Abstract
Public health strategies targeting the prevention of poor bone health on a population-wide basis are urgently required, with particular emphasis being placed on modifiable factors such as nutrition. The aim of this review was to assess the impact of a vegetarian diet on indices of skeletal integrity to address specifically whether vegetarians have a normal bone mass. Analysis of existing literature, through a combination of observational, clinical and intervention studies were assessed in relation to bone health for the following: lacto-ovo-vegetarian and vegan diets versus omnivorous, predominantly meat diets, consumption of animal versus vegetable protein, and fruit and vegetable consumption. Mechanisms of action for a dietary “component” effect were examined and other potential dietary differences between vegetarians and non-vegetarians were also explored. Key findings included: (i) no differences in bone health indices between lacto-ovo-vegetarians and omnivores; (ii) conflicting data for protein effects on bone with high protein consumption (particularly without supporting calcium/alkali intakes) and low protein intake (particularly with respect to vegan diets) being detrimental to the skeleton; (iii) growing support for a beneficial effect of fruit and vegetable intake on bone, with mechanisms of action currently remaining unclarified. The impact of a “vegetarian” diet on bone health is a hugely complex area since: 1) components of the diet (such as calcium, protein, alkali, vitamin K, phytoestrogens) may be varied; 2) key lifestyle factors which are important to bone (such as physical activity) may be different; 3) the tools available for assessing consumption of food are relatively weak. However, from data available and given the limitations stipulated above, “vegetarians” do certainly appear to have “normal” bone mass. What remains our challenge is to determine what components of a vegetarian diet are of particular benefit to bone, at what levels and under which mechanisms.
Similar content being viewed by others
References
World Health Organisation (1994) Assessment of osteoporotic fracture risk and its role for screening for postmenopausal osteoporosis. WHO technical report series. WHO, Geneva
Goulding A (2003) In: New SA, Bonjour JP (eds) Nutritional aspects of bone health. The Royal Society of Chemistry, Cambridge, pp 709–732
National Dairy Council (2002) Fact sheet 10. Vegetarian diets. NDC, London
Gregory J, Lowe S, Bates CJ, Prentice A, Jackson LV, Smithers G, Wenlock R, Farron M (2000) National Diet and Nutrition Survey (NDNS) of people aged 4–18 years, volume 1. HMSO, London
White R, Frank E (1994) Health effects and prevalence of vegetarianism. West J Med 60:465–471
Heaney RP, Abrams S, Dawson-Hughes B, Looker A, Marcus R, Matkovic V, Weaver C (2000) Peak bone mass. Osteoporos Int 11:985–1009
Sanders TAB (1999) The nutritional adequacy of plant-based diets. Proc Nutr Soc 58:265–269
Bushinsky DA (1998) Acid-base imbalance and the skeleton. In: Burckhardt P, Dawson-Hughes, B, Heaney RP (eds) Nutritional aspects of osteoporosis ‘97. Proceedings of the 3rd International Symposium on Nutritional Aspects of Osteoporosis, Switzerland, 1997. Ares-Serono Symposia Publications, Italy, pp 208–217
Green J, Kleeman R (1991) Role of bone in regulation of systematic acid-base balance (Editorial Review). Kidney Int 39:9–26
Frassetto LA, Morris RC Jr, Sebastian A (1996) Effect of age on blood acid-base composition in adult humans: role of age-related renal functional decline. Am J Physiol (Renal Fluid Electrolyte Physiol 40) 271:F1114–1122
Frassetto LA, Sebastian A (1996) Age and systemic acid-base equilibrium: analysis of published data. J Gerontol 51A:B91–9
Goto K (1918) Mineral metabolism in experimental acidosis. J Biol Chem 36:355–376
