We use cookies to improve your experience. By continuing to browse this site, you accept our cookie policy.×
Skip main navigation
Aging Health
Bioelectronics in Medicine
Biomarkers in Medicine
Breast Cancer Management
CNS Oncology
Colorectal Cancer
Concussion
Epigenomics
Future Cardiology
Future Medicine AI
Future Microbiology
Future Neurology
Future Oncology
Future Rare Diseases
Future Virology
Hepatic Oncology
HIV Therapy
Immunotherapy
International Journal of Endocrine Oncology
International Journal of Hematologic Oncology
Journal of 3D Printing in Medicine
Lung Cancer Management
Melanoma Management
Nanomedicine
Neurodegenerative Disease Management
Pain Management
Pediatric Health
Personalized Medicine
Pharmacogenomics
Regenerative Medicine

Glycoproteomics-based liquid biopsy: translational outlook for colorectal cancer clinical management in Southeast Asia

    Gaayathri Kumarasamy

    Institute for Research in Molecular Medicine, Universiti Sains Malaysia, Pulau Pinang, 11800, Malaysia

    ,
    Nurul Hakimah Mohd Salim

    Department of Pathology, School of Medical Sciences, Universiti Sains Malaysia, Kubang Kerian, Kelantan, 16150, Malaysia

    ,
    Nur Syafiqah Mohd Afandi

    Analytical Biochemistry Research Centre, Universiti Sains Malaysia, Bayan Lepas, Pulau Pinang, 11900, Malaysia

    ,
    Mohd Afiq Hazlami Habib

    Analytical Biochemistry Research Centre, Universiti Sains Malaysia, Bayan Lepas, Pulau Pinang, 11900, Malaysia

    ,
    Nor Datiakma Mat Amin

    Analytical Biochemistry Research Centre, Universiti Sains Malaysia, Bayan Lepas, Pulau Pinang, 11900, Malaysia

    Nature Products Division, Forest Research Institute Malaysia, Kepong, Selangor, 52109, Malaysia

    ,
    Mohd Nazri Ismail

    Institute for Research in Molecular Medicine, Universiti Sains Malaysia, Pulau Pinang, 11800, Malaysia

    Analytical Biochemistry Research Centre, Universiti Sains Malaysia, Bayan Lepas, Pulau Pinang, 11900, Malaysia

    &
    Marahaini Musa

    *Author for correspondence: Tel.: +60 9767 6794;

    E-mail Address: marahaini.musa@usm.my

    Human Genome Centre, School of Medical Sciences, Universiti Sains Malaysia, Kubang Kerian, Kelantan, 16150, Malaysia

    Published Online:https://doi.org/10.2217/fon-2023-0704

    Colorectal cancer (CRC) signifies a significant healthcare challenge in Southeast Asia. Despite advancements in screening approaches and treatment modalities, significant medical gaps remain, ranging from prevention and early diagnosis to determining targeted therapy and establishing personalized approaches to managing CRC. There is a need to expand more validated biomarkers in clinical practice. An advanced technique incorporating high-throughput mass spectrometry as a liquid biopsy to unravel a repertoire of glycoproteins and glycans would potentially drive the development of clinical tools for CRC screening, diagnosis and monitoring, and it can be further adapted to the existing standard-of-care procedure. Therefore this review offers a perspective on glycoproteomics-driven liquid biopsy and its potential integration into the clinical care of CRC in the southeast Asia region.

    Tweetable abstract

    Colorectal cancer (CRC) is a significant concern in Southeast Asia, with gaps in prevention, diagnosis and therapy. Finding glycoproteins’ and glycans’ potentials as CRC biomarkers could revolutionize CRC care, from screening to treatment, across the region.

