Shuji Ogino Explained

is a molecular pathological epidemiologist, pathologist, and epidemiologist. He is currently Professor of Pathology at Harvard Medical School and Brigham and Women's Hospital, and Professor in the Department of Epidemiology at Harvard T.H. Chan School of Public Health. He is also Chief of Program in MPE Molecular Pathological Epidemiology at Brigham and Women's Hospital,[1] and an associate member of Broad Institute of MIT and Harvard.[2] He has been known for his work on establishing a new discipline, molecular pathological epidemiology (abbreviated as MPE), which represents an interdisciplinary science of molecular pathology and epidemiology.

Education, training, and positions

Ogino graduated from University of Tokyo School of Medicine, and from University of Tokyo Graduate School of Medicine. He underwent internship at U.S. Naval Hospital Okinawa in Japan from 1994 to 1995. After coming to the United States, Ogino underwent residency training in anatomic pathology and clinical pathology at Allegheny General Hospital (Drexel University) from 1995 to 1997, and at Case Western Reserve University/University Hospitals Case Medical Center from 1997 to 1999. He underwent fellowship training in molecular pathology at University of Pennsylvania Medical Center from 1999 to 2000. After postdoctoral fellowship at University of Pennsylvania, he joined Dana–Farber Cancer Institute, Brigham and Women's Hospital, and Harvard Medical School as Instructor in Pathology in 2001. Ogino was promoted to Assistant Professor in 2004, to Associate Professor in 2008, and to Professor of the institutes in 2015. He received a Master of Science in Epidemiology degree from Harvard T.H. Chan School of Public Health in 2010, and then subsequently obtained a secondary faculty appointment (Associate Professor) in 2012, promoted to Professor at that school in 2015. Ogino became Chief of Program in MPE Molecular Pathological Epidemiology at Brigham and Women's Hospital in 2016, and an associate member of Broad Institute of MIT and Harvard in 2017.

Career in MPE and colorectal cancer research

Ogino proposed that research into molecular pathology with epidemiologic settings should be regarded as a distinct field, and used the term “Molecular Pathological Epidemiology (MPE)” in 2010.[3] Since his proposal, the MPE concept and paradigm have been in widespread use,[4] [5] [6] [7] [8] [9] [10] [11] [12] [13] [14] [15] [16] [17] [18] [19] [20] and MPE has been a subject of international conferences such as American Association for Cancer Research (AACR),[21] Society for Epidemiologic Research (SER),[22] and the American Society of Preventive Oncology (ASPO).[23] The MPE approach aims to elucidate etiology of disease at molecular, individual, and population levels, applying molecular pathology to epidemiology. Utilizing tissue pathology resource and data within existing epidemiology studies, he has been publishing a large number of original articles proving the interrelationship between exposure to risk factors (e.g., environmental, dietary, lifestyle and genetic factors) and molecular pathologic signature of disease (e.g., PIK3CA mutation in colorectal cancer) including some of influential papers in the field,[24] [25] [26] [27] [28] [29] [30] [31] [32] [33] as well as papers which have developed the concepts of MPE.[34] [35] [36] [37] [38] [39] [40] [41] Ogino's discoveries with the MPE approach include the interaction between aspirin use and PIK3CA mutation in colorectal cancer,[42] and the interaction between endoscopy screening and post-colonoscopy colorectal cancer with CIMP and microsatellite instability MSI.[43] He initiated the International Molecular Pathological Epidemiology (MPE) Meeting Series in 2013,[44] and has been serving as the conference chairperson. Its second, third and fourth meetings were held in Boston, in December 2014,[45] [46] May 2016,[47] and May 2018[48] respectively.

