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Are milk and alternatives and fruit and vegetable intakes during adolescence associated with cortical and trabecular bone structure, density, and strength in adulthood?

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Abstract

Summary

We investigated the impact of food group intake during adolescence on bone structure and strength during adulthood. In females, we found a beneficial effect of adolescent milk and alternatives and fruit and vegetable intake on adult radius shaft and distal tibia bone structure, respectively. No association was observed in males.

Introduction

The purpose of this study was to investigate whether adolescents with high intake of milk and alternatives (M&A) or fruit and vegetables (F&V) had better adult bone structure and strength compared to those with low intake levels.

Methods

We analyzed data from 47 males and 69 females enrolled in the Pediatric Bone Mineral Accrual Study (PBMAS 1991–2011), who had one peripheral quantitative computed tomography scan at age 29 ± 2 years. We measured radius and tibia shaft total area (ToA), cortical area (CoA), cortical content (CoC), cortical density, bone strength (SSIp), and muscle area, as well as distal radius and tibia ToA, total density, trabecular area, trabecular content, trabecular density, and bone strength (BSIc). Sequential 24-h recalls were used to assess M&A and F&V intake; participants were grouped for their mean intake during adolescence (low = bottom quartile, moderate = middle quartiles, high = top quartile) and were compared using multivariate analysis of covariance while adjusting for adult height, muscle area, physical activity, energy and calcium intake and adolescent energy intake, and physical activity.

Results

Females with high M&A intake compared to low M&A intake group (mean 3.8 vs. 1.3 servings/day, respectively) had greater adult ToA (14 %, p < 0.05), CoA (15 %, p < 0.01), and CoC (16 %, p < 0.01) at radius shaft. Females with moderate F&V intake compared to low F&V intake group (mean 3.7 vs. 2.1 servings/day, respectively) had greater adult ToA (8.5 %, p < 0.05) at distal tibia.

Conclusion

Higher intake of M&A or F&V during adolescence had a long-term beneficial effect on bone structure in females, an association not observed in males.

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Abbreviations

ANOVA:

Analysis of variance

BSIc:

Bone strength index in compression

CoA:

Cortical area

CoC:

Cortical content

CoD:

Cortical density

DXA:

Dual-energy X-ray absorptiometry

F&V:

Fruit and vegetables

M&A:

Milk and alternatives

MANCOVA:

Multivariate analysis of covariance

PA:

Physical activity

PAQ:

Physical activity questionnaire

PBMAS:

Pediatric Bone Mineral Accrual Study

PHV:

Peak height velocity

pQCT:

Peripheral quantitative computed tomography

SE:

Standard errors

SSIp:

Bone strength in torsion

ToA:

Total area

ToD:

Total density

TrA:

Trabecular area

TrC:

Trabecular content

TrD:

Trabecular density

References

  1. Baxter-Jones AD, Mirwald RL, McKay HA, Bailey DA (2003) A longitudinal analysis of sex differences in bone mineral accrual in healthy 8-19-year-old boys and girls. Ann Hum Biol 30(2):160–175

    Article  CAS  PubMed  Google Scholar 

  2. Bailey DA, McKay HA, Mirwald RL, Crocker PR, Faulkner RA (1999) A six-year longitudinal study of the relationship of physical activity to bone mineral accrual in growing children: the university of Saskatchewan bone mineral accrual study. J Bone Miner Res 14(10):1672–1679

    Article  CAS  PubMed  Google Scholar 

  3. Baxter-Jones AD, Faulkner RA, Forwood MR, Mirwald RL, Bailey DA (2011) Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. JBMR 26(8):1729–1739

    Article  Google Scholar 

  4. Kontulainen SA, Macdonald HM, Khan KM, McKay HA (2005) Examining bone surfaces across puberty: a 20-month pQCT trial. J Bone Miner Res 20(7):1202–1207

    Article  PubMed  Google Scholar 

  5. Rauch F (2005) Bone growth in length and width: the Yin and Yang of bone stability. J Musculoskelet Neuronal Interact 5(3):194–201

    CAS  PubMed  Google Scholar 

  6. Bouxsein ML, Seeman E (2009) Quantifying the material and structural determinants of bone strength. Best Pract Res Clin Rheumatol 23(6):741–753

    Article  PubMed  Google Scholar 

  7. Kontulainen SA, Hughes JM, Macdonald HM, Johnson JD (2007) The biomechanical basis of bone strength development during growth. Med Sport Sci 51:13–32

    Article  PubMed  Google Scholar 

  8. Bala Y, Bui QM, Wang XF, Iuliano S, Wang Q, Ghasem-Zadeh A, Rozental TD, Bouxsein ML, Zebaze RM, Seeman E (2015) Trabecular and cortical microstructure and fragility of the distal radius in women. J Bone Miner Res 30(4):621–629

