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Published in: BMC Medicine 1/2022

Open Access 01-12-2022 | Colorectal Cancer | Research article

Short-chain fatty acid concentrations in the incidence and risk-stratification of colorectal cancer: a systematic review and meta-analysis

Authors: Ehsan Alvandi, Wilson K. M. Wong, Mugdha V. Joglekar, Kevin J. Spring, Anandwardhan A. Hardikar

Published in: BMC Medicine | Issue 1/2022

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Abstract

Background

The beneficial role of gut microbiota and bacterial metabolites, including short-chain fatty acids (SCFAs), is well recognized, although the available literature around their role in colorectal cancer (CRC) has been inconsistent.

Methods

We performed a systematic review and meta-analysis to examine the associations of fecal SCFA concentrations to the incidence and risk of CRC. Data extraction through Medline, Embase, and Web of Science was carried out from database conception to June 29, 2022. Predefined inclusion/exclusion criteria led to the selection of 17 case-control and six cross-sectional studies for quality assessment and analyses. Studies were categorized for CRC risk or incidence, and RevMan 5.4 was used to perform the meta-analyses. Standardized mean differences (SMD) with 95% confidence intervals (CI) were calculated using a random-effects model. Studies lacking quantitation were included in qualitative analyses.

Results

Combined analysis of acetic, propionic, and butyric acid revealed significantly lower concentrations of these SCFAs in individuals with a high-risk of CRC (SMD = 2.02, 95% CI 0.31 to 3.74, P = 0.02). Additionally, CRC incidence was higher in individuals with lower levels of SCFAs (SMD = 0.45, 95% CI 0.19 to 0.72, P = 0.0009), compared to healthy individuals. Qualitative analyses identified 70.4% of studies reporting significantly lower concentrations of fecal acetic, propionic, butyric acid, or total SCFAs in those at higher risk of CRC, while 66.7% reported significantly lower concentrations of fecal acetic and butyric acid in CRC patients compared to healthy controls.

Conclusions

Overall, lower fecal concentrations of the three major SCFAs are associated with higher risk of CRC and incidence of CRC.
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Literature
1.
go back to reference 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):209–49.PubMedCrossRef 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):209–49.PubMedCrossRef
2.
go back to reference Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut. 2017;66(4):683–91.PubMedCrossRef Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut. 2017;66(4):683–91.PubMedCrossRef
3.
go back to reference Nguyen LH, Goel A, Chung DC. Pathways of colorectal carcinogenesis. Gastroenterology. 2020;158(2):291–302.PubMedCrossRef Nguyen LH, Goel A, Chung DC. Pathways of colorectal carcinogenesis. Gastroenterology. 2020;158(2):291–302.PubMedCrossRef
4.
go back to reference Dekker E, Tanis PJ, Vleugels JLA, Kasi PM, Wallace MB. Colorectal cancer. Lancet. 2019;394(10207):1467–80.PubMedCrossRef Dekker E, Tanis PJ, Vleugels JLA, Kasi PM, Wallace MB. Colorectal cancer. Lancet. 2019;394(10207):1467–80.PubMedCrossRef
5.
go back to reference Mármol I, Sánchez-De-Diego C, Pradilla Dieste A, Cerrada E, Rodriguez YM. Colorectal carcinoma: a general overview and future perspectives in colorectal cancer. Int J Mol Sci. 2017;18(1):197.PubMedCentralCrossRef Mármol I, Sánchez-De-Diego C, Pradilla Dieste A, Cerrada E, Rodriguez YM. Colorectal carcinoma: a general overview and future perspectives in colorectal cancer. Int J Mol Sci. 2017;18(1):197.PubMedCentralCrossRef
6.
go back to reference Wong SH, Yu J. Gut microbiota in colorectal cancer: mechanisms of action and clinical applications. Nat Rev Gastroenterol Hepatol. 2019;16(11):690–704.PubMedCrossRef Wong SH, Yu J. Gut microbiota in colorectal cancer: mechanisms of action and clinical applications. Nat Rev Gastroenterol Hepatol. 2019;16(11):690–704.PubMedCrossRef
7.
go back to reference Zhao Z, Feng Q, Yin Z, Shuang J, Bai B, Yu P, et al. Red and processed meat consumption and colorectal cancer risk: a systematic review and meta-analysis. Oncotarget. 2017;8(47):83306–14.PubMedPubMedCentralCrossRef Zhao Z, Feng Q, Yin Z, Shuang J, Bai B, Yu P, et al. Red and processed meat consumption and colorectal cancer risk: a systematic review and meta-analysis. Oncotarget. 2017;8(47):83306–14.PubMedPubMedCentralCrossRef
8.
