Where do we stand with screening for colorectal cancer and advanced adenoma based on serum protein biomarkers? A systematic review.
colorectal cancer
protein biomarkers
screening
serum
Journal
Molecular oncology
ISSN: 1878-0261
Titre abrégé: Mol Oncol
Pays: United States
ID NLM: 101308230
Informations de publication
Date de publication:
30 Sep 2024
30 Sep 2024
Historique:
revised:
08
08
2024
received:
01
07
2024
accepted:
09
09
2024
medline:
30
9
2024
pubmed:
30
9
2024
entrez:
30
9
2024
Statut:
aheadofprint
Résumé
Colorectal cancer (CRC) screening has been proven to reduce both mortality and the incidence of this disease. Most CRC screening programs are based on fecal immunochemical tests (FITs), which have a low participation rate. Searching for blood protein biomarkers can lead to the development of a more accepted screening test. The aim of this systematic review was to compare the diagnostic potential of the most promising serum protein biomarkers. A systematic review based on PRISMA guidelines was conducted in the PubMed and Web of Science databases between January 2010 and December 2023. Studies assessing blood protein biomarkers for CRC screening were included. The sensitivity, specificity, and area under the ROC curve of each biomarker were collected. Among 4685 screened studies, 94 were considered for analysis. Most of them were case-control studies, leading to an overestimation of the performance of candidate biomarkers. The performance of no protein biomarker or combination of biomarkers appears to match that of the FIT. Studies with a suitable design and population, testing new assay techniques, or based on algorithms combining FIT with serum tests are needed.
Identifiants
pubmed: 39344882
doi: 10.1002/1878-0261.13734
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024 The Author(s). Molecular Oncology published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
Références
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–249.
Rawla P, Sunkara T, Barsouk A. Epidemiology of colorectal cancer: incidence, mortality, survival, and risk factors. Prz Gastroenterol. 2019;14(2):89–103.
Cardoso R, Guo F, Heisser T, De Schutter H, Van Damme N, Nilbert MC, et al. Proportion and stage distribution of screen‐detected and non‐screen‐detected colorectal cancer in nine European countries: an international, population‐based study. Lancet Gastroenterol Hepatol. 2022;7(8):711–723.
Cardoso R, Guo F, Heisser T, Hackl M, Ihle P, De Schutter H, et al. Colorectal cancer incidence, mortality, and stage distribution in European countries in the colorectal cancer screening era: an international population‐based study. Lancet Oncol. 2021;22(7):1002–1013.
Lee JK, Liles EG, Bent S, Levin TR, Corley DA. Accuracy of fecal immunochemical tests for colorectal cancer: systematic review and meta‐analysis. Ann Intern Med. 2014;160(3):171.
Selby K, Levine EH, Doan C, Gies A, Brenner H, Quesenberry C, et al. Effect of sex, age, and positivity threshold on fecal immunochemical test accuracy: a systematic review and meta‐analysis. Gastroenterology. 2019;157(6):1494–1505.
Grobbee EJ, Wisse PH, Schreuders EH, van Roon A, van Dam L, Zauber AG, et al. Guaiac‐based faecal occult blood tests versus faecal immunochemical tests for colorectal cancer screening in average‐risk individuals. Cochrane Database Syst Rev. 2022;6(6):CD009276.
Imperiale TF, Gruber RN, Stump TE, Emmett TW, Monahan PO. Performance characteristics of fecal immunochemical tests for colorectal cancer and advanced adenomatous polyps: a systematic review and meta‐analysis. Ann Intern Med. 2019;170(5):319–329.
Moss S, Ancelle‐Park R, Brenner H, International Agency for Research on Cancer. European guidelines for quality assurance in colorectal cancer screening and diagnosis. First edition—evaluation and interpretation of screening outcomes. Endoscopy. 2012;44(Suppl 3):SE49–SE64.
Le Bonniec A, Meade O, Fredrix M, Morrissey E, O'Carroll RE, Murphy PJ, et al. Exploring non‐participation in colorectal cancer screening: a systematic review of qualitative studies. Soc Sci Med. 2023;329:116022.
