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Protein intake and blood pressure in cardiovascular disease

Published online by Cambridge University Press:  05 March 2007

Paul Elliott
Paul Elliott*
Affiliation:
Department of Epidemiology and Public Health, Imperial College, London, St Mary's Campus, Norfolk Place, London, W2 1PG, UK
*
Corresponding author: Dr Paul Elliott, fax +44 20 7262 1034, p.elliott@ic.ac.uk
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Abstract

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Raised blood pressure (BP) is a major cause of CHD and the leading cause of stroke. Although BP rises with age in most populations, there are remote populations around the world where BP does not rise with age and where the high prevalence of high BP and frank hypertension seen in the UK and other Western countries in the older age-groups is not found. However, when such populations migrate to urban settings, their BPs rise, indicating that the population-wide BP problem is largely environmental in origin. Thus, a substantial body of evidence has accumulated on the importance of dietary factors in BP (Na and alcohol intakes (direct relationship) and K intake (inverse relationship)) as well as body weight (direct relationship). More recently, attention has shifted to other dietary factors that might affect BP. Data from studies of vegetarians (who tend to have lower BP than meat-eating populations) as well as clinical data on the adverse effects of protein intake in patients with renal insufficiency led to the view in Western countries that dietary (animal or total) protein had an adverse effect on BP. By contrast, studies in Japan and China suggested that dietary protein might be protective of high BP and stroke. Recent epidemiological studies have found inverse associations between dietary protein intake and BP, consistent with this view, and supported by some evidence from animal studies. Recent controlled clinical trials of soyabean supplementation have also suggested a BP-lowering effect of protein intake. Results of further large-scale epidemiological studies of protein and BP are awaited.

Keywords

Blood pressureProtein intakeCardiovascular disease riskWestern lifestyleEpidemiological data
Type
Macronutrient Group Symposium on ‘Protein intake and chronic disease’
Information
Proceedings of the Nutrition Society , Volume 62 , Issue 2 , May 2003 , pp. 495 - 504
Copyright
Copyright © The Nutrition Society 2003

References

Anderson, GH (1986) Proteins and amino acids: effects on the sympathetic nervous system and blood pressure regulation. Canadian Journal of Physiology and Pharmacology 64, 863–870Google Scholar
Appel, L & Elliott, P (2003) The effects of macronutrients, fiber, cholesterol, and dietary patterns on blood pressure. In Hypertension Prevention and Treatment: From Lifestyle Modification to Public Health Policy [Whelton P, J, He and Louis, GT, editors]. New York: Marcel Dekker.Google Scholar
Appel, LJ, Moore, TJ, Obarzanek, E, Vollmer, WM, Svetkey, LP, Sacks, FM, Bray, GA, Vogt, TM, Cutler, JA, Windhauser, MM, Lin, P-H, Karanja, N, for, the, DASH, Collaborative & Research, Group (1997) A clinical trial of the effect of dietary patterns on blood pressure. New England Journal of Medicine 336, 1117–1124Google Scholar
Armstrong, B, van, Merwyk, AJ, Coates H (1977) Blood pressure in Seventh-day Adventists. American Journal of Epidemiology 105, 444–449CrossRefGoogle Scholar
Boulton, TJC (1981) Nutrition in childhood and its relationship to early somatic growth, body fat, blood pressure and physical fitness. Acta Paediatrica Scandinavica 284, 68–79 Suppl.Google ScholarPubMed
