Archives of Osteoporosis

, 13:135 | Cite as

Bone mineral density, vitamin D status, and calcium intake in healthy female university students from different socioeconomic groups in Turkey

  • Betül ErsoyEmail author
  • Deniz Özalp Kizilay
  • Seniha Kiremitci Yilmaz
  • Fatma Taneli
  • Gül Gümüşer
Original Article



Peak bone mass is reached in late adolescence. Low peak bone mass is a well recognized risk factor for osteoporosis later in life. Our data do not support a link between vitamin D status, bone mineral density (BMD), and socioeconomic status (SES). However, there was a marked inadequacy of daily calcium intake and a high presence of osteopenia in females with low SES.


Our aims were to (1) examine the effects of different SES on BMD, vitamin D status, and daily calcium intake and (2) investigate any association between vitamin D status and BMD in female university students.

Subjects and methods

A questionnaire was used to obtain information about SES, daily calcium intake, and physical activity in 138 healthy, female university students (age range 18–22 years). Subjects were stratified into lower, middle, and higher SES according to the educational and occupational levels of their parents. All serum samples were collected in spring for 25-hydroxyvitamin D concentration (25OHD). Lumbar spine and total body BMD was obtained by dual-energy X-ray absorptiometry (DXA) scan (Lunar DPX series). Osteopenia was defined as a BMD between − 1.0 and − 2.5 standard deviations (SDs) below the mean for healthy young adults on lumbar spine DXA.


No significant difference was found between the three socioeconomic groups in terms of serum 25OHD concentration, BMD levels, or BMD Z scores (p > 0.05). Both the daily intake of calcium was significantly lower (p = 0.02), and the frequency of osteopenia was significantly higher in girls with low SES (p = 0.02). There was no correlation between serum 25OHD concentration and calcium intake and BMD values and BMD Z scores (p > 0.05). The most important factor affecting BMD was weight (β = 0.38, p < 0.001).


Low SES may be associated with sub-optimal bone health and predispose to osteopenia in later life, even in female university students.


