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Meta-analysis of MTHFR 677C→ T polymorphism and coronary heart disease: does totality of evidence support causal role for homocysteine and preventive potential of folate?

BMJ 2005; 331 doi: https://doi.org/10.1136/bmj.38611.658947.55 (Published 03 November 2005) Cite this as: BMJ 2005;331:1053

Data supplement

  • References to studies included in the meta analysis

    w1 Zheng YZ, Tong J, Do XP, Pu XQ, Zhou BT. Prevalence of methylenetetrahydrofolate reductase C667T and its association with arterial and venous thrombosis in the Chinese population. Br J Haematol 2000;109:870-4.

    w2 Chambers JC, Ireland H, Thompson E, Reilly P, Obeid OA, Refsum H, et al. Methylenetetrahydrofolate reductase 677 C→T mutation and coronary heart disease in UK Indian Asians. Arterioscler Thromb Vasc Biol 2000;20:2448-52.

    w3 Fernandez-Arcas N, Diegues-Lucena JL, Munoz-Moran E, Ruiz-Galdon M, Espinosa-Caliani S, Aranda-Lara P, et al. The genotype interactions of methylenetetrahydrofolate reductase and renin-angiotensin system genes are associated with myocardial infarction. Atherosclerosis 1999;145:293-300.

    w4 Chao CL, Tsai HH, Lee CM, Hsu SM, Kao JT, Chien KL, et al. The graded effect of hyperhomocysteinemia on the severity and extent of coronary atherosclerosis. Atherosclerosis 1999;147:379-86.

    w5 Brulhart MC, Dussoix P, Ruiz J, Passa P, Froguel P, James RW. The (Ala-Val) mutation of methylenetetrahydrofolate reductase as a genetic risk factor for vascular disease in non-insulin-dependent diabetic patients. Am J Hum Genet 1997;60:228-9.

    w6a Tsai MY, Welge BG, Hanson NQ, Bignell MK, Vessey J, Schwichtenberg K, et al. Genetic causes of mild hyperhomocysteinemia in patients with premature occlusive coronary artery diseases. Atherosclerosis 1999;143:163-70.

    w6b Hanson NQ, Aras O, Yang F and Tsai MY. C677T and A1298C polymorphisms of the methylenetetrahydrofolate reducatase gene: incidence and effect of combined genotypes on plasma fasting and post-methionine load homocysteine in vascular disease. Clinical Chem 2001;47:661-6.

    w7a Girelli D, Martinelli N, Pizzolo F, Friso S, Olivieri O, Stranieri C, et al. The interaction between MTHFR 677 C-->T genotype and folate status is a determinant of coronary atherosclerosis risk. J Nutr 2003;133:1281-5.7b.

    w7b Girelli D, Friso S, Trabetti E, Olivieri O, Russo C, Pessotto R, et al. Methylenetetrahydrofolate reductase C677 mutation, plasma homocysteine, and folate in subjects from northern Italy with and without severe coronary atherosclerotic disease: evidence for an important genetic-environment interaction. Blood 1998;91:4158-63. 8.

    w8 Brugada R, Marian AJ. A common mutation in methylenetetrahydrofolate reductase gene is not a major risk of coronary artery disease or myocardial infarction. Atherosclerosis 1997;128:107-12.

    w9 Adams M, Smith PD, Martin D, Thomson JR, Lodwick D, Samani NJ. Genetic analysis of thermolabile methylenetetrahydrofolate reductase as a risk factor for myocardial infarction. Q J Med 1996;89:437-44.

    w10 Schmitz C, Lindpainter K, Verhoef P, Gaziano JM, Buring J. Genetic polymorphism of methylenetetrahydrofolate reductase and myocardial infarction: a case-control study. Circulation 1996;94:1812-14.

    w11 Ardissino D, Mannucci PM, Merlini PA, Duca F, Fetiveau R, Tagliabue L, et al. Prothrombotic genetic risk factors in young survivors of myocardial infarction. Blood 1999;94:46-51.

    w12 Meisel C, Cascorbi I, Gerloff T, Stangl V, Laule M, Müller J, et al. Identification of six methylenetetrahydrofolate reductase (MTHFR) genotypes resulting from common polymorphisms: impact on plasma homocysteine levels and development of coronary artery disease. Atherosclerosis 2001;154:651-8.

    w13 Verhoef P, Rimm EB, Hunter DJ, Chen J, Willett WC, Kelsey K, et al. A common mutation in the methylenetetrahydrofolate reductase gene and risk of coronary heart disease: results among US men. J Am Coll Cardiol 1998;32:253-9.