Lemann J Jr, Litzow JR, Lennon EJ (1966) The effects of chronic acid load in normal man: further evidence for the participation of bone mineral in the defence against chronic metabolic acidosis. J Clin Invest 45:1608–1614
Barzel US, Jowsey J (1969) The effects of chronic acid and alkali administration on bone turnover in adult rats. Clin Sci 36:517–524
Arnett TR, Dempster DW (1986) Effect of pH on bone resorption by rat osteoclasts in vitro. Endocrinology 119:119–124
Kreiger NA, Sessler NE, Bushinsky DA (1992) Acidosis inhibits osteoblastic and stimulates osteoclastic activity in vitro. Am J Physiol 262:F442–F448
Arnett TR, Spowage M (1996) Modulation of the resorptive activity of rat osteoclasts by small changes in extracellular pH near the physiological range. Bone 18:277–279
Bushinsky DA (1996) Metabolic alkalosis decreases bone calcium efflux by suppressing osteoclasts and stimulating osteoblasts. Am J Physiol 271:F216–F222
Meghji S, Morrison MS, Henderson B, Arnett TR (2001) PH dependence of bone resorption: mouse calvarial osteoclasts are activated by acidosis. Am J Physiol Endocrinol Metabol 280:E112–E119
Bushinsky DA, Sessler NE, Glena RE, Featherstone JDB. (1994) Proton induced physicochemical calcium release from ceramic apatite disks. J Bone Miner Res 9:213–220
Wachman A, Bernstein DS (1968) Diet and osteoporosis. Lancet I:958–959
Barzel US, Massey LK (1998) Excess dietary protein can adversely affect bone. J Nutr 128:1051–1053
Ellis FR, Holesh S, Ellis JW (1972) Incidence of osteoporosis in vegetarians and omnivores. Am J Clin Nutr 25:555–558
Ellis FR, Holesh S, Sanders TA (1974) Osteoporosis in British vegetarians and omnivores. Am J Clin Nutr 24:769–770
Marsh AG, Sanchez TV, Micklesen O, Keiser J, Major G (1980) Cortical bone density of adult lactoovovegetarians and omnivorous women. J Am Diet Ass 76:148–151
Marsh AG, Sanchez TV, Chaffee FL, Mayor GH, Mickelsen O (1983) Bone mineral mass in adult lactoovovegetarian and omnivorous males. Am J Clin Nutr 83:155–162
Marsh AG, Sanchez TV, Michelsen O, Chaffee FL, Fagal SM (1988) Vegetarian lifestyle and bone mineral density. Am J Clin Nutr 48:837–841
Tylavsky F, Anderson JJB (1988) Bone health of elderly lactoovovegetarian and omnivorous women. Am J Clin Nutr 48:842–849
Hunt IF, Murphy NJ, Henderson C, Clark VA, Jacobs RM, Johnston PK, Coulson AH (1989) Bone mineral content in postmenopausal women: comparison of omnivores and vegetarians. Am J Clin Nutr 50:517–523
Meema HE (1973) Photographic density versus bone density. Am J Clin Nutr 26:687 [Letter]
Meema HE (1996) What’s good for the heart is not good for the bones? J Bone Miner Res 11:704 [Letter]
Barzel US (1996) Ne’ertheless, an acidogenic diet may impair bone. J Bone Miner Res 11:704 [Letter]
Lloyd T, Schaeffer JM, Walker MA, Demers LM (1991) Urinary hormonal concentrations and spinal bone densities of premenopausal vegetarian and nonvegetarian women. Am J Clin Nutr 54:1005–1010
Tesar R, Notelovitz M, Shim E, Kauwell G, Brown J (1992) Axial and peripheral bone density and nutrient intakes of postmenopausal vegetarian and omnivorous women. Am J Clin Nutr 56:699–704
Reed JA, Anderson JBB, Tylavsky FA, Gallagher PN Jnr (1994) Comparative changes in radial bone density of elderly female lactoovovegetarians and omnivores. Am J Clin Nutr 59:1197S–1202S
Chiu JF, Lan SJ, Yang CY, Wang PW, Yao WJ, Su LH, Hsieh CC (1997) Long term vegetarian diet and bone mineral density in postmenopausal Taiwanese women. Calcif Tissue Int 60:245–249
Lau EM, Kwok T, Woo J, Ho SC (1998) Bone mineral density in Chinese elderly female vegetarians, vegans, lactoovovegetarians and omnivores. Eur J Clin Nutr 52:60–64
Mazess RB, Mather WE (1974) Bone mineral content of North Alaskan Eskimos. Am J Clin Nutr 27:916–925