Ogino employed the MPE concept to propose a paradigm shift in colorectal cancer research. His proposal for a transition from the two-colon concept (the proximal and distal colon)[49] [50] [51] [52] to the colorectal continuum model[53] was supported by an observed linear relationship between the location on the colon and Microsatellite instability (MSI), CpG island methylator phenotype (CIMP) and BRAF mutation frequency from the database analyses of over 1,400 colorectal cancer cases.[54] This colorectal continuum model has been supported by others.[55] [56] [57]

Ogino has introduced several new paradigms and research frameworks, including “the GWAS-MPE approach”,[58] “the unique tumor principal”,[59] “the unique disease principle”,[60] “the etiologic field effect model”,[61] "the integrative lifecourse epidemiology - MPE model",[62] “the pharmaco-MPE model”[63] and “the immunology-MPE model”,[64] all of which are related to the field of MPE.

Honors and awards

External links

Notes and References

  1. Web site: Program in Molecular Pathological Epidemiology (MPE) . Brigham and Women's Hospital . 2 September 2021.
  2. Web site: Our faculty: Associate and affiliate members . Broad Institute . 8 May 2008 . 2 September 2021.
  3. Ogino . S . Stampfer . M . 2010 . Lifestyle factors and microsatellite instability in colorectal cancer: the evolving field of molecular pathological epidemiology . J Natl Cancer Inst . 102 . 6. 365–367 . 10.1093/jnci/djq031 . 20208016 . 2841039.
  4. 10.4061/2011/902674 . 21559209 . 3090226 . CpG Island Methylation in Colorectal Cancer: Past, Present and Future . Pathology Research International . 2011 . 902674 . 2011 . Curtin . Karen . Slattery . Martha L . Samowitz . Wade S . free .
  5. 10.1186/1479-5876-10-205 . 23034130 . 3554496 . Cancer classification using the Immunoscore: A worldwide task force . Journal of Translational Medicine . 10 . 205 . 2012 . Galon . Jérôme . Pagès . Franck . Marincola . Francesco M . Angell . Helen K . Thurin . Magdalena . Lugli . Alessandro . Zlobec . Inti . Berger . Anne . Bifulco . Carlo . Botti . Gerardo . Tatangelo . Fabiana . Britten . Cedrik M . Kreiter . Sebastian . Chouchane . Lotfi . Delrio . Paolo . Arndt . Hartmann . Asslaber . Martin . Maio . Michele . Masucci . Giuseppe V . Mihm . Martin . Vidal-Vanaclocha . Fernando . Allison . James P . Gnjatic . Sacha . Hakansson . Leif . Huber . Christoph . Singh-Jasuja . Harpreet . Ottensmeier . Christian . Zwierzina . Heinz . Laghi . Luigi . Grizzi . Fabio . 29 . free .
  6. 10.1038/modpathol.2012.62 . 22522846 . Gene discovery in familial cancer syndromes by exome sequencing: Prospects for the elucidation of familial colorectal cancer type X . Modern Pathology . 25 . 8 . 1055–68 . 2012 . Ku . Chee-Seng . Cooper . David N . Wu . Mengchu . Roukos . Dimitrios H . Pawitan . Yudi . Soong . Richie . Iacopetta . Barry . free .
  7. 10.1016/j.annepidem.2012.03.001 . 22481034 . 3596808 . Can Tissue-Based Immune Markers be Used for Studying the Natural History of Cancer? . Annals of Epidemiology . 22 . 7 . 520–30 . 2012 . Koshiol . Jill . Lin . Shih-Wen. Jill Koshiol.
  8. Fini L, Grizzi F, Laghi L (2012). Ettarh R, ed. Adaptive and Innate Immunity, Non Clonal Players in Colorectal Cancer Progression. InTech. pp. 323–40. .
  9. 10.1158/1078-0432.CCR-11-3265 . 23014527 . 3500422 . Molecular Epidemiology of EGFR and KRAS Mutations in 3,026 Lung Adenocarcinomas: Higher Susceptibility of Women to Smoking-Related KRAS-Mutant Cancers . Clinical Cancer Research . 18 . 22 . 6169–77 . 2012 . Dogan . S . Shen . R . Ang . D. C . Johnson . M. L . d'Angelo . S. P . Paik . P. K . Brzostowski . E. B . Riely . G. J . Kris . M. G . Zakowski . M. F . Ladanyi . M .
