Skip to main content
Top
Published in: BMC Medicine 1/2020

Open Access 01-12-2020 | Ankle Fracture | Research article

Vegetarian and vegan diets and risks of total and site-specific fractures: results from the prospective EPIC-Oxford study

Authors: Tammy Y. N. Tong, Paul N. Appleby, Miranda E. G. Armstrong, Georgina K. Fensom, Anika Knuppel, Keren Papier, Aurora Perez-Cornago, Ruth C. Travis, Timothy J. Key

Published in: BMC Medicine | Issue 1/2020

Login to get access

Abstract

Background

There is limited prospective evidence on possible differences in fracture risks between vegetarians, vegans, and non-vegetarians. We aimed to study this in a prospective cohort with a large proportion of non-meat eaters.

Methods

In EPIC-Oxford, dietary information was collected at baseline (1993–2001) and at follow-up (≈ 2010). Participants were categorised into four diet groups at both time points (with 29,380 meat eaters, 8037 fish eaters, 15,499 vegetarians, and 1982 vegans at baseline in analyses of total fractures). Outcomes were identified through linkage to hospital records or death certificates until mid-2016. Using multivariable Cox regression, we estimated the risks of total (n = 3941) and site-specific fractures (arm, n = 566; wrist, n = 889; hip, n = 945; leg, n = 366; ankle, n = 520; other main sites, i.e. clavicle, rib, and vertebra, n = 467) by diet group over an average of 17.6 years of follow-up.

Results

Compared with meat eaters and after adjustment for socio-economic factors, lifestyle confounders, and body mass index (BMI), the risks of hip fracture were higher in fish eaters (hazard ratio 1.26; 95% CI 1.02–1.54), vegetarians (1.25; 1.04–1.50), and vegans (2.31; 1.66–3.22), equivalent to rate differences of 2.9 (0.6–5.7), 2.9 (0.9–5.2), and 14.9 (7.9–24.5) more cases for every 1000 people over 10 years, respectively. The vegans also had higher risks of total (1.43; 1.20–1.70), leg (2.05; 1.23–3.41), and other main site fractures (1.59; 1.02–2.50) than meat eaters. Overall, the significant associations appeared to be stronger without adjustment for BMI and were slightly attenuated but remained significant with additional adjustment for dietary calcium and/or total protein. No significant differences were observed in risks of wrist or ankle fractures by diet group with or without BMI adjustment, nor for arm fractures after BMI adjustment.