    References

    • 1. Xi Y, Xu P. Global colorectal cancer burden in 2020 and projections to 2040. Transl. Oncol. 14(10), 101174 (2021).
    • 2. Sung H, Ferlay J, Siegel RL et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 71(3), 209–249 (2021).
    • 3. Hossain MS, Karuniawati H, Jairoun AA et al. Colorectal cancer: a review of carcinogenesis, global. Cancer 14(1732), 1–25 (2022).
    • 4. UNESCAP. South-East Asia: demographic indicators. www.population-trends-asiapacific.org/data/sea
    • 5. Ouakrim DA, Pizot C, Boniol M et al. Trends in colorectal cancer mortality in Europe: retrospective analysis of the WHO mortality database. BMJ 351, h4970 (2015).
    • 6. Rustgi AK. The genetics of hereditary colon cancer. Genes Dev. 21(20), 2525–2538 (2007).
    • 7. Wang H, Seow A, Lee HP. Trends in cancer incidence among Singapore Malays: a low-risk population. Ann. Med. Singapore 33(1), 57–62 (2004).
    • 8. Hassan MRA, Ismail I, Suan MAM et al. Incidence and mortality rates of colorectal cancer in Malaysia. Epidemiol. Health 38, e2016007 (2016).
    • 9. UNESCAP. Economic and social survey of Asia and the Pacific 2017: governance and fiscal management (2017). www.unescap.org/publications/economic-and-social-survey-asia-and-pacific-2017
    • 10. Bailey CE, Hu C-Y, You YN et al. Increasing disparities in the age-related incidences of colon and rectal cancers in the United States, 1975-2010. JAMA Surg. 150(1), 17–22 (2015).
    • 11. Mauri G, Vitiello PP, Sogari A et al. Liquid biopsies to monitor and direct cancer treatment in colorectal cancer. Br. J. Cancer 127(3), 394–407 (2022).
    • 12. Ding Y, Li W, Wang K, Xu C, Hao M, Ding L. Perspectives of the application of liquid biopsy in colorectal cancer. Biomed Res. Int. 2020, 6843180 (2020).
    • 13. Marcuello M, Vymetalkova V, Neves RPL et al. Circulating biomarkers for early detection and clinical management of colorectal cancer. Mol. Aspects Med. 69, 107–122 (2019).
    • 14. Normanno N, Cervantes A, Ciardiello F, De Luca A, Pinto C. The liquid biopsy in the management of colorectal cancer patients: current applications and future scenarios. Cancer Treat. Rev. 70, 1–8 (2018).
    • 15. Zhang W, Yang Z, Gao X, Wu Q. Advances in the discovery of novel biomarkers for cancer: spotlight on protein N-glycosylation. Biomark. Med. 14(11), 1031–1045 (2020).
    • 16. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 61(5), 759–767 (1990).
    • 17. Smith G, Carey FA, Beattie J et al. Mutations in APC, Kirsten-ras, and p53 – alternative genetic pathways to colorectal cancer. Proc. Natl Acad. Sci. USA 99(14), 9433–9438 (2002).
    • 18. Rex DK, Sullivan AW, Perkins AJ, Vemulapalli KC. Colorectal polyp prevalence and aspirational detection targets determined using high definition colonoscopy and a high level detector in 2017. Dig. Liver Dis. 52(1), 72–78 (2020).
    • 19. Corley DA, Jensen CD, Marks AR et al. Adenoma detection rate and risk of colorectal cancer and death. N. Engl. J. Med. 370(14), 1298–1306 (2014).
    • 20. Binefa G, Rodríguez-Moranta F, Teule A, Medina-Hayas M. Colorectal cancer: from prevention to personalized medicine. World J. Gastroenterol. 20(22), 6786 (2014).
    • 21. Schliemann D, Paramasivam D, Dahlui M et al. Change in public awareness of colorectal cancer symptoms following the Be Cancer Alert Campaign in the multi-ethnic population of Malaysia. BMC Cancer 20(1), 1–12 (2020).
    • 22. Hassan MRA, Khazim WKW, Mustapha NRN, Othman Z. National cancer patient registry-colorectal cancer in Malaysia. Ann. Oncol. 24, iv97 (2013).
    • 23. Siegel RL, Miller KD, Goding Sauer A et al. Colorectal cancer statistics, 2020. CA Cancer J. Clin. 70(3), 145–164 (2020).
    • 24. Andrei P, Battuello P, Grasso G, Rovera E, Tesio N, Bardelli A. Integrated approaches for precision oncology in colorectal cancer: the more you know, the better. Semin. Cancer Biol. 84, 199–213 (2021).
    • 25. American Cancer Society Cancer facts and statistics (2015). www.cancer.org/research/cancer-facts-statistics/all-cancer-facts-figures/cancer-facts-figures-2015.html
    • 26. Levin B, Lieberman DA, McFarland B et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. Gastroenterology 134(5), 1570–1595 (2008).