go back to reference Chan DS, Lau R, Aune D, Vieira R, Greenwood DC, Kampman E, et al. Red and processed meat and colorectal cancer incidence: meta-analysis of prospective studies. PLoS One. 2011;6(6):e20456.PubMedPubMedCentralCrossRef Chan DS, Lau R, Aune D, Vieira R, Greenwood DC, Kampman E, et al. Red and processed meat and colorectal cancer incidence: meta-analysis of prospective studies. PLoS One. 2011;6(6):e20456.PubMedPubMedCentralCrossRef
9.
go back to reference Nucci D, Fatigoni C, Salvatori T, Nardi M, Realdon S, Gianfredi V. Association between dietary fibre intake and colorectal adenoma: a systematic review and meta-analysis. Int J Environ Res Public Health. 2021;18(8):4168. Nucci D, Fatigoni C, Salvatori T, Nardi M, Realdon S, Gianfredi V. Association between dietary fibre intake and colorectal adenoma: a systematic review and meta-analysis. Int J Environ Res Public Health. 2021;18(8):4168.
10.
go back to reference Oh H, Kim H, Lee DH, Lee A, Giovannucci EL, Kang SS, et al. Different dietary fibre sources and risks of colorectal cancer and adenoma: a dose-response meta-analysis of prospective studies. Br J Nutr. 2019;122(6):605–15.PubMedCrossRef Oh H, Kim H, Lee DH, Lee A, Giovannucci EL, Kang SS, et al. Different dietary fibre sources and risks of colorectal cancer and adenoma: a dose-response meta-analysis of prospective studies. Br J Nutr. 2019;122(6):605–15.PubMedCrossRef
11.
go back to reference Gianfredi V, Salvatori T, Villarini M, Moretti M, Nucci D, Realdon S. Is dietary fibre truly protective against colon cancer? A systematic review and meta-analysis. Int J Food Sci Nutr. 2018;69(8):904–15.PubMedCrossRef Gianfredi V, Salvatori T, Villarini M, Moretti M, Nucci D, Realdon S. Is dietary fibre truly protective against colon cancer? A systematic review and meta-analysis. Int J Food Sci Nutr. 2018;69(8):904–15.PubMedCrossRef
13.
14.
go back to reference Alexander C, Swanson KS, Fahey GC Jr, Garleb KA. Perspective: Physiologic importance of short-chain fatty acids from nondigestible carbohydrate fermentation. Adv Nutr. 2019;10(4):576–89.PubMedPubMedCentralCrossRef Alexander C, Swanson KS, Fahey GC Jr, Garleb KA. Perspective: Physiologic importance of short-chain fatty acids from nondigestible carbohydrate fermentation. Adv Nutr. 2019;10(4):576–89.PubMedPubMedCentralCrossRef
15.
go back to reference Parada Venegas D, De la Fuente MK, Landskron G, González MJ, Quera R, Dijkstra G, et al. Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol. 2019;10(277):1-16. Parada Venegas D, De la Fuente MK, Landskron G, González MJ, Quera R, Dijkstra G, et al. Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol. 2019;10(277):1-16.
16.
go back to reference Liu P, Wang Y, Yang G, Zhang Q, Meng L, Xin Y, et al. The role of short-chain fatty acids in intestinal barrier function, inflammation, oxidative stress, and colonic carcinogenesis. Pharmacol Res. 2021;165:105420.PubMedCrossRef Liu P, Wang Y, Yang G, Zhang Q, Meng L, Xin Y, et al. The role of short-chain fatty acids in intestinal barrier function, inflammation, oxidative stress, and colonic carcinogenesis. Pharmacol Res. 2021;165:105420.PubMedCrossRef
17.
go back to reference van der Beek CM, Dejong CHC, Troost FJ, Masclee AAM, Lenaerts K. Role of short-chain fatty acids in colonic inflammation, carcinogenesis, and mucosal protection and healing. Nutr Rev. 2017;75(4):286–305.PubMedCrossRef van der Beek CM, Dejong CHC, Troost FJ, Masclee AAM, Lenaerts K. Role of short-chain fatty acids in colonic inflammation, carcinogenesis, and mucosal protection and healing. Nutr Rev. 2017;75(4):286–305.PubMedCrossRef
18.