Conclusions

Non-meat eaters, especially vegans, had higher risks of either total or some site-specific fractures, particularly hip fractures. This is the first prospective study of diet group with both total and multiple specific fracture sites in vegetarians and vegans, and the findings suggest that bone health in vegans requires further research.
Appendix
Available only for authorised users
Literature
1.
go back to reference Odén A, McCloskey EV, Kanis JA, Harvey NC, Johansson H. Burden of high fracture probability worldwide: secular increases 2010–2040. Osteoporos Int. 2015;26:2243–8. Odén A, McCloskey EV, Kanis JA, Harvey NC, Johansson H. Burden of high fracture probability worldwide: secular increases 2010–2040. Osteoporos Int. 2015;26:2243–8.
11.
go back to reference Yao P, Bennett D, Mafham M, Lin X, Chen Z, Armitage J, et al. Vitamin D and calcium for the prevention of fracture: a systematic review and meta-analysis. JAMA Netw Open. 2019;2:e1917789. Yao P, Bennett D, Mafham M, Lin X, Chen Z, Armitage J, et al. Vitamin D and calcium for the prevention of fracture: a systematic review and meta-analysis. JAMA Netw Open. 2019;2:e1917789.
15.
go back to reference Karavasiloglou N, Selinger E, Gojda J, Rohrmann S, Kühn T. Differences in bone mineral density between adult vegetarians and nonvegetarians become marginal when accounting for differences in anthropometric factors. J Nutr. 2020;:1–6. https://doi.org/10.1093/jn/nxaa018. Karavasiloglou N, Selinger E, Gojda J, Rohrmann S, Kühn T. Differences in bone mineral density between adult vegetarians and nonvegetarians become marginal when accounting for differences in anthropometric factors. J Nutr. 2020;:1–6. https://​doi.​org/​10.​1093/​jn/​nxaa018.
20.
go back to reference Bingham SA, Gill C, Welch A, Day K, Cassidy A, Khaw KT, et al. Comparison of dietary assessment methods in nutritional epidemiology: weighed records v. 24 h recalls, food-frequency questionnaires and estimated-diet records. Br J Nutr. 1994;72:619. https://doi.org/10.1079/BJN19940064. Bingham SA, Gill C, Welch A, Day K, Cassidy A, Khaw KT, et al. Comparison of dietary assessment methods in nutritional epidemiology: weighed records v. 24 h recalls, food-frequency questionnaires and estimated-diet records. Br J Nutr. 1994;72:619. https://​doi.​org/​10.​1079/​BJN19940064.
21.
go back to reference Bingham S, Cassidy A, Cole TJ, Welch A, Runswick S, Black a E, et al. Validation of weighed records and other methods of dietary assessment using the 24 h urine nitrogen technique and other biological markers. Br J Nutr. 1995;73:531–50. https://doi.org/10.1079/BJN19950057. Bingham S, Cassidy A, Cole TJ, Welch A, Runswick S, Black a E, et al. Validation of weighed records and other methods of dietary assessment using the 24 h urine nitrogen technique and other biological markers. Br J Nutr. 1995;73:531–50. https://​doi.​org/​10.​1079/​BJN19950057.
22.
go back to reference Bingham SA, Gill C, Welch A, Cassidy A, Runswick SA, Oakes S, et al. Validation of dietary assessment methods in the UK arm of EPIC using weighed records, and 24-hour urinary nitrogen and potassium and serum vitamin C and carotenoids as biomarkers. Int J Epidemiol. 1997;26(Suppl 1):S137–51. Bingham SA, Gill C, Welch A, Cassidy A, Runswick SA, Oakes S, et al. Validation of dietary assessment methods in the UK arm of EPIC using weighed records, and 24-hour urinary nitrogen and potassium and serum vitamin C and carotenoids as biomarkers. Int J Epidemiol. 1997;26(Suppl 1):S137–51.
23.
go back to reference Ministry of Agriculture Fisheries and Food. Food portion sizes. 2nd ed. London: Her Majesty’s Stationary Office; 1993. Ministry of Agriculture Fisheries and Food. Food portion sizes. 2nd ed. London: Her Majesty’s Stationary Office; 1993.
24.
go back to reference Holland B, Welch A, Unwin I, Buss D, Paul A, Southgate DAT. McCance and Widdowson’s the composition of foods. 5th ed. Cambridge: Royal Society of Chemistry; 1991. Holland B, Welch A, Unwin I, Buss D, Paul A, Southgate DAT. McCance and Widdowson’s the composition of foods. 5th ed. Cambridge: Royal Society of Chemistry; 1991.