    • 27. Simon K. Colorectal cancer development and advances in screening. Clin. Interv. Aging 11, 967 (2016).
    • 28. Mandel JS, Bond JH, Church TR et al. Reducing mortality from colorectal cancer by screening for fecal occult blood. N. Engl. J. Med. 328(19), 1365–1371 (1993).
    • 29. Bailey JR, Aggarwal A, Imperiale TF. Colorectal cancer screening: stool DNA and other noninvasive modalities. Gut Liver 10(2), 204 (2016).
    • 30. Schreuders EH, Grobbee EJ, Spaander MCW, Kuipers EJ. Advances in fecal tests for colorectal cancer screening. Curr. Treat. Options Gastroenterol. 14(1), 152–162 (2016).
    • 31. Dhaliwal A, Vlachostergios PJ, Oikonomou KG, Moshenyat Y. Fecal DNA testing for colorectal cancer screening: molecular targets and perspectives. World J. Gastrointest. Oncol. 7(10), 178 (2015).
    • 32. Ebell MH. Accuracy of fecal DNA and fecal immunochemical test for colorectal cancer detection. Am. Fam. Physician 90(5), 326 (2014).
    • 33. Vacante M, Ciuni R, Basile F, Biondi A. The liquid biopsy in the management of colorectal cancer: an overview. Biomedicines 8(9), 308 (2020).
    • 34. Nakayama G, Tanaka C, Kodera Y. Current options for the diagnosis, staging and therapeutic management of colorectal cancer. Gastrointest. Tumors 1(1), 25–32 (2014).
    • 35. Zauber AG, Winawer SJ, O’Brien MJ et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N. Engl. J. Med. 366, 687–696 (2012).
    • 36. De Wijkerslooth TR, Bossuyt PM, Dekker E. Strategies in screening for colon carcinoma. Neth. J. Med. 69(3), 112–119 (2011).
    • 37. Baxter N, Rabeneck L. New findings about the risks and limitations of colonoscopy used in the early detection of colorectal cancer. Healthc. Q. 12(2), 24–25 (2009).
    • 38. Cuyle P-J, Prenen H. Current and future biomarkers in the treatment of colorectal cancer. Acta Clin. Belg. 72(2), 103–115 (2017).
    • 39. Tournigand C, Andre T, Bonnetain F et al. Adjuvant therapy with fluorouracil and oxaliplatin in stage II and elderly patients (between ages 70 and 75 years) with colon cancer: subgroup analyses of the multicenter international study of oxaliplatin, fluorouracil, and leucovorin in the adjuvant treatment of colon cancer trial. J. Clin. Oncol. 30(27), 3353–3360 (2012).
    • 40. Andre T, Boni C, Mounedji-Boudiaf L et al. Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer. N. Engl. J. Med. 350(23), 2343–2351 (2004).
    • 41. Haller DG, Tabernero J, Maroun J et al. Capecitabine plus oxaliplatin compared with fluorouracil and folinic acid as adjuvant therapy for stage III colon cancer. J. Clin. Oncol. 29(11), 1465–1471 (2011).
    • 42. Yothers G, O’Connell MJ, Allegra CJ et al. Oxaliplatin as adjuvant therapy for colon cancer: updated results of NSABP C-07 trial, including survival and subset analyses. J. Clin. Oncol. 29(28), 3768 (2011).
    • 43. Ciombor KK, Wu C, Goldberg RM. Recent therapeutic advances in the treatment of colorectal cancer. Annu. Rev. Med. 66, 83–95 (2015).
    • 44. Carethers JM. Systemic treatment of advanced colorectal cancer: tailoring therapy to the tumor. Therap. Adv. Gastroenterol. 1(1), 33–42 (2008).
    • 45. Wolpin BM, Mayer RJ. Systemic treatment of colorectal cancer. Gastroenterology. 134(5), 1296–1310 (2008).
    • 46. Imperiale TF, Ransohoff DF, Itzkowitz SH et al. Multitarget stool DNA testing for colorectal-cancer screening. N. Engl. J. Med. 370(14), 1287–1297 (2014).
    • 47. Inadomi JM, Vijan S, Janz NK et al. Adherence to colorectal cancer screening: a randomized clinical trial of competing strategies. Arch. Intern. Med. 172(7), 575–582 (2012).
    • 48. Lone SN, Nisar S, Masoodi T et al. Liquid biopsy: a step closer to transform diagnosis, prognosis and future of cancer treatments. Mol. Cancer 21(1), 1–22 (2022).
    • 49. Oshi M, Murthy V, Takahashi H et al. Urine as a source of liquid biopsy for cancer. Cancers (Basel). 13(11), 2652 (2021).
    • 50. Lim M, Kim C-J, Sunkara V, Kim M-H, Cho Y-K. Liquid biopsy in lung cancer: clinical applications of circulating biomarkers (CTCs and ctDNA). Micromachines 9(3), 100 (2018).
    • 51. Kudryavtseva AV, Lipatova AV, Zaretsky AR et al. Important molecular genetic markers of colorectal cancer. Oncotarget 7(33), 53959 (2016).