  10. 10.1158/2159-8290.CD-12-0424 . 23230187 . 3531829 . Integrative Cancer Epidemiology--The Next Generation . Cancer Discovery . 2 . 12 . 1087–90 . 2012 . Spitz . M. R . Caporaso . N. E . Sellers . T. A .
  11. 10.1016/j.jmoldx.2012.06.007 . 23127612 . Conventional and Nanotechniques for DNA Methylation Profiling . The Journal of Molecular Diagnostics . 15 . 1 . 17–26 . 2013 . Shanmuganathan . Rajasree . Basheer . Nazeema B . Amirthalingam . Laxmi . Muthukumar . Harshiny . Kaliaperumal . Rajendran . Shanmugam . Kumaran . free .
  12. 10.1158/0008-5472.CAN-12-4306 . 23801749 . The CpG Island Methylator Phenotype: What's in a Name? . Cancer Research . 73 . 19 . 5858–68 . 2013 . Hughes . L. A. E . Melotte . V . De Schrijver . J . De Maat . M . Smit . V. T. H. B. M . Bovee . J. V. M. G . French . P. J . Van Den Brandt . P. A . Schouten . L. J . De Meyer . T . Van Criekinge . W . Ahuja . N . Herman . J. G . Weijenberg . M. P . Van Engeland . M . free .
  13. 10.1016/j.canlet.2014.02.026 . 24614287 . Cellular metabolism in colorectal carcinogenesis: Influence of lifestyle, gut microbiome and metabolic pathways . Cancer Letters . 356 . 2 . 273–80 . 2015 . Hagland . Hanne R . Søreide . Kjetil . free . 1956/8817 . free .
  14. 10.3748/wjg.v20.i20.6055 . 24876728 . 4033445 . Epidemiological transition of colorectal cancer in developing countries: Environmental factors, molecular pathways, and opportunities for prevention . World Journal of Gastroenterology . 20 . 20 . 6055–72 . 2014 . Bishehsari . Faraz . Mahdavinia . M . Vacca . M . Malekzadeh . R . Mariani-Costantini . R . free .
  15. Hughes LAE, Simons CCJM, van den Brandt PA, van Engeland M, Weijenberg MP. Lifestyle, Diet, and Colorectal Cancer Risk According to (Epi)genetic Instability: Current Evidence and Future Directions of Molecular Pathological Epidemiology. Curr Colorectal Cancer Rep. 2017;13(6):455-469.
  16. 10.3390/molecules22010105 . Bioactive Nutrients and Nutrigenomics in Age-Related Diseases . Molecules . 22 . 105 . 2017 . Rescigno . Tania . Micolucci . Luigina . Tecce . Mario . Capasso . Anna . 1 . 6155887 . 28075340. free .
  17. 10.1016/j.bbcan.2016.08.002 . Aspirin in pancreatic cancer: Chemopreventive effects and therapeutic potentials . Biochimica et Biophysica Acta (BBA) - Reviews on Cancer . 1866 . 2 . 163–76 . 2016 . Jiang . Ming-jie . Dai . Juan-Juan . Gu . Dian-na . Huang . Qian . Tian . Ling . 27567928 .
  18. 10.1186/s12967-016-0772-5 . Obesity and colorectal cancer: Molecular features of adipose tissue . Journal of Translational Medicine . 14 . 2016 . Martinez-Useros . Javier . Garcia-Foncillas . Jesus . 21 . 4722674 . 26801617 . free .
  19. 10.1080/17460441.2017.1271321 . 27960558 . Developing drugs that target the Wnt pathway: Recent approaches in cancer and neurodegenerative diseases . Expert Opinion on Drug Discovery . 12 . 2 . 169–186 . 2016 . Serafino . Annalucia . Sferrazza . Gianluca . Colini Baldeschi . Arianna . Nicotera . Giuseppe . Andreola . Federica . Pittaluga . Eugenia . Pierimarchi . Pasquale . 205918130 .
  20. 10.1007/s10654-017-0253-z . 28497292 . Cancer subtypes in aetiological research . European Journal of Epidemiology . 32 . 5 . 353–361 . 2017 . Richiardi . Lorenzo . Barone-Adesi . Francesco . Pearce . Neil . 3940690 .