Osborne J, Wilson C, Moore V, Gregory T, Flight I, Young G. Sample preference for colorectal cancer screening tests: blood or stool? Open J Prev Med. 2012;2:326–331. https://doi.org/10.4236/ojpm.2012.23047
Osborne JM, Flight I, Wilson CJ, Chen G, Ratcliffe J, Young GP. The impact of sample type and procedural attributes on relative acceptability of different colorectal cancer screening regimens. Patient Prefer Adherence. 2018;12:1825–1836.
Liang PS, Zaman A, Kaminsky A, Cui Y, Castillo G, Tenner CT, et al. Blood test increases colorectal cancer screening in persons who declined colonoscopy and fecal immunochemical test: a randomized controlled trial. Clin Gastroenterol Hepatol. 2023;21(11):2951–2957.e2.
Nikolaou S, Qiu S, Fiorentino F, Rasheed S, Tekkis P, Kontovounisios C. Systematic review of blood diagnostic markers in colorectal cancer. Tech Coloproctol. 2018;22(7):481–498.
Church TR, Wandell M, Lofton‐Day C, Mongin SJ, Burger M, Payne SR, et al. Prospective evaluation of methylated SEPT9 in plasma for detection of asymptomatic colorectal cancer. Gut. 2014;63(2):317–325.
Chung DC, Gray DM, Singh H, Issaka RB, Raymond VM, Eagle C, et al. A cell‐free DNA blood‐based test for colorectal cancer screening. N Engl J Med. 2024;390(11):973–983.
Liu Z, Zhang Y, Niu Y, Li K, Liu X, Chen H, et al. A systematic review and meta‐analysis of diagnostic and prognostic serum biomarkers of colorectal cancer. PLoS One. 2014;9(8):e103910.
Qian J, Tikk K, Werner S, Balavarca Y, Saadati M, Hechtner M, et al. Biomarker discovery study of inflammatory proteins for colorectal cancer early detection demonstrated importance of screening setting validation. J Clin Epidemiol. 2018;104:24–34.
McInnes MDF, Moher D, Thombs BD, McGrath TA, Bossuyt PM, the PRISMA‐DTA Group, et al. Preferred reporting items for a systematic review and meta‐analysis of diagnostic test accuracy studies: the PRISMA‐DTA statement. JAMA. 2018;319(4):388–396.
Whiting PF, Rutjes AWS, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al. QUADAS‐2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155(8):529–536.
Attallah AM, El‐Far M, Ibrahim AR, El‐Desouky MA, Omran MM, Elbendary MS, et al. Clinical value of a diagnostic score for colon cancer based on serum CEA, CA19‐9, cytokeratin‐1 and mucin‐1. Br J Biomed Sci. 2018;75(3):122–127.
Atwa RA, Abdelrazek MA, Attallah AM. Evaluation of metalloprotenase‐1 in early diagnosis of colon cancer. Biosci Res. 2020;17:2816–2824.
Bedin C, Crotti S, Ragazzi E, Pucciarelli S, Agatea L, Tasciotti E, et al. Alterations of the plasma peptidome profiling in colorectal cancer progression. J Cell Physiol. 2016;231(4):915–925.
Bhardwaj M, Weigl K, Tikk K, Benner A, Schrotz‐King P, Brenner H. Multiplex screening of 275 plasma protein biomarkers to identify a signature for early detection of colorectal cancer. Mol Oncol. 2020;14(1):8–21.
Bhardwaj M, Weigl K, Tikk K, Holland‐Letz T, Schrotz‐King P, Borchers CH, et al. Multiplex quantitation of 270 plasma protein markers to identify a signature for early detection of colorectal cancer. Eur J Cancer. 2020;127:30–40.
Bünger S, Haug U, Kelly M, Posorski N, Klempt‐Giessing K, Cartwright A, et al. A novel multiplex‐protein array for serum diagnostics of colon cancer: a case‐control study. BMC Cancer. 2012;12:393.
Cai L, Tu M, Yin X, Zhang S, Zhuang W, Xia Y, et al. Combination of serum CST4 and DR‐70 contributes to early diagnosis of colorectal cancer. Clin Chim Acta. 2022;531:318–324.
