Dietary patterns and longitudinal change in hip bone mineral density among older men

  • T. S. Rogers
  • S. Harrison
  • S. Judd
  • E. S. Orwoll
  • L. M. Marshall
  • J. Shannon
  • L. Langsetmo
  • N. E. Lane
  • J. M. Shikany
  • for the Osteoporotic Fractures in Men (MrOS) Study Research Group
Original Article

Abstract

Summary

Studying dietary patterns is often more informative than individual nutrients or foods. We found that a Prudent dietary pattern (rich in vegetables and fish) was associated with reduced loss of total hip BMD in older men. A Prudent dietary pattern may be a potential lifestyle strategy for minimizing bone loss.

Introduction

This study aimed to identify baseline dietary patterns using factor analysis in a cohort of older men and to evaluate whether the dietary patterns were associated with bone mineral density change (%ΔBMD) at the total hip and femoral neck over time.

Methods

Participants (n = 4379; mean age 72.9 ± 5.5 years) were from the Osteoporotic Fractures in Men (MrOS) prospective cohort study and had dietary data collected at baseline (March 2000–April 2002) and BMD measured at baseline and Visit 2 (March 2005–May 2006). Dietary intake was assessed with a brief Block food frequency questionnaire (FFQ); factor analysis was used to derive dietary patterns. BMD was measured by dual-energy x-ray absorptiometry (DXA); %ΔBMD was calculated from baseline to Visit 2. We used generalized linear regression to estimate least square (LS) means of %ΔBMD in quartiles of the dietary pattern scores adjusted for potential confounding factors.

Results

Two major dietary patterns were derived: Prudent (abundant in vegetables, salad, and non-fried fish) and Western (rich in hamburger, fries, processed meats, cheese, and sweets/desserts). There was an inverse association between adherence to the Prudent pattern and total hip %ΔBMD (p-trend = 0.028 after adjusting for age and clinical site; p-trend = 0.033 after further adjustment for smoking, calcium supplement use, diabetes, hypertension, and total energy intake). No other consistent associations between dietary patterns and %ΔBMD were observed.

Conclusions

Greater adherence to a Prudent dietary pattern may attenuate total hip BMD loss (%ΔBMD) in older men.

Keywords

BMD change Dietary pattern Factor analysis Older men Prudent Western 

Notes

Compliance with ethical standards

Conflicts of interest

None.

Ethical approval

All procedures performed in the MrOS study were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The study was approved by the Institutional Review Board at each clinic site, and all participants provided written informed consent. For this type of retrospective analysis, additional formal consent was not required.

Supplementary material

198_2018_4388_MOESM1_ESM.pdf (49 kb)
Online resource 1 (PDF 48 kb).
198_2018_4388_MOESM2_ESM.pdf (69 kb)
Online resource 2 (PDF 68 kb).
198_2018_4388_MOESM3_ESM.pdf (42 kb)
Online resource 3 (PDF 42 kb).