go back to reference Boutron-Ruault MC, Marteau P, Lavergne-Slove A, Myara A, Gerhardt MF, Franchisseur C, et al. Effects of a 3-mo consumption of short-chain fructo-oligosaccharides on parameters of colorectal carcinogenesis in patients with or without small or large colorectal adenomas. Nutr Cancer. 2005;53(2):160–8.PubMedCrossRef Boutron-Ruault MC, Marteau P, Lavergne-Slove A, Myara A, Gerhardt MF, Franchisseur C, et al. Effects of a 3-mo consumption of short-chain fructo-oligosaccharides on parameters of colorectal carcinogenesis in patients with or without small or large colorectal adenomas. Nutr Cancer. 2005;53(2):160–8.PubMedCrossRef
19.
go back to reference Bridges KM, Diaz FJ, Wang Z, Ahmed I, Sullivan DK, Umar S, et al. Relating stool microbial metabolite levels, inflammatory markers and dietary behaviors to screening colonoscopy findings in a racially/ethnically diverse patient population. Genes. 2018;9(3):119. Bridges KM, Diaz FJ, Wang Z, Ahmed I, Sullivan DK, Umar S, et al. Relating stool microbial metabolite levels, inflammatory markers and dietary behaviors to screening colonoscopy findings in a racially/ethnically diverse patient population. Genes. 2018;9(3):119.
20.
go back to reference Chen CY, Niu M, Pan JX, Du N, Liu SM, Li HQ, et al. Bacteroides, butyric acid and t10,c12-CLA changes in colorectal adenomatous polyp patients. Gut Pathogens. 2021;13(1):9.CrossRef Chen CY, Niu M, Pan JX, Du N, Liu SM, Li HQ, et al. Bacteroides, butyric acid and t10,c12-CLA changes in colorectal adenomatous polyp patients. Gut Pathogens. 2021;13(1):9.CrossRef
21.
go back to reference Chen HM, Yu YN, Wang JL, Lin YW, Kong X, Yang CQ, et al. Decreased dietary fiber intake and structural alteration of gut microbiota in patients with advanced colorectal adenoma. Am J Clin Nutr. 2013;97(5):1044–52.PubMedCrossRef Chen HM, Yu YN, Wang JL, Lin YW, Kong X, Yang CQ, et al. Decreased dietary fiber intake and structural alteration of gut microbiota in patients with advanced colorectal adenoma. Am J Clin Nutr. 2013;97(5):1044–52.PubMedCrossRef
22.
go back to reference Kashtan H, Stern HS, Jenkins DJA, Jenkins AL, Thompson LU, Hay K, et al. Colonic fermentation and markers of colorectal-cancer risk. Am J Clin Nutr. 1992;55(3):723–8.PubMedCrossRef Kashtan H, Stern HS, Jenkins DJA, Jenkins AL, Thompson LU, Hay K, et al. Colonic fermentation and markers of colorectal-cancer risk. Am J Clin Nutr. 1992;55(3):723–8.PubMedCrossRef
23.
go back to reference Lin Y, Ma C, Liu C, Wang Z, Yang J, Liu X, et al. NMR-based fecal metabolomics fingerprinting as predictors of earlier diagnosis in patients with colorectal cancer. Oncotarget. 2016;7(20):29454–64.PubMedPubMedCentralCrossRef Lin Y, Ma C, Liu C, Wang Z, Yang J, Liu X, et al. NMR-based fecal metabolomics fingerprinting as predictors of earlier diagnosis in patients with colorectal cancer. Oncotarget. 2016;7(20):29454–64.PubMedPubMedCentralCrossRef
24.
go back to reference Lin Y, Ma CC, Bezabeh T, Wang ZN, Liang JH, Huang Y, et al. H-1 NMR-based metabolomics reveal overlapping discriminatory metabolites and metabolic pathway disturbances between colorectal tumor tissues and fecal samples. Int J Cancer. 2019;145(6):1679–89.PubMedCrossRef Lin Y, Ma CC, Bezabeh T, Wang ZN, Liang JH, Huang Y, et al. H-1 NMR-based metabolomics reveal overlapping discriminatory metabolites and metabolic pathway disturbances between colorectal tumor tissues and fecal samples. Int J Cancer. 2019;145(6):1679–89.PubMedCrossRef
25.
go back to reference Monleon D, Morales JM, Barrasa A, Lopez JA, Vazquez C, Celda B. Metabolite profiling of fecal water extracts from human colorectal cancer. NMR Biomed. 2009;22(3):342–8.PubMedCrossRef Monleon D, Morales JM, Barrasa A, Lopez JA, Vazquez C, Celda B. Metabolite profiling of fecal water extracts from human colorectal cancer. NMR Biomed. 2009;22(3):342–8.PubMedCrossRef
26.