    w14 Ma J, Stampfer MJ, Hennekens CH, Frosst P, Selhub J, Horsford J, et al. Methylenetetrahydrofolate reductase polymorphism, plasma folate, homocysteine and risk of myocardial infarction in US physicians. Circulation 1996;94:2410-6.

    w15 Dilley A, Hooper WC, El-Jamil M, Renshaw M, Wenger NK, Evatt BL. Mutations in the genes regulating methylenetetrahydrofolate reductase (MTHFR C→ T677) and cystathione β-synthase (CBS G→A919, CBS T→ c833) are not associated with myocardial infarction in African Americans. Thromb Res 2001;103:109-15.

    w16 Schwartz SM, Siscovick DS, Malinow MR, Rosendaal FR, Beverly RK, Hess DL, et al. Myocardial infarction in young women in relation to plasma total homocysteine, folate, and a common variant in the methylenetetrahydrofolate reductase gene. Circulation 1997;96:412-7.

    w17 Hsu L-A, Jo Y-L, Wand S-M, Chang C-J, Hsu T-S, Chiang C-W, et al. The C677T mutation of the methylenetetrahydrofolate reductase gene is not associated with the risk of coronary artery disease or venous thrombosis among Chinese in Taiwan. Hum Hered 2001;51:41-5.

    w18 van Bockxmeer FM, Mamotte CDS, Vasikaran SD, Taylor RR. Methylenetetrahydrofolate reductase gene and coronary artery disease. Circulation 1997;95:21-3.

    w19 Abbate R, Sardi I, Pepe G, Marcucci R, Brunelli T, Prisco D, et al. The high prevalence of the thermolabile 5,10-methylenetetrahydrofolate reductase (MTHFR) in Italians is not associated with an increased risk for coronary artery disease (CAD). Thromb Haemost 1998;79:727-30.

    w20 Wilcken DEL, Wang XL, Sim AS, McCredie M. Distribution in healthy and coronary populations of the methylenetetrahydrofolate reductase (MTHFR) C677T mutation. Arterioscler Thromb Vasc Biol 1996;16:878-82.

    w21 Pintó X, Vilaseca MA, Garcia-Giralt N, Ferrer I, Palá M, Meco JF, et al. Homocysteine and the MTHFR 677C→ T allele in premature coronary artery disease. Case control and family studies. Eur J Clin Invest 2001;31:24-30.

    w22 Kim C-H, Hwang K-Y, Choi T-M, Shin W-Y, Hong S-Y. The methylenetetrahydrofolate reductase gene polymorphism in Koreans with coronary artery disease. Int J Cardiol 2001;78:13-17.

    w23 Anderson JL, King GJ, Thomson MJ, Todd M, Bair TL, Muhlestein JB, et al. A mutation in the methylenetetrahydrofolate reductase gene is not associated with increased risk for coronary artery disease or myocardial infarction. J Am Coll Cardiol 1997;30:1206-11.

    w24 Kluijtmans LAJ, Kastelein JJP, Lindemans J, Boers GHJ, Heil SG, Bruschke AVG, et al. Thermolabile methylenetetrahydrofolate reductase in coronary artery disease. Circulation 1997;96:2573-7.

    w25 Fowkes FG, Lee AJ, Hau CM, Cooke A, Connor JM, Lowe GD. Methylenetetrahydrofolate reductase (MTHFR) and nitric oxide synthase (ecNOS) genes and risks of peripheral and arterial disease and coronary heart disease: Edinburgh Artery Study. Atherosclerosis 2000;150:179-85.

    w26 Christensen B, Frosst P, Lussier-Cacan S, Selhub J, Goyette P, Rosenblatt DS, et al. Correlation of a common mutation in the methylenetetrahydrofolate reductase gene with plasma homocysteine in patients with premature coronary artery disease. Arterioscler Thromb Vasc Biol 1997;17:569-73. 27.

    w27 Gardemann A, Weidemann H, Philpp M, Katz N, Tillmanns H, Wilhelm Herlein F, et al. The TT genotype of the methylenetetrahydrofolate reductase C677T gene polymorphism is associated with the extent of coronary atherosclerosis in patients at high risk of coronary artery disease. Eur Heart J 1999;20:584-92.

    w28 Todesco L, Angst C, Litynski P, Loehrer F, Fowler B, Haefeli WE. Methylenetetrahydrofolate reductase polymorphism, plasma homocysteine and age. Eur J Clin Invest 1999;29:1003-9.