Mazess RB, Mather WE (1975) Bone mineral content in Canadian Eskimos. Hum Biol 47:45
Mann G (1975) Bone mineral content of North Alaskan Eskimos. Am J Clin Nutr 28:566–567 [Letter]
Mazess RB, Mather WE (1975) Bone mineral content of North Alaskan Eskimos. Am J Clin Nutr 28:567 [Letter]
Remer T, Manz F (1995) Potential renal acid load of foods and its influence on urine pH. J Am Diet Assoc 95:791–797
Fox D (2001) Hard cheese. New Scientist 2329:42–45
New SA, Macdonald HM, Reid DM, Dixon AStJ (2002) Hold the soda. New Scientist 2330:54–55 [Letter]
Janelle KC, Barr SI (1995) Nutrient intakes and eating behaviour scores of vegetarian and nonvegetarian women. Osteoporos Int 95:180–186
Larsson CL, Johansson GK (2002) Dietary intakes and nutritional status of young vegans and omnivores in Sweden. Am J Clin Nutr 76:100–106
Hunt IF, Murphy NJ, Henderson C (1988) Food and nutrient intake of seventh-day Adventist women. Am J Clin Nutr 48:850–851
Shearer MJ (1997) The roles of vitamin D and vitamin K in bone health and osteoporosis prevention. Proc Nutr Soc 56:915–937
Booth SL (2003) Dietary vitamin K and skeletal health. In: New SA, Bonjour JP (2003) Nutritional aspects of bone health. Royal Society of Chemistry, Cambridge, pp 323–338
Braam L, Knapen M, Geusens P, Brouns F, Hamulyak K, Gerichhausen M, Vermeer C (2003) Vitamin K1 supplementation retards bone loss in postmenopausal women between 50 and 60 years of age. Calcif Tissue Int 73:21–26
Booth S, Sadowski J, Weihrauch J, Ferland G (1993) Vitamin K1 (phylloquinone) content of foods: a provisional table. J Food Compos Anal 6:109–120
Bolton-Smith C, Price RJ, Fenton ST, Harrington DJ, Shearer MJ (2000) Compilation of a provisional UK database for the phylloquinone (vitamin K1) content of foods. Br J Nutr 83:389–399
Kurzer MS, Xu X (1997) Dietary phytoestrogens. Annu Rev Nutr 17:353–381
Ishida H, Uesugi T, Hirai K, Toda T, Nukaya H, Yokotsuka K, Tsuji K (1998) Preventative effects of the plant isoflavones, daidzein and genistein, on bone loss in ovariectomized rats fed a calcium-deficient diet. Biol Pharmacol Bull 21:62–66
Cai DJ, Spence LA, Weaver CM (2003) Soy isoflavones and bone health. In: New SA, Bonjour JP (eds) Nutritional aspects of bone health. Royal Society of Chemistry, Cambridge, pp 421–438
Massey LK, Whiting SJ. Excess dietary protein and bone health. In: New SA, Bonjour JP (eds) Nutritional aspects of bone health. Royal Society of Chemistry, Cambridge pp 213–228
Anderson JJ, Metz JA (1995) Adverse association of high protein intake to bone density. Challenges Modern Medicine 7:407–412
Metz JA, Anderson JJ, Gallagher J PN (1993) Intakes of calcium, phosphorus and protein and physical activity level are related to radial bone mass in young adult women. Am J Clin Nutr 58:537–542
Feskanich D, Willett WC, Stampfer MJ, Colditz GA (1996) Protein consumption and bone fractures in women. Am J Epidemiol 143:472–479
Teegarden D, Lyle RM, McCabe GP, McCabe LD, Proulx WR, Michon K, Knight AP, Johnston CC, Weaver CM (1998) Dietary calcium, protein and phosphorus are related to bone mineral density and content in young women. Am J Clin Nutr 68:749–754
Cooper C, Atkinson EJ, Hensrud DD, Wahner HW, O’Fallon WM, Riggs BL, Melton III LJ (1996) Dietary protein intake and bone mass in women. Calcif Tissue Int 58:320–325
Munger RG, Cerhan JR, Chiu BC (1999) Prospective study of dietary protein intake and risk of hip fracture in postmenopausal women. Am J Clin Nutr 69:147–152
Hannan MT, Tucker KL, Dawson-Hughes B, Cupples LA, Felson DT, Kiel DP (2000) Effect of dietary protein on bone loss in elderly men and women: the Framingham Osteoporosis Study. J Bone Miner Res 15:2504–2512
Rizzoli R, Ammann P, Chevalley T, Bonjour J-P (2003) Effects of dietary protein insufficiency on the skeleton. In: New SA, Bonjour JP (eds) Nutritional aspects of bone health. Royal Society of Chemistry, Cambridge, pp 193–212