  21. Ogino S. Molecular pathological epidemiology (MPE): Overview of its paradigm and wide applicability even without tumor tissue. In: Proceedings of the Twelfth Annual AACR International Conference on Frontiers in Cancer Prevention Research; 2013 Oct 27-30; National Harbor, MD. Cancer Prev Res (Phila). 2013;6(11 suppl):CN06-1.
  22. Kuller . LH . Bracken . MB . Ogino . S . Prentice . RL . Tracy . RP . 2013 . The role of epidemiology in the era of molecular epidemiology and genomics: Summary of the 2013 AJE-sponsored Society of Epidemiologic Research Symposium . Am J Epidemiol . 178 . 9. 1350–4 . 10.1093/aje/kwt239 . 24105654 . 3988450 .
  23. 10.1158/1055-9965.EPI-14-0848 . 25277796 . 4221505 . Challenges and Opportunities in International Molecular Cancer Prevention Research: An ASPO Molecular Epidemiology and the Environment and International Cancer Prevention Interest Groups Report . Cancer Epidemiology, Biomarkers & Prevention . 23 . 11 . 2613–7 . 2014 . Epplein . M . Bostick . R. M . Mu . L . Ogino . S . Braithwaite . D . Kanetsky . P. A .
  24. Chan . AT . Ogino . S . Fuchs . CS . 2007 . Aspirin use and risk of colorectal cancer according to cyclooxygenase-2 expression . N Engl J Med . 356 . 21. 2131–42 . 10.1056/nejmoa067208. 17522398 . 38606047 . free .
  25. Chan . AT . Ogino . S . Fuchs . CS . 2009 . Aspirin use and survival after diagnosis of colorectal cancer . JAMA . 302 . 6. 649–658 . 10.1001/jama.2009.1112. 19671906 . 2848289 . free .
  26. Morikawa . T . Kuchiba . A . Yamauchi . M . Meyerhardt . JA . Shima . K . Nosho . K . Chan . AT . Giovannucci . E . Fuchs . CS . Ogino . S . 2011 . Association of CTNNB1 (β-catenin) alterations, body mass index, and physical activity with survival in patients with colorectal cancer . JAMA . 305 . 16. 1685–1694 . 3087286. 10.1001/jama.2011.513 . 21521850.
  27. Straussman . R . Morikawa . T . Shee . K . Barzily-Rokni . M . Qian . ZR . Du . J . Davis . A . Mongare . MM . Gould . J . Frederick . DT . Cooper . ZA . Chapman . PB . Solit . DB . Ribas . A . Lo . RS . Flaherty . KT . Ogino . S . Wargo . JA . Golub . TR . 2012 . Tumor microenvironment contributes to innate RAF-inhibitor resistance through HGF secretion . Nature . 487 . 7408. 500–504 . 3711467 . 22763439 . 10.1038/nature11183 .
  28. Nishihara . R . Lochhead . P . Kuchiba . A . Jung . S . Yamauchi . M . Liao . X . Imamura . Y . Qian . ZR . Morikawa . T . Wang . M . Spiegelman . D . Cho . E . Giovannucci . E . Fuchs . CS . Chan . AT . Ogino . S . 2013 . Aspirin use and colorectal cancer incidence risk according to BRAF mutation status . JAMA . 309 . 24. 2563–2571 . 10.1001/jama.2013.6599. 23800934 . 3743040 . free .
  29. Ogino . S . Liao . X . Imamura . Y . Yamauchi . M . McCleary . NJ . Ng . K . Niedzwiecki . D . Saltz . LB . Mayer . RJ . Whittom . R . Hantel . A . Benson . III AB . Mowat . RB . Spiegelman . D . Goldberg . RM . Bertagnolli . MM . Meyerhardt . JA . Fuchs . CS . 2013 . Predictive and prognostic analysis of PIK3CA mutation in stage III colon cancer intergroup trial . J Natl Cancer Inst . 105 . 23. 1789–1798 . 10.1093/jnci/djt298. 24231454 . 3848984 . free .