    w29 Reinhardt D, Sigush HH, Vogt SF, Farker K, Muller S, Hoffman A. Absence of association between common mutation in the methylenetetrahydrofolate reductase gene and the risk of coronary artery disease. Eur J Clin Invest 1998;28:20-3.

    w30 Verhoef P, Kok FJ, Kluijtmans LAJ, Blom HJ, Refsum H, Ueland PM, et al. The 677C→ T mutation in the methylenetetrahydrofolate reductase gene: associations with plasma total homocysteine levels and risk for coronary atherosclerotic disease. Atherosclerosis 1997;132:105-13.

    w31 Kihara T, Abe S, Saigo M, Kaieda H, Obata H, Eto H, et al. Methylenetetrahydrofolate reductase gene polymorphism and premature myocardial infarction. Circulation 1997;96:101-I.

    w32 Araujo F, Lopes M, Goncalves L, Maiciel MJ, Cunha-Ribeiro LM. Hyperhomocysteinemia, MTHFR C667T genotype and low folate levels: a risk combination for acute coronary disease in a Portuguese population. Thromb Haemost 2000;83:517-8.

    w33 Tokgozoglu SL, Alikasifoglu M, Unsal I, Atalar E, Aytemir K, Ozer N, et al. Methylenetetrahydrofolate reductase genotype and the risk and extent of coronary artery disease in a population with low plasma folate. Heart 1999;81:518-22.

    w34 Malik NM, Syrris P, Schwartsman R, Kaski JC, Crossman DC, Francis SE, et al. Methylenetetrahydrofolate reductase polymorphism (C-677T) and coronary artery disease. Clin Sci 1998;95:311-5.

    w35 Thögersen AM, Nilsson TK, Dahlen G, Jansson J-H, Boman K, Huhtasaari F, et al. Homozygosity for the C677→ T mutation of 5,10-methylenetetrahydrofolate reductase and total plasma homocyst(e)ine are not associated with greater than normal risk of a first myocardial infarction in northern Sweden. Coron Artery Dis 2001;12:85-90.

    w36 Izumi M, Iwai N, Ohmichi N, Nakamura Y, Shimoike H, Kinoshita M. Molecular variant of 5,10-methylenetetrahydrofolate reductase is a risk factor of ischaemic heart disease in the Japanese population. Atherosclerosis 1996;121:293-4.

    w37 Nakai K, Fusazaki T, Suzuki T, Ohsawa M, Kamata J, Kawazoe K, et al. Genetic polymorphism of 5,10-methylenetetrahydrofolate increases risk of myocardial infarction and is correlated to elevated levels of homocysteine in the Japanese general population. Coron Artery Dis 2000;11:47-51.

    w38 Morita H, Taguchi J, Kurihara H, Kitaoka M, Kaneda H, Kurihara Y, et al. Genetic polymorphism of 5,10-methylenetetrahydrofolate reductase (MTHFR) as a risk factor for coronary artery disease. Circulation 1997;95:2032-6.

    w39 Szczeklik A, Sanak M, Jankowski M, Dropinski J, Czachór R, Musial L, et al. Mutation A1298C of methylenetetrahydrofolate reductase: risk for early coronary disease not associated with hyperhomocysteinemia. Am J Med Genet 2001;101:36-9.

    w40 Ou T, Kobayashi Y, Yamakawa K, Arinami T, Amemiya H, Fujiwara H, et al. Methylenetetrahydrofolate reductase and apolipoprotein E polymorphisms are independent risk factors for coronary heart disease in Japanese: a case control study. Atherosclerosis 1998;137:23-8.

    w41 Malinow MR, Nieto FJ, Kruger WD, Duell PB, Hess DL, Gluckman RA, et al. The effects of folic acid supplementation on plasma total homocysteine are modulated by multivitamin use and methylenetetrahydrofolate reductase genotypes. Arterioscler Thromb Vasc Biol 1997;17:1157-62.

    w42 Kawashiri M, Kajinami K, Nohara A, Yagi K, Inazu A, Koizumi J, et al. Effect of common methylenetetrahydrofolate reductase gene mutation on coronary artery disease in familial hypercholesterolaemia. Am J Cardiol 2000;86:840-5.

    w43 Gallagher PM, Meleady R, Shields DC, Soon Tan K, McMaster D, Rozen R, et al. Homocysteine and risk of premature coronary heart disease: evidence for a common gene mutation. Circulation 1996;94:2154-8.

    w44 Mager A, Lalezari S, Shohat T, Birnbaum Y, Adler Y, Magal N, et al. Methylenetetrahydrofolate reductase genotypes and early onset coronary artery disease. Circulation 1999;100:2406-10.