Brod, J, Bahlmann, J, Cachovan, M & Pretschner, P (1983) Development of hypertension in renal disease. Clinical Science 64, 141–152Google Scholar
Burke, V, Beilin, LJ & Sciarrone, S (1994) Vegetarian diets, protein and fibre. In Textbook of Hypertension, pp. 619–632 [Swales, JD, editors]. Oxford: Blackwell.Google Scholar
Burke, V, Hodgson, JM, Beilin, LJ, Giangiulioi, N, Rogers, P & Puddey, IB (2001) Dietary protein and soluble fiber reduce ambulatory blood pressure in treated hypertensives. Hypertension 38, 821–826Google Scholar
Carvalho, JJM, Baruzzi, RG, Howard, P, Poulter, N, Alpers, MP, Franco, LJ, Marcopito, LF, Spooner, VJ, Dyer, AR, Elliott, P, Stamler, J & Stamler, R (1989) Blood pressure in four remote populations in the INTERSALT study. Hypertension 14, 238–246Google Scholar
Crouse, JR, Morgan, T, Terry, J, Ellis, J, Vitolins, M & Burke, G (1999) A randomizing trial comparing the effect of casein with that of soy protein containing varying amounts of isoflavones on plasma concentrations of lipids and lipoproteins. Archives of Internal Medicine 159, 2070–2076Google Scholar
Dawber, TR, Kannel, WB, Kagan, A, Donabedian, RK, McNamara, PM & Pearson, G (1967) Environmental factors in hypertension. In The Epidemiology of Hypertension, pp. 255–288 [Stamler, J, Stamler, J and Pullman, TN, editors]. New York: Grune & Stratton.Google Scholar
Dyer, AR, Elliott, P & Shipley, M (1994a) Urinary electrolyte excretion in 24-hours and blood pressure in the INTERSALT Study. II. Estimates of electrolyte-blood pressure associations corrected for regression dilution bias. American Journal of Epidemiology 139, 940–951Google Scholar
Dyer, AR, Shipley, M & Elliott, P (1994b) Urinary electrolyte excretion in 24-hours and blood pressure in the INTERSALT Study. I. Estimates of reliability. American Journal of Epidemiology 139, 927–939Google Scholar
Elliott, P, Fehily, AM, Sweetnam, PM & Yarnell, JWG (1987) Diet, alcohol, body mass, and social factors in relation to blood pressure: the Caerphilly Heart Study. Journal of Epidemiology and Community Health 41, 37–43Google Scholar
Elliott, P, Freeman, J, Pryer, J, Brunner, E & Marmot, M (1992) Dietary protein and blood pressure: A report from the Dietary and Nutritional Survey of British Adults. Journal of Hypertension 109, S141 Abstr Suppl. 1Google Scholar
Elliott, P, Stamler, J, Nichols, R, Dyer, AR, Stamler, R, Kestloot, H, Marmot, M for the INTERSALT Cooperative & Research Group (1996) INTERSALT revisited: Further analyses of 24-hour sodium excretion and blood pressure within and across populations. British Medical Journal 312, 1249–1253CrossRefGoogle Scholar
Erens, B & Primatesta, P (1999) Health Survey for England. Risk Factors for Cardiovascular Disease 1998 London The Stationery OfficeGoogle Scholar
Fehily, AM, Milbank, JE, Yarnell, JWG, Hayes, TM, Kubiki, AJ & Eastham, RD (1982) Dietary determinants of lipoproteins, total cholesterol, viscosity, fibrinogen, and blood pressure. American Journal of Clinical Nutrition 36, 890–896Google Scholar
Frank, GC, Berenson, GS & Webber, F (1978) Dietary studies and the relationship of diet to cardiovascular disease risk factor variables in 10-year old children–the Bogalusa Heart Study. American Journal of Clinical Nutrition 31, 328–340Google Scholar
Gruchow, HW, Sobocinski, KA & Barboriak, JJ (1985) Alcohol, nutrient intake, and hypertension in US adults. Journal of the American Medical Association 253, 1567–1570Google Scholar
Hajjar, I, Grim, CE, Varghese, G & Kotchen, TA (2001) Impact of diet on blood pressure and age-related changes in blood pressure in the US population: Analysis of NHANES III. Archives of Internal Medicine 161, 589–593CrossRefGoogle ScholarPubMed