References

  1. 1.
    Lappe JM, Heaney RP (2012) Why randomized controlled trials of calcium and vitamin D sometimes fail. Dermatoendocrinol 4(2):95–100.  https://doi.org/10.4161/derm.19833 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Tucker KL, Chen H, Hannan MT, Cupples LA, Wilson PW, Felson D, Kiel DP (2002) Bone mineral density and dietary patterns in older adults: the Framingham Osteoporosis Study. Am J Clin Nutr 76(1):245–252CrossRefPubMedGoogle Scholar
  3. 3.
    Edwards MH, Jameson K, Denison H, Harvey NC, Sayer AA, Dennison EM, Cooper C (2013) Clinical risk factors, bone density and fall history in the prediction of incident fracture among men and women. Bone 52(2):541–547.  https://doi.org/10.1016/j.bone.2012.11.006 CrossRefPubMedGoogle Scholar
  4. 4.
    Hardcastle AC, Aucott L, Fraser WD, Reid DM, Macdonald HM (2011) Dietary patterns, bone resorption and bone mineral density in early post-menopausal Scottish women. Eur J Clin Nutr 65(3):378–385.  https://doi.org/10.1038/ejcn.2010.264 CrossRefPubMedGoogle Scholar
  5. 5.
    Ward KA, Prentice A, Kuh DL, Adams JE, Ambrosini GL (2016) Life course dietary patterns and bone health in later life in a British birth cohort study. J Bone Miner Res 31(6):1167–1176.  https://doi.org/10.1002/jbmr.2798 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Movassagh EZ, Vatanparast H (2017) Current evidence on the association of dietary patterns and bone health: a scoping review. Adv Nutr 8(1):1–16.  https://doi.org/10.3945/an.116.013326 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Langsetmo L, Barr SI, Dasgupta K, Berger C, Kovacs CS, Josse RG, Adachi JD, Hanley DA, Prior JC, Brown JP, Morin SN, Davison KS, Goltzman D, Kreiger N (2016) Dietary patterns in men and women are simultaneously determinants of altered glucose metabolism and bone metabolism. Nutr Res 36(4):328–336.  https://doi.org/10.1016/j.nutres.2015.12.010 CrossRefPubMedGoogle Scholar
  8. 8.
    Isanejad M, Sirola J, Mursu J, Rikkonen T, Kroger H, Tuppurainen M, Erkkila AT (2017) Association of the Baltic Sea and Mediterranean diets with indices of sarcopenia in elderly women, OSPTRE-FPS study. Eur J Nutr.  https://doi.org/10.1007/s00394-017-1422-2
  9. 9.
    Shin S, Sung J, Joung H (2015) A fruit, milk and whole grain dietary pattern is positively associated with bone mineral density in Korean healthy adults. Eur J Clin Nutr 69(4):442–448.  https://doi.org/10.1038/ejcn.2014.231 CrossRefPubMedGoogle Scholar
  10. 10.
    Judd SE, Letter AJ, Shikany JM, Roth DL, Newby PK (2014) Dietary patterns derived using exploratory and confirmatory factor analysis are stable and generalizable across race, region, and gender subgroups in the REGARDS Study. Front Nutrition 1:29.  https://doi.org/10.3389/fnut.2014.00029 Google Scholar
  11. 11.
    Langsetmo L, Hanley DA, Prior JC, Barr SI, Anastassiades T, Towheed T, Goltzman D, Morin S, Poliquin S, Kreiger N (2011) Dietary patterns and incident low-trauma fractures in postmenopausal women and men aged >/= 50 y: a population-based cohort study. Am J Clin Nutr 93(1):192–199.  https://doi.org/10.3945/ajcn.110.002956 CrossRefPubMedGoogle Scholar
  12. 12.
    Langsetmo L, Poliquin S, Hanley DA, Prior JC, Barr S, Anastassiades T, Towheed T, Goltzman D, Kreiger N (2010) Dietary patterns in Canadian men and women ages 25 and older: relationship to demographics, body mass index, and bone mineral density. BMC Musculoskelet Disord 11:20.  https://doi.org/10.1186/1471-2474-11-20 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Shikany JM, Safford MM, Newby PK, Durant RW, Brown TM, Judd SE (2015) Southern dietary pattern is associated with hazard of acute coronary heart disease in the Reasons for Geographic and Racial Differences in Stroke (REGARDS) Study. Circulation 132(9):804–814.  