    • 52. Watanabe T, Kanazawa T, Kazama Y, Tanaka J, Tanaka T, Nagawa H. Microsatellite instability in adenoma as a possible marker to identify HNPCC patients. Am. J. Gastroenterol. 101(1), 204 (2006).
    • 53. Ellegren H. Microsatellites: simple sequences with complex evolution. Nat. Rev. Genet. 5(6), 435–445 (2004).
    • 54. Yamamoto H, Imai K. Microsatellite instability: an update. Arch. Toxicol. 89(6), 899–921 (2015).
    • 55. Setaffy L, Langner C. Microsatellite instability in colorectal cancer: clinicopathological significance. Polish J. Pathol. 66(3), 203–218 (2015).
    • 56. Casak SJ, Marcus L, Fashoyin-Aje L et al. FDA approval summary: pembrolizumab for the first-line treatment of patients with MSI-H/dMMR advanced unresectable or metastatic colorectal carcinoma. Clin. Cancer Res. 27(17), 4680–4684 (2021).
    • 57. Aguiar-Ibáñez R, Hardern C, van Hees F et al. Cost–effectiveness of pembrolizumab for the first-line treatment of patients with unresectable or metastatic MSI-H/dMMR colorectal cancer in the United States. J. Med. Econ. 25(1), 469–480 (2022).
    • 58. Lofton-Day C, Model F, DeVos T et al. DNA methylation biomarkers for blood-based colorectal cancer screening. Clin. Chem. 54(2), 414–423 (2008).
    • 59. Han M, Liew CT, Zhang HW et al. Novel blood-based, five-gene biomarker set for the detection of colorectal cancer. Clin. Cancer Res. 14(2), 455–460 (2008).
    • 60. Oh T, Kim N, Moon Y et al. Genome-wide identification and validation of a novel methylation biomarker, SDC2, for blood-based detection of colorectal cancer. J. Mol. Diagnostics 15(4), 498–507 (2013).
    • 61. Thierry AR, Mouliere F, El Messaoudi S et al. Clinical validation of the detection of KRAS and BRAF mutations from circulating tumor DNA. Nat. Med. 20(4), 430–435 (2014).
    • 62. Yen L-C, Yeh Y-S, Chen C-W et al. Detection of KRAS oncogene in peripheral blood as a predictor of the response to cetuximab plus chemotherapy in patients with metastatic colorectal cancer. Clin. Cancer Res. 15(13), 4508–4513 (2009).
    • 63. Habermann JK, Roblick UJ, Luke BT et al. Increased serum levels of complement C3a anaphylatoxin indicate the presence of colorectal tumors. Gastroenterology 131(4), 1020–1029 (2006).
    • 64. Albrethsen J, Bøgebo R, Gammeltoft S, Olsen J, Winther B, Raskov H. Upregulated expression of human neutrophil peptides 1, 2 and 3 (HNP 1-3) in colon cancer serum and tumours: a biomarker study. BMC Cancer 5(1), 1–10 (2005).
    • 65. Lee H, Rhee H, Kang HJ et al. Macrophage migration inhibitory factor may be used as an early diagnostic marker in colorectal carcinomas. Am. J. Clin. Pathol. 129(5), 772–779 (2008).
    • 66. Mroczko B, Groblewska M, Wereszczynska-Siemiatkowska U, Kedra B, Konopko M, Szmitkowski M. The diagnostic value of G-CSF measurement in the sera of colorectal cancer and adenoma patients. Clin. Chim. Acta 371(1–2), 143–147 (2006).
    • 67. Yu J, Zhai X, Li X et al. Identification of MST1 as a potential early detection biomarker for colorectal cancer through a proteomic approach. Sci. Rep. 7(1), 1–10 (2017).
    • 68. Xie Y-H, Chen Y-X, Fang J-Y. Comprehensive review of targeted therapy for colorectal cancer. Signal Transduct. Target. Ther. 5(1), 1–30 (2020).
    • 69. Alix-Panabieres C, Pantel K. Clinical applications of circulating tumor cells and circulating tumor DNA as liquid biopsy. Cancer Discov. 6(5), 479–491 (2016).
    • 70. Markou A, Tzanikou E, Lianidou E. The potential of liquid biopsy in the management of cancer patients. Semin. Cancer Biol. 84, 69–79 (2022).
    • 71. Dasari A, Morris VK, Allegra CJ et al. ctDNA applications and integration in colorectal cancer: an NCI Colon and Rectal–Anal Task Forces whitepaper. Nat. Rev. Clin. Oncol. 17(12), 757–770 (2020).
    • 72. Batth IS, Mitra A, Manier S et al. Circulating tumor markers: harmonizing the yin and yang of CTCs and ctDNA for precision medicine. Ann. Oncol. 28(3), 468–477 (2017).
    • 73. Siravegna G, Marsoni S, Siena S, Bardelli A. Integrating liquid biopsies into the management of cancer. Nat. Rev. Clin. Oncol. 14(9), 531–548 (2017).
    • 74. Yu W, Hurley J, Roberts D et al. Exosome-based liquid biopsies in cancer: opportunities and challenges. Ann. Oncol. 32(4), 466–477 (2021).