25.
go back to reference Townsend P. Poverty in the United Kingdom: a survey of household resources and standards of living. London, UK; 1979. Townsend P. Poverty in the United Kingdom: a survey of household resources and standards of living. London, UK; 1979.
26.
go back to reference Wareham NJ, Jakes RW, Rennie KL, Schuit J, Mitchell J, Hennings S, et al. Validity and repeatability of a simple index derived from the short physical activity questionnaire used in the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Public Health Nutr. 2003;6:407–13. https://doi.org/10.1079/PHN2002439.CrossRef Wareham NJ, Jakes RW, Rennie KL, Schuit J, Mitchell J, Hennings S, et al. Validity and repeatability of a simple index derived from the short physical activity questionnaire used in the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Public Health Nutr. 2003;6:407–13. https://​doi.​org/​10.​1079/​PHN2002439.CrossRef
28.
go back to reference Tong TYN, Appleby PN, Bradbury KE, Perez-Cornago A, Travis RC, Clarke R, et al. Risks of ischaemic heart disease and stroke in meat eaters, fish eaters, and vegetarians over 18 years of follow-up: results from the prospective EPIC-Oxford study. BMJ. 2019;366:l4897. https://doi.org/10.1136/bmj.l4897.CrossRef Tong TYN, Appleby PN, Bradbury KE, Perez-Cornago A, Travis RC, Clarke R, et al. Risks of ischaemic heart disease and stroke in meat eaters, fish eaters, and vegetarians over 18 years of follow-up: results from the prospective EPIC-Oxford study. BMJ. 2019;366:l4897. https://​doi.​org/​10.​1136/​bmj.​l4897.CrossRef
32.
go back to reference Lousuebsakul-Matthews V, Thorpe DL, Knutsen R, Beeson WL, Fraser GE, Knutsen SF. Legumes and meat analogues consumption are associated with hip fracture risk independently of meat intake among Caucasian men and women: the Adventist Health Study-2. Public Health Nutr. 2013;17:2333–43. Lousuebsakul-Matthews V, Thorpe DL, Knutsen R, Beeson WL, Fraser GE, Knutsen SF. Legumes and meat analogues consumption are associated with hip fracture risk independently of meat intake among Caucasian men and women: the Adventist Health Study-2. Public Health Nutr. 2013;17:2333–43.
33.
go back to reference Thorpe DL, Knutsen SF, Lawrence Beeson W, Rajaram S, Fraser GE. Effects of meat consumption and vegetarian diet on risk of wrist fracture over 25 years in a cohort of peri- and postmenopausal women. Public Health Nutr. 2008;11:564–72. Thorpe DL, Knutsen SF, Lawrence Beeson W, Rajaram S, Fraser GE. Effects of meat consumption and vegetarian diet on risk of wrist fracture over 25 years in a cohort of peri- and postmenopausal women. Public Health Nutr. 2008;11:564–72.
34.
go back to reference De Laet C, Kanis JA, Odén A, Johanson H, Johnell O, Delmas P, et al. Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int. 2005;16:1330–8. De Laet C, Kanis JA, Odén A, Johanson H, Johnell O, Delmas P, et al. Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int. 2005;16:1330–8.
37.
go back to reference Appleby PN, Allen NE, Roddam AW, Key TJ. Physical activity and fracture risk: a prospective study of 1898 incident fractures among 34 696 British men and women. J Bone Miner Metab. 2008;26:191–8. Appleby PN, Allen NE, Roddam AW, Key TJ. Physical activity and fracture risk: a prospective study of 1898 incident fractures among 34 696 British men and women. J Bone Miner Metab. 2008;26:191–8.
41.
go back to reference Key TJ, Appleby PN, Spencer EA, Roddam AW, Neale RE, Allen NE. Calcium, diet and fracture risk: a prospective study of 1898 incident fractures among 34696 British women and men. Public Health Nutr. 2007;10:1314–20. Key TJ, Appleby PN, Spencer EA, Roddam AW, Neale RE, Allen NE. Calcium, diet and fracture risk: a prospective study of 1898 incident fractures among 34696 British women and men. Public Health Nutr. 2007;10:1314–20.
