Skip to main content
SpringerLink
Log in

Fecal Fatty Acid Profiling as a Potential New Screening Biomarker in Patients with Colorectal Cancer

  • Original Article
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

Background

The fatty acid profile of the fecal metabolome and its association with colorectal cancer (CRC) has not been fully evaluated.

Aims

We aimed to compare the fecal fatty acid profiles of CRC patients and healthy controls.

Methods

We enrolled 26 newly diagnosed CRC patients and 28 healthy individuals between July 2014 and August 2014 from our institute. Long- and short-chain fatty acids were extracted from fecal samples and analyzed using gas chromatography–mass spectrometry.

Results

Regarding fecal long-chain fatty acids, the levels of total ω-6 polyunsaturated fatty acids and, particularly, of linoleic acid (C18:2ω-6) were significantly higher in male CRC patients than in healthy men (2.750 ± 2.583 vs. 1.254 ± 0.966 µg/mg feces, P = 0.040; 2.670 ± 2.507 vs. 1.226 ± 0.940 µg/mg feces, P = 0.034, respectively). In addition, the levels of total monounsaturated fatty acid and, particularly, of oleic acid (C18:1ω-9) were significantly higher in male CRC patients than in healthy men (1.802 ± 1.331 vs. 0.977 ± 0.625 µg/mg feces, P = 0.027; 1.749 ± 1.320 vs. 0.932 ± 0.626 µg/mg feces, P = 0.011, respectively). However, those differences were not shown in female gender. The level of fecal short-chain fatty acids was not different between CRC patients and healthy controls.

Conclusions

There were changes in the profiles of fecal fatty acid metabolomes in CRC patients compared to healthy controls, implying that fecal fatty acids could be used as a novel screening tool for CRC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55:74–108.

    Article  PubMed  Google Scholar 

  2. Haggar FA, Boushey RP. Colorectal cancer epidemiology: incidence, mortality, survival, and risk factors. Clin Colon Rectal Surg. 2009;22:191–197.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bingham SA. Diet and colorectal cancer prevention. Biochem Soc Trans. 2000;28:12–16.

    Article  CAS  PubMed  Google Scholar 

  4. Park SY, Boushey CJ, Wilkens LR, Haiman CA, Le Marchand L. High-quality diets associate with reduced risk of colorectal cancer: analyses of diet quality indexes in the multiethnic cohort. Gastroenterology. 2017;153:386–394.

    Article  PubMed  Google Scholar 

  5. Das S, Martinez LR, Ray S. Phospholipid remodeling and eicosanoid signaling in colon cancer cells. Indian J Biochem Biophys. 2014;51:512–519.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Bamia C, Lagiou P, Buckland G, et al. Mediterranean diet and colorectal cancer risk: results from a European cohort. Eur J Epidemiol. 2013;28:317–328.

    Article  CAS  PubMed  Google Scholar 

  7. De Filippo C, Cavalieri D, Di Paola M, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010;107:14691–14696.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Walker AW, Ince J, Duncan SH, et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011;5:220–230.

    Article  CAS  PubMed  Google Scholar 

  9. Xiao L, Sonne SB, Feng Q, et al. High-fat feeding rather than obesity drives taxonomical and functional changes in the gut microbiota in mice. Microbiome. 2017;5:43.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Quigley EM. Gut bacteria in health and disease. Gastroenterol Hepatol (N Y). 2013;9:560–569.

    Google Scholar 

  11. Sobhani I, Tap J, Roudot-Thoraval F, et al. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS One. 2011;6:e16393.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Castellarin M, Warren RL, Freeman JD, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 2012;22:299–306.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Jacob H, Toyonaga T, Ohara Y, et al. Endoscopic submucosal dissection of cecal lesions in proximity to the appendiceal orifice. Endoscopy. 2016;48:829–836.

    Article  PubMed  Google Scholar 

  14. Wisniewski JR, Dus-Szachniewicz K, Ostasiewicz P, Ziolkowski P, Rakus D, Mann M. Absolute proteome analysis of colorectal mucosa, adenoma, and cancer reveals drastic changes in fatty acid metabolism and plasma membrane transporters. J Proteome Res. 2015;14:4005–4018.