Harlan, WR, Hull, AL, Schmouder, RL, Landis, JR, Thompson, FE & Larkin, FA (1984) Blood pressure and nutrition in adults. The National Health and Nutrition Examination Survey. American Journal of Epidemiology 120, 17–28Google Scholar
Havlik, RJ, Fabsitz, RR, Kalousdian, S, Borhani, NO & Christain, JC (1990) Dietary protein and blood pressure in monozygotic twins. Preventive Medicine 19, 31–39Google Scholar
He, J, Klag, MJ, Whelton, PK, Chen, J-Y, Qian, M-C, He, G-Q (1995) Dietary macronutrients and blood pressure in southwestern China. Journal of Hypertension 13, 1267–1274Google Scholar
He, J, Loria, C, Vupputuri, S & Whelton, PK (1998) Dietary macronutrient intake and level of blood pressure: Results from the Third National Health and Nutrition Examination Survey (NHANES III). Circulation 98 858Abstr Suppl. 1.Google Scholar
He, J & Whelton, PK (1999) Effect of dietary fiber and protein intake on blood pressure: A review of epidemiologic evidence. Clinical and Experimental Hypertension 21, 785–796Google Scholar
He, J, Wu, XG, Gu, DF, Duan, XF & Whelton, PK (2000) Soybean protein supplementation and blood pressure: a randomized, controlled clinical trial. Circulation 101, 711 AbstrGoogle Scholar
Hermansen, K, Sondergaard, M, Hoie, L, Carstensen, M & Brock, B (2001) Beneficial effects of a soy-based dietary supplement on lipid levels and cardiovascular risk markers in Type 2 diabetic subjects. Diabetes Care 24, 228–233Google Scholar
Hodgson, JM, Puddey, I, Beilin, LJ, Mori, TA, Burke, V, Croft, KD & Rogers, PB (1999) Effects of isoflavonoids on blood pressure in subjects with high-normal ambulatory blood pressure levels. A randomized controlled trial. American Journal of Hypertension 12, 47–53Google Scholar
Ihle, BU, Becker, GJ, Whitworth, JA, Charlwood, RA, Kincaid-Smith, PS (1989) The effect of protein restriction on the progression of renal insufficiency. New England Journal of Medicine 321, 1773–1777Google Scholar
INTERSALT, Cooperative & Research, Group (1988) INTERSALT: An international study of electrolyte excretion and blood pressure. Results for 24-hour urinary sodium and potassium. British Medical Journal 297, 319–328Google Scholar
Jenner, DA, English, DR, Vandongen, R, Beilin, L, Armstrong, BK, Miller, MR & Dunbar, D (1988) Diet and blood pressure in 9-year-old Australian children. American Journal of Clinical Nutrition 47, 1052–1059Google Scholar
Joffres, MR, Reed, DM & Yano, K (1987) Relationship of magnesium intake and other dietary factors to blood pressure: the Honolulu Heart Study. American Journal of Clinical Nutrition 45, 469–475Google Scholar
Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure (1997) The sixth report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure (JNC VI). Archives of Internal Medicine 157, 2413–2446Google Scholar
Kempner, W (1948) Treatment of hypertensive vascular disease with rice diet. American Journal of Medicine 4, 545–577Google Scholar
Kihara, M, Fujikawa, J, Ohtaka, M, Mano, M, Nara, Y, Horie, R, Tsunematsu, T, Note, S, Fukase, M & Yamori, Y (1984) Interrelationships between blood pressure, sodium, potassium, serum cholesterol, and protein intake in Japanese. Hypertension 6, 736–742Google Scholar
Liu, L (1989) Hypertension studies in China. Clinical and Experimental Hypertension 11, 859–868Google Scholar
Liu, K, Ruth, KJ, Flack, JM, Jones-Webb, R, Burke, G, Savage, PJ & Hulley, SB (1996) Blood pressure in young blacks and whites: relevance of obesity and lifestyle factors determining differences. The CARDIA Study. Circulation 93, 60–66CrossRefGoogle ScholarPubMed
Liu, LJ, Ikeda, K & Yamori, Y (2000a) Twenty-four hour urinary sodium and 3-methylhistidine excretion in relation to blood pressure in Chinese: Results from the China–Japan cooperative research for the WHO-CARDIAC Study. Hypertension Research 23, 151–157Google Scholar