  30. Barry . ER . Morikawa . T . Butler . BL . Shrestha . K . de la Rosa . R . Yan . KS . Fuchs . CS . Magness . ST . Smits . R . Ogino . S . Kuo . CJ . Camargo . FD . 2013 . Restriction of intestinal stem cell expansion and the regenerative response by YAP . Nature . 493 . 7430. 106–110 . 3536889 . 23178811 . 10.1038/nature11693 . 2013Natur.493..106B .
  31. Fink SP, Yamauchi M, Nishihara R, Jung S, Kuchiba A, Wu K, Cho E, Giovannucci E, Fuchs CS, Ogino S, Markowitz SD, Chan AT. "Aspirin and the risk of colorectal cancer in relation to the expression of 15-hydroxyprostaglandin dehydrogenase (HPGD). Sci Transl Med 2014;6:233re2.
  32. Mehta . RS . Nishihara . R . Cao . Y . Song . M . Mima . K . Qian . ZR . Nowak . JA . Kosumi . K . Hamada . T . Masugi . Y . Bullman . S . Drew . DA . Kostic . AD . Fung . TT . Garrett . WS . Huttenhower . C . Wu . K . Meyerhardt . JA . Zhang . X . Willett . WC . Giovannucci . EL . Fuchs . CS . Chan . AT . Ogino . S . 2017 . Dietary patterns and risk of colorectal cancer subtypes classified by Fusobacterium nucleatum in tumor tissue . JAMA Oncol . 3 . 7. 921–927 . 10.1001/jamaoncol.2016.6374. 28125762 . 5502000 . free .
  33. Hamada . T . Cao . Y . Qian . ZR . Masugi . Y . Nowak . JA . Yang . J . Song . M . Mima . K . Kosumi . K . Liu . L . Shi . Y . Silva Ad . Gu M . Li . W . Keum . N . Zhang . X . Wu . K . Meyerhardt . JA . Giovannucci . EL . Giannakis . M . Rodig . SJ . Freeman . GJ . Nevo . D . Wang . M . Chan . AT . Fuchs . CS . Nishihara . R . Ogino . S . 2017 . Aspirin use and colorectal cancer survival according to tumor CD274 (programmed cell death 1 ligand 1) expression status . J Clin Oncol . 35 . 16. 1836–1844 . 10.1200/jco.2016.70.7547. 5455595 . 28406723 .
  34. Ogino . S . Galon . J . Fuchs . CS . Dranoff . G . Cancer immunology – integrated analysis of host and tumor factors for personalized medicine . Nat Rev Clin Oncol . 2011 . 8. 711–719 .
  35. Ogino . S . King . EE . Beck . AH . Sherman . ME . Milner . DA . Giovannucci . E . 2012 . Interdisciplinary education to integrate pathology and epidemiology: Towards molecular and population-level health science . Am J Epidemiol . 176 . 8. 659–667 . 10.1093/aje/kws226 . 22935517 . 3571252.
  36. Ogino . S . Giovannucci . E . 2012 . Lifestyle factors and colorectal cancer microsatellite instability – Molecular pathological epidemiology science, based on unique tumour principle . Int J Epidemiol . 41 . 4. 1072–1074 . 10.1093/ije/dys076. 22596930 . 3429874 . free .
  37. Ogino . S . Fuchs . CS . Giovannucci . E . 2012 . How many molecular subtypes? Implications of the unique tumor principle in personalized medicine . Expert Rev Mol Diagn . 12 . 6. 621–628 . 10.1586/erm.12.46 . 22845482 . 3492839.
  38. Ogino . S . Lochhead . P . Chan . AT . Nishihara . R . Cho . E . Wolpin . BM . Meyerhardt . JA . Meissner . A . Schernhammer . ES . Fuchs . CS . Giovannucci . E . 2013 . Molecular pathological epidemiology of epigenetics: emerging integrative science to analyze environment, host, and disease . Modern Pathology . 26 . 4. 465–84 . 10.1038/modpathol.2012.214 . 23307060 . 3637979.
