Cited by 24Extracellular vesicles in diseaseMicroRNA in disease regulationCancer Genomics and Diagnostics

Diagnostic Potential of Exosomal microRNAs in Colorectal Cancer

Open access
Dohmen, Jonas, Semaan, Alexander, Kobilay, Makbule, Zaleski, Martin, Branchi, Vittorio, Schlierf, Anja, Hettwer, Karina, Uhlig, Steffen +5 more·2022·Diagnostics

Abstract

Background: Despite the significance of colonoscopy for early diagnosis of colorectal adenocarcinoma (CRC), population-wide screening remains challenging, mainly because of low acceptance rates. Herein, exosomal (exo-miR) and free circulating microRNA (c-miR) may be used as liquid biopsies in CRC to identify individuals at risk. Direct comparison of both compartments has shown inconclusive results, which is why we directly compared a panel of 10 microRNAs in this entity. Methods: Exo-miR and c-miR levels were measured using real-time quantitative PCR after isolation from serum specimens in a cohort of 69 patients. Furthermore, results were compared to established tumor markers CEA and CA 19-9. Results: Direct comparison of exo- and c-miR biopsy results showed significantly higher microRNA levels in the exosomal compartment (p < 0.001). Exo-Let7, exo-miR-16 and exo-miR-23 significantly differed between CRC and healthy controls (all p < 0.05), while no c-miR showed this potential. Sensitivity and specificity can be further enhanced using combinations of multiple exosomal miRNAs. Conclusions: Exosomal microRNA should be considered as a promising biomarker in CRC for future studies. Nonetheless, results may show interference with common comorbidities, which must be taken into account in future studies.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/diagnostics12061413

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • miR-23 expression is upregulated in colorectal cancer and gastric cancer patients, including in serum exosomes, blood tissues, and gastric cancer tissues.

    “upregulation of miR-23 expression has been detected in both colorectal cancer and gastric cancer patients, such as in serum exosomes, blood tissues, and gastric cancer tissues [[78], [79], [80]].”

    From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [78]

    The Results (§3.2; page not provided) report significantly higher exosomal miR-23 in colorectal cancer patients than in healthy controls. The Discussion (§4; page not provided) also notes reports of elevated miR-23 in cancer tissue and serum, but this paper does not establish the claim about gastric cancer patients, blood tissues, or gastric cancer tissues. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 76 · Cited by 24

