Relationship between Sources of Dietary Fiber Intake and Homocysteine Metabolism in Relation to Serum Homocysteine Concentrations
Abstract
:1. Introduction
2. Materials and Methods
2.1. Data Used for Analysis
2.2. Measurement of Serum Homocysteine Metabolites
2.3. Statistical Analysis
3. Results
3.1. Sample Characteristics
3.2. Serum Homocysteine Concentrations in Relation to Dietary Fiber Sources by Food Group
3.3. Serum Homocysteine Concentration in Relation to Dietary Fiber Sources (Tertiles) by Food Group
3.4. Homocysteine Metabolites in Relation to Dietary Fiber Sources by Food Group
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- McCully, K.S. Vascular pathology of homocysteinemia: Implications for the pathogenesis of arteriosclerosis. Am. J. Pathol. 1969, 56, 111–128. [Google Scholar] [PubMed]
- McCully, K.S. Homocysteine, vitamins, and vascular disease prevention. Am. J. Clin. Nutr. 2007, 86, 1563s–1568s. [Google Scholar] [CrossRef] [PubMed]
- Welch, G.N.; Loscalzo, J. Homocysteine and atherothrombosis. N. Engl. J. Med. 1998, 338, 1042–1050. [Google Scholar] [CrossRef]
- Den Heijer, M.; Lewington, S.; Clarke, R. Homocysteine, MTHFR and risk of venous thrombosis: A meta-analysis of published epidemiological studies. J. Thromb. Haemost. 2005, 3, 292–299. [Google Scholar] [CrossRef] [PubMed]
- Refsum, H.; Ueland, P.M.; Nygård, O.; Vollset, S.E. Homocysteine and cardiovascular disease. Annu. Rev. Med. 1998, 49, 31–62. [Google Scholar] [CrossRef]
- Setién-Suero, E.; Suárez-Pinilla, M.; Suárez-Pinilla, P.; Crespo-Facorro, B.; Ayesa-Arriola, R. Homocysteine and cognition: A systematic review of 111 studies. Neurosci. Biobehav. Rev. 2016, 69, 280–298. [Google Scholar] [CrossRef]
- Behera, J.; Bala, J.; Nuru, M.; Tyagi, S.C.; Tyagi, N. Homocysteine as a Pathological Biomarker for Bone Disease. J. Cell. Physiol. 2017, 232, 2704–2709. [Google Scholar] [CrossRef]
- Ota, K.; Takahashi, T.; Han, A.; Damvaeba, S.; Mizunuma, H.; Kwak-Kim, J. Effects of MTHFR C677T polymorphism on vitamin D, homocysteine and natural killer cell cytotoxicity in women with recurrent pregnancy losses. Hum. Reprod. 2020, 35, 1276–1287. [Google Scholar] [CrossRef]
- Mao, D.; Che, J.; Li, K.; Han, S.; Yue, Q.; Zhu, L.; Zhang, W.; Li, L. Association of homocysteine, asymmetric dimethylarginine, and nitric oxide with preeclampsia. Arch. Gynecol. Obstet. 2010, 282, 371–375. [Google Scholar] [CrossRef]
- Qiu, X.; Gao, F.; Qiu, Y.; Bao, J.; Gu, X.; Long, Y.; Liu, F.; Cai, M.; Liu, H. Association of maternal serum homocysteine concentration levels in late stage of pregnancy with preterm births: A nested case-control study. J. Matern. Fetal Neonatal Med. 2018, 31, 2673–2677. [Google Scholar] [CrossRef]
- Goddijn-Wessel, T.A.; Wouters, M.G.; van de Molen, E.F.; Spuijbroek, M.D.; Steegers-Theunissen, R.P.; Blom, H.J.; Boers, G.H.; Eskes, T.K. Hyperhomocysteinemia: A risk factor for placental abruption or infarction. Eur. J. Obstet. Gynecol. Reprod. Biol. 1996, 66, 23–29. [Google Scholar] [CrossRef]