go back to reference Niccolai E, Baldi S, Ricci F, Russo E, Nannini G, Menicatti M, et al. Evaluation and comparison of short chain fatty acids composition in gut diseases. World J Gastroenterol. 2019;25(36):5543–58.PubMedPubMedCentralCrossRef Niccolai E, Baldi S, Ricci F, Russo E, Nannini G, Menicatti M, et al. Evaluation and comparison of short chain fatty acids composition in gut diseases. World J Gastroenterol. 2019;25(36):5543–58.PubMedPubMedCentralCrossRef
27.
go back to reference Ohigashi S, Sudo K, Kobayashi D, Takahashi O, Takahashi T, Asahara T, et al. Changes of the intestinal microbiota, short chain fatty acids, and fecal pH in patients with colorectal cancer. Dig Dis Sci. 2013;58(6):1717–26.PubMedCrossRef Ohigashi S, Sudo K, Kobayashi D, Takahashi O, Takahashi T, Asahara T, et al. Changes of the intestinal microbiota, short chain fatty acids, and fecal pH in patients with colorectal cancer. Dig Dis Sci. 2013;58(6):1717–26.PubMedCrossRef
28.
go back to reference Song EM, Byeon JS, Lee SM, Yoo HJ, Kim SJ, Lee SH, et al. Fecal fatty acid profiling as a potential new screening biomarker in patients with colorectal cancer. Dig Dis Sci. 2018;63(5):1229–36.PubMedCrossRef Song EM, Byeon JS, Lee SM, Yoo HJ, Kim SJ, Lee SH, et al. Fecal fatty acid profiling as a potential new screening biomarker in patients with colorectal cancer. Dig Dis Sci. 2018;63(5):1229–36.PubMedCrossRef
29.
go back to reference Sze MA, Topcuoglu BD, Lesniak NA, Ruffin MT, Schloss PD. Fecal short-chain fatty acids are not predictive of colonic tumor status and cannot be predicted based on bacterial community structure. mBio. 2019;10(4):e01454-19. Sze MA, Topcuoglu BD, Lesniak NA, Ruffin MT, Schloss PD. Fecal short-chain fatty acids are not predictive of colonic tumor status and cannot be predicted based on bacterial community structure. mBio. 2019;10(4):e01454-19.
30.
go back to reference Torii T, Kanemitsu K, Hagiwara A. Simultaneous assay of fecal short-chain fatty and bile acids and ratio of total bile acids to butyrate in colon cancer. Chromatography. 2019;40(2):49–57.CrossRef Torii T, Kanemitsu K, Hagiwara A. Simultaneous assay of fecal short-chain fatty and bile acids and ratio of total bile acids to butyrate in colon cancer. Chromatography. 2019;40(2):49–57.CrossRef
31.
go back to reference Weaver GA, Krause JA, Miller TL, Wolin MJ. Short chain fatty acid distributions of enema samples from a sigmoidoscopy population: an association of high acetate and low butyrate ratios with adenomatous polyps and colon cancer. Gut. 1988;29(11):1539–43.PubMedPubMedCentralCrossRef Weaver GA, Krause JA, Miller TL, Wolin MJ. Short chain fatty acid distributions of enema samples from a sigmoidoscopy population: an association of high acetate and low butyrate ratios with adenomatous polyps and colon cancer. Gut. 1988;29(11):1539–43.PubMedPubMedCentralCrossRef
32.
go back to reference 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(8):e70803. 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(8):e70803.
33.
go back to reference Yusuf F, Adewiah S, Fatchiyah F. The level short chain fatty acids and HSP 70 in colorectal cancer and non-colorectal cancer. Acta Informatica Medica. 2018;26(3):160–3.PubMedPubMedCentralCrossRef Yusuf F, Adewiah S, Fatchiyah F. The level short chain fatty acids and HSP 70 in colorectal cancer and non-colorectal cancer. Acta Informatica Medica. 2018;26(3):160–3.PubMedPubMedCentralCrossRef
34.
go back to reference Nannini G, Meoni G, Tenori L, Ringressi MN, Taddei A, Niccolai E, et al. Fecal metabolomic profiles: a comparative study of patients with colorectal cancer vs adenomatous polyps. World J Gastroenterol. 2021;27(38):6430–41.PubMedPubMedCentralCrossRef Nannini G, Meoni G, Tenori L, Ringressi MN, Taddei A, Niccolai E, et al. Fecal metabolomic profiles: a comparative study of patients with colorectal cancer vs adenomatous polyps. World J Gastroenterol. 2021;27(38):6430–41.PubMedPubMedCentralCrossRef
35.
