Advertisement

Total and lean fish intake is positively associated with bone mineral density in older women in the community-based Hordaland Health Study

  • Hanne Rosendahl-Riise
  • Therese Karlsson
  • Christian A. Drevon
  • Ellen M. Apalset
  • Ottar K. Nygård
  • Grethe S. Tell
  • Jutta Dierkes
Original Contribution

Abstract

Purpose

Fish is a source of various nutrients beneficial for bone health, but few studies have investigated the association between bone mineral density (BMD) and fish consumption. Thus, the aim was to investigate the relationship between total fish intake and BMD and between both lean and fatty fish intake and BMD.

Method

These cross-sectional analyses include 4656 participants in the Hordaland Health Study, a community-based study conducted in 1997–1999. The study includes two birth cohorts of men and women from Hordaland county (Norway) born in 1950–1951 and 1925–1927. BMD was measured by dual-energy X-ray absorptiometry and dietary intake was obtained from a semi-quantitative food-frequency questionnaire.

Results

The average total fish intake was 33 ± 18 g/1000 kcal and was primarily lean fish. Older women had significantly lower BMD than older men and middle-aged men and women. In older women, total and lean fish intake (50 g/1000 kcal) was significantly and positively associated with BMD also after multivariate adjustments (β-coefficient 0.018, p = 0.017 and 0.026, p = 0.021).

Conclusion

A high intake of fish, in particular lean fish, was positively associated with BMD in older women. No association between intake of fatty fish and BMD was found in either of the age and sex groups.

Keywords

Diet Food-frequency questionnaire Fatty fish Lean fish Bone mineral density Osteoporosis 

Abbreviations

BMD

Bone mineral density

DHA

Docosahexaenoic acid

DPA

Docosapentaenoic acid

DXA

Dual-energy X-ray absorptiometry

EPA

Eicosapentaenoic acid

FFQ

Food-frequency questionnaire

HUSK

Hordaland Health Study

NNR 2012

Nordic Nutritional Recommendation 2012

n3 PUFA

Omega-3 polyunsaturated fatty acids

Notes

Acknowledgements

The Norwegian Seafood Research Fund (FHF) supported this work through fellowship funding the primary author. The funder had no role in the study design, analysis or interpretation of data, or in the writing of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

HUSK was performed according to the declaration of Helsinki and all participants provided written informed consent. The study protocol was approved by the Data Inspectorate and the Regional Committee for Medical Research Ethics.