Chen H, Werner S, Butt J, Zörnig I, Knebel P, Michel A, et al. Prospective evaluation of 64 serum autoantibodies as biomarkers for early detection of colorectal cancer in a true screening setting. Oncotarget. 2016;7(13):16420–16432.
Chen H, Qian J, Werner S, Cuk K, Knebel P, Brenner H. Development and validation of a panel of five proteins as blood biomarkers for early detection of colorectal cancer. Clin Epidemiol. 2017;9:517–526.
Chen M, Lin X, Zhang L, Yu L, Wu Q, Zhang S, et al. Development of a panel of serum IgG and IgA autoantibodies for early diagnosis of colon cancer. Int J Med Sci. 2020;17(17):2744–2750.
Christensen IJ, Brünner N, Dowell B, Davis G, Nielsen HJ, Newstead G, et al. Plasma TIMP‐1 and CEA as markers for detection of primary colorectal cancer: a prospective validation study including symptomatic and non‐symptomatic individuals. Anticancer Res. 2015;35(9):4935–4941.
Dai C, Zhang X, Ma Y, Chen Z, Chen S, Zhang Y, et al. Serum macrophage inhibitory cytokine‐1 serves as a novel diagnostic biomarker of early‐stage colorectal cancer. Biomarkers. 2021;26(7):598–605.
De Chiara L, Rodríguez‐Piñeiro AM, Rodríguez‐Berrocal FJ, Cordero OJ, Martínez‐Ares D, Páez de la Cadena M. Serum CD26 is related to histopathological polyp traits and behaves as a marker for colorectal cancer and advanced adenomas. BMC Cancer. 2010;10:333.
De Chiara L, Barcia‐Castro L, Gallardo‐Gomez M, Paez de la Cadena M, Martinez‐Zorzano VS, Rodriguez‐Berrocal FJ, et al. Evaluation of blood soluble CD26 as a complementary biomarker for colorectal cancer screening programs. Cancers (Basel). 2022;14(19):4563.
Deng B‐G, Yao J‐H, Liu Q‐Y, Feng X‐J, Liu D, Zhao L, et al. Comparative serum proteomic analysis of serum diagnosis proteins of colorectal cancer based on magnetic bead separation and maldi‐tof mass spectrometry. Asian Pac J Cancer Prev. 2013;14(10):6069–6075.
Dowling P, Hughes DJ, Larkin AM, Meiller J, Henry M, Meleady P, et al. Elevated levels of 14‐3‐3 proteins, serotonin, gamma enolase and pyruvate kinase identified in clinical samples from patients diagnosed with colorectal cancer. Clin Chim Acta. 2015;441:133–141.
Dressen K, Hermann N, Manekeller S, Walgenbach‐Bruenagel G, Schildberg FA, Hettwer K, et al. Diagnostic performance of a novel multiplex immunoassay in colorectal cancer. Anticancer Res. 2017;37(5):2477–2486.
Farshidfar F, Weljie AM, Kopciuk KA, Hilsden R, McGregor SE, Buie WD, et al. A validated metabolomic signature for colorectal cancer: exploration of the clinical value of metabolomics. Br J Cancer. 2016;115(7):848–857.
Fitzgerald S, O'Reilly J‐A, Wilson E, Joyce A, Farrell R, Kenny D, et al. Measurement of the IgM and IgG autoantibody immune responses in human serum has high predictive value for the presence of colorectal cancer. Clin Colorectal Cancer. 2019;18(1):e53–e60.
Garranzo‐Asensio M, San Segundo‐Acosta P, Povés C, Fernández‐Aceñero MJ, Martínez‐Useros J, Montero‐Calle A, et al. Identification of tumor‐associated antigens with diagnostic ability of colorectal cancer by in‐depth immunomic and seroproteomic analysis. J Proteomics. 2020;214:103635.
Gawel SH, Lucht M, Gomer H, Treado P, Christensen IJ, Nielsen HJ, et al. Evaluation of algorithm development approaches: development of biomarker panels for early detection of colorectal lesions. Clin Chim Acta. 2019;498:108–115.