go back to reference Ocvirk S, Posma JM, Li JV, Koller KR, Day GM, Flanagan CA, et al. A prospective cohort analysis of gut microbial co-metabolism in Alaska Native and rural African people at high and low risk of colorectal cancer. Am J Clin Nutr. 2020;111(2):406–19.PubMedCrossRef Ocvirk S, Posma JM, Li JV, Koller KR, Day GM, Flanagan CA, et al. A prospective cohort analysis of gut microbial co-metabolism in Alaska Native and rural African people at high and low risk of colorectal cancer. Am J Clin Nutr. 2020;111(2):406–19.PubMedCrossRef
36.
go back to reference Katsidzira L, Ocvirk S, Wilson A, Li J, Mahachi CB, Soni D, et al. Differences in fecal gut microbiota, short-chain fatty acids and bile acids link colorectal cancer risk to dietary changes associated with urbanization among Zimbabweans. Nutr Cancer. 2019;71(8):1313–24.PubMedCrossRef Katsidzira L, Ocvirk S, Wilson A, Li J, Mahachi CB, Soni D, et al. Differences in fecal gut microbiota, short-chain fatty acids and bile acids link colorectal cancer risk to dietary changes associated with urbanization among Zimbabweans. Nutr Cancer. 2019;71(8):1313–24.PubMedCrossRef
37.
go back to reference Hester CM, Jala VR, Langille MGI, Umar S, Greiner KA, Haribabu B. Fecal microbes, short chain fatty acids, and colorectal cancer across racial/ethnic groups. World J Gastroenterol. 2015;21(9):2759–69.PubMedPubMedCentralCrossRef Hester CM, Jala VR, Langille MGI, Umar S, Greiner KA, Haribabu B. Fecal microbes, short chain fatty acids, and colorectal cancer across racial/ethnic groups. World J Gastroenterol. 2015;21(9):2759–69.PubMedPubMedCentralCrossRef
38.
go back to reference Ou J, Carbonero F, Zoetendal EG, DeLany JP, Wang M, Newton K, et al. Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am J Clin Nutr. 2013;98(1):111–20.PubMedPubMedCentralCrossRef Ou J, Carbonero F, Zoetendal EG, DeLany JP, Wang M, Newton K, et al. Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am J Clin Nutr. 2013;98(1):111–20.PubMedPubMedCentralCrossRef
39.
go back to reference Ou J, DeLany JP, Zhang M, Sharma S, O'Keefe SJD. Association between low colonic short-chain fatty acids and high bile acids in high colon cancer risk populations. Nutr Cancer. 2012;64(1):34–40.PubMedCrossRef Ou J, DeLany JP, Zhang M, Sharma S, O'Keefe SJD. Association between low colonic short-chain fatty acids and high bile acids in high colon cancer risk populations. Nutr Cancer. 2012;64(1):34–40.PubMedCrossRef
40.
go back to reference O'Keefe SJD, Ou J, Aufreiter S, O'Connor D, Sharma S, Sepulveda J, et al. Products of the colonic microbiota mediate the effects of diet on colon cancer risk. J Nutr. 2009;139(11):2044–8.PubMedPubMedCentralCrossRef O'Keefe SJD, Ou J, Aufreiter S, O'Connor D, Sharma S, Sepulveda J, et al. Products of the colonic microbiota mediate the effects of diet on colon cancer risk. J Nutr. 2009;139(11):2044–8.PubMedPubMedCentralCrossRef
41.
go back to reference Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Bmj. 2021;372:n71.PubMedPubMedCentralCrossRef Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Bmj. 2021;372:n71.PubMedPubMedCentralCrossRef
42.
go back to reference Muka T, Glisic M, Milic J, Verhoog S, Bohlius J, Bramer W, et al. A 24-step guide on how to design, conduct, and successfully publish a systematic review and meta-analysis in medical research. Eur J Epidemiol. 2020;35(1):49–60.PubMedCrossRef Muka T, Glisic M, Milic J, Verhoog S, Bohlius J, Bramer W, et al. A 24-step guide on how to design, conduct, and successfully publish a systematic review and meta-analysis in medical research. Eur J Epidemiol. 2020;35(1):49–60.PubMedCrossRef
44.
45.
go back to reference Ma LL, Wang YY, Yang ZH, Huang D, Weng H, Zeng XT. Methodological quality (risk of bias) assessment tools for primary and secondary medical studies: what are they and which is better? Mil Med Res. 2020;7(1):7.PubMedPubMedCentral Ma LL, Wang YY, Yang ZH, Huang D, Weng H, Zeng XT. Methodological quality (risk of bias) assessment tools for primary and secondary medical studies: what are they and which is better? Mil Med Res. 2020;7(1):7.PubMedPubMedCentral
47.
