The Effects of Vitamin D Fortified Products on Bone Biomarkers: A Systematic Review and Meta-Analysis
-
Maryam Emadzadeh
,
Atieh Mehdizadeh
,
Payam Sharifan
,
Mahdieh Khoshakhlagh
,
Reza Sahebi
,
Ramin Sadeghi
,
Gordon A. Ferns
,
Majid Ghayour-Mobarhan
Abstract
Background: Vitamin D plays an essential role in the regulation of bone metabolism. The current meta-analysis aimed to assess the effectiveness of vitamin D fortification on special bone biomarkers.
Methods: Five main databases (PubMed/Medline, ISI Web of Knowledge, Science Direct, Scopus, Cochrane Library as well as Science Direct, and Scopus) were considered for this systematic review, until Jan 2020. All randomized controlled trials were included to evaluate the probable relationship between consumption of vitamin D fortification products and bone biomarkers profile in this review.
Results: Among serum bone biomarkers (osteocalcin and telopeptides of type-1 collagen) investigated, only the level of telopeptides of type-1 collagen significantly decreased after fortification of vitamin D in the intervention group. A significant increase in vitamin D was seen in those older than 18 yr old, while the increase in younger children was not statistically significant between intervention and control groups.
Conclusion: Vitamin D fortification was not associated with a significant improvement in bone mass density (BMD), while it resulted in decreased PTH levels. Vitamin D fortified foods have some benefits on bone health due to increase in the level of vitamin D and IGF-1; and decreasing PTH and CTx levels.
1. Charoenngam N, Shirvani A, Holick MF (2019). Vitamin D for skeletal and non-skeletal health: What we should know. J Clin Orthop Trauma, 10:1082-1093.
2. Emadzadeh M, Rashidmayvan M, Sahebi R, et al (2020). The effect of vitamin D fortified products on anthropometric indices: A systematic review and meta-analysis. Complement Ther Clin Pract, 41:101242.
3. Emadzadeh M, Sahebi R, Khedmatgozar H, et al (2020). A systematic review and meta‐analysis of the effect of Vitamin D‐fortified food on glycemic indices. Biofactors, 46(4):502-513.
4. Tangestani H, Djafarian K, Emamat H, et al (2020). Efficacy of vitamin D fortified foods on bone mineral density and serum bone biomarkers: A systematic review and meta-analysis of interventional studies. Crit Rev Food Sci Nutr, 60(7):1094-1103.
5. Jafari T, Faghihimani E, Feizi A, Iraj B, et al (2016). Effects of vitamin D-fortified low fat yogurt on glycemic status, anthropometric indexes, inflammation, and bone turnover in diabetic postmenopausal women: A randomised controlled clinical trial. Clin Nutr, 35:67-76.
6. Moulas AN, Vaiou M (2018). Vitamin D fortification of foods and prospective health outcomes. J Biotechnol, 285:91-101.
7. Vasikaran S, Eastell R, Bruyere O, et al (2011). Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards. Osteoporos Int, 22:391-420.
8. Heshmat R, Mohammad K, Majdzadeh S, et al (2008). Vitamin D deficiency in Iran: A multi-center study among different urban areas. Iran J Public Health, 37(Supple 2):72-78.
9. Pilz S, März W, Cashman KD, et al (2018). Rationale and plan for vitamin D food fortification: a review and guidance paper. Front Endocrinol (Lausanne), 9:373.
10. Moher D, Liberati A, Tetzlaff J, Altman DG (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med, 151:264-269.
11. Jadad AR, Moore RA, Carroll D, et al (1996). Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials, 17:1-12.
12. Lundh A, Gøtzsche PC (2008). Recommendations by Cochrane Review Groups for assessment of the risk of bias in studies. BMC Med Res Methodol, 8:22.
13. Mostafai R, Mohammadi R, Nachvak SM, et al (2018). Fortified yogurt with vitamin D as a cost-effective food to prevent diabetes: A randomized double-blind clinical trial. J Funct Foods, 42:137-145.
14. Mazidi M, Gao H-K, Rezaie P, Ferns GA (2016). The effect of ginger supplementation on serum C-reactive protein, lipid profile and glycaemia: a systematic review and meta-analysis. Food Nutr Res, 60:32613.
15. Mazidi M, Rezaie P, Karimi E, Kengne AP (2017). The effects of bile acid sequestrants on lipid profile and blood glucose concentrations: a systematic review and meta-analysis of randomized controlled trials. Int J Cardiol, 227:850-857.