https://doi.org/10.1161/circulationaha.114.014421 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Fung TT, Feskanich D (2015) Dietary patterns and risk of hip fractures in postmenopausal women and men over 50 years. Osteoporos Int 26(6):1825–1830.  https://doi.org/10.1007/s00198-015-3081-6 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Orwoll E, Blank JB, Barrett-Connor E, Cauley J, Cummings S, Ensrud K, Lewis C, Cawthon PM, Marcus R, Marshall LM, McGowan J, Phipps K, Sherman S, Stefanick ML, Stone K (2005) Design and baseline characteristics of the osteoporotic fractures in men (MrOS) study—a large observational study of the determinants of fracture in older men. Contemp Clin Trials 26(5):569–585.  https://doi.org/10.1016/j.cct.2005.05.006 CrossRefPubMedGoogle Scholar
  16. 16.
    Shannon J, Shikany JM, Barrett-Connor E, Marshall LM, Bunker CH, Chan JM, Stone KL, Orwoll E (2007) Demographic factors associated with the diet quality of older US men: baseline data from the Osteoporotic Fractures in Men (MrOS) study. Public Health Nutr 10(8):810–818.  https://doi.org/10.1017/s1368980007258604 CrossRefPubMedGoogle Scholar
  17. 17.
    Shikany JM, Barrett-Connor E, Ensrud KE, Cawthon PM, Lewis CE, Dam TT, Shannon J, Redden DT (2014) Macronutrients, diet quality, and frailty in older men. J Gerontol A Biol Sci Med Sci 69(6):695–701.  https://doi.org/10.1093/gerona/glt196 CrossRefPubMedGoogle Scholar
  18. 18.
    Blank JB, Cawthon PM, Carrion-Petersen ML, Harper L, Johnson JP, Mitson E, Delay RR (2005) Overview of recruitment for the osteoporotic fractures in men study (MrOS). Contemp Clin Trials 26(5):557–568.  https://doi.org/10.1016/j.cct.2005.05.005 CrossRefPubMedGoogle Scholar
  19. 19.
    Block G, Hartman AM, Naughton D (1990) A reduced dietary questionnaire: development and validation. Epidemiology 1(1):58–64CrossRefPubMedGoogle Scholar
  20. 20.
    Langsetmo L, Shikany JM, Burghardt AJ, Cawthon PM, Orwoll ES, Cauley JA, Taylor BC, Schousboe JT, Bauer DC, Vo TN, Ensrud KE (2017) High dairy protein intake is associated with greater bone strength parameters at the distal radius and tibia in older men: a cross-sectional study. Osteoporos Int 29(1):69–77.  https://doi.org/10.1007/s00198-017-4261-3 CrossRefPubMedGoogle Scholar
  21. 21.
    Pahor M, Chrischilles EA, Guralnik JM, Brown SL, Wallace RB, Carbonin P (1994) Drug data coding and analysis in epidemiologic studies. Eur J Epidemiol 10(4):405–411CrossRefPubMedGoogle Scholar
  22. 22.
    Washburn RA, Smith KW, Jette AM, Janney CA (1993) The Physical Activity Scale for the Elderly (PASE): development and evaluation. J Clin Epidemiol 46(2):153–162CrossRefPubMedGoogle Scholar
  23. 23.
    Cawthon PM, Ewing SK, Mackey DC, Fink HA, Cummings SR, Ensrud KE, Stefanick ML, Bauer DC, Cauley JA, Orwoll ES (2012) Change in hip bone mineral density and risk of subsequent fractures in older men. J Bone Miner Res 27(10):2179–2188.  https://doi.org/10.1002/jbmr.1671 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Cummings SR, Bates D, Black DM (2002) Clinical use of bone densitometry: scientific review. JAMA 288(15):1889–1897CrossRefPubMedGoogle Scholar
  25. 25.
    Shepherd JA, Fan B, Lu Y, Lewiecki EM, Miller P, Genant HK (2006) Comparison of BMD precision for Prodigy and Delphi spine and femur scans. Osteoporos Int 17(9):1303–1308.  https://doi.org/10.1007/s00198-006-0127-9 CrossRefPubMedGoogle Scholar
  26. 26.
    Glymour MM, Weuve J, Berkman LF, Kawachi I, Robins JM (2005) When is baseline adjustment useful in analyses of change? An example with education and cognitive change. Am J Epidemiol 162(3):267–278.  https://doi.org/10.1093/aje/kwi187 CrossRefPubMedGoogle Scholar
  27. 27.
    Rizzoli R (2014) Dairy products, yogurts, and bone health. Am J Clin Nutr 99(5 Suppl):1256s–1262s.  https://doi.org/10.3945/ajcn.113.073056 CrossRefPubMedGoogle Scholar
  28. 28.
    Liu RH (2003) Health benefits of fruit and vegetables are from additive and synergistic combinations of phytochemicals. Am J Clin Nutr 78(3 Suppl):517s–520sCrossRefPubMedGoogle Scholar