44.
go back to reference Bonjour J-P. The dietary protein, IGF-I, skeletal health axis. Horm Mol Biol Clin Investig. 2016;28:39–53. Bonjour J-P. The dietary protein, IGF-I, skeletal health axis. Horm Mol Biol Clin Investig. 2016;28:39–53.
45.
go back to reference Locatelli V, Bianchi VE. Effect of GH/IGF-1 on bone metabolism and osteoporsosis. Int J Endocrinol. 2014;2014:1–25. Locatelli V, Bianchi VE. Effect of GH/IGF-1 on bone metabolism and osteoporsosis. Int J Endocrinol. 2014;2014:1–25.
46.
go back to reference Ohlsson C, Mellström D, Carlzon D, Orwoll E, Ljunggren Ö, Karlsson MK, et al. Older men with low serum IGF-1 have an increased risk of incident fractures: the MrOS Sweden study. J Bone Miner Res. 2011;26:865–72. Ohlsson C, Mellström D, Carlzon D, Orwoll E, Ljunggren Ö, Karlsson MK, et al. Older men with low serum IGF-1 have an increased risk of incident fractures: the MrOS Sweden study. J Bone Miner Res. 2011;26:865–72.
48.
go back to reference Fung TT, Meyer HE, Willett WC, Feskanich D. Protein intake and risk of hip fractures in postmenopausal women and men age 50 and older. Osteoporos Int. 2017;28:1401–11. Fung TT, Meyer HE, Willett WC, Feskanich D. Protein intake and risk of hip fractures in postmenopausal women and men age 50 and older. Osteoporos Int. 2017;28:1401–11.
50.
go back to reference Langsetmo L, Shikany JM, Cawthon PM, Cauley JA, Taylor BC, Vo TN, et al. The association between protein intake by source and osteoporotic fracture in older men: a prospective cohort study. J Bone Miner Res. 2017;32:592–600. Langsetmo L, Shikany JM, Cawthon PM, Cauley JA, Taylor BC, Vo TN, et al. The association between protein intake by source and osteoporotic fracture in older men: a prospective cohort study. J Bone Miner Res. 2017;32:592–600.
51.
go back to reference Darling AL, Manders RJF, Sahni S, Zhu K, Hewitt CE, Prince RL, et al. Dietary protein and bone health across the life-course: an updated systematic review and meta-analysis over 40 years. Osteoporos Int. 2019;30:741–61. Darling AL, Manders RJF, Sahni S, Zhu K, Hewitt CE, Prince RL, et al. Dietary protein and bone health across the life-course: an updated systematic review and meta-analysis over 40 years. Osteoporos Int. 2019;30:741–61.
52.
go back to reference Crowe FL, Steur M, Allen NE, Appleby PN, Travis RC, Key TJ. Plasma concentrations of 25-hydroxyvitamin D in meat eaters, fish eaters, vegetarians and vegans: results from the EPIC-Oxford study. Public Health Nutr. 2011;14:340–6. Crowe FL, Steur M, Allen NE, Appleby PN, Travis RC, Key TJ. Plasma concentrations of 25-hydroxyvitamin D in meat eaters, fish eaters, vegetarians and vegans: results from the EPIC-Oxford study. Public Health Nutr. 2011;14:340–6.
54.
go back to reference Gilsing AMJ, Crowe FL, Lloyd-Wright Z, Sanders TAB, Appleby PN, Allen NE, et al. Serum concentrations of vitamin B12 and folate in British male omnivores, vegetarians and vegans: results from a cross-sectional analysis of the EPIC-Oxford cohort study. Eur J Clin Nutr. 2010;64:933–9. https://doi.org/10.1038/ejcn.2010.142.CrossRef Gilsing AMJ, Crowe FL, Lloyd-Wright Z, Sanders TAB, Appleby PN, Allen NE, et al. Serum concentrations of vitamin B12 and folate in British male omnivores, vegetarians and vegans: results from a cross-sectional analysis of the EPIC-Oxford cohort study. Eur J Clin Nutr. 2010;64:933–9. https://​doi.​org/​10.​1038/​ejcn.​2010.​142.CrossRef
Metadata
Title
Vegetarian and vegan diets and risks of total and site-specific fractures: results from the prospective EPIC-Oxford study
Authors
Tammy Y. N. Tong
Paul N. Appleby
Miranda E. G. Armstrong
Georgina K. Fensom
Anika Knuppel
Keren Papier
Aurora Perez-Cornago
Ruth C. Travis
Timothy J. Key
Publication date
01-12-2020
Publisher
BioMed Central
Keyword
Ankle Fracture
Published in
BMC Medicine / Issue 1/2020
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/s12916-020-01815-3

Other articles of this Issue 1/2020

BMC Medicine 1/2020 Go to the issue