References

  1. 1.
    WHO Study Group (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. WHO Technical Report SeriesGoogle Scholar
  2. 2.
    Kanis JA, Melton LJ 3rd, Christiansen C, Johnston CC, Khaltaev N (1994) The diagnosis of osteoporosis. J Bone Miner Res 9(8):1137–1141.  https://doi.org/10.1002/jbmr.5650090802 CrossRefGoogle Scholar
  3. 3.
    Berger C, Goltzman D, Langsetmo L, Joseph L, Jackson S, Kreiger N, Tenenhouse A, Davison KS, Josse RG, Prior JC, Hanley DA (2010) Peak bone mass from longitudinal data: implications for the prevalence, pathophysiology, and diagnosis of osteoporosis. J Bone Miner Res 25(9):1948–1957.  https://doi.org/10.1002/jbmr.95 CrossRefGoogle Scholar
  4. 4.
    Khosla S, Melton LJ, Riggs BL (2011) The unitary model for estrogen deficiency and the pathogenesis of osteoporosis: is a revision needed? J Bone Miner Res 26(3):441–451.  https://doi.org/10.1002/jbmr.262 CrossRefGoogle Scholar
  5. 5.
    Alswat KA (2017) Gender disparities in osteoporosis. J Clin Med Res 9(5):382–387.  https://doi.org/10.14740/jocmr2970w CrossRefGoogle Scholar
  6. 6.
    Weaver CM, Gordon CM, Janz KF, Kalkwarf HJ, Lappe JM, Lewis R, O’Karma M, Wallace TC, Zemel BS (2016) The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int.  https://doi.org/10.1007/s00198-015-3440-3 Google Scholar
  7. 7.
    Seeman E, Hopper JL, Bach LA, Cooper ME, Parkinson E, McKay J, Jerums G (1989) Reduced bone mass in daughters of women with osteoporosis. N Engl J Med 320(9):554–558.  https://doi.org/10.1056/nejm198903023200903 CrossRefGoogle Scholar
  8. 8.
    Soroko SB, Barrett-Connor E, Edelstein SL, Kritz-Silverstein D (1994) Family history of osteoporosis and bone mineral density at the axial skeleton: the Rancho Bernardo Study. J Bone Miner Res 9(6):761–769.  https://doi.org/10.1002/jbmr.5650090602 CrossRefGoogle Scholar
  9. 9.
    Weaver CM, McCabe LD, McCabe GP, Novotny R, Van Loan M, Going S, Matkovic V, Boushey C, Savaiano DA (2007) Bone mineral and predictors of bone mass in white, Hispanic, and Asian early pubertal girls. Calcif Tissue Int 81(5):352–363.  https://doi.org/10.1007/s00223-007-9074-5 CrossRefGoogle Scholar
  10. 10.
    Bhudhikanok GS, Wang MC, Eckert K, Matkin C, Marcus R, Bachrach LK (1996) Differences in bone mineral in young Asian and Caucasian Americans may reflect differences in bone size. J Bone Miner Res 11(10):1545–1556.  https://doi.org/10.1002/jbmr.5650111023 CrossRefGoogle Scholar
  11. 11.
    Estrada K, Styrkarsdottir U, Evangelou E, Hsu YH, Duncan EL, Ntzani EE, Oei L, Albagha OM, Amin N, Kemp JP, Koller DL, Li G, Liu CT, Minster RL, Moayyeri A, Vandenput L, Willner D, Xiao SM, Yerges-Armstrong LM, Zheng HF, Alonso N, Eriksson J, Kammerer CM, Kaptoge SK, Leo PJ, Thorleifsson G, Wilson SG, Wilson JF, Aalto V, Alen M, Aragaki AK, Aspelund T, Center JR, Dailiana Z, Duggan DJ, Garcia M, Garcia-Giralt N, Giroux S, Hallmans G, Hocking LJ, Husted LB, Jameson KA, Khusainova R, Kim GS, Kooperberg C, Koromila T, Kruk M, Laaksonen M, Lacroix AZ, Lee SH, Leung PC, Lewis JR, Masi L, Mencej-Bedrac S, Nguyen TV, Nogues X, Patel MS, Prezelj J, Rose LM, Scollen S, Siggeirsdottir K, Smith AV, Svensson O, Trompet S, Trummer O, van Schoor NM, Woo J, Zhu K, Balcells S, Brandi ML, Buckley BM, Cheng S, Christiansen C, Cooper C, Dedoussis G, Ford I, Frost M, Goltzman D, Gonzalez-Macias J, Kahonen M, Karlsson M, Khusnutdinova E, Koh JM, Kollia P, Langdahl BL, Leslie WD, Lips P, Ljunggren O, Lorenc RS, Marc J, Mellstrom D, Obermayer-Pietsch B, Olmos JM, Pettersson-Kymmer U, Reid DM, Riancho JA, Ridker PM, Rousseau F, Slagboom PE, Tang NL, Urreizti R, Van Hul W, Viikari J, Zarrabeitia MT, Aulchenko YS, Castano-Betancourt M, Grundberg E, Herrera L, Ingvarsson T, Johannsdottir H, Kwan T, Li R, Luben R, Medina-Gomez C, Palsson ST, Reppe S, Rotter JI, Sigurdsson G, van Meurs JB, Verlaan D, Williams FM, Wood AR, Zhou Y, Gautvik KM, Pastinen T, Raychaudhuri S, Cauley JA, Chasman DI, Clark GR, Cummings