Gimeno‐García AZ, Triñanes J, Quintero E, Salido E, Nicolás‐Pérez D, Adrián‐de‐Ganzo Z, et al. Plasma matrix metalloproteinase 9 as an early surrogate biomarker of advanced colorectal neoplasia. Gastroenterol Hepatol. 2016;39(7):433–441.
Groblewska M, Mroczko B, Gryko M, Kędra B, Szmitkowski M. Matrix metalloproteinase 2 and tissue inhibitor of matrix metalloproteinases 2 in the diagnosis of colorectal adenoma and cancer patients. Folia Histochem Cytobiol. 2010;48(4):564–571.
Gu J, Xiao Y, Shu D, Liang X, Hu X, Xie Y, et al. Metabolomics analysis in serum from patients with colorectal polyp and colorectal cancer by 1H‐NMR spectrometry. Dis Markers. 2019;2019:3491852.
Gu Y, Duan B, Sha J, Zhang R, Fan J, Xu X, et al. Serum IgG N‐glycans enable early detection and early relapse prediction of colorectal cancer. Int J Cancer. 2023;152(3):536–547.
Han S, Wang J, Wang L, Jin G, Ying X, He C, et al. The role of RCAS1 as a biomarker in diagnosing CRC and monitoring tumor recurrence and metastasis. Tumour Biol. 2014;35(6):6149–6157.
Huang Z, Li Z, Chen X, Zhu X, Zhang J, Song Y, et al. Comparison between clinical utility of CXCL‐8 and clinical practice tumor markers for colorectal cancer diagnosis. Biomed Res Int. 2022;2022:1213968.
Huang M, Yang Z, Ren J, Wang T, Chen D, Zhan Y, et al. The diagnosis significance of serum cysteine protease inhibitors (CST4) in colorectal cancer. Technol Cancer Res Treat. 2023;22:15330338231164232.
Ivancic MM, Megna BW, Sverchkov Y, Craven M, Reichelderfer M, Pickhardt PJ, et al. Noninvasive detection of colorectal carcinomas using serum protein biomarkers. J Surg Res. 2020;246:160–169.
Jiang X, Wang J, Wang M, Xuan M, Han S, Li C, et al. ITGB4 as a novel serum diagnosis biomarker and potential therapeutic target for colorectal cancer. Cancer Med. 2021;10(19):6823–6834.
Johansen JS, Christensen IJ, Jørgensen LN, Olsen J, Rahr HB, Nielsen KT, et al. Serum YKL‐40 in risk assessment for colorectal cancer: a prospective study of 4,496 subjects at risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev. 2015;24(3):621–626.
Ke X, Liu W, Shen L, Zhang Y, Liu W, Wang C, et al. Early screening of colorectal precancerous lesions based on combined measurement of multiple serum tumor markers using artificial neural network analysis. Biosensors (Basel). 2023;13(7):685.
Kleif J, Jørgensen LN, Hendel JW, Madsen MR, Vilandt J, Brandsborg S, et al. Early detection of colorectal neoplasia: application of a blood‐based serological protein test on subjects undergoing population‐based screening. Br J Cancer. 2022;126(10):1387–1393.
Kraus S, Shapira S, Kazanov D, Naumov I, Moshkowitz M, Santo E, et al. Predictive levels of CD24 in peripheral blood leukocytes for the early detection of colorectal adenomas and adenocarcinomas. Dis Markers. 2015;2015:916098.
Li B, Shen K, Zhang J, Jiang Y, Yang T, Sun X, et al. Serum netrin‐1 as a biomarker for colorectal cancer detection. Cancer Biomark. 2020;28(3):391–396.
Li Q, Wang K, Su C, Fang J. Serum trefoil factor 3 as a protein biomarker for the diagnosis of colorectal cancer. Technol Cancer Res Treat. 2017;16(4):440–445.
Li S, Huang M, Liu Q, Wang D, Wu R, Zhang X, et al. Serum expression of β‐catenin is a potential detection marker in patients with colorectal cancer. Dis Markers. 2019;2019:5070524.