  39. Field . AE . Camargo Jr . CA . Ogino . 2013 . one size does not fit all . JAMA . 310 . 20. 2147–2148 . 10.1001/jama.2013.281501. 24189835 .
  40. Ogino . S . Lochhead . P . Giovannucci . E . Meyerhardt . JA . Fuchs . CS . Chan . AT . 2014 . Discovery of colorectal cancer PIK3CA mutation as potential predictive biomarker: power and promise of molecular pathological epidemiology . Oncogene . 33 . 23. 2949–2955 . 10.1038/onc.2013.244 . 23792451 . 3818472.
  41. Lochhead . P . Chan . AT . Giovannucci . E . Fuchs . CS . Wu . K . Nishihara . R . O'Brien . M . Ogino . S . 2014 . Progress and opportunities in molecular pathological epidemiology of colorectal premalignant lesions . Am J Gastroenterol . 109 . 8. 1205–1214 . 10.1038/ajg.2014.153. 4125459 . 24935274 .
  42. Liao . X . Lochhead . P . Nishihara . R . Morikawa . T . Kuchiba . A . Yamauchi . M . Imamura . Y . Qian . ZR . Baba . Y . Shima . K . Sun . R . Nosho . K . Meyerhardt . JA . Giovannucci . E . Fuchs . CS . Chan . AT . Ogino . S . 2012 . Aspirin use, tumor PIK3CA mutation, and colorectal-cancer survival . N Engl J Med . 367 . 17. 1596–1606 . 10.1056/NEJMoa1207756 . 23094721 . 3532946 .
  43. Nishihara . R . Wu . K . Lochhead . P . Morikawa . T . Liao . X . Qian . ZR . Inamura . K . Kim . SA . Kuchiba . A . Yamauchi . M . Imamura . Y . Willett . WC . Rosner . BA . Fuchs . CS . Giovannucci . E . Ogino . S . Chan . AT . 2013 . Long-term colorectal-cancer incidence and mortality after lower endoscopy . N Engl J Med . 369 . 12. 1095–1105 . 10.1056/nejmoa1301969. 3840160 . 24047059 .
  44. Web site: 1st International MPE Meeting . Harvard T.H. Chan School of Public Health . 26 February 2019 . 2 September 2021.
  45. Web site: Ogino MPE Lab . Dana–Farber Cancer Institute . 2 September 2021 . https://web.archive.org/web/20180813000556/http://ogino-mpe-lab.dana-farber.org/ . 13 August 2018 . dead.
  46. 10.1007/s10552-015-0596-2 . 25956270 . 4466011 . Proceedings of the second international molecular pathological epidemiology (MPE) meeting . Cancer Causes & Control . 26 . 7 . 959–72 . 2015 . Ogino . Shuji . Campbell . Peter T . Nishihara . Reiko . Phipps . Amanda I . Beck . Andrew H . Sherman . Mark E . Chan . Andrew T . Troester . Melissa A . Bass . Adam J . Fitzgerald . Kathryn C . Irizarry . Rafael A . Kelsey . Karl T . Nan . Hongmei . Peters . Ulrike . Poole . Elizabeth M . Qian . Zhi Rong . Tamimi . Rulla M . Tchetgen Tchetgen . Eric J . Tworoger . Shelley S . Zhang . Xuehong . Giovannucci . Edward L . Van Den Brandt . Piet A . Rosner . Bernard A . Wang . Molin . Chatterjee . Nilanjan . Begg . Colin B .
  47. 10.1007/s10552-016-0845-z . 28097472 . 5303153 . Proceedings of the third international molecular pathological epidemiology (MPE) meeting . Cancer Causes & Control . 28 . 2 . 167–176 . 2017 . Campbell . Peter T . Rebbeck . Timothy R . Nishihara . Reiko . Beck . Andrew H . Begg . Colin B . Bogdanov . Alexei A . Cao . Yin . Coleman . Helen G . Freeman . Gordon J . Heng . Yujing J . Huttenhower . Curtis . Irizarry . Rafael A . Kip . N. Sertac . Michor . Franziska . Nevo . Daniel . Peters . Ulrike . Phipps . Amanda I . Poole . Elizabeth M . Qian . Zhi Rong . Quackenbush . John . Robins . Harlan . Rogan . Peter K . Slattery . Martha L . Smith-Warner . Stephanie A . Song . Mingyang . Vanderweele . Tyler J . Xia . Daniel . Zabor . Emily C . Zhang . Xuehong . Wang . Molin . 29 .