go back to reference Baldi S, Menicatti M, Nannini G, Niccolai E, Russo E, Ricci F, et al. Free fatty acids signature in human intestinal disorders: Significant association between butyric acid and celiac disease. Nutrients. 2021;13(3):1–14.CrossRef Baldi S, Menicatti M, Nannini G, Niccolai E, Russo E, Ricci F, et al. Free fatty acids signature in human intestinal disorders: Significant association between butyric acid and celiac disease. Nutrients. 2021;13(3):1–14.CrossRef
48.
go back to reference Bartolucci G, Pallecchi M, Menicatti M, Moracci L, Pucciarelli S, Agostini M, et al. A method for assessing plasma free fatty acids from C2 to C18 and its application for the early detection of colorectal cancer. J Pharm Biomed Anal. 2022;215:114762.PubMedCrossRef Bartolucci G, Pallecchi M, Menicatti M, Moracci L, Pucciarelli S, Agostini M, et al. A method for assessing plasma free fatty acids from C2 to C18 and its application for the early detection of colorectal cancer. J Pharm Biomed Anal. 2022;215:114762.PubMedCrossRef
49.
go back to reference Genua F, Mirković B, Mullee A, Levy M, Gallagher WM, Vodicka P, et al. Association of circulating short chain fatty acid levels with colorectal adenomas and colorectal cancer. Clin Nutr ESPEN. 2021;46:297–304.PubMedCrossRef Genua F, Mirković B, Mullee A, Levy M, Gallagher WM, Vodicka P, et al. Association of circulating short chain fatty acid levels with colorectal adenomas and colorectal cancer. Clin Nutr ESPEN. 2021;46:297–304.PubMedCrossRef
50.
go back to reference Amiot A, Dona AC, Wijeyesekera A, Tournigand C, Baumgaertner I, Lebaleur Y, et al. H-1 NMR spectroscopy of fecal extracts enables detection of advanced colorectal neoplasia. J Proteome Res. 2015;14(9):3871–81.PubMedCrossRef Amiot A, Dona AC, Wijeyesekera A, Tournigand C, Baumgaertner I, Lebaleur Y, et al. H-1 NMR spectroscopy of fecal extracts enables detection of advanced colorectal neoplasia. J Proteome Res. 2015;14(9):3871–81.PubMedCrossRef
51.
go back to reference Segal I, Hassan H, Walker ARP, Becker P, Braganza J. Fecal short chain fatty acids in South African urban Africans and whites. Dis Colon Rectum. 1995;38(7):732–4.PubMedCrossRef Segal I, Hassan H, Walker ARP, Becker P, Braganza J. Fecal short chain fatty acids in South African urban Africans and whites. Dis Colon Rectum. 1995;38(7):732–4.PubMedCrossRef
52.
go back to reference Wang X, Wang J, Rao B, Deng LI. Gut flora profiling and fecal metabolite composition of colorectal cancer patients and healthy individuals. Exper Therapeutic Med. 2017;13(6):2848–54.CrossRef Wang X, Wang J, Rao B, Deng LI. Gut flora profiling and fecal metabolite composition of colorectal cancer patients and healthy individuals. Exper Therapeutic Med. 2017;13(6):2848–54.CrossRef
53.
go back to reference Song M, Chan AT, Sun J. Influence of the gut microbiome, diet, and environment on risk of colorectal cancer. Gastroenterology. 2020;158(2):322–40.PubMedCrossRef Song M, Chan AT, Sun J. Influence of the gut microbiome, diet, and environment on risk of colorectal cancer. Gastroenterology. 2020;158(2):322–40.PubMedCrossRef
54.
go back to reference Borges-Canha M, Portela-Cidade JP, Dinis-Ribeiro M, Leite-Moreira AF, Pimentel-Nunes P. Role of colonic microbiota in colorectal carcinogenesis: a systematic review. Rev Esp Enferm Dig. 2015;107(11):659–71.PubMed Borges-Canha M, Portela-Cidade JP, Dinis-Ribeiro M, Leite-Moreira AF, Pimentel-Nunes P. Role of colonic microbiota in colorectal carcinogenesis: a systematic review. Rev Esp Enferm Dig. 2015;107(11):659–71.PubMed
55.
go back to reference Rao M, Gao C, Hou J, Gu J, Law BYK, Xu Y. Non-digestible carbohydrate and the risk of colorectal neoplasia: a systematic review. Nutr Cancer. 2021;73(1):31–44.PubMedCrossRef Rao M, Gao C, Hou J, Gu J, Law BYK, Xu Y. Non-digestible carbohydrate and the risk of colorectal neoplasia: a systematic review. Nutr Cancer. 2021;73(1):31–44.PubMedCrossRef
56.