Research works printed but not linked: 70

  1. [1]Sung H. Ferlay J. Siegel R.L. Laversanne M. Soerjomataram I. Jemal A. Bray F. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries CA Cancer J. Clin. 2021 71 209 249 10.3322/caac.21660 33538338 · DOI · Paper page
  2. [2]Fearon E.R. Molecular genetics of colorectal cancer Annu. Rev. Pathol. 2011 6 479 507 10.1146/annurev-pathol-011110-130235 21090969 · DOI · Paper page
  3. [3]Brenner H. Kloor M. Pox C.P. Colorectal cancer Lancet 2014 383 1490 1502 10.1016/S0140-6736(13)61649-9 24225001 · DOI
  4. [4]Burch J.A. Soares-Weiser K. St John D.J. Duffy S. Smith S. Kleijnen J. Westwood M. Diagnostic accuracy of faecal occult blood tests used in screening for colorectal cancer: A systematic review J. Med. Screen 2007 14 132 137 10.1258/096914107782066220 17925085 · DOI
  5. [5]Robertson D.J. Lee J.K. Boland C.R. Dominitz J.A. Giardiello F.M. Johnson D.A. Kaltenbach T. Lieberman D. Levin T.R. Rex D.K. Recommendations on Fecal Immunochemical Testing to Screen for Colorectal Neoplasia: A Consensus Statement by the US Multi-Society Task Force on Colorectal Cancer Gastroenterology 2017 152 1217 1237 10.1053/j.gastro.2016.08.053 27769517 · DOI
  6. [6]Lieberman D.A. Clinical practice. Screening for colorectal cancer N. Engl. J. Med. 2009 361 1179 1187 10.1056/NEJMcp0902176 19759380 · DOI
  7. [7]Burt R.W. Barthel J.S. Dunn K.B. David D.S. Drelichman E. Ford J.M. Giardiello F.M. Gruber S.B. Halverson A.L. Hamilton S.R. NCCN clinical practice guidelines in oncology. Colorectal cancer screening JNCCN J. Natl. Compr. Cancer Netw. 2010 8 8 61 10.6004/jnccn.2010.0003 20064289 · DOI
  8. [8]Schmoll H.J. Van Cutsem E. Stein A. Valentini V. Glimelius B. Haustermans K. Nordlinger B. van de Velde C.J. Balmana J. Regula J. ESMO Consensus Guidelines for management of patients with colon and rectal cancer. a personalized approach to clinical decision making Ann. Oncol. 2012 23 2479 2516 10.1093/annonc/mds236 23012255 · DOI
  9. [9]Duffy M.J. van Dalen A. Haglund C. Hansson L. Holinski-Feder E. Klapdor R. Lamerz R. Peltomaki P. Sturgeon C. Topolcan O. Tumour markers in colorectal cancer: European Group on Tumour Markers (EGTM) guidelines for clinical use Eur. J. Cancer 2007 43 1348 1360 10.1016/j.ejca.2007.03.021 17512720 · DOI
  10. [10]Mokhles S. Macbeth F. Farewell V. Fiorentino F. Williams N.R. Younes R.N. Takkenberg J.J. Treasure T. Meta-analysis of colorectal cancer follow-up after potentially curative resection Br. J. Surg. 2016 103 1259 1268 10.1002/bjs.10233 27488593 PMC5031212 · DOI
  11. [11]Diaz L.A. Jr. Bardelli A. Liquid biopsies: Genotyping circulating tumor DNA J. Clin. Oncol. 2014 32 579 586 10.1200/JCO.2012.45.2011 24449238 PMC4820760 · DOI · Paper page
  12. [12]Iwakawa H.O. Tomari Y. The Functions of MicroRNAs: mRNA Decay and Translational Repression Trends Cell Biol. 2015 25 651 665 10.1016/j.tcb.2015.07.011 26437588 · DOI
  13. [13]Hollis M. Nair K. Vyas A. Chaturvedi L.S. Gambhir S. Vyas D. MicroRNAs potential utility in colon cancer: Early detection, prognosis, and chemosensitivity World J. Gastroenterol. 2015 21 8284 8292 10.3748/wjg.v21.i27.8284 26217080 PMC4507098 · DOI
  14. [14]Cekaite L. Eide P.W. Lind G.E. Skotheim R.I. Lothe R.A. MicroRNAs as growth regulators, their function and biomarker status in colorectal cancer Oncotarget 2016 7 6476 6505 10.18632/oncotarget.6390 26623728 PMC4872728 · DOI
  15. [15]Yan L. Zhao W. Yu H. Wang Y. Liu Y. Xie C. A Comprehensive Meta-Analysis of MicroRNAs for Predicting Colorectal Cancer Medicine 2016 95 e2738 10.1097/MD.0000000000002738 26945359 PMC4782843 · DOI