Liu, LJ, Liu, LS, Ding, Y, Huang, ZD, He, BX, Sun, SF, Zhao, GS, Zhang, HX, Miki, T, Mizushima, S, Ikeda, K, Nara, Y & Yamori, Y (2001) Ethnic and environmental differences in various markers of dietary intake and blood pressure among Chinese Han and three other minority peoples of China: Results from the WHO Cardiovascular Diseases and Alimentary Comparison (CARDIAC) Study. Hypertension Research 24, 315–322Google Scholar
Liu, LJ, Mizushima, S, Ikeda, K, Hattori, H, Miura, A, Gao, M, Nara, Y & Yamori, Y (2000b) Comparative studies of diet-related factors and blood pressure among Chinese and Japanese: results from the China–Japan Cooperative Research of the WHO-CARDIAC Study. Hypertension Research 23, 413–420Google Scholar
Ludwig, DS, Pereira, MA, Kroenke, CH, Hilner, JE, Van, Horn, L, Slattery, ML Jacobs, DR (1999) Dietary fiber, weight gain, and cardiovascular disease risk factors in young adults. Journal of the American Medical Association 282, 1539–1546Google Scholar
McCarron, DA, Henry, HJ & Morris, CD (1982) Human nutrition and blood pressure regulation: An integrated approach. Hypertension 4 III-2–III–13 Suppl. IIICrossRefGoogle ScholarPubMed
McCarron, DA, Morris, CD, Henry, HJ & Stanton, JL (1984) Blood pressure and nutrient intake in the United States. Science 224, 1392–1398CrossRefGoogle ScholarPubMed
Margetts, BM, Beilin, LJ, Vandongen, R & Armstrong, BK (1986) Vegetarian diet in mild hypertension: A randomised controlled trial. British Medical Journal 293, 1468–1471Google Scholar
Meyer, TW, Anderson, S & Brenner, BM (1983) Dietary protein intake and progressive glomerular sclerosis: The role of capillary hypertension and hyperperfusion in the progression of renal disease. Annals of Internal Medicine 98, 832–838Google Scholar
Moncada, S & Higgs, A (1993) The L-arginine-nitric oxide pathway. New England Journal of Medicine 329, 2003–2012Google Scholar
Morris, CD, Jacobson, S-L, Anand, R, Ewell, MG, Hauth, JC, Curet, LB, Catalano, PM, Sibai, BM & Levine, RJ (2001) Nutrient intake and hypertensive disorders of pregnancy: evidence from a large prospective cohort. American Journal of Obstetrics and Gynecology 184, 643–651CrossRefGoogle ScholarPubMed
Murray, CJL & Lopez, AD (1996) Quantifying the burden of disease and injury attributable to ten major risk factors. In The Global Burden of Disease. A Comprehensive Assessment of Mortality and Disability from Diseases, Injuries, and Risk Factors in 1990 and Projected to 2020, pp. 295–324 [Murray, CJL and Lopez, AD, editors]. Boston: Harvard School of Public Health/WHO/World Bank.Google Scholar
National, Research Council (1989) Diet and Health: Implications for Reducing Chronic Disease Washington, DC National Academy PressGoogle Scholar
Nestel, PJ, Yamashita, T, Takayuki, S, Pomeroy, S, Dart, A, Komesaroff, P, Owen, A & Abbey, M (1997) Soy isoflavones improve systemic arterial compliance but not plasma lipids in menopausal and perimenopausal women. Arteriosclerosis Thrombosis and Vascular Biology 17, 3392–3398Google Scholar
Obar-zanek, E, Velletri, PA & Cutler, JA (1996) Dietary protein and blood pressure. Journal of the American Medical Association 275, 1598–1603Google Scholar
Poulter, NR, Khaw, KT, Hopwood, BEC, Mugambi, M, Peart, WS, Rose, G & Sever, PS (1990) The Kenyan Luo migration study: Observations on the initiation of a rise in blood pressure. British Medical Journal 300, 967–972Google Scholar
Pearson, TA, Jamison, DT, Trejo-Gutierrez, J (1993) Cardiovascular disease. In Disease Control Priorities in Developing Countries, pp 577–594 [Jamison, DT, Mosley, WH, Measham, AR and Bobadilla, JL, editors]. Oxford: Oxford University Press.Google Scholar