- Jiang, H.L.; Cao, L.Q.; Chen, H.Y. Blood folic acid, vitamin B12, and homocysteine levels in pregnant women with fetal growth restriction. Genet. Mol. Res. 2016, 15, gmr15048890. [Google Scholar] [CrossRef]
- Seghieri, G.; Breschi, M.C.; Anichini, R.; De Bellis, A.; Alviggi, L.; Maida, I.; Franconi, F. Serum homocysteine levels are increased in women with gestational diabetes mellitus. Metabolism 2003, 52, 720–723. [Google Scholar] [CrossRef]
- Guven, M.A.; Kilinc, M.; Batukan, C.; Ekerbicer, H.C.; Aksu, T. Elevated second trimester serum homocysteine levels in women with gestational diabetes mellitus. Arch. Gynecol. Obstet. 2006, 274, 333–337. [Google Scholar] [CrossRef] [PubMed]
- Nasri, K.; Ben Fradj, M.K.; Touati, A.; Aloui, M.; Ben Jemaa, N.; Masmoudi, A.; Elmay, M.V.; Omar, S.; Feki, M.; Kaabechi, N.; et al. Association of maternal homocysteine and vitamins status with the risk of neural tube defects in Tunisia: A case-control study. Birth Defects Res. A Clin. Mol. Teratol. 2015, 103, 1011–1020. [Google Scholar] [CrossRef] [PubMed]
- D’Souza, S.W.; Glazier, J.D. Homocysteine Metabolism in Pregnancy and Developmental Impacts. Front. Cell Dev. Biol. 2022, 10, 802285. [Google Scholar] [CrossRef]
- Hashimoto, T.; Shinohara, Y.; Hasegawa, H. Homocysteine metabolism. Yakugaku Zasshi 2007, 127, 1579–1592. [Google Scholar] [CrossRef]
- Esse, R.; Barroso, M.; Tavares de Almeida, I.; Castro, R. The Contribution of Homocysteine Metabolism Disruption to Endothelial Dysfunction: State-of-the-Art. Int. J. Mol. Sci. 2019, 20, 867. [Google Scholar] [CrossRef]
- Tajima, A.; Kubo, Y.; Horiguchi, S.; Shoji, K.; Kawabata, T. Relationship between Serum Homocysteine Concentration and Dietary Factors in Young Japanese Women. Nutrients 2023, 15, 4740. [Google Scholar] [CrossRef]
- Kubo, Y.; Shoji, K.; Tajima, A.; Horiguchi, S.; Fukuoka, H.; Nishikawa, M.; Kagawa, Y.; Kawabata, T. Serum 5-Methyltetrahydrofolate Status Is Associated with One-Carbon Metabolism-Related Metabolite Concentrations and Enzyme Activity Indicators in Young Women. Int. J. Mol. Sci. 2023, 24, 10993. [Google Scholar] [CrossRef]
- Fuller, S.; Beck, E.; Salman, H.; Tapsell, L. New Horizons for the Study of Dietary Fiber and Health: A Review. Plant Foods Hum. Nutr. 2016, 71, 1–12. [Google Scholar] [CrossRef]
- Denko, C.W.; Grundy, W.E.; Porter, J.W.; Berryman, G.H. The excretion of B-complex vitamins in the urine and feces of seven normal adults. Arch. Biochem. 1946, 10, 33–40. [Google Scholar]
- Pompei, A.; Cordisco, L.; Amaretti, A.; Zanoni, S.; Raimondi, S.; Matteuzzi, D.; Rossi, M. Administration of folate-producing bifidobacteria enhances folate status in Wistar rats. J. Nutr. 2007, 137, 2742–2746. [Google Scholar] [CrossRef]
- Rioux, L.E.; Turgeon, S.L.; Beaulieu, M. Structural characterization of laminaran and galactofucan extracted from the brown seaweed Saccharina longicruris. Phytochemistry 2010, 71, 1586–1595. [Google Scholar] [CrossRef] [PubMed]
- Kofuji, K.; Aoki, A.; Tsubaki, K.; Konishi, M.; Isobe, T.; Murata, Y. Antioxidant Activity of β-Glucan. ISRN Pharm. 2012, 2012, 125864. [Google Scholar] [CrossRef] [PubMed]