Liu L, He Q, Li Y, Zhang B, Sun X, Shan J, et al. Serum SYPL1 is a promising diagnostic biomarker for colorectal cancer. Clin Chim Acta. 2020;509:36–42.
Liu Z, Tang H, Zhang W, Wang J, Wan L, Li X, et al. Coupling of serum CK20 and hyper‐methylated CLIP4 as promising biomarker for colorectal cancer diagnosis: from bioinformatics screening to clinical validation. Aging (Albany NY). 2021;13(24):26161–26179.
Meng W, Zhu H‐H, Xu Z‐F, Cai S‐R, Dong Q, Pan Q‐R, et al. Serum M2‐pyruvate kinase: a promising non‐invasive biomarker for colorectal cancer mass screening. World J Gastrointest Oncol. 2012;4(6):145–151.
Montero‐Calle A, Garranzo‐Asensio M, Torrente‐Rodríguez RM, Ruiz‐Valdepeñas Montiel V, Poves C, Dziaková J, et al. p53 and p63 proteoforms derived from alternative splicing possess differential seroreactivity in colorectal cancer with distinct diagnostic ability from the canonical proteins. Cancers (Basel). 2023;15(7):2102.
Moravkova P, Kohoutova D, Vavrova J, Bures J. Serum S100A6, S100A8, S100A9 and S100A11 proteins in colorectal neoplasia: results of a single centre prospective study. Scand J Clin Lab Invest. 2020;80(3):173–178.
Mroczko B, Groblewska M, Okulczyk B, Kedra B, Szmitkowski M. The diagnostic value of matrix metalloproteinase 9 (MMP‐9) and tissue inhibitor of matrix metalloproteinases 1 (TIMP‐1) determination in the sera of colorectal adenoma and cancer patients. Int J Colorectal Dis. 2010;25(10):1177–1184.
Nielsen HJ, Brünner N, Jorgensen LN, Olsen J, Rahr HB, Thygesen K, et al. Plasma TIMP‐1 and CEA in detection of primary colorectal cancer: a prospective, population based study of 4509 high‐risk individuals. Scand J Gastroenterol. 2011;46(1):60–69.
Otero‐Estévez O, De Chiara L, Rodríguez‐Berrocal FJ, Páez de la Cadena M, Cubiella J, Castro I, et al. Serum sCD26 for colorectal cancer screening in family‐risk individuals: comparison with faecal immunochemical test. Br J Cancer. 2015;112(2):375–381.
Otero‐Estévez O, De Chiara L, Rodríguez‐Girondo M, Rodríguez‐Berrocal FJ, Cubiella J, Castro I, et al. Serum matrix metalloproteinase‐9 in colorectal cancer family‐risk population screening. Sci Rep. 2015;5:13030.
Otero‐Estévez O, De Chiara L, Barcia‐Castro L, Páez de la Cadena M, Rodríguez‐Berrocal FJ, Cubiella J, et al. Evaluation of serum nucleoside diphosphate kinase A for the detection of colorectal cancer. Sci Rep. 2016;6:26703.
Overholt BF, Wheeler DJ, Jordan T, Fritsche HA. CA11‐19: a tumor marker for the detection of colorectal cancer. Gastrointest Endosc. 2016;83(3):545–551.
Ozemir IA, Aslan S, Eren T, Bayraktar B, Bilgic C, Isbilen B, et al. The diagnostic and prognostic significance of serum neutrophil gelatinase‐associated lipocalin levels in patients with colorectal cancer. Chirurgia (Bucur). 2016;111(5):414–421.
Özgür E, Keskin M, Yörüker EE, Holdenrieder S, Gezer U. Plasma histone H4 and H4K20 trimethylation levels differ between colon cancer and precancerous polyps. In Vivo. 2019;33(5):1653–1658.
Pan Y, Zhang L, Zhang R, Han J, Qin W, Gu Y, et al. Screening and diagnosis of colorectal cancer and advanced adenoma by bionic glycome method and machine learning. Am J Cancer Res. 2021;11(6):3002–3020.
Pan Z, Hu Z, Guan L, Zhang L, Gao X, Yang L, et al. Diagnostic value of serum sphingolipids in patients with colorectal cancer. Analyst. 2022;147(10):2189–2197.