  48. Campbell . Peter T. . Ambrosone . Christine B. . Nishihara . Reiko . Aerts . Hugo J.W.L. . Bondy . Melissa . Chatterjee . Nilanjan . Garcia-Closas . Montserrat . Giannakis . Marios . Golden . Jeffrey A. . Heng . Yujing J. . Sertac Kip . N. . Koshiol . Jill . Shirley Liu . X. . Lopes-Ramos . Camila M. . Mucci . Lorelei A. . Nowak . Jonathan A. . Phipps . Amanda I. . Quackenbush . John . Schoen . Robert E. . Sholl . Lynette M. . Tamimi . Rulla M. . Wang . Molin . Weijenberg . Matty P. . Wu . Catherine J. . Wu . Kana . Yao . Song . Yu . Kun-Hsing . Zhang . Xuehong . Rebbeck . Timothy R. . Ogino . Shuji . Proceedings of the fourth international molecular pathological epidemiology (MPE) meeting . Cancer Causes & Control . 2019 . 30 . 8 . 799–811 . 10.1007/s10552-019-01177-z . 31069578 . 6614001 .
  49. 10.1002/ijc.10635 . 12216066 . Are there two sides to colorectal cancer? . International Journal of Cancer . 101 . 5 . 403–8 . 2002 . Iacopetta . Barry . 25714067 . free .
  50. 10.1002/jso.20156 . 15565587 . Two colons-two cancers: Paradigm shift and clinical implications . Journal of Surgical Oncology . 88 . 4 . 261–6 . 2004 . Gervaz . Pascal . Bucher . Pascal . Morel . Philippe . 23197513 .
  51. 10.1053/j.gastro.2011.06.029 . 21708155 . 3424279 . One Colon Lumen but Two Organs . Gastroenterology . 141 . 2 . 411–2 . 2011 . Carethers . John M .
  52. 10.1016/j.bbcan.2011.07.005 . 21855610 . Colorectal cancers choosing sides . Biochimica et Biophysica Acta (BBA) - Reviews on Cancer . 1816 . 2 . 219–31 . 2011 . Albuquerque . Cristina . Bakker . Elvira R.M . Van Veelen . Wendy . Smits . Ron . free .
  53. 10.1136/gutjnl-2013-305209 . 23749607 . Colorectal cancer: Dichotomous or continuum model? Perhaps, a combination of both: Table 1 . Gut . 62 . 10 . 1519–20 . 2013 . Papagiorgis . Petros . 390756 . free .
  54. 10.1136/gutjnl-2011-300865 . 22427238 . 3345105 . Assessment of colorectal cancer molecular features along bowel subsites challenges the conception of distinct dichotomy of proximal versus distal colorectum . Gut . 61 . 6 . 847–54 . 2012 . Yamauchi . Mai . Morikawa . Teppei . Kuchiba . Aya . Imamura . Yu . Qian . Zhi Rong . Nishihara . Reiko . Liao . Xiaoyun . Waldron . Levi . Hoshida . Yujin . Huttenhower . Curtis . Chan . Andrew T . Giovannucci . Edward . Fuchs . Charles . Ogino . Shuji .
  55. 10.1136/bmjopen-2013-002608 . 23793665 . 3657647 . A nationwide Danish cohort study challenging the categorisation into right-sided and left-sided colon cancer . BMJ Open . 3 . 5 . e002608 . 2013 . Jess . Per . Hansen . Iben Onsberg . Gamborg . Michael . Jess . Tine .
  56. 10.1136/gutjnl-2013-305209 . 23749607 . Colorectal cancer: Dichotomous or continuum model? Perhaps, a combination of both: Table 1 . Gut . 62 . 10 . 1519–20 . 2013 . Papagiorgis . Petros . 390756 . free .