    • 75. Ludwig JA, Weinstein JN. Biomarkers in cancer staging, prognosis and treatment selection. Nat. Rev. Cancer 5(11), 845–856 (2005).
    • 76. Gutierrez-Reyes CD, Jiang P, Atashi M et al. Advances in mass spectrometry-based glycoproteomics: an update covering the period 2017–2021. Electrophoresis 43(1–2), 370–387 (2022).
    • 77. Peixoto A, Relvas-Santos M, Azevedo R, Santos LL, Ferreira JA. Protein glycosylation and tumor microenvironment alterations driving cancer hallmarks. Front. Oncol. 9(9), 380 (2019).
    • 78. Hanzawa K, Tanaka-Okamoto M, Murakami H et al. Increased levels of acidic free-N-glycans, including multi-antennary and fucosylated structures, in the urine of cancer patients. PLOS ONE 17(4), e0266927 (2022).
    • 79. Azevedo R, Peixoto A, Gaiteiro C et al. Over forty years of bladder cancer glycobiology: where do glycans stand facing precision oncology? Oncotarget 8(53), 91734–91764 (2017).
    • 80. Reily C, Stewart TJ, Renfrow MB, Novak J. Glycosylation in health and disease. Nat. Rev. Nephrol. 15(6), 346–366 (2019).
    • 81. Bennett EP, Mandel U, Clausen H, Gerken TA, Fritz TA, Tabak LA. Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology 22(6), 736–756 (2012).
    • 82. Schjoldager KT, Narimatsu Y, Joshi HJ, Clausen H. Global view of human protein glycosylation pathways and functions. Nat. Rev. Mol. Cell Biol. 21(12), 729–749 (2020).
    • 83. Kailemia MJ, Park D, Lebrilla CB. Glycans and glycoproteins as specific biomarkers for cancer. Anal. Bioanal. Chem. 409, 395–410 (2017).
    • 84. Locker GY, Hamilton S, Harris J et al. ASCO 2006 update of recommendations for the use of tumor markers in gastrointestinal cancer. J. Clin. Oncol. 24(33), 5313–5327 (2006).
    • 85. Duffy MJ. Carcinoembryonic antigen as a marker for colorectal cancer: is it clinically useful? Clin. Chem. 47(4), 624–630 (2001).
    • 86. Xie H-L, Gong Y-Z, Kuang J-A, Gao F, Tang S-Y, Gan J-L. The prognostic value of the postoperative serum CEA levels/preoperative serum CEA levels ratio in colorectal cancer patients with high preoperative serum CEA levels. Cancer Manag. Res. 11, 7499 (2019).
    • 87. Ferreira JA, Magalhaes A, Gomes J et al. Protein glycosylation in gastric and colorectal cancers: toward cancer detection and targeted therapeutics. Cancer Lett. 387, 32–45 (2017).
    • 88. Pinho SS, Reis CA. Glycosylation in cancer: mechanisms and clinical implications. Nat. Rev. Cancer 15(9), 540–555 (2015).
    • 89. Mereiter S, Balmana M, Campos D, Gomes J, Reis CA. Glycosylation in the era of cancer-targeted therapy: where are we heading? Cancer Cell 36(1), 6–16 (2019).
    • 90. Marcos NT, Bennett EP, Gomes J et al. ST6GalNAc-I controls expression of sialyl-Tn antigen in gastrointestinal tissues. Front. Biosci. 3(4), 1443–1455 (2011).
    • 91. Reis CA, Osorio H, Silva L, Gomes C, David L. Alterations in glycosylation as biomarkers for cancer detection. J. Clin. Pathol. 63(4), 322–329 (2010).
    • 92. Fernandes E, Sores J, Cotton S et al. Esophageal, gastric and colorectal cancers: looking beyond classical serological biomarkers towards glycoproteomics-assisted precision oncology. Theranostics 10(11), 4903–4928 (2020).
    • 93. Van’t Veer LJ, Dai H, Van De Vijver MJ et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 415(6871), 530–536 (2002).
    • 94. Espina V, Woodhouse EC, Wulfkuhle J, Asmussen HD, Petricoin EF III, Liotta LA. Protein microarray detection strategies: focus on direct detection technologies. J. Immunol. Methods 290(1–2), 121–133 (2004).
    • 95. Kulasingam V, Diamandis EP. Strategies for discovering novel cancer biomarkers through utilization of emerging technologies. Nat. Clin. Pract. Oncol. 5(10), 588–599 (2008).
    • 96. Abrahams JL, Taherzadeh G, Jarvas G, Guttman A, Zhou Y, Campbell MP. Recent advances in glycoinformatic platforms for glycomics and glycoproteomics. Curr. Opin. Struct. Biol. 62, 56–69 (2020).
    • 97. Ruhaak LR, Zauner G, Huhn C, Bruggink C, Deelder AM, Wuhrer M. Glycan labeling strategies and their use in identification and quantification. Anal. Bioanal. Chem. 397(8), 3457–3481 (2010).
    • 98. Kay Li Q, Gabrielson E, Zhang H. Application of glycoproteomics for the discovery of biomarkers in lung cancer. Proteomics Clin. Appl. 6(5–6), 244–256 (2012).
