GM, Saboorian MH, Genta RM, et al. (2009) Adherence to biopsy guidelines for Barrett’s esophagus surveillance in the community setting in the United States. Clin Gastroenterol Hepatol 7: 736–742. doi: 10.1016/j.cgh.2008.12.027 19268726
30. O’Connor J, Falk G, Richter J, (1999) The incidence of adenocarcinoma and dysplasia in Barrett’s esophagus report on the cleveland clinic barrett’s esophagus registry. Am J Gastroenterol 94: 2037–2042. doi: 10.1016/S0002-9270(99)00331-7 10445525
31. Conio M, Blanchi S, Lapertosa G, Ferraris R, Sablich R, et al. (2003) Long-term endoscopic surveillance of patients with Barrett’s esophagus. incidence of dysplasia and adenocarcinoma: A prospective study. Am J Gastroenterol 98: 1931–1939. doi: 10.1111/j.1572-0241.2003.07666.x 14499768
32. Sharma P, Falk G, Weston A, Reker D, Johnston M, et al. (2006) Dysplasia and cancer in a large multicenter cohort of patients with Barrett’s esophagus. Clin Gastroeneterol H 4: 566–572. doi: 10.1016/j.cgh.2006.03.001
33. Guardino J, Khandwala F, Lopez R, Wachsberger D, Richter J, et al. (2006) Barrett’s esophagus at a tertiary care center: Association of age on incidence and prevalence of dysplasia and adenocarcinoma. Am J Gastroenterol 101: 2187–2193. doi: 10.1111/j.1572-0241.2006.00736.x 17032182
34. Weston A, Badr A, Hassanein R, (1999) Prospective multivariate analysis of clinical, endoscopic, and histological factors predictive of the development of Barrett’s multifocal high-grade dysplasia or adenocarcinoma. Am J Gastroenterol 94: 3413–3419. doi: 10.1111/j.1572-0241.1999.01602.x 10606296
35. Jeon J, Meza R, Moolgavkar S, Luebeck G, (2008) Evaluation of screening strategies for pre-malignant lesions using a biomathematical approach. Math Biosci 213: 56–70. doi: 10.1016/j.mbs.2008.02.006 18374369
36. Reid B, Blount P, Feng Z, (2000) Optimizing endoscopic biopsy detection of early cancers in Barrett’s high-grade dysplasia. Am J Gastroenterol 95: 3089–3096. doi: 10.1111/j.1572-0241.2000.03182.x 11095322
37. Tschanz E, (2005) Do 40% of patients resected for Barrett esophagus with high-grade dysplasia have unsuspected adenocarcinoma? Arch Pathol Lab Med 129: 177–180. 15679415
38. Falk G, Rice T, Goldblum J, Richter J, (1999) Jumbo biopsy forceps protocol still misses unsuspected cancer in Barrett’s esophagus with high-grade dysplasia. Gastrointest Endosc 49: 170–176. doi: 10.1016/S0016-5107(99)70482-7 9925694
39. Cameron A, Carpenter H, (1997) Barrett’s esophagus, high-grade dysplasia, and early adenocarcinoma: A pathological study. Am J Gastroenterol 92: 586–591. 9128304
40. Peters JH, Clark G, Ireland AP, Chandrasoma P, Smyrk TC, et al. (1994) Outcome of adenocarcinoma arising in Barrett’s esophagus in endoscopically surveyed and nonsurveyed patients. J Thorac Cardiovasc Surg 108: 813–21. 7967662
41. Konda V, Waxman I, (2011) Low risk of prevalent submucosal invasive cancer among patients undergoing esophagectomy for treatment of Barrett’s esophagus with high grade dysplasia. J Gastrointest Oncol 2: 1–4. doi: 10.3978/j.issn.2078-6891.2011.005 22811818
42. Heitmiller R, Redmond M, Hamilton S, (1996) Barrett’s esophagus with high-grade dysplasia, an indication for prophylactic esophagectomy. Ann Surg 224: 66–71. doi: 10.1097/00000658-199607000-00010 8678620
43. (2014). URL http://www.cancer.org/.