- Fukada, S.; Setoue, M.; Morita, T.; Sugiyama, K. Dietary eritadenine suppresses guanidinoacetic Acid-induced hyperhomocysteinemia in rats. J. Nutr. 2006, 136, 2797–2802. [Google Scholar] [CrossRef] [PubMed]
- Yang, H.; Hwang, I.; Kim, S.; Ahn, C.; Hong, E.J.; Jeung, E.B. Preventive effects of Lentinus edodes on homocysteinemia in mice. Exp. Ther. Med. 2013, 6, 465–468. [Google Scholar] [CrossRef] [PubMed]
- Kriebitzsch, C.; Verlinden, L.; Eelen, G.; van Schoor, N.M.; Swart, K.; Lips, P.; Meyer, M.B.; Pike, J.W.; Boonen, S.; Carlberg, C.; et al. 1,25-dihydroxyvitamin D3 influences cellular homocysteine levels in murine preosteoblastic MC3T3-E1 cells by direct regulation of cystathionine β-synthase. J. Bone Miner. Res. 2011, 26, 2991–3000. [Google Scholar] [CrossRef]
- Detopoulou, P.; Damigou, E.; Antonopoulou, S.; Fragopoulou, E.; Chysohoou, C.; Pitsavos, C.; Panagiotakos, D. Food Compass Score and its association with inflammatory markers and homocysteine in cardiovascular disease-free adults: A cross-sectional analysis of the ATTICA epidemiological study. Eur. J. Clin. Nutr. 2023, 77, 998–1004. [Google Scholar] [CrossRef]
- Kagawa, Y.; Hiraoka, M.; Kageyama, M.; Kontai, Y.; Yurimoto, M.; Nishijima, C.; Sakamoto, K. Medical cost savings in Sakado City and worldwide achieved by preventing disease by folic acid fortification. Congenit. Anom. 2017, 57, 157–165. [Google Scholar] [CrossRef]
Variables | Overall (n = 227) | ||
---|---|---|---|
5MTHF | (µmol/L) | 0.019 | [0.014, 0.024] |
Betaine | (µmol/L) | 39.1 | ±9.1 |
Choline | (µmol/L) | 7.5 | ±1.4 |
Cystathionine | (µmol/L) | 0.090 | [0.073, 0.111] |
Cysteine | (µmol/L) | 198.4 | ±20.5 |
DMG | (µmol/L) | 3.0 | [2.5, 3.6] |
Glycine | (µmol/L) | 201.5 | [179.5, 224.5] |
Homocysteine | (µmol/L) | 6.4 | [5.5, 7.4] |
Methionine | (µmol/L) | 24.5 | ±3.7 |
Riboflavin | (µmol/L) | 0.012 | [0.008, 0.017] |
SAH | (µmol/L) | 0.014 | [0.012, 0.017] |
SAM | (µmol/L) | 0.056 | ±0.008 |
Serine | (µmol/L) | 148.7 | ±24.6 |
Taurine | (µmol/L) | 112.3 | ±22.0 |
FA | (µmol/L) | 0.001 | [0.001, 0.002] |
Model 1 ¶ | Model 2 ¶ | Model 3 ¶ | |||||
---|---|---|---|---|---|---|---|
(mg/1000 kcal) | β Coefficient | p Value | β Coefficient | p Value | β Coefficient | p Value | |
Cereals | Soluble dietary fiber | −0.046 | 0.4986 | −0.066 | 0.3269 | −0.103 | 0.1264 |
Insoluble dietary fiber | −0.075 | 0.2668 | −0.102 | 0.1349 | −0.124 | 0.0630 | |
Total fiber | −0.068 | 0.3157 | −0.095 | 0.1647 | −0.125 | 0.0630 | |
Tubers and root vegetables | Soluble dietary fiber | −0.020 | 0.7656 | −0.027 | 0.6977 | 0.005 | 0.9385 |
Insoluble dietary fiber | −0.049 | 0.4753 | −0.048 | 0.4945 | −0.011 | 0.8741 | |
Total fiber | −0.041 | 0.5468 | −0.043 | 0.5411 | −0.007 | 0.9243 | |
Nuts | Soluble dietary fiber | −0.007 | 0.9147 | −0.016 | 0.8167 | 0.007 | 0.9181 |
Insoluble dietary fiber | 0.009 | 0.8933 | 0.000 | 0.9988 | 0.004 | 0.9485 | |
Total fiber | 0.007 | 0.9213 | −0.002 | 0.9735 | 0.004 | 0.9501 | |
Green and yellow vegetables | Soluble dietary fiber | −0.130 | 0.0531 | −0.111 | 0.1274 | 0.002 | 0.9762 |
Insoluble dietary fiber | −0.144 | 0.0321 | −0.130 | 0.0746 | −0.022 | 0.7942 | |