Vitamin D Osteopenia Bone mineral density 


Compliance with ethical standards

Conflicts of interest



  1. 1.
    Saggese G, Baroncelli GI, Bertelloni S (2000) Puberty and bone development. Best Pract Res Clin Endocrinol Metab 16(1):53–64CrossRefGoogle Scholar
  2. 2.
    Yilmaz D, Ersoy B, Bilgin E, Gümüşer G, Onur E, Pinar ED (2005) Bone mineral density in girls and boys at different pubertal stages: relation with gonadal steroids, bone formation markers, and growth parameters. J Bone Miner Metab 23(6):476–482PubMedCrossRefGoogle Scholar
  3. 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. J Bone Miner Res 26(8):1729–1739PubMedCrossRefGoogle Scholar
  4. 4.
    Bachrach LK, Hastie T, Wang MC, Narasimhan B, Marcus R (1999) Bone mineral acquisition in healthy Asian, Hispanic, black, and Caucasian youth: a longitudinal study. J Clin Endocrinol Metab 84(12):4702–4712PubMedGoogle Scholar
  5. 5.
    Heaney RP, Abrams S, Dawson-Hughes B, Looker A, Marcus R, Matkovic V, Weaver C (2000) Peak bone mass. Osteoporos Int 11(12):985–1009PubMedCrossRefGoogle Scholar
  6. 6.
    Bachrach LK (2005) Osteoporosis and measurement of bone mass in children and adolescents. Endocrinol Metab Clin N Am 34(3):521–535CrossRefGoogle Scholar
  7. 7.
    Branca F, Valtueña S (2001) Calcium, physical activity and bone health—building bones for a stronger future. Public Health Nutr 4(1A):117–123PubMedCrossRefGoogle Scholar
  8. 8.
    Gracia-Marco L, Ortega FB, Casajús JA, Sioen I, Widhalm K, Béghin L, Vicente-Rodríguez G, Moreno LA (2012) Socioeconomic status and bone mass in Spanish adolescents. The HELENA study. J Adolesc Health 50(5):484–490PubMedCrossRefGoogle Scholar
  9. 9.
    Brennan SL, Pasco JA, Urquhart DM, Oldenburg B, Wang Y, Wluka AE (2011) Association between socioeconomic status and bone mineral density in adults: a systematic review. Osteoporos Int 22(2):517–527PubMedCrossRefGoogle Scholar
  10. 10.
    Brown AJ, Dusso A, Slatopolsky E (1999) Vitamin D. Am J Phys 277(2 Pt 2):F157–F175Google Scholar
  11. 11.
    Bischoff-Ferrari HA, Dietrich T, Orav EJ, Dawson-Hughes B (2004) Positive association between 25-hydroxy vitamin D levels and bone mineral density: a population-based study of younger and older adults. Am J Med 116(9):634–639PubMedCrossRefGoogle Scholar
  12. 12.
    Lehtonen-Veromaa MK, Möttenen TT, Nuotio IO, Irjala KM, Leino AE, Vikari JS (2002) Vitamin D and attainment of peak bone mass among peripubertal Finnish girls: a 3-y prospective study. Am J Clin Nutr 76(6):1446–1453PubMedCrossRefGoogle Scholar
  13. 13.
    Gordon CM, DePeter KC, Feldman HA, Grace E, Emans SJ (2004) Prevalence of vitamin D deficiency among healthy adolescents. Arch Pediatr Adolesc Med 158(6):531–537PubMedCrossRefGoogle Scholar
  14. 14.
    Lehtonen-Veromaa MK, Möttönen T, Irjala K, Kärkkäinen M, Lamberg-Allardt C, Hakola P, Viikari J (1999) Vitamin D intake is low and hypovitaminosis D common in healthy 9- to 15-year-old Finnish girls. Eur J Clin Nutr 53(9):746–751PubMedCrossRefGoogle Scholar
  15. 15.
    El-Hajj Fuleihan G, Nabulsi M, Choucair M, Salamoun M, Hajj Shahine C, Kizirian A, Tannous R (2001) Hypovitaminosis D in healthy schoolchildren. Pediatrics 107(4):E53PubMedCrossRefGoogle Scholar
  16. 16.
    Puri S, Marwaha RK, Agarwal N, Tandon N, Agarwal R, Grewal K, Reddy DH, Singh S (2008) Vitamin D status of apparently healthy schoolgirls from two different socioeconomic strata in Delhi: relation to nutrition and lifestyle. Br J Nutr 99(4):876–882PubMedCrossRefGoogle Scholar
  17. 17.
    Hollingshead A (1957) Two factor index of social position. Yale Univ. Press, New HeavenGoogle Scholar
  18. 18.
    Lewiecki EM, Gordon CM, Baim S, Leonard MB, Bishop NJ, Bianchi ML, Kalkwarf HJ, Langman CB, Plotkin H, Rauch F, Zemel BS, Binkley N, Bilezikian JP, Kendler DL, Hans DB, Silverman S (2008) International Society for Clinical Densitometry 2007 adult and pediatric official positions. Bone 43(6):1115–1121PubMedCrossRefGoogle Scholar
  19. 19.
    Karagüzel G, Holick MF (2010) Diagnosis and treatment of osteopenia. Rev Endocr Metab Disord 11(4):237–251PubMedCrossRefGoogle Scholar
  20. 20.
    Sanchez MM, Gisanz V (2005) Pediatric DXA bone measurements. Pediatr Endocrinol Rev 2(Suppl 3):337–341PubMedGoogle Scholar
  21. 21.
    Committee to Review Dietary Reference Intakes for Vitamin D and Calcium, Food and Nutrition Board, Institute of Medicine (2010) Dietary reference intakes for calcium and vitamin D. National Academy Press, Washington, DCGoogle Scholar
  22. 22.
    Turkish Food Composition Database. Gıda, Tarım ve Hayvancılık Bakanlığı
  23. 23.
    Committee PAGA. Physical activity guidelines advisory committee report. 2012. Accessed 01 Dec 2014