    Article  CAS  PubMed  Google Scholar 

  15. Jacobs DM, Deltimple N, van Velzen E, et al. (1)H NMR metabolite profiling of feces as a tool to assess the impact of nutrition on the human microbiome. NMR Biomed. 2008;21:615–626.

    Article  CAS  PubMed  Google Scholar 

  16. Matsumoto M, Benno Y. Consumption of Bifidobacterium lactis LKM512 yogurt reduces gut mutagenicity by increasing gut polyamine contents in healthy adult subjects. Mutat Res. 2004;568:147–153.

    Article  CAS  PubMed  Google Scholar 

  17. Awad AB, Chattopadhyay JP, Danahy ME. Effect of dietary fat composition on rat colon plasma membranes and fecal lipids. J Nutr. 1989;119:1376–1382.

    Article  CAS  PubMed  Google Scholar 

  18. Park Y, Lee J, Oh JH, Shin A, Kim J. Dietary patterns and colorectal cancer risk in a Korean population: a case-control study. Medicine (Baltimore). 2016;95:e3759.

    Article  CAS  Google Scholar 

  19. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226:497–509.

    CAS  PubMed  Google Scholar 

  20. Pickens CA, Albuquerque Pereira MF, Fenton JI. Long-chain omega-6 plasma phospholipid polyunsaturated fatty acids and association with colon adenomas in adult men: a cross-sectional study. Eur J Cancer Prev. 2017;26:497–505.

    Article  CAS  PubMed  Google Scholar 

  21. McEntee MF, Whelan J. Dietary polyunsaturated fatty acids and colorectal neoplasia. Biomed Pharmacother. 2002;56:380–387.

    Article  CAS  PubMed  Google Scholar 

  22. Hodge AM, Williamson EJ, Bassett JK, MacInnis RJ, Giles GG, English DR. Dietary and biomarker estimates of fatty acids and risk of colorectal cancer. Int J Cancer. 2015;137:1224–1234.

    Article  CAS  PubMed  Google Scholar 

  23. Weijenberg MP, Luchtenborg M, de Goeij AF, et al. Dietary fat and risk of colon and rectal cancer with aberrant MLH1 expression, APC or KRAS genes. Cancer Causes Control. 2007;18:865–879.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Cottet V, Collin M, Gross AS, et al. Erythrocyte membrane phospholipid fatty acid concentrations and risk of colorectal adenomas: a case-control nested in the French E3 N-EPIC cohort study. Cancer Epidemiol Biomarkers Prev. 2013;22:1417–1427.

    Article  CAS  PubMed  Google Scholar 

  25. Macquart-Moulin G, Riboli E, Cornee J, Charnay B, Berthezene P, Day N. Case-control study on colorectal cancer and diet in Marseilles. Int J Cancer. 1986;38:183–191.

    Article  CAS  PubMed  Google Scholar 

  26. Bartoli R, Fernandez-Banares F, Navarro E, et al. Effect of olive oil on early and late events of colon carcinogenesis in rats: modulation of arachidonic acid metabolism and local prostaglandin E(2) synthesis. Gut. 2000;46:191–199.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Audano M, Maldini M, De Fabiani E, Mitro N, Caruso D. Gender-related metabolomics and lipidomics: from experimental animal models to clinical evidence. J Proteomics. 2017. https://doi.org/10.1016/j.jprot.2017.11.001.

    PubMed  Google Scholar 

  28. Psihogios NG, Gazi IF, Elisaf MS, Seferiadis KI, Bairaktari ET. Gender-related and age-related urinalysis of healthy subjects by NMR-based metabonomics. NMR Biomed. 2008;21:195–207.