    Article  PubMed  Google Scholar 

  9. Bergstrom U, Bjornstig U, Stenlund H, Jonsson H, Svensson O (2008) Fracture mechanisms and fracture pattern in men and women aged 50 years and older: a study of a 12-year population based injury register, Umea, Sweden. Osteoporos Int 19(9):1267–1273

    Article  CAS  PubMed  Google Scholar 

  10. Mouratidou T, Vicente-Rodriguez G, Gracia-Marco L, Huybrechts I, Sioen I, Widhalm K, Valtuena J, Gonzalez-Gross M, Moreno LA, HELENA Study Group (2013) Associations of dietary calcium, vitamin D, milk intakes, and 25-hydroxyvitamin D with bone mass in Spanish adolescents: the HELENA study. J Clin Densitom 16(1):110–117

    Article  PubMed  Google Scholar 

  11. Esterle L, Sabatier JP, Guillon-Metz F, Walrant-Debray O, Guaydier-Souquières G, Jehan F, Garabédian M (2009) Milk, rather than other foods, is associated with vertebral bone mass and circulating IGF-1 in female adolescents. Osteoporos Int 20(4):567–575

    Article  CAS  PubMed  Google Scholar 

  12. Du XQ, Greenfield H, Fraser DR, Ge KY, Liu ZH, He W (2002) Milk consumption and bone mineral content in Chinese adolescent girls. Bone 30(3):521–528

    Article  CAS  PubMed  Google Scholar 

  13. Li JJ, Huang ZW, Wang RQ, Ma XM, Zhang ZQ, Liu Z, Chen YM, Su YX (2013) Fruit and vegetable intake and bone mass in Chinese adolescents, young and postmenopausal women. Public Health Nutr 16(1):78–86

    Article  CAS  PubMed  Google Scholar 

  14. Prynne CJ, Mishra GD, O’Connell MA, Muniz G, Laskey MA, Yan L, Prentice A, Ginty F (2006) Fruit and vegetable intakes and bone mineral status: a cross sectional study in 5 age and sex cohorts. Am J Clin Nutr 83(6):1420–1428

    CAS  PubMed  Google Scholar 

  15. Vatanparast H, Baxter-Jones AD, Faulkner RA, Bailey DA, Whiting SJ (2005) Positive effects of vegetable and fruit consumption and calcium intake on bone mineral accrual in boys during growth from childhood to adolescence: the University of Saskatchewan Pediatric Bone Mineral Accrual Study. Am J Clin Nutr 82(3):700–706

    CAS  PubMed  Google Scholar 

  16. McGartland CP, Robson PJ, Murray LJ, Cran GW, Savage MJ, Watkins DC, Rooney MM, Boreham CA (2004) Fruit and vegetable consumption and bone mineral density: the Northern Ireland Young Hearts Project. Am J Clin Nutr 80(4):1019–1023

    CAS  PubMed  Google Scholar 

  17. Tylavsky FA, Holliday K, Danish R, Womack C, Norwood J, Carbone L (2004) Fruit and vegetable intakes are an independent predictor of bone size in early pubertal children. Am J Clin Nutr 79(2):311–317

    CAS  PubMed  Google Scholar 

  18. Genant HK, Engelke K, Prevrhal S (2008). Advanced CT bone imaging in osteoporosis. Rheumatology (Oxford) 47 Suppl 4:iv9-16.

  19. Petit MA, Beck TJ, Kontulainen SA (2005) Examining the developing bone: what do we measure and how do we do it? J Musculoskelet Neuronal Interact 5(3):213–224

    CAS  PubMed  Google Scholar 

  20. Cheng S, Lyytikäinen A, Kröger H, Lamberg-Allardt C, Alen M, Koistinen A, Wang QJ, Suurinieni M, Suominen H, Mahonen A et al (2005) Effects of calcium, dairy product, and vitamin D supplementation on bone mass accrual and body composition in 10-12-y-old girls: a 2-y randomized trial. Am J Clin Nutr 82(5):1115–1126

    CAS  PubMed  Google Scholar 

  21. Bailey DA (1997) The Saskatchewan pediatric bone mineral accrual study: bone mineral acquisition during the growing years. Int J Sports Med 18(Suppl 3):S191–S194

    Article  PubMed  Google Scholar 

  22. Eating Well with Canada’s Food Guide. Ottawa, ON: Health Canada. 2007- [cited 2016 May 13, 2016] Available from: http://healthycanadians.gc.ca/eating-nutrition/food-guide-aliment/index-eng.php

  23. Duckham R, Baxter-Jones AD, Johnston JD, Vatanparast H, Cooper D, Kontulainen S (2014) Does physical activity in adolescence have site-specific and sex-specific benefits on young adult bone size, content, and estimated strength? JBMR 29(2):479–486