  24. 24.
    Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon CM, Hanley DA, Heaney RP, Murad MH, Weaver CM, Endocrine Society (2011) Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 96(7):1911–1930PubMedCrossRefGoogle Scholar
  25. 25.
    Du Y, Zhao LJ, Xu Q, Wu KH, Denk HW (2017) Socioeconomic status and bone mineral density in adults by race/ethnicity and gender: the Louisiana osteoporosis study. Osteoporos Int 28(5):1699–1709PubMedCrossRefGoogle Scholar
  26. 26.
    Crandall CJ, Merkin SS, Seeman TE, Greendale GA, Binkley N, Karlamangla AS (2012) Socioeconomic status over the life-course and adult bone mineral density: the midlife in the U.S. study. Bone 51(1):107–113PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Oliveira CM, Economou T, Bailey T, Mendonça D, Pina MF (2015) The interactions between municipal socioeconomic status and age on hip fracture risk. Osteoporos Int 26(2):489–498PubMedCrossRefGoogle Scholar
  28. 28.
    Tatsumi Y, Higashiyama A, Kubota Y, Sugiyama D, Nishida Y, Hirata T, Kadota A, Nishimura K, Imano H, Miyamatsu N, Miyamoto Y, Okamura T (2016) Underweight young women without later weight gain are at high risk for osteopenia after midlife: the KOBE study. J Epidemiol 26(11):572–578PubMedCrossRefGoogle Scholar
  29. 29.
    Hossein-nezhad A, Holick MF (2013) Vitamin D for health: a global perspective. Mayo Clin Proc 88(7):720–755PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Carnevale V, Modoni S, Pileri M, Di Giorgio A, Chiodini I, Minisola S, Vieth R, Scillitani A (2001) Longitudinal evaluation of vitamin D status in healthy subjects from southern Italy: seasonal and gender differences. Osteoporos Int 12(12):1026–1030PubMedCrossRefGoogle Scholar
  31. 31.
    Kaehler ST, Baumgartner H, Jeske M, Anliker M, Schennach H, Marschang P, Ratt A, Colvin AC, Falk J, Gasser A, Kirchebner J, Scherer C, Purtscher AE, Griesmacher A, Striessnig J (2012) Prevalence of hypovitaminosis D and folate deficiency in healthy young female Austrian students in a health care profession. Eur J Nutr 51(8):1021–1031PubMedCrossRefGoogle Scholar
  32. 32.
    Callegari ET, Garland SM, Gorelik A, Wark JD (2017) Determinants of bone mineral density in young Australian women; results from the safe-D study. Osteoporos Int 28(9):2619–2631PubMedCrossRefGoogle Scholar
  33. 33.
    Winzenberg T, Powell S, Shaw KA, Jones G (2011) Effects of vitamin D supplementation on bone density in healthy children: systematic review and meta-analysis. BMJ 342:c7254PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Winzenberg TM, Shaw K, Fryer J, Jones G (2006) Calcium supplementation for improving bone mineral density in children. Cochrane database Syst Rev (2):CD005119Google Scholar
  35. 35.
    Closa-Monasterolo R, Zaragoza-Jordana M, Ferré N, Luque V, Grote V, Koletzko B, Verduci E, Vecchi F, Escribano J (2017) Childhood obesity project group. Adequate calcium intake during long periods improves bone mineral density in healthy children. Data from the Childhood Obesity Project. Clin Nutr S0261-5614(17):30102–30104Google Scholar
  36. 36.
    Neville CE, Robson PJ, Murray LJ, Strain JJ, Twisk J, Gallagher AM, McGuinness M, Cran GW, Ralston SH, Boreham CA (2002) The effect of nutrient intake on bone mineral status in young adults: the Northern Ireland young hearts project. Calcif Tissue Int 70(2):89–98PubMedCrossRefGoogle Scholar
  37. 37.
    Valimaki MJ, Karkkainen M, Lamberg-Allardt C, Laitinen K, Alhava E, Heikkinen J, Impivaara O, Makela P, Palmgren J, Seppannen R, Vuori I, and the Cardiovascular Risk in Young Finns Study Group (1994) Exercise, smoking, and calcium intake during adolescence and early adulthood as determinants of peak bone mass: cardiovascular risk in young Finns study group. BMJ 309:230–235PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Rubin LA, Hawker GA, Peltekova VD, Fielding LJ, Ridout R, Cole DE (1999) Determinants of peak bone mass: clinical and genetic analyses in a young female Canadian cohort. J Bone Miner Res 14(4):633–643PubMedCrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2018

Authors and Affiliations

  • Betül Ersoy
    • 1
    Email author
  • Deniz Özalp Kizilay
    • 1
  • Seniha Kiremitci Yilmaz
    • 1
  • Fatma Taneli
    • 2
  • Gül Gümüşer
    • 3
  1. 1.Division of Pediatric Endocrinology and MetabolismSchool of Medicine, Celal Bayar UniversityManisaTurkey
  2. 2.Department of Clinical Biochemistry, School of MedicineCelal Bayar UniversityManisaTurkey
  3. 3.Department of Nuclear Medicine, School of MedicineCelal Bayar UniversityManisaTurkey

Personalised recommendations