    Article  CAS  PubMed  Google Scholar 

  29. Krumsiek J, Mittelstrass K, Do KT, et al. Gender-specific pathway differences in the human serum metabolome. Metabolomics. 2015;11:1815–1833.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Jove M, Mate I, Naudi A, et al. Human aging is a metabolome-related matter of gender. J Gerontol A Biol Sci Med Sci. 2016;71:578–585.

    Article  CAS  PubMed  Google Scholar 

  31. Gonzalez-Covarrubias V, Beekman M, Uh HW, et al. Lipidomics of familial longevity. Aging Cell. 2013;12:426–434.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Farshidfar F, Weljie AM, Kopciuk KA, et al. A validated metabolomic signature for colorectal cancer: exploration of the clinical value of metabolomics. Br J Cancer. 2016;115:848–857.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Xie G, Wang X, Zhao A, et al. Sex-dependent effects on gut microbiota regulate hepatic carcinogenic outcomes. Sci Rep. 2017;7:45232.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Ridlon JM, Ikegawa S, Alves JM, et al. Clostridium scindens: a human gut microbe with a high potential to convert glucocorticoids into androgens. J Lipid Res. 2013;54:2437–2449.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Weir TL, Manter DK, Sheflin AM, Barnett BA, Heuberger AL, Ryan EP. Stool microbiome and metabolome differences between colorectal cancer patients and healthy adults. PLoS One. 2013;8:e70803.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Bornet FR, Brouns F, Tashiro Y, Duvillier V. Nutritional aspects of short-chain fructooligosaccharides: natural occurrence, chemistry, physiology and health implications. Dig Liver Dis. 2002;34:S111–S120.

    Article  CAS  PubMed  Google Scholar 

  37. Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol. 2006;40:235–243.

    Article  CAS  PubMed  Google Scholar 

  38. Wang T, Cai G, Qiu Y, et al. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J. 2012;6:320–329.

    Article  CAS  PubMed  Google Scholar 

  39. Deda O, Gika H, Panagoulis T, Taitzoglou I, Raikos N, Theodoridis G. Impact of exercise on fecal and cecal metabolome over aging: a longitudinal study in rats. Bioanalysis. 2017;9:21–36.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, 88, Olympic-ro 43-gil, Songpa-gu, Seoul, 05505, Korea

    Eun Mi Song, Jeong-Sik Byeon, Sun-Ho Lee, Kiju Chang, Sung Wook Hwang & Dong-Hoon Yang

  2. Department of Convergence Medicine, Asan Medical Center, Asan Institute for Life Sciences, University of Ulsan College of Medicine, 88, Olympic-ro 43-gil, Songpa-gu, Seoul, 05505, Korea

    Sun Mi Lee, Hyun Ju Yoo, Su Jung Kim & Jin-Yong Jeong

Authors
  1. Eun Mi Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeong-Sik Byeon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sun Mi Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hyun Ju Yoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Su Jung Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sun-Ho Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kiju Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sung Wook Hwang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Dong-Hoon Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jin-Yong Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

EMS, JSB, and JYJ designed the study; SML, HJY, SJK, SHL, KJC, SWH, and DHY collected, interpreted, and analyzed the data; EMS performed the statistical analysis; SHL, KJC, SWH, and DHY cared for the patients and critically reviewed the manuscript; EMS, JSB, and JYJ drafted the manuscript; and JSB and JYJ are the guarantors of the article and approved the final manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Jeong-Sik Byeon or Jin-Yong Jeong.

Ethics declarations

Conflict of interest

Eun Mi Song, Jeong-Sik Byeon, Sun Mi Lee, Hyun Ju Yoo, Su Jung Kim, Sun-Ho Lee, Kiju Chang, Sung Wook Hwang, Dong-Hoon Yang, and Jin-Yong Jeong have no conflict of interest or financial ties to declare.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 26 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, E.M., Byeon, JS., Lee, S.M. et al. Fecal Fatty Acid Profiling as a Potential New Screening Biomarker in Patients with Colorectal Cancer. Dig Dis Sci 63, 1229–1236 (2018). https://doi.org/10.1007/s10620-018-4982-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10620-018-4982-y

Keywords

Search

Navigation