  16. [16]Zeng W. Tu Y. Zhu Y. Wang Z. Li C. Lao L. Wu G. Predictive power of circulating miRNAs in detecting colorectal cancer Tumour Biol. 2015 36 2559 2567 10.1007/s13277-014-2872-2 25527153 · DOI
  17. [17]Thery C. Cancer: Diagnosis by extracellular vesicles Nature 2015 523 161 162 10.1038/nature14626 26106856 · DOI
  18. [18]Hingorani S.R. Intercepting Cancer Communiques: Exosomes as Heralds of Malignancy Cancer Cell 2015 28 151 153 10.1016/j.ccell.2015.07.015 26267532 · DOI
  19. [19]Matsumura T. Sugimachi K. Iinuma H. Takahashi Y. Kurashige J. Sawada G. Ueda M. Uchi R. Ueo H. Takano Y. Exosomal microRNA in serum is a novel biomarker of recurrence in human colorectal cancer Br. J. Cancer 2015 113 275 281 10.1038/bjc.2015.201 26057451 PMC4506387 · DOI
  20. [20]Lin J. Li J. Huang B. Liu J. Chen X. Chen X.M. Xu Y.M. Huang L.F. Wang X.Z. Exosomes: Novel biomarkers for clinical diagnosis Sci. World J. 2015 2015 657086 10.1155/2015/657086 PMC4322857 25695100 · DOI
  21. [21]Brinton L.T. Sloane H.S. Kester M. Kelly K.A. Formation and role of exosomes in cancer Cell Mol. Life Sci. 2015 72 659 671 10.1007/s00018-014-1764-3 25336151 PMC5489338 · DOI
  22. [22]Melo S.A. Luecke L.B. Kahlert C. Fernandez A.F. Gammon S.T. Kaye J. LeBleu V.S. Mittendorf E.A. Weitz J. Rahbari N. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer Nature 2015 523 177 182 10.1038/nature14581 26106858 PMC4825698 · DOI · Paper page
  23. [23]El Andaloussi S. Mager I. Breakefield X.O. Wood M.J. Extracellular vesicles: Biology and emerging therapeutic opportunities Nat. Rev. Drug. Discov. 2013 12 347 357 10.1038/nrd3978 23584393 · DOI · Paper page
  24. [24]Taverna S. Giallombardo M. Pucci M. Flugy A. Manno M. Raccosta S. Rolfo C. De Leo G. Alessandro R. Curcumin inhibits in vitro and in vivo chronic myelogenous leukemia cells growth: A possible role for exosomal disposal of miR-21 Oncotarget 2015 6 21918 21933 10.18632/oncotarget.4204 26116834 PMC4673136 · DOI
  25. [26]Zhu M. Huang Z. Zhu D. Zhou X. Shan X. Qi L.W. Wu L. Cheng W. Zhu J. Zhang L. A panel of microRNA signature in serum for colorectal cancer diagnosis Oncotarget 2017 8 17081 17091 10.18632/oncotarget.15059 28177881 PMC5370024 · DOI
  26. [27]Nedaeinia R. Manian M. Jazayeri M.H. Ranjbar M. Salehi R. Sharifi M. Mohaghegh F. Goli M. Jahednia S.H. Avan A. Circulating exosomes and exosomal microRNAs as biomarkers in gastrointestinal cancer Cancer Gene Ther. 2017 24 48 56 10.1038/cgt.2016.77 27982021 · DOI
  27. [28]Uratani R. Toiyama Y. Kitajima T. Kawamura M. Hiro J. Kobayashi M. Tanaka K. Inoue Y. Mohri Y. Mori T. Diagnostic Potential of Cell-Free and Exosomal MicroRNAs in the Identification of Patients with High-Risk Colorectal Adenomas PLoS ONE 2016 11 e0160722 10.1371/journal.pone.0160722 27760147 PMC5070810 · DOI
  28. [29]Nagtegaal I. Arends M. Salto-Tellez M. Colorectal Adenocarcinoma: Tumours of the Colon and Rectum World Health Organization Classification of Tumours of the Digestive System IARC Press Basel, Switzerland 2019 177 187
  29. [30]Brierley J.D. Gospodarowicz M.K. Wittekind C. TNM Classification of Malignant Tumours John Wiley & Sons Hoboken, NY, USA 2016
  30. [31]Conteduca V. Sansonno D. Russi S. Dammacco F. Precancerous colorectal lesions (Review) Int. J. Oncol. 2013 43 973 984 10.3892/ijo.2013.2041 23900573 · DOI