SR, Danoy P, Dennison EM, Eastell R, Eisman JA, Gudnason V, Hofman A, Jackson RD, Jones G, Jukema JW, Khaw KT, Lehtimaki T, Liu Y, Lorentzon M, McCloskey E, Mitchell BD, Nandakumar K, Nicholson GC, Oostra BA, Peacock M, Pols HA, Prince RL, Raitakari O, Reid IR, Robbins J, Sambrook PN, Sham PC, Shuldiner AR, Tylavsky FA, van Duijn CM, Wareham NJ, Cupples LA, Econs MJ, Evans DM, Harris TB, Kung AW, Psaty BM, Reeve J, Spector TD, Streeten EA, Zillikens MC, Thorsteinsdottir U, Ohlsson C, Karasik D, Richards JB, Brown MA, Stefansson K, Uitterlinden AG, Ralston SH, Ioannidis JP, Kiel DP, Rivadeneira F (2012) Genome-wide meta-analysis identifies 56 bone mineral density loci and reveals 14 loci associated with risk of fracture. Nat Genet 44(5):491–501.  https://doi.org/10.1038/ng.2249 CrossRefGoogle Scholar
  12. 12.
    Tang BM, Eslick GD, Nowson C, Smith C, Bensoussan A (2007) Use of calcium or calcium in combination with vitamin D supplementation to prevent fractures and bone loss in people aged 50 years and older: a meta-analysis. Lancet 370(9588):657–666.  https://doi.org/10.1016/s0140-6736(07)61342-7 CrossRefGoogle Scholar
  13. 13.
    Holvik K, Ahmed LA, Forsmo S, Gjesdal CG, Grimnes G, Samuelsen SO, Schei B, Blomhoff R, Tell GS, Meyer HE (2013) Low serum levels of 25-hydroxyvitamin D predict hip fracture in the elderly: a NOREPOS study. J Clin Endocrinol Metab 98(8):3341–3350.  https://doi.org/10.1210/jc.2013-1468 CrossRefGoogle Scholar
  14. 14.
    Booth SL, Tucker KL, Chen H, Hannan MT, Gagnon DR, Cupples LA, Wilson PW, Ordovas J, Schaefer EJ, Dawson-Hughes B, Kiel DP (2000) Dietary vitamin K intakes are associated with hip fracture but not with bone mineral density in elderly men and women. Am J Clin Nutr 71(5):1201–1208CrossRefGoogle Scholar
  15. 15.
    Finnes TE, Lofthus CM, Meyer HE, Sogaard AJ, Tell GS, Apalset EM, Gjesdal C, Grimnes G, Schei B, Blomhoff R, Samuelsen SO, Holvik K (2015) A combination of low serum concentrations of vitamins K and D is associated with increased risk of hip fractures in elderly Norwegians: a NOREPOS study. Osteoporos Int.  https://doi.org/10.1007/s00198-015-3435-0 Google Scholar
  16. 16.
    Maggio M, Artoni A, Lauretani F, Borghi L, Nouvenne A, Valenti G, Ceda GP (2009) The impact of omega-3 fatty acids on osteoporosis. Curr Pharm Des 15(36):4157–4164CrossRefGoogle Scholar
  17. 17.
    Orchard TS, Pan X, Cheek F, Ing SW, Jackson RD (2012) A systematic review of omega-3 fatty acids and osteoporosis. Br J Nutr 107(Suppl 2):S253–S260.  https://doi.org/10.1017/s0007114512001638 CrossRefGoogle Scholar
  18. 18.
    Darling AL, Millward DJ, Torgerson DJ, Hewitt CE, Lanham-New SA (2009) Dietary protein and bone health: a systematic review and meta-analysis. Am J Clin Nutr 90(6):1674–1692.  https://doi.org/10.3945/ajcn.2009.27799 CrossRefGoogle Scholar
  19. 19.
    Shams-White MM, Chung M, Du M, Fu Z, Insogna KL, Karlsen MC, LeBoff MS, Shapses SA, Sackey J, Wallace TC, Weaver CM (2017) Dietary protein and bone health: a systematic review and meta-analysis from the National Osteoporosis Foundation. Am J Clin Nutr.  https://doi.org/10.3945/ajcn.116.145110 Google Scholar
  20. 20.
    Farina EK, Kiel DP, Roubenoff R, Schaefer EJ, Cupples LA, Tucker KL (2011) Protective effects of fish intake and interactive effects of long-chain polyunsaturated fatty acid intakes on hip bone mineral density in older adults: the Framingham Osteoporosis Study. Am J Clin Nutr 93(5):1142–1151.  https://doi.org/10.3945/ajcn.110.005926 CrossRefGoogle Scholar
  21. 21.
    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 CrossRefGoogle Scholar
  22. 22.
    Chen YM, Ho SC, Lam SS (2010) Higher sea fish intake is associated with greater bone mass and lower osteoporosis risk in postmenopausal Chinese women. Osteoporos Int 21(6):939–946.  https://doi.org/10.1007/s00198-009-1029-4 CrossRefGoogle Scholar
  23. 23.