Peltier J, Roperch J‐P, Audebert S, Borg J‐P, Camoin L. Quantitative proteomic analysis exploring progression of colorectal cancer: modulation of the serpin family. J Proteomics. 2016;148:139–148.
Petersen MM, Kleif J, Jørgensen LN, Hendel JW, Seidelin JB, Madsen MR, et al. Optimizing screening for colorectal cancer: an algorithm combining fecal immunochemical test, blood‐based cancer‐associated proteins and demographics to reduce colonoscopy burden. Clin Colorectal Cancer. 2023;22(2):199–210.
Qian J, Tikk K, Weigl K, Balavarca Y, Brenner H. Fibroblast growth factor 21 as a circulating biomarker at various stages of colorectal carcinogenesis. Br J Cancer. 2018;119(11):1374–1382.
Qiu S, Nikolaou S, Fiorentino F, Rasheed S, Darzi A, Cunningham D, et al. Exploratory analysis of plasma neurotensin as a novel biomarker for early detection of colorectal polyp and cancer. Horm Cancer. 2019;10(2–3):128–135.
Rasmussen L, Nielsen HJ, Christensen IJ. Evaluation of a 92 multiplex protein panel in detection of colorectal cancer and high‐risk adenoma in 784 symptomatic individuals. Cancer Biomark. 2021;32(1):73–84.
Rho J‐H, Ladd JJ, Li CI, Potter JD, Zhang Y, Shelley D, et al. Protein and glycomic plasma markers for early detection of adenoma and colon cancer. Gut. 2018;67(3):473–484.
Rigi F, Jannatabad A, Izanloo A, Roshanravan R, Hashemian HR, Kerachian MA. Expression of tumor pyruvate kinase M2 isoform in plasma and stool of patients with colorectal cancer or adenomatous polyps. BMC Gastroenterol. 2020;20(1):241.
Solé X, Crous‐Bou M, Cordero D, Olivares D, Guinó E, Sanz‐Pamplona R, et al. Discovery and validation of new potential biomarkers for early detection of colon cancer. PLoS One. 2014;9(9):e106748.
Song YF, Xu ZB, Zhu XJ, Tao X, Liu JL, Gao FL, et al. Serum Cyr61 as a potential biomarker for diagnosis of colorectal cancer. Clin Transl Oncol. 2017;19(4):519–524.
Song W‐Y, Zhang X, Zhang Q, Zhang P‐J, Zhang R. Clinical value evaluation of serum markers for early diagnosis of colorectal cancer. World J Gastrointest Oncol. 2020;12(2):219–227.
Storm L, Christensen IJ, Jensenius JC, Nielsen HJ, Thiel S, Danish Study Group on Early Detection of Colorectal Cancer. Evaluation of complement proteins as screening markers for colorectal cancer. Cancer Immunol Immunother. 2015;64(1):41–50.
Sun F, Tan Y‐A, Gao Q‐F, Li S‐Q, Zhang J, Chen Q‐G, et al. Circulating fibrinogen to pre‐albumin ratio is a promising biomarker for diagnosis of colorectal cancer. J Clin Lab Anal. 2019;33(1):e22635.
Taguchi A, Rho J‐H, Yan Q, Zhang Y, Zhao Y, Xu H, et al. MAPRE1 as a plasma biomarker for early‐stage colorectal cancer and adenomas. Cancer Prev Res (Phila). 2015;8(11):1112–1119.
Tao S, Haug U, Kuhn K, Brenner H. Comparison and combination of blood‐based inflammatory markers with faecal occult blood tests for non‐invasive colorectal cancer screening. Br J Cancer. 2012;106(8):1424–1430.
Thomas DS, Fourkala E‐O, Apostolidou S, Gunu R, Ryan A, Jacobs I, et al. Evaluation of serum CEA, CYFRA21‐1 and CA125 for the early detection of colorectal cancer using longitudinal preclinical samples. Br J Cancer. 2015;113(2):268–274.