  29. 29.
    Sahni S, Cupples LA, McLean RR, Tucker KL, Broe KE, Kiel DP, Hannan MT (2010) Protective effect of high protein and calcium intake on the risk of hip fracture in the Framingham offspring cohort. J Bone Miner Res 25(12):2770–2776.  https://doi.org/10.1002/jbmr.194 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Byberg L, Bellavia A, Orsini N, Wolk A, Michaelsson K (2015) Fruit and vegetable intake and risk of hip fracture: a cohort study of Swedish men and women. J Bone Miner Res 30(6):976–984.  https://doi.org/10.1002/jbmr.2384 CrossRefPubMedGoogle Scholar
  31. 31.
    Zeng FF, Wu BH, Fan F, Xie HL, Xue WQ, Zhu HL, Chen YM (2013) Dietary patterns and the risk of hip fractures in elderly Chinese: a matched case-control study. J Clin Endocrinol Metab 98(6):2347–2355.  https://doi.org/10.1210/jc.2013-1190 CrossRefPubMedGoogle Scholar
  32. 32.
    Lemann J Jr, Gray RW, Pleuss JA (1989) Potassium bicarbonate, but not sodium bicarbonate, reduces urinary calcium excretion and improves calcium balance in healthy men. Kidney Int 35(2):688–695CrossRefPubMedGoogle Scholar
  33. 33.
    Macdonald HM, New SA, Fraser WD, Campbell MK, Reid DM (2005) Low dietary potassium intakes and high dietary estimates of net endogenous acid production are associated with low bone mineral density in premenopausal women and increased markers of bone resorption in postmenopausal women. Am J Clin Nutr 81(4):923–933CrossRefPubMedGoogle Scholar
  34. 34.
    New SA, MacDonald HM, Campbell MK, Martin JC, Garton MJ, Robins SP, Reid DM (2004) Lower estimates of net endogenous non-carbonic acid production are positively associated with indexes of bone health in premenopausal and perimenopausal women. Am J Clin Nutr 79(1):131–138CrossRefPubMedGoogle Scholar
  35. 35.
    Bushinsky DA (1996) Metabolic alkalosis decreases bone calcium efflux by suppressing osteoclasts and stimulating osteoblasts. Am J Phys 271(1 Pt 2):F216–F222Google Scholar
  36. 36.
    Jeffery IB, O'Toole PW (2013) Diet-microbiota interactions and their implications for healthy living. Nutrients 5(1):234–252.  https://doi.org/10.3390/nu5010234 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Heaney RP, Weaver CM, Recker RR (1988) Calcium absorbability from spinach. Am J Clin Nutr 47(4):707–709CrossRefPubMedGoogle Scholar
  38. 38.
    Noonan SC, Savage GP (1999) Oxalate content of foods and its effect on humans. Asia Pac J Clin Nutr 8(1):64–74CrossRefPubMedGoogle Scholar
  39. 39.
    Kruger MC, Coetzee M, Haag M, Weiler H (2010) Long-chain polyunsaturated fatty acids: selected mechanisms of action on bone. Prog Lipid Res 49(4):438–449.  https://doi.org/10.1016/j.plipres.2010.06.002 CrossRefPubMedGoogle Scholar
  40. 40.
    Orchard TS, Cauley JA, Frank GC, Neuhouser ML, Robinson JG, Snetselaar L, Tylavsky F, Wactawski-Wende J, Young AM, Lu B, Jackson RD (2010) Fatty acid consumption and risk of fracture in the Women's Health Initiative. Am J Clin Nutr 92(6):1452–1460.  https://doi.org/10.3945/ajcn.2010.29955 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Farina EK, Kiel DP, Roubenoff R, Schaefer EJ, Cupples LA, Tucker KL (2011) Dietary intakes of arachidonic acid and alpha-linolenic acid are associated with reduced risk of hip fracture in older adults. J Nutr 141(6):1146–1153.  https://doi.org/10.3945/jn.110.133728 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Virtanen JK, Mozaffarian D, Cauley JA, Mukamal KJ, Robbins J, Siscovick DS (2010) Fish consumption, bone mineral density, and risk of hip fracture among older adults: the cardiovascular health study. J Bone Miner Res 25(9):1972–1979.  https://doi.org/10.1002/jbmr.87 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    McNaughton SA, Wattanapenpaiboon N, Wark JD, Nowson CA (2011) An energy-dense, nutrient-poor dietary pattern is inversely associated with bone health in women. J Nutr 141(8):1516–1523.  https://doi.org/10.3945/jn.111.138271 CrossRefPubMedGoogle Scholar