Schurch MA, Rizzoli R, Slosman D, Vadas L, Vergnaud P, Bonjour JP (1998) Protein supplements increase serum insulin-like growth factor-I levels and attenuate proximal femur bone loss in patients with recent hip fracture. A randomised, double-blind, placebo-controlled trial. Ann Int Med 128:801–809
Abelow BJ, Holford TR, Insogna KL (1992) Cross-cultural association between dietary animal protein and hip fracture: a hypothesis. Calcif Tissue Int 50:14–18
Frassetto LA, Todd KM, Morris RCJnr, Sebastian A (2000) World-wide incidence of hip fracture in older women: relation to consumption of animal and vegetable foods. J Gerontol 55A:M585–M592
Sellmeyer DE, Stone KL, Sebastian A, Cummings SR for the Study of Osteoporotic Fractures (2001) A high ratio of dietary animal to vegetable protein increases the rate of bone loss and the risk of fracture in postmenopausal women. Am J Clin Nutr 73:118–122
Heaney RP (2001) Protein intake and bone health: the influence of belief systems on the conduct of nutritional science (editorial). Am J Clin Nutr 73:3–4
Sebastian A, Sellmeyer DE, Stone KL, Cummings SR (2001) Dietary ratio of animal to vegetable protein and rate of bone loss and risk of fracture in postmenopausal women (letter). Am J Clin Nutr 74:411–412
Heaney RP (1998) Excess dietary protein may not adversely affect bone. J Nutr 128:1054–1057
Meyer HE, Pedersen JI, Loken EB, Tverdal A (1997) Dietary factors and the incidence of hip fracture in middle-aged Norwegians. Am J Epidemiol 145:117–123
Dawson-Hughes B, Harris SS (2002) Calcium intake influences the association of protein intake with rates of bone loss in elderly men and women. Am J Clin Nutr 75:773–779
Heaney RP (2002) Protein and calcium: antagonists or synergists? Am J Clin Nutr 75:609–610
New SA, Millward DJ (2003) Calcium, protein and fruit and vegetables as dietary determinants of bone health. Am J Clin Nutr 77:1340–1341 [Letter]
Dawson-Hughes B (2003) Calcium, protein and bone health. Am J Clin Nutr 77:1341 [Letter]
Frassetto L, Todd K, Morris RC Jr, Sebastian A (1998) Estimation of net endogenous noncarbonic acid production in humans from dietary protein and potassium contents. Am J Clin Nutr 68:576–583
New SA, Bolton-Smith C, Grubb DA, Reid DM (1997) Nutritional influences on bone mineral density: a cross-sectional study in premenopausal women. Am J Clin Nutr 65:1831–1839
New SA, Robins SP, Campbell MK, Martin JC, Garton MJ, Bolton-Smith C, Grubb DA, Lee SJ, Reid DM (2000) Dietary influences on bone mass and bone metabolism: further evidence of a positive link between fruit and vegetable consumption and bone health? Am J Clin Nutr 71:142–151
New SA, Macdonald HM, Campbell MK, Martin JM, Garton MJ, Reid DM (2004) Positive association between net endogenous non-carbonic acid production (NEAP) and indexes of bone health in peri and postmenopausal women. Am J Clin Nutr 79:131–138
Macdonald HM, New SA, Fraser WD, Reid DM (2002) Estimates of NEAP are associated with increased bone turnover in early postmenopausal women: findings from APOSS longitudinal. J Bone Miner Res 17:1131
Eaton-Evans J, McIlrath EM, Jackson WE, Bradley P, Strain JJ (1993) Dietary factors and vertebral bone density in perimenopausal women from a general medical practice in Northern Ireland. Proc Nutr Soc 52:44A [Abstract]
Michaelsson K, Holmberg L, Maumin H, Wolk A, Bergstrom R, Ljunghall S (1995) Diet, bone mass and osteocalcin; a cross-sectional study. Calcif Tissue Int 57:86–93
Tucker KL, Hannan MT, Chen H, Cupples A, Wilson PWF, Kiel DP (1999) Potassium and fruit and vegetables are associated with greater bone mineral density in elderly men and women. Am J Clin Nutr 69:727–736