  57. 10.1158/1078-0432.CCR-17-2484 . 29180604 . 5844818 . Classifying Colorectal Cancer by Tumor Location Rather than Sidedness Highlights a Continuum in Mutation Profiles and Consensus Molecular Subtypes . Clinical Cancer Research . 24 . 5 . 1062–1072 . 2018 . Loree . Jonathan M . Pereira . Allan A.L . Lam . Michael . Willauer . Alexandra N . Raghav . Kanwal . Dasari . Arvind . Morris . Van. K . Advani . Shailesh . Menter . David G . Eng . Cathy . Shaw . Kenna . Broaddus . Russell . Routbort . Mark J . Liu . Yusha . Morris . Jeffrey S . Luthra . Rajyalakshmi . Meric-Bernstam . Funda . Overman . Michael J . Maru . Dipen . Kopetz . Scott .
  58. 10.1136/gut.2010.217182 . 21036793 . 3040598 . Molecular pathological epidemiology of colorectal neoplasia: An emerging transdisciplinary and interdisciplinary field . Gut . 60 . 3 . 397–411 . 2010 . Ogino . S . Chan . A. T . Fuchs . C. S . Giovannucci . E .
  59. 10.1586/erm.12.46 . 22845482 . 3492839 . How many molecular subtypes? Implications of the unique tumor principle in personalized medicine . Expert Review of Molecular Diagnostics . 12 . 6 . 621–8 . 2014 . Ogino . Shuji . Fuchs . Charles S . Giovannucci . Edward .
  60. 10.1038/modpathol.2012.214 . 23307060 . 3637979 . Molecular pathological epidemiology of epigenetics: Emerging integrative science to analyze environment, host and disease . Modern Pathology . 26 . 4 . 465–84 . 2013 . Ogino . Shuji . Lochhead . Paul . Chan . Andrew T . Nishihara . Reiko . Cho . Eunyoung . Wolpin . Brian M . Meyerhardt . Jeffrey A . Meissner . Alexander . Schernhammer . Eva S . Fuchs . Charles S . Giovannucci . Edward . .
  61. 10.1038/modpathol.2014.81 . 24925058 . 4265316 . Etiologic field effect: Reappraisal of the field effect concept in cancer predisposition and progression . Modern Pathology . 28 . 1 . 14–29 . 2014 . Lochhead . Paul . Chan . Andrew T . Nishihara . Reiko . Fuchs . Charles S . Beck . Andrew H . Giovannucci . Edward . Ogino . Shuji .
  62. Nishi . A . Kawachi . I . Koenen . KC . Wu . K . Nishihara . R . Ogino . S . 2015 . Lifecourse epidemiology and molecular pathological epidemiology . Am J Prev Med . 48 . 1. 116–119 . 10.1016/j.amepre.2014.09.031. 4274745 . 25528613 .
  63. 10.1038/s41698-017-0042-x . Integration of pharmacology, molecular pathology, and population data science to support precision gastrointestinal oncology . npj Precision Oncology . 1 . 2017 . Ogino . Shuji . Jhun . Iny . Mata . Douglas A . Soong . Thing Rinda . Hamada . Tsuyoshi . Liu . Li . Nishihara . Reiko . Giannakis . Marios . Cao . Yin . Manson . Joann E . Nowak . Jonathan A . Chan . Andrew T . 29552640 . 5856171 . free .
  64. Ogino . S . Nishihara . R . VanderWeele . TJ . Wang . M . Nishi . A . Lochhead . P . Qian . ZR . Zhang . X . Wu . K . Nan . H . Yoshida . K . Milner . DA . Chan . AT . Field . AE . Camargo . CA . Williams . MA . Giovannucci . EL . 2016 . The role of molecular pathological epidemiology in the study of neoplastic and non-neoplastic diseases in the era of precision medicine . Epidemiology . 27 . 4. 602–611 . 10.1097/ede.0000000000000471. 4892980 . 26928707 .
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