    w45 Ferrer-Antunes C, Palmeiro A, Morais J, Lourenço M, Freitas M, Providência L. The mutation C677T in the methylenetetrahydrofolate reductase gene as a risk factor for myocardial infarction in the Portuguese population. Thromb Haemost 1998;80:521-2.

    w46 Güleç S, Aras Ö, Akar E, Tutar E, Ömürlü K, Avci F, et al. Methylenetetrahydrofolate reductase gene polymorphism and risk of premature myocardial infarction. Clin Cardiol 2001;24:281-4.

    w47 Frederiksen J, Juul K, Grande P, Jensen GB, Schroeder TV, Tybjaerg-Hansen A, Nordestgaard BG. Methylenetetrahydrofolate reductase polymorphism (C677T), hyperhomocysteinemia, and risk of ischemic cardiovascular disease and venous thromboembolism: prospective and case-control studies from the Copenhagen City Heart Study. Blood. 2004;104:3046-3051.

    w48 Tobin MD, Braund PS, Burton PR, Thompson JR, Steeds R, Channer K et al. Genotypes and haplotypes predisposing to myocardial infarction: a multilocus case-control study. European Heart J 2004;25:459-67.

    w49 Shioji K, Kokubo Y, Goto Y, Nonogi H, Iwai N. An association analysis between genetic polymorphisms of matrix metalloproteinase-3 and methylenetetrahydrofolate reductase and myocardial infarction in Japanese. J Thromb Haemost 2004;2:527-8.

    w50 Chen TY, Chen JH, Tsao C-J. Methylenetetrahydrofolate reductase gene polymorphism and coronary artery disease in Taiwan Chinese. Haematologica 2000;85:445-6.

    w51 Inbal A, Freimark D, Modan B, Chetrit A, Matetzky S, Rosenberg N et al. Synergistic effects of prothrombotic polymorphisms and atherogenic factors on the risk of myocardial infarction in young males. Blood 1999;93:2186-90.

    w52 Spiridonova MG, Stepanov VA, Puzyrev VP and Karpov RS. Analysis of gene complexes predisposing to coronary atherosclerosis. Russian J Genetics 2002;38:383-92.

    w53 Tanis BC, Blom HJ, Bloemenkamp DG, van den Bosch MA, Algra A, van der Graaf Y, Rosendaal FR. Folate, homocysteine levels, methylenetetrahydrofolate reductase (MTHFR) 677C--> T variant, and the risk of myocardial infarction in young women: effect of female hormones on homocysteine levels. J Thromb Haemost 2004;2:35-41.

    w54 Raslova K, Smolkova B, Vohnout B, Gasparovic J, Frohlich JJ. Risk factors for atherosclerosis in survivors of myocardial infarction and their spouses: comparison to controls without personal and family history of atherosclerosis. Metabolism 2001;50:24-9.

    w55 Rothenbacher D, Fischer HG, Hoffmeister A, Hoffmann MM, Marz W, Bode G et al. Homocysteine and methylenetetrahydrofolate reductase genotype: association with risk of coronary heart disease and relation to inflammatory, hemostatic, and lipid parameters. Atherosclerosis 2002;162:193-200.

    w56 Gorący I, Gorący J, Suliga M and Ciechanowicz A. C677T gene polymorphism of the methylenetetrahydrofolate reductase (MTHFR) in patients with myocardial infarction. Polskie Archiwum Medycyny Wewnętrznej 1999;4:849-854.

    w57 Zhang G, Dai C. Gene polymorphisms of homocysteine metabolism-related enzymes in Chinese patients with occlusive coronary artery or cerebral vascular diseases. Thromb Res 2001;104:187-95.

    w58 Benes P, Kankova K, Muzik J, Groch L, Benedik J, Elbl L et al. Methylenetetrahydrofolate reductase polymorphism, type II diabetes mellitus, coronary artery disease, and essential hypertension in the Czech population. Mol Genet Metab 2001;73:188-95.

    w59 Hong SH, Song J, Kim JQ. Genetic variation of the methylenetetrahydrofolate reductase and cystathionine beta-synthase genes in Korean patients with coronary artery disease and a new polymorphism in intron 7. Mol Cell Probes 2001;15:119-23.

    w60 Kostulas K, Crisby M, Huang WX, Lannfelt L, Hagenfeldt L, Eggertsen G et al. A methylenetetrahydrofolate reductase gene polymorphism in ischaemic stroke and in carotid artery stenosis. Eur J Clin Invest 1998;28:285-9.