Thorsen SB, Lundberg M, Villablanca A, Christensen SLT, Belling KC, Nielsen BS, et al. Detection of serological biomarkers by proximity extension assay for detection of colorectal neoplasias in symptomatic individuals. J Transl Med. 2013;11:253.
Uchiyama K, Yagi N, Mizushima K, Higashimura Y, Hirai Y, Okayama T, et al. Serum metabolomics analysis for early detection of colorectal cancer. J Gastroenterol. 2017;52(6):677–694.
Uchiyama K, Naito Y, Yagi N, Mizushima K, Higashimura Y, Hirai Y, et al. Selected reaction monitoring for colorectal cancer diagnosis using a set of five serum peptides identified by BLOTCHIP®‐MS analysis. J Gastroenterol. 2018;53(11):1179–1185.
van den Broek I, Sparidans RW, Engwegen JYMN, Cats A, Depla ACTM, Schellens JHM, et al. Evaluation of human neutrophil peptide‐1, ‐2 and ‐3 as serum markers for colorectal cancer. Cancer Biomark. 2010;7(2):109–115.
Wang J, Wang X, Lin S, Chen C, Wang C, Ma Q, et al. Identification of kininogen‐1 as a serum biomarker for the early detection of advanced colorectal adenoma and colorectal cancer. PLoS One. 2013;8(7):e70519.
Wang X, Yang Z, Tian H, Li Y, Li M, Zhao W, et al. Circulating MIC‐1/GDF15 is a complementary screening biomarker with CEA and correlates with liver metastasis and poor survival in colorectal cancer. Oncotarget. 2017;8(15):24892–24901.
Wang D, Yuan W, Wang Y, Wu Q, Yang L, Li F, et al. Serum CCL20 combined with IL‐17A as early diagnostic and prognostic biomarkers for human colorectal cancer. J Transl Med. 2019;17(1):253.
Wang Z, Wang S, Liu Y, Gao S, Yu Y, Hu Z. Serum levels of BDNF in patients with adenoma and colorectal cancer. Dis Markers. 2021;2021:8867368.
Wang H, Zhou Z, Li H, Xiang W, Lan Y, Dou X, et al. Blood biomarkers panels for screening of colorectal cancer and adenoma on a machine learning‐assisted detection platform. Cancer Control. 2023;30:10732748231222109.
Wang Q‐Q, Zhou L, Qin G, Tan C, Zhou Y‐C, Yao S‐K. Leukocyte immunoglobulin‐like receptor B2 overexpression as a promising therapeutic target and noninvasive screening biomarker for colorectal cancer. World J Gastroenterol. 2023;29(37):5313–5326.
Watany MM, Elmashad NM, Badawi R, Hawash N. Serum FBLN1 and STK31 as biomarkers of colorectal cancer and their ability to noninvasively differentiate colorectal cancer from benign polyps. Clin Chim Acta. 2018;483:151–155.
Weiss JV, Klein‐Scory S, Kübler S, Reinacher‐Schick A, Stricker I, Schmiegel W, et al. Soluble E‐cadherin as a serum biomarker candidate: elevated levels in patients with late‐stage colorectal carcinoma and FAP. Int J Cancer. 2011;128(6):1384–1392.
Werner S, Krause F, Rolny V, Strobl M, Morgenstern D, Datz C, et al. Evaluation of a 5‐marker blood test for colorectal cancer early detection in a colorectal cancer screening setting. Clin Cancer Res. 2016;22(7):1725–1733.
Wild N, Andres H, Rollinger W, Krause F, Dilba P, Tacke M, et al. A combination of serum markers for the early detection of colorectal cancer. Clin Cancer Res. 2010;16(24):6111–6121.
Wilhelmsen M, Christensen IJ, Rasmussen L, Jørgensen LN, Madsen MR, Vilandt J, et al. Detection of colorectal neoplasia: combination of eight blood‐based, cancer‐associated protein biomarkers. Int J Cancer. 2017;140(6):1436–1446.
Wilson S, Damery S, Stocken DD, Dowswell G, Holder R, Ward ST, et al. Serum matrix metalloproteinase 9 and colorectal neoplasia: a community‐based evaluation of a potential diagnostic test. Br J Cancer. 2012;106(8):1431–1438.