Total fiber | −0.142 | 0.0351 | −0.127 | 0.0831 | −0.016 | 0.8440 | |
Other vegetables | Soluble dietary fiber | −0.148 | 0.0273 | −0.124 | 0.0796 | −0.030 | 0.7014 |
Insoluble dietary fiber | −0.127 | 0.0583 | −0.101 | 0.1558 | 0.014 | 0.8592 | |
Total fiber | −0.136 | 0.0424 | −0.110 | 0.1200 | 0.001 | 0.9904 | |
Fruits | Soluble dietary fiber | −0.206 | 0.0022 | −0.196 | 0.0046 | −0.149 | 0.0352 |
Insoluble dietary fiber | −0.190 | 0.0048 | −0.183 | 0.0080 | −0.146 | 0.0364 | |
Total fiber | −0.199 | 0.0031 | −0.192 | 0.0056 | −0.150 | 0.0319 | |
Mushrooms | Soluble dietary fiber | −0.199 | 0.0031 | −0.178 | 0.0089 | −0.141 | 0.0398 |
Insoluble dietary fiber | −0.195 | 0.0037 | −0.174 | 0.0107 | −0.138 | 0.0436 | |
Total fiber | −0.197 | 0.0034 | −0.176 | 0.0100 | −0.150 | 0.0319 | |
Seaweed § | Total fiber | −0.107 | 0.1094 | −0.093 | 0.1614 | −0.067 | 0.3097 |
Pulses | Soluble dietary fiber | −0.126 | 0.0670 | −0.110 | 0.1120 | −0.045 | 0.5279 |
Insoluble dietary fiber | −0.065 | 0.3434 | −0.041 | 0.5592 | 0.046 | 0.5367 | |
Total fiber | −0.086 | 0.2114 | −0.064 | 0.3590 | 0.018 | 0.8103 | |
Confectionery | Soluble dietary fiber | 0.009 | 0.8965 | −0.024 | 0.7284 | −0.038 | 0.5787 |
Insoluble dietary fiber | −0.005 | 0.9439 | −0.036 | 0.5980 | −0.046 | 0.4953 | |
Total fiber | −0.009 | 0.9896 | −0.033 | 0.6301 | −0.044 | 0.5186 | |
Seasonings and spices | Soluble dietary fiber | 0.081 | 0.2351 | 0.116 | 0.0908 | 0.123 | 0.0665 |
Insoluble dietary fiber | −0.020 | 0.7670 | 0.016 | 0.8161 | 0.047 | 0.4894 | |
Total fiber | 0.007 | 0.9154 | 0.045 | 0.5167 | 0.071 | 0.2995 |
Amount of Intake (mg/1000 kcal) | Amount of Intake (mg/1000 kcal) | Amount of Intake (mg/1000 kcal) | p Value § | ||
---|---|---|---|---|---|
T1 (n = 75) | T2 (n = 76) | T3 (n = 76) | |||
Fruits | Soluble dietary fiber | 33.9 [10.8, 62.7] | 125.6 [87.5, 166.5] | 283.2 [213.1, 395.5] | 0.0104 |
Insoluble dietary fiber | 77.7 [29.1, 122.8] | 286.3 [231.2, 363.0] | 652.4 [495.4, 803.2] | 0.0052 | |
Total fiber | 112.7 [42.8, 178.6] | 424.8 [314.8, 546.4] | 915.9 [735.4, 1187.0] | 0.0054 | |
Mushrooms | Soluble dietary fiber | 2.2 [0.0, 4.1] | 11.0 [8.4, 15.2] | 25.6 [18.7, 34.2] | 0.0350 |
Insoluble dietary fiber | 55.8 [7.6, 84.5] | 208.1 [153.1, 245.5] | 495.1 [357.3, 640.5] | 0.0052 | |
Total fiber | 59.5 [8.0, 87.6] | 220.5 [168.3, 262.6] | 523.1 [380.1, 671.0] | 0.0050 |
Serum | |||||||||||
5MTHF | Betaine | Choline | Cystathionine | Cysteine | |||||||
(mg/1000 kcal) | β Coefficient | p Value | β Coefficient | p Value | β Coefficient | p Value | β Coefficient | p Value | β Coefficient | p Value | |
Fruits | Soluble dietary fiber | 0.192 | 0.0037 | 0.125 | 0.0800 | −0.011 | 0.8777 | −0.037 | 0.6061 | −0.050 | 0.4824 |
Insoluble dietary fiber | 0.193 | 0.0029 | 0.074 | 0.2885 | −0.034 | 0.6313 | −0.047 | 0.5074 | −0.066 | 0.3506 | |
Total fiber | 0.198 | 0.0025 | 0.091 | 0.1978 | −0.029 | 0.6887 | −0.047 | 0.5147 | −0.062 | 0.3834 | |
Mushrooms | Soluble dietary fiber | 0.070 | 0.2786 | 0.105 | 0.1261 | −0.012 | 0.8668 | 0.177 | 0.0108 | −0.012 | 0.8586 |