go back to reference Ma Y, Hu M, Zhou L, Ling S, Li Y, Kong B, et al. Dietary fiber intake and risks of proximal and distal colon cancers: a meta-analysis. Medicine (Baltimore). 2018;97(36):e11678.CrossRef Ma Y, Hu M, Zhou L, Ling S, Li Y, Kong B, et al. Dietary fiber intake and risks of proximal and distal colon cancers: a meta-analysis. Medicine (Baltimore). 2018;97(36):e11678.CrossRef
57.
go back to reference Sun Q, Jia Q, Song L, Duan L. Alterations in fecal short-chain fatty acids in patients with irritable bowel syndrome: a systematic review and meta-analysis. Medicine (Baltimore). 2019;98(7):e14513.CrossRef Sun Q, Jia Q, Song L, Duan L. Alterations in fecal short-chain fatty acids in patients with irritable bowel syndrome: a systematic review and meta-analysis. Medicine (Baltimore). 2019;98(7):e14513.CrossRef
58.
go back to reference Zhuang X, Li T, Li M, Huang S, Qiu Y, Feng R, et al. Systematic review and meta-analysis: short-chain fatty acid characterization in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2019;25(11):1751–63.PubMedCrossRef Zhuang X, Li T, Li M, Huang S, Qiu Y, Feng R, et al. Systematic review and meta-analysis: short-chain fatty acid characterization in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2019;25(11):1751–63.PubMedCrossRef
59.
go back to reference Rios-Covian D, González S, Nogacka AM, Arboleya S, Salazar N, Gueimonde M, et al. An overview on fecal branched short-chain fatty acids along human life and as related with body mass index: associated dietary and anthropometric factors. Front Microbiol. 2020;11:973.PubMedPubMedCentralCrossRef Rios-Covian D, González S, Nogacka AM, Arboleya S, Salazar N, Gueimonde M, et al. An overview on fecal branched short-chain fatty acids along human life and as related with body mass index: associated dietary and anthropometric factors. Front Microbiol. 2020;11:973.PubMedPubMedCentralCrossRef
60.
go back to reference Gill PA, van Zelm MC, Muir JG, Gibson PR. Review article: short chain fatty acids as potential therapeutic agents in human gastrointestinal and inflammatory disorders. Aliment Pharmacol Ther. 2018;48(1):15–34.PubMedCrossRef Gill PA, van Zelm MC, Muir JG, Gibson PR. Review article: short chain fatty acids as potential therapeutic agents in human gastrointestinal and inflammatory disorders. Aliment Pharmacol Ther. 2018;48(1):15–34.PubMedCrossRef
61.
go back to reference Shuwen H, Miao D, Quan Q, Wei W, Zhongshan Z, Chun Z, et al. Protective effect of the “food-microorganism-SCFAs” axis on colorectal cancer: from basic research to practical application. J Cancer Res Clin Oncol. 2019;145(9):2169–97.PubMedCrossRef Shuwen H, Miao D, Quan Q, Wei W, Zhongshan Z, Chun Z, et al. Protective effect of the “food-microorganism-SCFAs” axis on colorectal cancer: from basic research to practical application. J Cancer Res Clin Oncol. 2019;145(9):2169–97.PubMedCrossRef
62.
go back to reference Akimoto N, Ugai T, Zhong R, Hamada T, Fujiyoshi K, Giannakis M, et al. Rising incidence of early-onset colorectal cancer - a call to action. Nat Rev Clin Oncol. 2021;18(4):230–43.PubMedCrossRef Akimoto N, Ugai T, Zhong R, Hamada T, Fujiyoshi K, Giannakis M, et al. Rising incidence of early-onset colorectal cancer - a call to action. Nat Rev Clin Oncol. 2021;18(4):230–43.PubMedCrossRef
63.
go back to reference Burnett-Hartman AN, Lee JK, Demb J, Gupta S. An update on the epidemiology, molecular characterization, diagnosis, and screening strategies for early-onset colorectal cancer. Gastroenterology. 2021;160(4):1041–9.PubMedCrossRef Burnett-Hartman AN, Lee JK, Demb J, Gupta S. An update on the epidemiology, molecular characterization, diagnosis, and screening strategies for early-onset colorectal cancer. Gastroenterology. 2021;160(4):1041–9.PubMedCrossRef
64.
go back to reference Saad El Din K, Loree JM, Sayre EC, Gill S, Brown CJ, Dau H, et al. Trends in the epidemiology of young-onset colorectal cancer: a worldwide systematic review. BMC Cancer. 2020;20(1):288.PubMedCrossRef Saad El Din K, Loree JM, Sayre EC, Gill S, Brown CJ, Dau H, et al. Trends in the epidemiology of young-onset colorectal cancer: a worldwide systematic review. BMC Cancer. 2020;20(1):288.PubMedCrossRef
65.