  31. [32]King C.E. Wang L. Winograd R. Madison B.B. Mongroo P.S. Johnstone C.N. Rustgi A.K. LIN28B fosters colon cancer migration, invasion and transformation through let-7-dependent and -independent mechanisms Oncogene 2011 30 4185 4193 10.1038/onc.2011.131 21625210 PMC3165068 · DOI
  32. [33]Akao Y. Nakagawa Y. Naoe T. let-7 microRNA functions as a potential growth suppressor in human colon cancer cells Biol. Pharm. Bull. 2006 29 903 906 10.1248/bpb.29.903 16651716 · DOI
  33. [34]Hu J. Wang Z. Liao B.Y. Yu L. Gao X. Lu S. Wang S. Dai Z. Zhang X. Chen Q. Human miR-1228 as a stable endogenous control for the quantification of circulating microRNAs in cancer patients Int. J. Cancer 2014 135 1187 1194 10.1002/ijc.28757 24488924 · DOI
  34. [35]Zheng X. Chen F. Zhang J. Zhang Q. Lin J. Exosome analysis: A promising biomarker system with special attention to saliva J. Membr. Biol. 2014 247 1129 1136 10.1007/s00232-014-9717-1 25135166 · DOI
  35. [36]Ng E.K. Chong W.W. Jin H. Lam E.K. Shin V.Y. Yu J. Poon T.C. Ng S.S. Sung J.J. Differential expression of microRNAs in plasma of patients with colorectal cancer: A potential marker for colorectal cancer screening Gut 2009 58 1375 1381 10.1136/gut.2008.167817 19201770 · DOI · Paper page
  36. [37]Inoue A. Yamamoto H. Uemura M. Nishimura J. Hata T. Takemasa I. Ikenaga M. Ikeda M. Murata K. Mizushima T. MicroRNA-29b is a Novel Prognostic Marker in Colorectal Cancer Ann. Surg. Oncol. 2015 22 (Suppl. 3) S1410 S1418 10.1245/s10434-014-4255-8 25472644 · DOI
  37. [38]Aherne S.T. Madden S.F. Hughes D.J. Pardini B. Naccarati A. Levy M. Vodicka P. Neary P. Dowling P. Clynes M. Circulating miRNAs miR-34a and miR-150 associated with colorectal cancer progression BMC Cancer 2015 15 329 10.1186/s12885-015-1327-5 25924769 PMC4417244 · DOI
  38. [39]Gungormez C. Teker E. Atmanoglu S. Borazan E. miRNA Profile and Bioinformatic Analysis for Diagnosis in Patients with Stage IIIA Colon Cancer Biochem. Genet. 2022 60 191 203 10.1007/s10528-021-10096-1 34145496 · DOI
  39. [40]Zheng G. Du L. Yang X. Zhang X. Wang L. Yang Y. Li J. Wang C. Serum microRNA panel as biomarkers for early diagnosis of colorectal adenocarcinoma Br. J. Cancer 2014 111 1985 1992 10.1038/bjc.2014.489 25233400 PMC4229633 · DOI
  40. [41]Kara M. Yumrutas O. Ozcan O. Celik O.I. Bozgeyik E. Bozgeyik I. Tasdemir S. Differential expressions of cancer-associated genes and their regulatory miRNAs in colorectal carcinoma Gene 2015 567 81 86 10.1016/j.gene.2015.04.065 25925209 · DOI
  41. [42]Matsuzaki J. Suzuki H. Role of MicroRNAs-221/222 in Digestive Systems J. Clin. Med. 2015 4 1566 1577 10.3390/jcm4081566 26258795 PMC4555077 · DOI
  42. [43]Bitarte N. Bandres E. Boni V. Zarate R. Rodriguez J. Gonzalez-Huarriz M. Lopez I. Javier Sola J. Alonso M.M. Fortes P. MicroRNA-451 is involved in the self-renewal, tumorigenicity, and chemoresistance of colorectal cancer stem cells Stem Cells 2011 29 1661 1671 10.1002/stem.741 21948564 · DOI
  43. [44]Gu X. Xue J.Q. Han S.J. Qian S.Y. Zhang W.H. Circulating microRNA-451 as a predictor of resistance to neoadjuvant chemotherapy in breast cancer Cancer Biomark. 2016 16 395 403 10.3233/CBM-160578 27062696 PMC13016488 · DOI
  44. [45]Huang J.Y. Zhang K. Chen D.Q. Chen J. Feng B. Song H. Chen Y. Zhu Z. Lu L. De W. MicroRNA-451: Epithelial-mesenchymal transition inhibitor and prognostic biomarker of hepatocelluar carcinoma Oncotarget 2015 6 18613 18630 10.18632/oncotarget.4317 26164082 PMC4621914 · DOI
  45. [46]Shivapurkar N. Weiner L.M. Marshall J.L. Madhavan S. Deslattes Mays A. Juhl H. Wellstein A. Recurrence of early stage colon cancer predicted by expression pattern of circulating microRNAs PLoS ONE 2014 9 e84686 10.1371/annotation/86f9cc5c-58b7-4c07-8742-c3036c13e73a 24400111 PMC3882238 · DOI