    • 99. Engwegen JYMN, Helgason HH, Cats A et al. Identification of serum proteins discriminating colorectal cancer patients and healthy controls using surface-enhanced laser desorption ionisation-time of flight mass spectrometry. World J. Gastroenterol. 12(10), 1536 (2006).
    • 100. Mesri M. Advances in proteomic technologies and its contribution to the field of cancer. Adv. Med. 2014, 238045 (2014).
    • 101. Mendes ML, Dittmar G. Targeted proteomics on its way to discovery. Proteomics 22(15–16), 2100330 (2022).
    • 102. Riley NM, Bertozzi CR, Pitteri SJ. A pragmatic guide to enrichment strategies for mass spectrometry-based glycoproteomics. Mol. Cell. Proteomics 20, 100029 (2021).
    • 103. Shen F, Xiong Y, Zhang L et al. Rapid sample preparation workflow for serum sample analysis with different mass spectrometry acquisition strategies. Anal. Chem. 93(3), 1578–1585 (2020).
    • 104. Shinozaki E, Tanabe K, Akiyoshi T et al. Serum leucine-rich alpha-2-glycoprotein-1 with fucosylated triantennary N-glycan: a novel colorectal cancer marker. BMC Cancer 18, 406 (2018).
    • 105. Qiu Y, Patwa TH, Xu L et al. Plasma glycoprotein profiling for colorectal cancer biomarker identification by lectin glycoarray and lectin blot. J. Proteome Res. 7(4), 1693–1703 (2008).
    • 106. Lindpaintner K, Desai K, Xu G et al. Identifying potential glycoproteomic biomarkers for diagnosis of colorectal cancer (CRC). J. Clin. Oncol. 40(Suppl. 16), e15529 (2022).
    • 107. Wei H, Cheng Z, Ouyang C et al. Glycoprotein screening in colorectal cancer based on differentially expressed Tn antigen. Oncol. Rep. 36(3), 1313–1324 (2016).
    • 108. Gong Q, Zhang X, Liang A et al. Proteomic screening of potential N-glycoprotein biomarkers for colorectal cancer by TMT labeling combined with LC–MS/MS. Clin. Chim. Acta 521, 122–130 (2021).
    • 109. Lindpaintner K, Mitchell A, Pickering C et al. Glycoproteomics as a powerful liquid biopsy-based predictor of checkpoint inhibitor treatment benefit in metastatic malignant melanoma. J. Clin. Oncol. 40(Suppl. 16), 9545 (2022).
    • 110. Mitchell A, Srinivasan A, Xu G et al. Predicting breast cancer in women using liquid biopsy-derived glycoproteomic markers. J. Clin. Oncol. 40(Suppl. 16), e12545 (2022).
    • 111. Mitchell A, Pickering C, Xu G et al. Glycoproteomics as a powerful liquid biopsy-based screening tool for non-small cell lung cancer. J. Clin. Oncol. 40(Suppl. 16), e21148 (2022).
    • 112. Serie D, Moser K, Pickering C et al. Liquid-biopsy-derived glycoproteomic profiling as a novel means for noninvasive diagnosis of ovarian cancer. J. Clin. Oncol. 40(Suppl. 16), e17604 (2022).
    • 113. Serie D, Pickering C, Rice R et al. Serum glycoproteomic signatures and association with survival in patients with bone and soft tissue sarcoma treated with immune-checkpoint inhibitor therapy. J. Clin. Oncol. 40(Suppl. 16), 11546 (2022).
    • 114. Al-wajeeh AS, Ismail MN, Salhimi SM et al. Identification of glycobiomarker candidates for breast cancer using LTQ-Orbitrap fusion technique. Int. J. Pharmacol. 13(5), 425–437 (2017).
    • 115. Wong Y-L, Anand R, Yuen KM et al. Identification of potential glycoprotein biomarkers in oral squamous cell carcinoma using sweet strategies. Glycoconj. J. 38(1), 1–11 (2021).
    • 116. Chokchaichamnankit D, Watcharatanyatip K, Subhasitanont P et al. Urinary biomarkers for the diagnosis of cervical cancer by quantitative label-free mass spectrometry analysis. Oncol. Lett. 17(6), 5453–5468 (2019).
    • 117. Boonyapranai K, Ounjaijean S, Kulprachakarn K et al. Haptoglobin polymorphisms and fucosylation change: possible influence of variation on the identified lung cancer-relevant biomarkers. Curr. Proteomics 18(3), 380–389 (2020).
    • 118. Chantaraamporn J, Champattanachai V, Khongmanee A et al. Glycoproteomic analysis reveals aberrant expression of complement C9 and fibronectin in the plasma of patients with colorectal cancer. Proteomes 8(3), 26 (2020).
    • 119. Ye Z, Vakhrushev SY. The role of data-independent acquisition for glycoproteomics. Mol. Cell Proteomics 20, 100042 (2021).
    • 120. Iqbal MJ, Javed Z, Sadia H et al. Clinical applications of artificial intelligence and machine learning in cancer diagnosis: looking into the future. Cancer Cell Int. 21(1), 270 (2021).