go back to reference Vuik FE, Nieuwenburg SA, Bardou M, Lansdorp-Vogelaar I, Dinis-Ribeiro M, Bento MJ, et al. Increasing incidence of colorectal cancer in young adults in Europe over the last 25 years. Gut. 2019;68(10):1820–6.PubMedCrossRef Vuik FE, Nieuwenburg SA, Bardou M, Lansdorp-Vogelaar I, Dinis-Ribeiro M, Bento MJ, et al. Increasing incidence of colorectal cancer in young adults in Europe over the last 25 years. Gut. 2019;68(10):1820–6.PubMedCrossRef
66.
go back to reference Kastrinos F, Samadder NJ, Burt RW. Use of family history and genetic testing to determine risk of colorectal cancer. Gastroenterology. 2020;158(2):389–403.PubMedCrossRef Kastrinos F, Samadder NJ, Burt RW. Use of family history and genetic testing to determine risk of colorectal cancer. Gastroenterology. 2020;158(2):389–403.PubMedCrossRef
70.
go back to reference Ocvirk S, Wilson AS, Appolonia CN, Thomas TK, O'Keefe SJD. Fiber, fat, and colorectal cancer: new insight into modifiable dietary risk factors. Curr Gastroenterol Rep. 2019;21(11):62.PubMedCrossRef Ocvirk S, Wilson AS, Appolonia CN, Thomas TK, O'Keefe SJD. Fiber, fat, and colorectal cancer: new insight into modifiable dietary risk factors. Curr Gastroenterol Rep. 2019;21(11):62.PubMedCrossRef
72.
go back to reference Jia W, Xie G, Jia W. Bile acid-microbiota crosstalk in gastrointestinal inflammation and carcinogenesis. Nat Rev Gastroenterol Hepatol. 2018;15(2):111–28.PubMedCrossRef Jia W, Xie G, Jia W. Bile acid-microbiota crosstalk in gastrointestinal inflammation and carcinogenesis. Nat Rev Gastroenterol Hepatol. 2018;15(2):111–28.PubMedCrossRef
73.
go back to reference Davidson KW, Barry MJ, Mangione CM, Cabana M, Caughey AB, Davis EM, et al. Screening for colorectal cancer: US Preventive Services Task Force Recommendation Statement. Jama. 2021;325(19):1965–77.PubMedCrossRef Davidson KW, Barry MJ, Mangione CM, Cabana M, Caughey AB, Davis EM, et al. Screening for colorectal cancer: US Preventive Services Task Force Recommendation Statement. Jama. 2021;325(19):1965–77.PubMedCrossRef
74.
go back to reference Ferrari A, Neefs I, Hoeck S, Peeters M, Van Hal G. Towards novel non-invasive colorectal cancer screening methods: a comprehensive review. Cancers (Basel). 2021;13(8):1820. Ferrari A, Neefs I, Hoeck S, Peeters M, Van Hal G. Towards novel non-invasive colorectal cancer screening methods: a comprehensive review. Cancers (Basel). 2021;13(8):1820.
75.
go back to reference Jodal HC, Helsingen LM, Anderson JC, Lytvyn L, Vandvik PO, Emilsson L. Colorectal cancer screening with faecal testing, sigmoidoscopy or colonoscopy: a systematic review and network meta-analysis. BMJ Open. 2019;9(10):e032773.PubMedPubMedCentralCrossRef Jodal HC, Helsingen LM, Anderson JC, Lytvyn L, Vandvik PO, Emilsson L. Colorectal cancer screening with faecal testing, sigmoidoscopy or colonoscopy: a systematic review and network meta-analysis. BMJ Open. 2019;9(10):e032773.PubMedPubMedCentralCrossRef
76.
go back to reference 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):319–29.PubMedCrossRef 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):319–29.PubMedCrossRef
77.
go back to reference Anghel SA, Ionita-Mindrican CB, Luca I, Pop AL. Promising epigenetic biomarkers for the early detection of colorectal cancer: a systematic review. Cancers (Basel). 2021;13(19):4965. Anghel SA, Ionita-Mindrican CB, Luca I, Pop AL. Promising epigenetic biomarkers for the early detection of colorectal cancer: a systematic review. Cancers (Basel). 2021;13(19):4965.
Metadata
Title
Short-chain fatty acid concentrations in the incidence and risk-stratification of colorectal cancer: a systematic review and meta-analysis
Authors
Ehsan Alvandi
Wilson K. M. Wong
Mugdha V. Joglekar
Kevin J. Spring
Anandwardhan A. Hardikar
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2022
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/s12916-022-02529-4

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