    Article  Google Scholar 

  24. Kontulainen SA, Johnston JD, Liu D, Leung C, Oxland TR, McKay HA (2008) Strength indices from pQCT imaging predict up to 85% of variance in bone failure properties at tibial epiphysis and diaphysis. J Musculoskelet Neuronal Interact 8(4):401–409

    CAS  PubMed  Google Scholar 

  25. Frank-Wilson AW, Johnston JD, Olszynski WP, Kontulainen SA (2015) Measurement of muscle and fat in postmenopausal women: precision of previously reported pQCT imaging methods. Bone 75:49–54

    Article  PubMed  Google Scholar 

  26. Radavelli-Bagatini S, Zhu K, Lewis JR, Prince RL (2014) Dairy food intake, peripheral bone structure, and muscle mass in elderly ambulatory women. J Bone Miner Res 29(7):1691–1700

    Article  CAS  PubMed  Google Scholar 

  27. 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(1):142–151

    CAS  PubMed  Google Scholar 

  28. Welch AA, Mulligan A, Bingham SA, Khaw KT (2008) Urine pH is an indicator of dietary acid–base load, fruit and vegetables and meat intakes: results from the European Prospective Investigation into Cancer and Nutrition (EPIC)-Norfolk population study. Br J Nutr 99(6):1335–1343

    Article  CAS  PubMed  Google Scholar 

  29. Aghajanian P, Hall S, Wongworawat MD, Mohan S (2015) The roles and mechanisms of actions of vitamin C in bone: new developments. J Bone Miner Res 30(11):1945–1955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Weber P (2001) Vitamin K and bone health. Nutrition 17(10):880–887

    Article  CAS  PubMed  Google Scholar 

  31. Liu ZM, Leung J, Wong SY, Wong CK, Chan R, Woo J (2015) Greater fruit intake was associated with better bone mineral status among Chinese elderly men and women: results of Hong Kong Mr. Os and Ms. Os studies. J Am Med Dir Assoc 16(4):309–315

    Article  PubMed  Google Scholar 

  32. Weaver CM, Alekel DL, Ward WE, Ronis MJ (2012) Flavonoid intake and bone health. J Nutr Gerontol Geriatr 31(3):239–253

    Article  PubMed  PubMed Central  Google Scholar 

  33. Kant AK (2004) Dietary patterns and health outcomes. J Am Diet Assoc 104:615–635

    Article  PubMed  Google Scholar 

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Acknowledgments

All authors contributed to the final manuscript. The project was funded by the Canadian Institutes of Health Research (CIHR, MOP 98002; MOP57671). Dairy Farmers of Canada (DFC-417283) provided funding for the PhD student support. The authors (Movassagh, Kontulainen, Baxter-Jones, Whiting, Szafron, Papadimitropoulos, Vatanparast) have no conflict of interest to disclose.

Author information

Authors and Affiliations

  1. College of Pharmacy and Nutrition, University of Saskatchewan, 104 Clinic place, Saskatoon, SK, S7N 2Z4, Canada

    E. Z. Movassagh, S. Whiting, M. Papadimitropoulos & H. Vatanparast

  2. College of Kinesiology, University of Saskatchewan, 87 Campus Drive, Saskatoon, SK, S7N5B2, Canada

    S. Kontulainen & A. D. G. Baxter-Jones

  3. College of Graduate Studies and Research, University of Saskatchewan, 105 Administration place, Saskatoon, SK, S7N 5A2, Canada

    A. D. G. Baxter-Jones

  4. School of Public Health, University of Saskatchewan, 104 Clinic place, Saskatoon, SK, S7N 5E5, Canada

    M. Szafron & H. Vatanparast

Authors
  1. E. Z. Movassagh
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  2. S. Kontulainen
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  3. A. D. G. Baxter-Jones
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  4. S. Whiting
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  5. M. Szafron
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  6. M. Papadimitropoulos
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  7. H. Vatanparast
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Corresponding author

Correspondence to H. Vatanparast.

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Ethical approval

Ethics approval was obtained from the University of Saskatchewan and Royal Hospital advisory boards on ethics in human experimentation [21], and all procedures were in accordance with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants (or their parents) included in the study.

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Z. Movassagh, E., Kontulainen, S., Baxter-Jones, A.D.G. et al. Are milk and alternatives and fruit and vegetable intakes during adolescence associated with cortical and trabecular bone structure, density, and strength in adulthood?. Osteoporos Int 28, 609–619 (2017). https://doi.org/10.1007/s00198-016-3775-4

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  • DOI: https://doi.org/10.1007/s00198-016-3775-4

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