    Zalloua PA, Hsu YH, Terwedow H, Zang T, Wu D, Tang G, Li Z, Hong X, Azar ST, Wang B, Bouxsein ML, Brain J, Cummings SR, Rosen CJ, Xu X (2007) Impact of seafood and fruit consumption on bone mineral density. Maturitas 56(1):1–11.  https://doi.org/10.1016/j.maturitas.2006.05.001 CrossRefGoogle Scholar
  24. 24.
    Calderon-Garcia JF, Moran JM, Roncero-Martin R, Rey-Sanchez P, Rodriguez-Velasco FJ, Pedrera-Zamorano JD (2012) Dietary habits, nutrients and bone mass in Spanish premenopausal women: the contribution of fish to better bone health. Nutrients 5(1):10–22.  https://doi.org/10.3390/nu5010010 CrossRefGoogle Scholar
  25. 25.
    Totland TH, Melnæs BK, Lundberg-Hallén N, Helland-Kigen KM, Lund-Blix NA, Myhre JB, Johansen AMW, Løken EB, Andersen LF (2012) Norkost 3—a National Dietary Survey in among adults aged 18–70 years in Norway, 2010–2011Google Scholar
  26. 26.
    Johansson L, Solvoll K (1999) Norkost 1997—Landsomfattende kostholdsundersøkelse blant menn og kvinner i alderen 16–79 år. Statens råd for ernæring og fysisk aktivitetGoogle Scholar
  27. 27.
    Nes M, Frost Andersen L, Solvoll K, Sandstad B, Hustvedt BE, Lovo A, Drevon CA (1992) Accuracy of a quantitative food frequency questionnaire applied in elderly Norwegian women. Eur J Clin Nutr 46(11):809–821Google Scholar
  28. 28.
    Andersen LF, Solvoll K, Johansson LR, Salminen I, Aro A, Drevon CA (1999) Evaluation of a food frequency questionnaire with weighed records, fatty acids, and alpha-tocopherol in adipose tissue and serum. Am J Epidemiol 150(1):75–87CrossRefGoogle Scholar
  29. 29.
    Andersen LF, Solvoll K, Drevon CA (1996) Very-long-chain n-3 fatty acids as biomarkers for intake of fish and n-3 fatty acid concentrates. Am J Clin Nutr 64(3):305–311CrossRefGoogle Scholar
  30. 30.
    Nurk E, Drevon CA, Refsum H, Solvoll K, Vollset SE, Nygard O, Nygaard HA, Engedal K, Tell GS, Smith AD (2007) Cognitive performance among the elderly and dietary fish intake: the Hordaland Health Study. Am J Clin Nutr 86(5):1470–1478CrossRefGoogle Scholar
  31. 31.
    Willett WC, Howe GR, Kushi LH (1997) Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr 65 (4 Suppl):1220S–1228S (discussion 1229S–1231S)CrossRefGoogle Scholar
  32. 32.
    Nordic Council of Ministers 2014 (2012) Nordic Nutritional Recommendations 2012—integrating nutrition and physical activity, 5th edn. Nordic Council of Ministers, CopenhagenGoogle Scholar
  33. 33.
    Gjesdal CG, Aanderud SJ, Haga HJ, Brun JG, Tell GS (2004) Femoral and whole-body bone mineral density in middle-aged and older Norwegian men and women: suitability of the reference values. Osteoporos Int 15(7):525–534.  https://doi.org/10.1007/s00198-003-1573-2 CrossRefGoogle Scholar
  34. 34.
    Gjesdal CG, Halse JI, Eide GE, Brun JG, Tell GS (2008) Impact of lean mass and fat mass on bone mineral density: the Hordaland Health Study. Maturitas 59(2):191–200.  https://doi.org/10.1016/j.maturitas.2007.11.002 CrossRefGoogle Scholar
  35. 35.
    Vinknes KJ, Elshorbagy AK, Nurk E, Drevon CA, Gjesdal CG, Tell GS, Nygard O, Vollset SE, Refsum H (2013) Plasma stearoyl-CoA desaturase indices: association with lifestyle, diet, and body composition. Obesity 21(3):E294–E302.  https://doi.org/10.1002/oby.20011 CrossRefGoogle Scholar
  36. 36.
    Benowitz NL, Jacob P III, Ahijevych K, Jarvis MJ, Hall S, LeHouezec J, Hansson A, Lichtenstein E, Henningfield J, Tsoh J, Hurt RD (2002) Biochemical verification of tobacco use and cessation. Nicotine Tob Res 4 (2):149–159.  https://doi.org/10.1080/14622200210123581 CrossRefGoogle Scholar
  37. 37.
    Oyen J, Gram Gjesdal C, Nygard OK, Lie SA, Meyer HE, Apalset EM, Ueland PM, Pedersen ER, Midttun O, Vollset SE, Tell GS (2014) Smoking and body fat mass in relation to bone mineral density and hip fracture: the Hordaland Health Study. PLoS ONE 9(3):e92882.  https://doi.org/10.1371/journal.pone.0092882 CrossRefGoogle Scholar
  38. 38.
    Choi E, Park Y (2016) The association between the consumption of fish/shellfish and the risk of osteoporosis in men and postmenopausal women aged 50 years or older. Nutrients 8(3):113.  https://doi.org/10.3390/nu8030113 CrossRefGoogle Scholar