Jones G, Riley MD, Whiting S (2001) Association between urinary potassium, urinary sodium, current diet, and bone density in prepubertal children. Am J Clin Nutr 73:839–844
Chen Y, Ho SC, Lee R, Lam S, Woo J (2001) Fruit intake is associated with better bone mass among Hong Kong Chinese early postmenopausal women. J Bone Miner Res 16:S386
Miller DR, Krall EA, Anderson JJ, Rich SE, Rourke A, Chan J (2001) Dietary mineral intake and low bone mass in men: the VALOR study. J Bone Miner Res 16(S1):S395
Stone KL, Blackwell T, Orwoll ES, Cauley JC, Barrett-Connor E, Marcus R, Nevitt MC, Cummings SR (2001) The relationship between diet and bone mineral density in older men. J Bone Miner Res 16:S388
New SA, Smith R, Brown JC, Reid DM (2002) Positive associations between fruit and vegetable consumption and bone mineral density in late postmenopausal and elderly women. Osteoporos Int 13:S77
Macdonald HM, New SA, Fraser WD, Black AJ, Grubb DA, Reid DM (2002) Increased fruit and vegetable intake reduces bone turnover in early postmenopausal Scottish women. Osteoporos Int 13:S97
Macdonald HM, New SA, Golden MHN, Campbell MK, Reid DM (2004) Nutritional influences on bone loss during the menopausal transition: evidence for a beneficial effect of calcium, alcohol, and fruit and vegetable nutrients. Am J Clin Nutr 79:155–165
Appel LJ, Moore TJ, Obarzanek E, Vallmer WM, Svetkey LP, Sacks, FM, Bray GA, Vogt TM, Cutler JA (1997) A clinical trial of the effects of dietary patterns on blood pressure. N Engl J Med 336:1117–1124
Sacks FM, Svetley LP, Vollmer WM et al. (2001) Effects on blood pressure of reduced dietary sodium and the Dietary Approaches to Stop Hypertension (DASH) diet. N Engl J Med 344:3–10
Barzel US (1997) Dietary patterns and blood pressure. N Engl J Med 337:637 [Letter]
Lin P, Ginty F, Appel L, Aickin M, Bohannon A, Garnero P, Barclay D, Svetky L (2001) The DASH diet and sodium reduction improve markers of bone turnover and calcium metabolism in adults. J Nutr 133:3130–3136
Lemann J Jr, Pleuss JA, Gray RW, Hoffmann RG (1991) Potassium administration increases and potassium deprivation reduces urinary calcium excretion in healthy adults. Kidney Int 39:973–983
Bushinsky DA (1997) Decreased potassium stimulates bone resorption. Am J Physiol 272:F774–780
Sebastian A, Harris ST, Ottaway JH, Todd KM, Morris RC Jr (1994) Improved mineral balance and skeletal metabolism in postmenopausal women treated with potassium bicarbonate. N Engl J Med 330:1776–1781
Sellmeyer DE, Schloetter M, Sebastian A (2002) Potassium citrate prevents increased urine calcium excretion and bone resorption induced by a high sodium chloride diet. J Clin Endocrinol Metab 87:2008–2012
Buclin T, Cosma M, Appenzeller M, Jacquet AF, Decosterd LA, Biollaz J, Burckhardt P (2001) Diet acids and alkalis influence calcium retention in bone. Osteoporos Int 12:493–499
New SA (2002) The role of the skeleton in acid-base homeostasis. The 2001 Nutrition Society Medal Lecture. Proc Nutr Soc 61:151–164
Muhlbauer RC, Lozano AM, Reinli A (2002) Onion and a mixture of vegetables, salads and herbs affect bone resorption in the rat by a mechanism independent of their base excess. J Bone Miner Res 17:1230–1236
Muhlbauer RC, Felix R, Lozano A, Palacio S, Reinli A (2003) Common herbs, essential oils and monoterpenes potently modulate bone metabolism. Bone 32:372–380
Oh MS, Uribarri J (1996) Bone buffering of acid: fact or fancy? J Nephrol 9:261–262
Acknowledgements
The author would like to acknowledge formally and in turn express her sincere thanks to the thoroughness of the Osteoporosis International review process.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
New, S.A. Do vegetarians have a normal bone mass?. Osteoporos Int 15, 679–688 (2004). https://doi.org/10.1007/s00198-004-1647-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00198-004-1647-9