  44. 44.
    Monma Y, Niu K, Iwasaki K, Tomita N, Nakaya N, Hozawa A, Kuriyama S, Takayama S, Seki T, Takeda T, Yaegashi N, Ebihara S, Arai H, Nagatomi R, Tsuji I (2010) Dietary patterns associated with fall-related fracture in elderly Japanese: a population based prospective study. BMC Geriatr 10:31.  https://doi.org/10.1186/1471-2318-10-31 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Bailey RL, Gahche JJ, Miller PE, Thomas PR, Dwyer JT (2013) Why US adults use dietary supplements. JAMA Intern Med 173(5):355–361.  https://doi.org/10.1001/jamainternmed.2013.2299 CrossRefPubMedGoogle Scholar
  46. 46.
    Peacock M, Liu G, Carey M, McClintock R, Ambrosius W, Hui S, Johnston CC (2000) Effect of calcium or 25OH vitamin D3 dietary supplementation on bone loss at the hip in men and women over the age of 60. J Clin Endocrinol Metab 85(9):3011–3019.  https://doi.org/10.1210/jcem.85.9.6836 PubMedGoogle Scholar
  47. 47.
    Hannan MT, Felson DT, Dawson-Hughes B, Tucker KL, Cupples LA, Wilson PW, Kiel DP (2000) Risk factors for longitudinal bone loss in elderly men and women: the Framingham Osteoporosis Study. J Bone Miner Res 15(4):710–720.  https://doi.org/10.1359/jbmr.2000.15.4.710 CrossRefPubMedGoogle Scholar
  48. 48.
    Slemenda CW, Christian JC, Reed T, Reister TK, Williams CJ, Johnston CC Jr (1992) Long-term bone loss in men: effects of genetic and environmental factors. Ann Intern Med 117(4):286–291CrossRefPubMedGoogle Scholar
  49. 49.
    Burger H, de Laet CE, van Daele PL, Weel AE, Witteman JC, Hofman A, Pols HA (1998) Risk factors for increased bone loss in an elderly population: the Rotterdam Study. Am J Epidemiol 147(9):871–879CrossRefPubMedGoogle Scholar
  50. 50.
    Willcox BJ, He Q, Chen R, Yano K, Masaki KH, Grove JS, Donlon TA, Willcox DC, Curb JD (2006) Midlife risk factors and healthy survival in men. JAMA 296(19):2343–2350.  https://doi.org/10.1001/jama.296.19.2343 CrossRefPubMedGoogle Scholar
  51. 51.
    Farhat GN, Strotmeyer ES, Newman AB, Sutton-Tyrrell K, Bauer DC, Harris T, Johnson KC, Taaffe DR, Cauley JA (2006) Volumetric and areal bone mineral density measures are associated with cardiovascular disease in older men and women: the health, aging, and body composition study. Calcif Tissue Int 79(2):102–111.  https://doi.org/10.1007/s00223-006-0052-0 CrossRefPubMedGoogle Scholar
  52. 52.
    Antonopoulou M, Bahtiyar G, Banerji MA, Sacerdote AS (2013) Diabetes and bone health. Maturitas 76(3):253–259.  https://doi.org/10.1016/j.maturitas.2013.04.004 CrossRefPubMedGoogle Scholar
  53. 53.
    Newby PK, Muller D, Hallfrisch J, Andres R, Tucker KL (2004) Food patterns measured by factor analysis and anthropometric changes in adults. Am J Clin Nutr 80(2):504–513CrossRefPubMedGoogle Scholar
  54. 54.
    Hannan MT, Mangano KM, Sahni S (2015) Do nutrients influence bone health? A commentary on new findings in the field. J Bone Miner Res 30(6):967–969.  https://doi.org/10.1002/jbmr.2526 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2018

Authors and Affiliations

  • T. S. Rogers
    • 1
  • S. Harrison
    • 2
  • S. Judd
    • 3
  • E. S. Orwoll
    • 4
  • L. M. Marshall
    • 4
  • J. Shannon
    • 4
  • L. Langsetmo
    • 5
  • N. E. Lane
    • 1
  • J. M. Shikany
    • 3
  • for the Osteoporotic Fractures in Men (MrOS) Study Research Group
  1. 1.Center for Musculoskeletal Health and Department of Internal MedicineUniversity of California - Davis Medical CenterSacramentoUSA
  2. 2.California Pacific Medical Center Research InstituteSan FranciscoUSA
  3. 3.University of Alabama at BirminghamBirminghamUSA
  4. 4.Oregon Health and Science UniversityPortlandUSA
  5. 5.University of Minnesota Epidemiology and Community HealthMinneapolisUSA

Personalised recommendations