  46. [47]Sanders I. Holdenrieder S. Walgenbach-Brunagel G. von Ruecker A. Kristiansen G. Muller S.C. Ellinger J. Evaluation of reference genes for the analysis of serum miRNA in patients with prostate cancer, bladder cancer and renal cell carcinoma Int. J. Urol. 2012 19 1017 1025 10.1111/j.1442-2042.2012.03082.x 22788411 · DOI
  47. [48]Sauer E. Madea B. Courts C. An evidence based strategy for normalization of quantitative PCR data from miRNA expression analysis in forensically relevant body fluids Forensic Sci. Int. Genet. 2014 11 174 181 10.1016/j.fsigen.2014.03.011 24792917 · DOI
  48. [49]Livak K.J. Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 2001 25 402 408 10.1006/meth.2001.1262 11846609 · DOI · Paper page
  49. [50]Ishikawa H. Yamada H. Taromaru N. Kondo K. Nagura A. Yamazaki M. Ando Y. Munetsuna E. Suzuki K. Ohashi K. Stability of serum high-density lipoprotein-microRNAs for preanalytical conditions Ann. Clin. Biochem. 2017 54 134 142 10.1177/0004563216647086 27166305 · DOI
  50. [51]Tsui N.B. Ng E.K. Lo Y.M. Stability of endogenous and added RNA in blood specimens, serum, and plasma Clin. Chem. 2002 48 1647 1653 10.1093/clinchem/48.10.1647 12324479 · DOI
  51. [52]Gallo A. Tandon M. Alevizos I. Illei G.G. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes PLoS ONE 2012 7 e30679 10.1371/journal.pone.0030679 22427800 PMC3302865 · DOI · Paper page
  52. [53]Tanaka Y. Kamohara H. Kinoshita K. Kurashige J. Ishimoto T. Iwatsuki M. Watanabe M. Baba H. Clinical impact of serum exosomal microRNA-21 as a clinical biomarker in human esophageal squamous cell carcinoma Cancer 2013 119 1159 1167 10.1002/cncr.27895 23224754 · DOI · Paper page
  53. [54]Thakur B.K. Zhang H. Becker A. Matei I. Huang Y. Costa-Silva B. Zheng Y. Hoshino A. Brazier H. Xiang J. Double-stranded DNA in exosomes: A novel biomarker in cancer detection Cell Res. 2014 24 766 769 10.1038/cr.2014.44 24710597 PMC4042169 · DOI
  54. [55]Bettegowda C. Sausen M. Leary R.J. Kinde I. Wang Y. Agrawal N. Bartlett B.R. Wang H. Luber B. Alani R.M. Detection of circulating tumor DNA in early- and late-stage human malignancies Sci. Transl. Med. 2014 6 224ra224 10.1126/scitranslmed.3007094 24553385 PMC4017867 · DOI · Paper page
  55. [56]Sohn W. Kim J. Kang S.H. Yang S.R. Cho J.Y. Cho H.C. Shim S.G. Paik Y.H. Serum exosomal microRNAs as novel biomarkers for hepatocellular carcinoma Exp. Mol. Med. 2015 47 e184 10.1038/emm.2015.68 26380927 PMC4650928 · DOI
  56. [57]Clancy C. Khan S. Glynn C.L. Holian E. Dockery P. Lalor P. Brown J.A. Joyce M.R. Kerin M.J. Dwyer R.M. Screening of exosomal microRNAs from colorectal cancer cells Cancer Biomark. 2016 17 427 435 10.3233/CBM-160659 27802194 PMC13020523 · DOI
  57. [58]Diamantopoulos M.A. Kontos C.K. Kerimis D. Papadopoulos I.N. Scorilas A. Upregulated miR-16 expression is an independent indicator of relapse and poor overall survival of colorectal adenocarcinoma patients Clin. Chem. Lab. Med. 2017 55 737 747 10.1515/cclm-2016-0756 27930363 · DOI
  58. [59]Qian J. Jiang B. Li M. Chen J. Fang M. Prognostic significance of microRNA-16 expression in human colorectal cancer World J. Surg. 2013 37 2944 2949 10.1007/s00268-013-2205-4 24045965 · DOI
  59. [60]Xiao G. Tang H. Wei W. Li J. Ji L. Ge J. Aberrant Expression of MicroRNA-15a and MicroRNA-16 Synergistically Associates with Tumor Progression and Prognosis in Patients with Colorectal Cancer Gastroenterol. Res. Pract. 2014 2014 364549 10.1155/2014/364549 25435873 PMC4236961 · DOI