    • 121. Nabirotchkin S, Peluffo AE, Rinaudo P, Yu J, Hajj R, Cohen D. Next-generation drug repurposing using human genetics and network biology. Curr. Opin. Pharmacol. 51, 78–92 (2020).
    • 122. Lindpaintner K. Glycoproteomics: a new era in biomarkers (2021). www.labnews.co.uk/article/2031446/glycoproteomics-a-new-era-in-biomarkers
    • 123. Ginghina O, Hudita A, Zamfir M et al. Liquid biopsy and artificial intelligence as tools to detect signatures of colorectal malignancies: a modern approach in patient’s stratification. Front. Oncol. 12(March), 1–22 (2022).
    • 124. Dlamini Z, Francies FZ, Hull R, Marima R. Artificial intelligence (AI) and big data in cancer and precision oncology. Comput. Struct. Biotechnol. J. 18, 2300–2311 (2020).
    • 125. Wang Y, He X, Nie H, Zhou J, Cao P, Ou C. Application of artificial intelligence to the diagnosis and therapy of colorectal cancer. Am. J. Cancer Res. 10(11), 3575–3598 (2020).
    • 126. Kasi PM, Shen L, Ramachandran P et al. Serum glycoproteomic-based liquid biopsy for the detection of pancreatic ductal adenocarcinoma. J. Clin. Oncol. 38(Suppl. 4), 763 (2020).
    • 127. Lindpaintner K, Cheng M, Prendergast J et al. Blood-based glycoprotien signatures in advanced non-small-cell lung carcinoma (NSCLC) receiving first-line immune checkpoint blockade. J. Immunother. Cancer 9(Suppl. 2), A35 (2021).
    • 128. Ramachandran P, Xu G, Huang HH et al. Serum glycoprotein markers in nonalcoholic steatohepatitis and hepatocellular carcinoma. J. Proteome Res. 21(4), 1083–1094 (2022).
    • 129. Pickering C, Zhou B, Xu G et al. Differential peripheral blood glycoprotein profiles in symptomatic and asymptomatic COVID-19. Viruses 14(3), 553 (2022).
    • 130. Mitsala A, Tsalikidis C, Pitiakoudis M, Simopoulos C, Tsaroucha AK. Artificial intelligence in colorectal cancer screening, diagnosis and treatment. A new era. Curr. Oncol. 28(3), 1581–1607 (2021).
    • 131. Zhou H, Zhu L, Song J et al. Liquid biopsy at the frontier of detection, prognosis and progression monitoring in colorectal cancer. Mol. Cancer 21(1), 86 (2022).
    • 132. Taghiakbari M, Mori Y, von Renteln D. Artificial intelligence-assisted colonoscopy: a review of current state of practice and research. World J. Gastroenterol. 27(47), 8103 (2021).
    • 133. Wang W, Yin Y, Shan X et al. The value of plasma-based microRNAs as diagnostic biomarkers for ovarian cancer. Am. J. Med. Sci. 358(4), 256–267 (2019).
    • 134. Chen H, Zhou Q. Detecting liquid remnants of solid tumors treated with curative intent: circulating tumor DNA as a biomarker of minimal residual disease. Oncol. Rep. 49(5), 1–13 (2023).
    • 135. Almeida A, Kolarich D. The promise of protein glycosylation for personalised medicine. Biochim. Biophys. Acta 1860(8), 1583–1595 (2016).
    • 136. Jain KK. Role of oncoproteomics in the personalized management of cancer. Expert Rev. Proteomics 1(1), 49–55 (2004).
    • 137. Gubatan J, Levitte S, Patel A, Balabanis T, Wei MT, Sinha SR. Artificial intelligence applications in inflammatory bowel disease: emerging technologies and future directions. World J. Gastroenterol. 27(17), 1920 (2021).
    • 138. Liu Y, Zhang C, Wang Q et al. Global, regional, and national burden of colorectal cancer and attributable risk factors, from 1990 to 2019: updated results from the Global Burden of Disease Study 2019. Res. Square 7(7), 627–647 (2022).
    • 139. Soon S, Chia JW, Chew MH, Tan WS, Yang XY, Wee HL. Gender-specific patterns of productivity loss in colorectal cancer survivors in a multi-ethnic Asian population. Value Health 19(7), A807 (2016).
    • 140. WHO. Cardiovascular diseases, diabetes and cancer cost nearly RM 9 billion productivity losses annually to Malaysian economy (2020). www.who.int/malaysia/news/detail/08-09-2020-cardiovascular-diseases-diabetes-and-cancer-cost-nearly-rm-9-billion-productivity-losses-annually-to-malaysian-economy
    • 141. Kong Y-C, Sakti V-V, Sullivan R, Bhoo-Pathy N. Cancer and COVID-19: economic impact on households in southeast Asia. Ecancermedicalscience 14, 1134 (2020).