    w61 Abu-Amero KK, Wyngaard CA, Dzimiri N. Prevalence and role of methylenetetrahydrofolate reductase 677 C→T and 1298 A→C polymorphisms in coronary artery disease in Arabs. Arch Pathol Lab Med 2003;127:1349-1352.

    w62 Brilakis ES, Berger PB, Ballman KV, Rozen R. Methylenetetrahydrofolate reductase (MTHFR) 677C>T and methionine synthase reductase (MTRR) 66A>G polymorphisms: association with serum homocysteine and angiographic coronary artery disease in the era of flour products fortified with folic acid. Atherosclerosis 2003;168:315-22.

    w63 Žuntar I, Topic E, Vukosavic D, Vukovic V, Demarin V, Begonja A et al. Croatian population data for the C677T polymorphism in methylenetetrahydrofolate reductase: frequencies in healthy and atherosclerotic study groups. Clin Chim Acta 2003;335:95-100.

    w64 Kölling K, Ndrepepa G, Koch W, Braun S, Mehilli J, Schomig A, Kastrati A. Methylenetetrahydrofolate reductase gene C677T and A1298C polymorphisms, plasma homocysteine, folate, and vitamin B12 levels and the extent of coronary artery disease. Am J Cardiol 2004;93:1201-6.

    w65 Topol EJ, McCarthy J, Gabriel S, Moliterno DJ, Rogers WJ, Newby LK et al. Single nucleotide polymorphisms in multiple novel thrombospondin genes may be associated with familial premature myocardial infarction. Circulation 2001;104:2641-4.

    w66 Kou M-C, Wang L, Liang K-J and Wu M-J. Genotyping 5,10-methylenetetrahydrofolate reductase for patients with coronary artery disease in southern Taiwan. J Food Drug Anal 2001;9:173-7.

    w67 Jang Y, Park HY, Lee JH, Ryu HJ, Kim JY, Kim OY. A polymorphism of the methylenetetrahydrofolate reducatase and methionine synthase gene in CAD patients: association with plasma folate, vitamin B12 and homocysteine. Nutri Res 2002;22:965-76.

    w68 Folsom AR, Nieto FJ, McGovern PG, Tsai MY, Malinow MR, Eckfeldt JH et al. Prospective study of coronary heart disease incidence in relation to fasting total homocysteine, related genetic polymorphisms, and B vitamins: the Atherosclerosis Risk in Communities (ARIC) study. Circulation 1998 ;98:204-10.

    w69 Verhoeff BJ, Trip MD, Prins MH, Kastelein JJ, Reitsma PH. The effect of a common methylenetetrahydrofolate reductase mutation on levels of homocysteine, folate, vitamin B12 and on the risk of premature atherosclerosis. Atherosclerosis 1998;141:161-6.

    w70 Kądziela J, Janas J, Dzielińska Z, Szperl M, Chotkowska D, Piotrowski W and Rużyllo. The C677T mutation in methylenetetrahydrofolate reductase gene, plasma homocysteine concentration and the risk of coronary artery disease. Polish Heart J 2003;59:17-25.

    w71 Roest M, van der Schouw YT, Grobbee DE, Tempelman MJ, de Groot PG, Sixma JJ, Banga JD. Methylenetetrahydrofolate reductase 677 C/T genotype and cardiovascular disease mortality in postmenopausal women. Am J Epidemiol 2001;153:673-9.

    w72 Gemmati D, Serino ML, Trivellato C, Fiorini S, Scapoli GL. C677T substitution in the methylenetetrahydrofolate reductase gene as a risk factor for venous thrombosis and arterial disease in selected patients. Haematologica 1999;84:824-8.

    w73 Atherosclerosis, Thrombosis, and Vascular Biology Italian Study Group. No evidence of association between prothrombotic gene polymorphisms and the development of myocardial infarction at a young age. Circulation 2003;107:1117-1122.

    w74 Meleady R, Ueland PM, Blom H, Whitehead AS, Refsum H, Daly LE et al; EC Concerted Action Project: Homocysteine and Vascular Disease. Thermolabile methylenetetrahydrofolate reductase, homocysteine, and cardiovascular disease risk: the European Concerted Action Project. Am J Clin Nutr 2003;77:63-70.

    w75 Payne DA, Chamoun AJ, Seifert SL, Stouffer GA. MTHFR 677 C-->T mutation: a predictor of early-onset coronary artery disease risk. Thromb Res 2001;103:275-9.


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