Insoluble dietary fiber | 0.050 | 0.4382 | 0.032 | 0.6429 | −0.089 | 0.2015 | 0.159 | 0.0225 | −0.101 | 0.1459 | |
Total fiber | 0.052 | 0.4221 | 0.036 | 0.6017 | −0.086 | 0.2183 | 0.161 | 0.0207 | −0.097 | 0.1612 | |
Serum | |||||||||||
DMG | Glycine | Methionine | SAM | SAH | |||||||
(mg/1000 kcal) | β Coefficient | p Value | β Coefficient | p Value | β Coefficient | p Value | β Coefficient | p Value | β Coefficient | p Value | |
Fruits | Soluble dietary fiber | −0.051 | 0.4825 | −0.028 | 0.6927 | 0.038 | 0.5761 | −0.025 | 0.7293 | 0.047 | 0.5039 |
Insoluble dietary fiber | −0.043 | 0.5513 | −0.012 | 0.8581 | 0.035 | 0.6025 | 0.012 | 0.8667 | 0.038 | 0.5882 | |
Total fiber | −0.047 | 0.5117 | −0.016 | 0.8134 | 0.034 | 0.5830 | 0.001 | 0.9925 | 0.040 | 0.5698 | |
Mushrooms | Soluble dietary fiber | −0.005 | 0.9452 | −0.126 | 0.0622 | −0.161 | 0.0144 | −0.030 | 0.6675 | −0.006 | 0.9339 |
Insoluble dietary fiber | −0.030 | 0.6736 | −0.141 | 0.0369 | −0.148 | 0.0249 | −0.020 | 0.7724 | −0.004 | 0.9563 | |
Total fiber | −0.029 | 0.6829 | −0.142 | 0.0357 | −0.150 | 0.0229 | −0.021 | 0.7694 | −0.003 | 0.9632 | |
Serum | |||||||||||
Serine | Taurine | FA | Riboflavin | ||||||||
(mg/1000 kcal) | β Coefficient | p Value | β Coefficient | p Value | β Coefficient | p Value | β Coefficient | p Value | |||
Fruits | Soluble dietary fiber | 0.020 | 0.7803 | 0.008 | 0.9156 | −0.063 | 0.3776 | −0.034 | 0.6459 | ||
Insoluble dietary fiber | 0.005 | 0.9397 | 0.020 | 0.7821 | −0.090 | 0.2021 | −0.113 | 0.1155 | |||
Total fiber | 0.011 | 0.8744 | 0.016 | 0.8226 | −0.084 | 0.2358 | −0.095 | 0.1910 | |||
Mushrooms | Soluble dietary fiber | −0.010 | 0.8916 | −0.110 | 0.1160 | −0.058 | 0.4024 | −0.013 | 0.8569 | ||
Insoluble dietary fiber | −0.079 | 0.2633 | −0.055 | 0.4322 | −0.009 | 0.8968 | −0.017 | 0.8066 | |||
Total fiber | −0.076 | 0.2820 | −0.058 | 0.4069 | −0.012 | 0.8618 | −0.016 | 0.8185 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Tajima, A.; Kubo, Y.; Horiguchi, S.; Shoji, K.; Kagawa, Y.; Kawabata, T. Relationship between Sources of Dietary Fiber Intake and Homocysteine Metabolism in Relation to Serum Homocysteine Concentrations. Dietetics 2024, 3, 308-317. https://doi.org/10.3390/dietetics3030024
Tajima A, Kubo Y, Horiguchi S, Shoji K, Kagawa Y, Kawabata T. Relationship between Sources of Dietary Fiber Intake and Homocysteine Metabolism in Relation to Serum Homocysteine Concentrations. Dietetics. 2024; 3(3):308-317. https://doi.org/10.3390/dietetics3030024
Chicago/Turabian StyleTajima, Akiko, Yoshinori Kubo, Sayaka Horiguchi, Kumiko Shoji, Yasuo Kagawa, and Terue Kawabata. 2024. "Relationship between Sources of Dietary Fiber Intake and Homocysteine Metabolism in Relation to Serum Homocysteine Concentrations" Dietetics 3, no. 3: 308-317. https://doi.org/10.3390/dietetics3030024
APA StyleTajima, A., Kubo, Y., Horiguchi, S., Shoji, K., Kagawa, Y., & Kawabata, T. (2024). Relationship between Sources of Dietary Fiber Intake and Homocysteine Metabolism in Relation to Serum Homocysteine Concentrations. Dietetics, 3(3), 308-317. https://doi.org/10.3390/dietetics3030024