    • 142. Azzani M, Dahlui M, Ishak WZW, Roslani AC, Su TT. Provider costs of treating colorectal cancer in government hospital of Malaysia. Malaysian J. Med. Sci. 26(1), 73 (2019).
    • 143. Bradley CJ, Lansdorp-Vogelaar I, Yabroff KR et al. Productivity savings from colorectal cancer prevention and control strategies. Am. J. Prev. Med. 41(2), e5–e14 (2011).
    • 144. Heavener T, McStay FW, Jaeger V et al. Assessing adherence and cost-benefit of colorectal cancer screening for accountable providers. Presented at: Baylor University Medical Center Proceedings. Taylor & Francis. 32(4), 490–497 (2019).
    • 145. van Ballegooijen M, Habbema JDF, Boer R et al. Acomparison of the cost-effectiveness of fecal occult blood tests with different test characteristics in the context of annual screening in the Medicare population. (2015).
    • 146. UKM. Colorectal Cancer Screening | The Malaysian Cohort. https://www.ukm.my/mycohort/ms/colorectal-cancer-screening/
    • 147. Cologuard® Cost | Cologuard Patient Site. https://www.cologuard.com/affordable
    • 148. Guardant Health, Inc. Guardant Health Receives ADLT Status from CMS for FDA-Approved Guardant360R CDx Test. https://investors.guardanthealth.com/press-releases/press-releases/2021/Guardant-Health-Receives-ADLT-Status-from-CMS-for-FDA-Approved-Guardant360-CDx-Test/default.aspx
    • 149. Karol D, McKinnon M, Mukhtar L et al. The impact of foundation medicine testing on cancer patients: A single academic centre experience. Front. Oncol. 11, 687730 (2021).
    • 150. Young PE, Womeldorph CM. Colonoscopy for colorectal cancer screening. J. Cancer 4(3), 217–226 (2013).
    • 151. Osborne JM, Wilson C, Moore V, Gregory T, Flight I, Young GP. Sample preference for colorectal cancer screening tests: blood or stool? Open J. Prev. Med. 2(3), 326–331 (2012).
    • 152. Precedence Research. Liquid Biopsy Market Size to Hit US$ 26.2 Billion by 2030 (2021). www.globenewswire.com/en/news-release/2021/12/14/2351913/0/en/Liquid-Biopsy-Market-Size-to-Hit-US-26-2-Billion-by-2030.html
    • 153. Timothy G. ‘Singapore medical company invents non-invasive cancer screening tests; receives US$20m in funding | The Straits Times’ (2019). www.straitstimes.com/singapore/health/singapore-medical-company-invents-non-invasive-cancer-screening-tests-receives
    • 154. Mazouji O, Ouhajjou A, Incitti R, Mansour H. Updates on clinical use of liquid biopsy in colorectal cancer screening, diagnosis, follow-up, and treatment guidance. Front. Cell Dev. Biol. 9(May), 660924 (2021).
    • 155. Bakker E, Hendrikse NM, Ehmann F et al. Biomarker qualification at the European Medicines Agency: a review of biomarker qualification procedures from 2008 to 2020. Clin. Pharmacol. Ther. 112(1), 69–80 (2022).
    • 156. Food and Drug Administration. HHS. International conference on harmonisation; guidance on e16 biomarkers related to drug or biotechnology product development: context, structure, and format of qualification submissions; availability. Notice. Federal register 76(155), 49773–49774 (2011).
    • 157. Menetski JP, Hoffmann SC, Cush SS et al. The Foundation for the National Institutes of Health Biomarkers Consortium: past accomplishments and new strategic direction. Clin. Pharmacol. Ther. 105(4), 829–843 (2019).
    • 158. See HY, Mohamed MS, Nor SNM, Low WY. Challenges in the ethical review of clinical and biomedical research in Malaysia: a mixed methods study. J. Empir. Res. Hum. Res. Ethics 16(5), 487–500 (2021).
    • 159. Glasziou P, Scott AM, Chalmers I, Kolstoe SE, Davies HT. Improving research ethics review and governance can improve human health. J. R. Soc. Med. 114(12), 556–562 (2021).
    • 160. Universiti Kebangsaan Malaysia. BIOBANK | UKM Medical Molecular Biology Institute (2022). www.ukm.my/umbi/?s=BIOBANK
    • 161. Zain RB, Athirajan V, Ghani WMN et al. An oral cancer biobank initiative: a platform for multidisciplinary research in a developing country. Cell Tissue Bank. 14(1), 45–52 (2013).
    • 162. Baláž V, Jeck T, Balog M. Economics of biobanking: business or public good? Literature review, structural and thematic analysis. Soc. Sci. 11(7), 288 (2022).
    • 163. Chong HY, Allotey PA, Chaiyakunapruk N. Current landscape of personalized medicine adoption and implementation in southeast Asia. BMC Med. Genomics 11(1), 1–15 (2018).