Wu S, Qi Y, Niu LM, Xie DX, Cui XL, Liu ZH. Activin A as a novel biomarker for colorectal adenocarcinoma in humans. Eur Rev Med Pharmacol Sci. 2015;19(22):4371–4378.
Xie H, Guo J‐H, An W‐M, Tian S‐T, Yu H‐P, Yang X‐L, et al. Diagnostic value evaluation of trefoil factors family 3 for the early detection of colorectal cancer. World J Gastroenterol. 2017;23(12):2159–2167.
Xu W, Hu Y, Li J, He X, Fu Z, Pan T, et al. Study of distinct serum proteomics for the biomarkers discovery in colorectal cancer. Discov Med. 2015;20(110):239–253.
Yao L, Lao W, Zhang Y, Tang X, Hu X, He C, et al. Identification of EFEMP2 as a serum biomarker for the early detection of colorectal cancer with lectin affinity capture assisted secretome analysis of cultured fresh tissues. J Proteome Res. 2012;11(6):3281–3294.
Ye H‐M, Lu Y‐Z, Liang X‐M, Lin Y‐Z, Li Y, Zhang Z‐Y, et al. Clinical significance of combined testing of YKL‐40 with CEA in Chinese colorectal cancer patients. Clin Lab. 2014;60(3):397–405.
Yildirim K, Colak E, Aktimur R, Gun S, Taskin MH, Nigdelioglu A, et al. Clinical value of CXCL5 for determining of colorectal cancer. Asian Pac J Cancer Prev. 2018;19(9):2481–2484.
Zekri A‐RN, Bakr YM, Ezzat MM, Zakaria MSE, Elbaz TM. Circulating levels of adipocytokines as potential biomarkers for early detection of colorectal carcinoma in Egyptian patients. Asian Pac J Cancer Prev. 2015;16(16):6923–6928.
Zhang S‐Y, Lin M, Zhang H‐B. Diagnostic value of carcinoembryonic antigen and carcinoma antigen 19‐9 for colorectal carcinoma. Int J Clin Exp Pathol. 2015;8(8):9404–9409.
Zhou M, Li M, Liang X, Zhang Y, Huang H, Feng Y, et al. The significance of serum S100A9 and TNC levels as biomarkers in colorectal cancer. J Cancer. 2019;10(22):5315–5323.
Zhu C‐B, Wang C‐X, Zhang X, Zhang J, Li W. Serum sHLA‐G levels: a useful indicator in distinguishing colorectal cancer from benign colorectal diseases. Int J Cancer. 2011;128(3):617–622.
Zhu J, Djukovic D, Deng L, Gu H, Himmati F, Chiorean EG, et al. Colorectal cancer detection using targeted serum metabolic profiling. J Proteome Res. 2014;13(9):4120–4130.
Click B, Pinsky PF, Hickey T, Doroudi M, Schoen RE. Association of colonoscopy adenoma findings with long‐term colorectal cancer incidence. JAMA. 2018;319(19):2021–2031.
Hundt S, Haug U, Brenner H. Blood markers for early detection of colorectal cancer: a systematic review. Cancer Epidemiol Biomarkers Prev. 2007;16(10):1935–1953.
Bresalier RS, Senore C, Young GP, Allison J, Benamouzig R, Benton S, et al. An efficient strategy for evaluating new non‐invasive screening tests for colorectal cancer: the guiding principles. Gut. 2023;72(10):1904–1918.
Dwan K, Gamble C, Williamson PR, Kirkham JJ, Reporting Bias Group. Systematic review of the empirical evidence of study publication bias and outcome reporting bias—an updated review. PLoS One. 2013;8(7):e66844.
Etzioni R, Kooperberg C, Pepe M, Smith R, Gann PH. Combining biomarkers to detect disease with application to prostate cancer. Biostatistics. 2003;4(4):523–538.
Rex DK, Lehman GA, Ulbright TM, Smith JJ, Pound DC, Hawes RH, et al. Colonic neoplasia in asymptomatic persons with negative fecal occult blood tests: influence of age, gender, and family history. Am J Gastroenterol. 1993;88(6):825–831.