Pellum, LK & Madeiros, DM (1983) Blood pressure in young adult normotensives: effect of protein, fat, and cholesterol intakes. Nutrition Reports International 27, 1277–1285Google Scholar
Pryer, JA, Vrijheid, M, Nichols, R, Kiggins, M & Elliott, P (1997) Who are the ‘low energy reporters’ in the Dietary and Nutritional Survey of British Adults?. International Journal of Epidemiology 26, 146–153CrossRefGoogle ScholarPubMed
Rafie, M, Boshtam, M, SarrafZadegan, N, Abdar, N, Sedigheh, K, Asgary, S & Naderi, G (1998) The impact of macro and micronutrients daily intake on blood pressure. Atherosclerosis 136 S62Abstr Suppl. 1Google Scholar
Reed, D, McGee, D, Yano, K & Hankin, J (1985) Diet, blood pressure, and multicollinearity. Hypertension 7, 405–410Google Scholar
Rose, G (1985) Sick individuals and sick populations. International Journal of Epidemiology 14, 32–38Google Scholar
Rose, G (1992) The Strategy of Preventive Medicine. Oxford: Oxford University Press.Google Scholar
Rouse, IL, Beilin, LJ, Armstrong, BK & Vandongen, R (1983) Blood pressure-lowering effect of a vegetarian diet: controlled trial in normotensive subjects. Lancet i, 5–10Google Scholar
Sacks, FM, Donner, A, Castelli, WP, Gronemeyer, J, Pletka, P, Margolius, HS, Landsberg, L & Kass, EH (1981) Effect of ingestion of meat on plasma cholesterol of vegetarians. Journal of the American Medical Association 246, 640–646Google Scholar
Sacks, FM & Kass, EH (1988) Low blood pressure in vegetarians; effects of specific foods and nutrients. American Journal of Clinical Nutrition 48, 795–800 Suppl.Google Scholar
Sacks, FM, Marais, GE, Handysides, GH, Salazar, J, Miller, L, Foster, JM, Rosner, B & Kass, EH (1984a) Lack of an effect of dietary saturated fat and cholesterol on blood pressure in normotensives. Hypertension 6, 193–198Google Scholar
Sacks, FM, Rosner, B & Kass, EH (1974) Blood pressure in vegetarians. American Journal of Epidemiology 100, 390–398Google Scholar
Sacks, FM, Wood, PG & Kass, EH (1984b) Stability of blood pressure in vegetarians receiving dietary protein supplements. Hypertension 6, 199–201Google Scholar
Shaper, AG (1972) Cardiovascular disease in the tropics–III, Blood pressure and hypertension. British Medical Journal iii, 805–807Google Scholar
Simons-Morton, DG, Hunsberger, SA, van, Horn, L, Barton, BA, Robson, AM, McMahon, RP, Muhonen, LE, Kwiterovich, PO, Lasser, NL, Kimm, SYS Greenlick, MR (1997) Nutrient intake and blood pressure in the Dietary Intervention Study in Children. Hypertension 29, 930–936Google Scholar
Slattery, ML, Bishop, DT, French, TK, Hunt, SC, Meikle, AW & Williams, RR (1988) Lifestyle and blood pressure levels in twins in Utah. Genetic Epidemiology 5, 277–287CrossRefGoogle ScholarPubMed
Stamler, J (1992) Established major coronary risk factors. In Coronary Heart Disease Epidemiology: From Aetiology to Public Health, pp. 35–66 [Marmot, M and Elliott, P, editors]. Oxford: Oxford University Press.Google Scholar
Stamler, J, Caggiula, AW & Grandits, GA (1997) Relation of body mass and alcohol, nutrient, fiber, and caffeine intakes to blood pressure in the special intervention and usual care groups in the Multiple Risk Factor Intervention Trial. American Journal of Clinical Nutrition 65, 338S–365S Suppl.Google Scholar
Stamler, J, Caggiula, A, Grandits, GA, Kjelsberg, M, Cutler, JA, for, the Research Group (1996a) Relationship to blood pressure of combinations of dietary macronutrients. Findings of the Multiple Risk Factor Intervention Trial (MRFIT). Circulation 94, 2417–2423Google Scholar
Stamler, J, Elliot, P, Dennis, B, Dyer, AR, Kerseloof, H, Lin, K, Ueshima, H, Zhou, B for the INTERMAP Research Group (2003) INTERMAP: background, aims, design, methods and descriptive statistics (non-dietary) Journal of Human HypertensionGoogle Scholar