  39. 39.
    Chan R, Woo J, Leung J (2011) Effects of food groups and dietary nutrients on bone loss in elderly Chinese population. J Nutr Health Aging 15(4):287–294CrossRefGoogle Scholar
  40. 40.
    Melaku YA, Gill TK, Adams R, Shi Z (2016) Association between dietary patterns and low bone mineral density among adults aged 50 years and above: findings from the North West Adelaide Health Study (NWAHS). Br J Nutr 116(8):1437–1446.  https://doi.org/10.1017/s0007114516003366 CrossRefGoogle Scholar
  41. 41.
    Okubo H, Sasaki S, Horiguchi H, Oguma E, Miyamoto K, Hosoi Y, Kim MK, Kayama F (2006) Dietary patterns associated with bone mineral density in premenopausal Japanese farmwomen. Am J Clin Nutr 83(5):1185–1192CrossRefGoogle Scholar
  42. 42.
    Erkkila AT, Sadeghi H, Isanejad M, Mursu J, Tuppurainen M, Kroger H (2017) Associations of Baltic Sea and Mediterranean dietary patterns with bone mineral density in elderly women. Public Health Nutr.  https://doi.org/10.1017/s1368980017001793 Google Scholar
  43. 43.
    Tang BMP, Eslick GD, Nowson C, Smith C, Bensoussan A (2007) Use of calcium or calcium in combination with vitamin D supplementation to prevent fractures and bone loss in people aged 50 years and older: a meta-analysis. Lancet 370(9588):657–666.  https://doi.org/10.1016/S0140-6736(07)61342-7 CrossRefGoogle Scholar
  44. 44.
    Heaney RP (2007) Effects of protein on the calcium economy. Int Congr Ser 1297:191–197.  https://doi.org/10.1016/j.ics.2006.08.025 CrossRefGoogle Scholar
  45. 45.
    Deutz NE, Bauer JM, Barazzoni R, Biolo G, Boirie Y, Bosy-Westphal A, Cederholm T, Cruz-Jentoft A, Krznaric Z, Nair KS, Singer P, Teta D, Tipton K, Calder PC (2014) Protein intake and exercise for optimal muscle function with aging: recommendations from the ESPEN Expert Group. Clin Nutr 33(6):929–936.  https://doi.org/10.1016/j.clnu.2014.04.007 CrossRefGoogle Scholar
  46. 46.
    Heaney RP (1998) Excess dietary protein may not adversely affect bone. J Nutr 128(6):1054–1057CrossRefGoogle Scholar
  47. 47.
    Allison RJ, Farooq A, Cherif A, Hamilton B, Close GL, Wilson MG (2017) Why don’t serum vitamin D concentrations associate with BMD by DXA? A case of being ‘bound’ to the wrong assay? Implications for vitamin D screening. Br J Sports Med.  https://doi.org/10.1136/bjsports-2016-097130 Google Scholar
  48. 48.
    Lu Z, Chen TC, Zhang A, Persons KS, Kohn N, Berkowitz R, Martinello S, Holick MF (2007) An evaluation of the vitamin D3 content in fish: is the vitamin D content adequate to satisfy the dietary requirement for vitamin D? J Steroid Biochem Mol Biol 103(3–5):642–644.  https://doi.org/10.1016/j.jsbmb.2006.12.010 CrossRefGoogle Scholar
  49. 49.
    Lehmann U, Gjessing HR, Hirche F, Mueller-Belecke A, Gudbrandsen OA, Ueland PM, Mellgren G, Lauritzen L, Lindqvist H, Hansen AL, Erkkila AT, Pot GK, Stangl GI, Dierkes J (2015) Efficacy of fish intake on vitamin D status: a meta-analysis of randomized controlled trials. Am J Clin Nutr 102(4):837–847.  https://doi.org/10.3945/ajcn.114.105395 CrossRefGoogle Scholar
  50. 50.
    Efsa Panel on Dietetic Products, Nutrition and Allergies (2012) Scientific opinion on the tolerable upper intake level of vitamin D. EFSA J.  https://doi.org/10.2903/j.efsa.2012.2813 Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Clinical Science, Faculty of MedicineUniversity of BergenBergenNorway
  2. 2.Department of Nutrition, Institute of Basic Medical Sciences, Faculty of MedicineUniversity of OsloOsloNorway
  3. 3.Department of RheumatologyHaukeland University HospitalBergenNorway
  4. 4.Department of Global Public Health and Primary CareUniversity of BergenBergenNorway
  5. 5.Department of Heart DiseaseHaukeland University HospitalBergenNorway
  6. 6.Department of Clinical Medicine, Faculty of MedicineUniversity of BergenBergenNorway

Personalised recommendations