  60. [61]You C. Liang H. Sun W. Li J. Liu Y. Fan Q. Zhang H. Yue X. Li J. Chen X. Deregulation of the miR-16-KRAS axis promotes colorectal cancer Sci. Rep. 2016 6 37459 10.1038/srep37459 27857191 PMC5114589 · DOI
  61. [63]Jahid S. Sun J. Edwards R.A. Dizon D. Panarelli N.C. Milsom J.W. Sikandar S.S. Gumus Z.H. Lipkin S.M. miR-23a promotes the transition from indolent to invasive colorectal cancer Cancer Discov. 2012 2 540 553 10.1158/2159-8290.CD-11-0267 22628407 PMC3651884 · DOI
  62. [64]Wang K. Yuan Y. Cho J.H. McClarty S. Baxter D. Galas D.J. Comparing the MicroRNA spectrum between serum and plasma PLoS ONE 2012 7 e41561 10.1371/journal.pone.0041561 22859996 PMC3409228 · DOI
  63. [65]Fang W.J. Lin C.Z. Zhang H.H. Qian J. Zhong L. Xu N. Detection of let-7a microRNA by real-time PCR in colorectal cancer: A single-centre experience from China J. Int. Med. Res. 2007 35 716 723 10.1177/147323000703500518 17944059 · DOI
  64. [66]Ghanbari R. Mosakhani N. Sarhadi V.K. Armengol G. Nouraee N. Mohammadkhani A. Khorrami S. Arefian E. Paryan M. Malekzadeh R. Simultaneous Underexpression of let-7a-5p and let-7f-5p microRNAs in Plasma and Stool Samples from Early Stage Colorectal Carcinoma Biomark Cancer 2015 7 39 48 10.4137/BIC.S25252 26793011 PMC4711391 · DOI
  65. [67]Lee Y.S. Dutta A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene Genes Dev. 2007 21 1025 1030 10.1101/gad.1540407 17437991 PMC1855228 · DOI
  66. [68]Dou R. Nishihara R. Cao Y. Hamada T. Mima K. Masuda A. Masugi Y. Shi Y. Gu M. Li W. MicroRNA let-7, T Cells, and Patient Survival in Colorectal Cancer Cancer Immunol. Res. 2016 4 927 935 10.1158/2326-6066.CIR-16-0112 27737877 PMC5115629 · DOI
  67. [69]Ohshima K. Inoue K. Fujiwara A. Hatakeyama K. Kanto K. Watanabe Y. Muramatsu K. Fukuda Y. Ogura S. Yamaguchi K. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line PLoS ONE 2010 5 e13247 10.1371/journal.pone.0013247 20949044 PMC2951912 · DOI
  68. [71]Cho K.R. Vogelstein B. Genetic alterations in the adenoma--carcinoma sequence Cancer 1992 70 1727 1731 10.1002/1097-0142(19920915)70:4+<1727::AID-CNCR2820701613>3.0.CO;2-P 1516027 · DOI
  69. [72]Bateman A.C. Pathology of serrated colorectal lesions J. Clin. Pathol. 2014 67 865 874 10.1136/jclinpath-2014-202175 24561317 · DOI
  70. [73]Leggett B. Whitehall V. Role of the Serrated Pathway in Colorectal Cancer Pathogenesis Gastroenterology 2010 138 2088 2100 10.1053/j.gastro.2009.12.066 20420948 · DOI

Authors
Dohmen, J., Semaan, A., Kobilay, M., Zaleski, M., Branchi, V., Schlierf, A., Hettwer, K., Uhlig, S., Hartmann, G., Kalff, J. C., Matthaei, H., Lingohr, P., & Holdenrieder, S.
Affiliations
  • University Hospital Bonn (DE)
  • QuoData (Germany) (DE)
Corresponding author
Holdenrieder, Stefan
Venue
Diagnostics
Publisher
MDPI AG
Published
2022-06-08
Volume
12
Issue
6
Pages
1413
ISSN
2075-4418 (ISSN-L)
OpenAlex
W4281824272
Cited by
24
References
76
Citations by year
2026: 3 · 2025: 6 · 2024: 9 · 2023: 5 · 2022: 1
FWCI
1.71
Type
journal article
Language
en
Open access
Locations
  • Diagnostics (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
German Federal Ministry of Education and Research–BMBF (Grant Nr. 13N12852)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
Keywords
colorectal cancer, exosomal microRNAs, circulating microRNAs, liquid biopsy, tumor markers, CEA, CA19-9, serum microRNA, early cancer detection

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review