Stamler, J, Elliott, P, Kesteloot, H, Nichols, R, Claeys, G, Dyer, AR, Stamler, R for the INTERSALT Cooperative & Research Group (1996b) Inverse relation of dietary protein markers with blood pressure. Findings for 10020 men and women in the INTERSALT Study. Circulation 94, 1629–1634Google Scholar
Stamler, J, Liu, K, Ruth, KJ, Pryer, J & Greenland, P (2002) Eight-year blood pressure change in middle-aged men: Relationship to multiple nutrients. Hypertension 39, 1000–1006Google Scholar
Stamler, J, Stamler, R & Neaton, JD (1993) Blood pressure, systolic and diastolic, and cardiovascular risks. US population data. Archives of Internal Medicine 153, 598–615Google Scholar
Sved, AF, Fernstrom, JD & Wurtman, RJ (1979) Tyrosine administration reduces blood pressure and enhances brain norepinephrine release in spontaneously hypertensive rats. Proceedings of the National Academy of Sciences USA 76, 3511–3514Google Scholar
Sved, AF, van, Itallie, CM, Fernstrom JD (1982) Studies on the antihypertensive action of L-tryptophan. Journal of Pharmacology and Experimental Therapeutics 221, 329–333Google Scholar
Teede, HJ, Dalais, FS, Kotsopoulos, D, Liang, Y-L, Davis, S & McGrath, BP (2001) Dietary soy has both beneficial and potentially adverse cardiovascular effects: a placebo-controlled study in men and postmenopausal women. Journal of Clinical Endocrinology and Metabolism 86, 3053–3060Google Scholar
Viart, P (1977) Hemodynamic findings in severe protein–calorie malnutrition. American Journal of Clinical Nutrition 30, 334–348Google Scholar
Vupputuri, S, He, J, Ogden, LG, Loria, C & Whelton, PK (1998) Dietary intake of macronutrients and risk of hypertension: A prospective study using the First National Health and Nutrition Examination Survey (NHANES) Cohort. Circulation 98, 859 Suppl. 1Google Scholar
Washburn, S, Burke, GL, Morgan, T & Anthony, M (1999) Effect of soy protein supplementation on serum lipoproteins, blood pressure, and menopausal symptoms in perimenopausal women. Menopause 6, 7–13Google Scholar
Watkin, DM, Froeb, HF, Hatch, FT & Gutman, AB (1950) Effect of diet in essential hypertension. II Results with unmodified Kempner rice diet in fifty hospitalized patients. American Journal of Medicine 9, 441–493Google Scholar
Willett, W & Stampfer, M (1998) Implications of total energy intake for epidemiologic analyses. In Nutritional Epidemiology, pp. 2nd ed. 273–301 [Willett, W, editors]. Oxford: Oxford University Press.Google Scholar
Williams, JL, McCoy, RA, Martin, DS & Albers, JE (1999) Effects of a soy diet on blood pressure and vascular reactivity in hypertensive men and postmenopausal women. Presented at the Third International Symposium on the role of soy in preventing and treating chronic disease, Washington DC, Oct 31–Nov 3, Abstr.Google Scholar
Yamori, Y, Horie, R, Nara, Y, Kihara, M, Ikeda, K, Mano, M & Fujiwara, K (1984) Dietary prevention of hypertension in animal models and its applicability to humans. Annals of Clinical Research 16, 28–31 Suppl. 43Google Scholar
Yamori, Y, Kihara, M, Nara, Y, Ohtaka, M, Horie, R, Tsunematsu, T & Note, S (1981) Hypertension and diet: multiple regression analysis in a Japanese farming community. Lancet i, 1204–1205Google Scholar
Zhou, B-F, Wu, X-G, Tao, S-Q, Yang, J, Cao, T-X, Zheng, R-P, Tian, X-Z, Lu, C-Q, Miao, H-Y, Ye, F-M, Zhu, L-G, Zhu, C, Jiang, J-P, He, Hou-Q, Ma, F, Du, F-C & Wang, B (1989) Dietary patterns in 10 groups and the relationship with blood pressure. Chinese Medical Journal 102, 257–261Google Scholar
Zhou, B, Zhang, X, Zhu, A, Zhao, L, Zhu, S, Ruan, L, Zhu, L & Liang, S (1994) The relationship of dietary animal protein and electrolytes to blood pressure: a study on three Chinese populations. International Journal of Epidemiology 23, 716–722Google Scholar