16. Zein H, Tran VL-H, Abdelmotaleb Ghazy A, et al (2015). How to extract data from graphs using plot digitizer or Getdata graph digitizer. Technical Report.
17. Borenstein M, Hedges L, Higgins J, Rothstein H (2005). “Comprehensive meta analysis Version 2”Biostat. https://www.meta-analysis.com/downloads/Meta-Analysis-Manual.pdf
18. Keane EM, Rochfort A, Cox J, et al (1992). Vitamin-D-fortified liquid milk–a highly effective method of vitamin D administration for house-bound and institutionalised elderly. Gerontology, 38:280-284.
19. Moschonis G, Manios Y (2006). Skeletal site-dependent response of bone mineral density and quantitative ultrasound parameters following a 12-month dietary intervention using dairy products fortified with calcium and vitamin D: the Postmenopausal Health Study. Br J Nutr, 96:1140-1148.
20. Manios Y, Moschonis G, Trovas G, Lyritis GP (2007). Changes in biochemical indexes of bone metabolism and bone mineral density after a 12-mo dietary intervention program: the Postmenopausal Health Study. Am J Clin Nutr, 86:781-789.
21. Manios Y, Moschonis G, Panagiotakos DB, et al (2009). Changes in biochemical indices of bone metabolism in post-menopausal women following a dietary intervention with fortified dairy products. J Hum Nutr Diet, 22:156-65.
22. Green TJ, Skeaff CM, Rockell JE (2010). Milk fortified with the current adequate intake for vitamin D (5μg) increases serum 25-hydroxyvitamin D compared to control milk but is not sufficient to prevent a seasonal decline in young women. Asia Pac J Clin Nutr, 19:195-199.
23. Moschonis G, Katsaroli I, Lyritis GP, Manios Y (2010). The effects of a 30-month dietary intervention on bone mineral density: the Postmenopausal Health Study. Br J Nutr, 104:100-107.
24. Manios Y, Moschonis G, Lyritis G (2011). Seasonal variations of vitamin D status in Greek postmenopausal women receiving enriched dairy products for 30 months: the Postmenopausal Health Study. Eur J Clin Nutr, 65:412-4.
25. Tenta R, Moschonis G, Koutsilieris M, Manios Y (2011). Calcium and vitamin D supplementation through fortified dairy products counterbalances seasonal variations of bone metabolism indices: the Postmenopausal Health Study. Eur J Nutr, 50:341-349.
26. Kanellakis S, Moschonis G, Tenta R, et al (2012). Changes in parameters of bone metabolism in postmenopausal women following a 12-month intervention period using dairy products enriched with calcium, vitamin D, and phylloquinone (vitamin K 1) or menaquinone-7 (vitamin K 2): the Postmenopausal Health Study II. Calcif Tissue Int, 90:251-262.
27. Bonjour J-P, Benoit V, Payen F, Kraenzlin M (2013). Consumption of yogurts fortified in vitamin D and calcium reduces serum parathyroid hormone and markers of bone resorption: a double-blind randomized controlled trial in institutionalized elderly women. J Clin Endocrinol Metab, 98:2915-2921.
28. Bonjour J-P, Benoit V, Atkin S, Walrand S (2015). Fortification of yogurts with vitamin D and calcium enhances the inhibition of serum parathyroid hormone and bone resorption markers: A double blind randomized controlled trial in women over 60 living in a community dwelling home. J Nutr Health Aging, 19:563-569.
29. Itkonen ST, Skaffari E, Saaristo P, et al (2016). Effects of vitamin D 2-fortified bread v. supplementation with vitamin D 2 or D 3 on serum 25-hydroxyvitamin D metabolites: an 8-week randomised-controlled trial in young adult Finnish women. Br J Nutr, 115:1232-1239.
30. Tripkovic L, Wilson LR, Hart K, et al (2017). Daily supplementation with 15 μg vitamin D2 compared with vitamin D3 to increase wintertime 25-hydroxyvitamin D status in healthy South Asian and white European women: a 12-wk randomized, placebo-controlled food-fortification trial. Am J Clin Nutr, 106:481-490.
31. Bonjour J-P, Dontot-Payen F, Rouy E, et al (2018). Evolution of Serum 25OHD in Response to Vitamin D3–Fortified Yogurts Consumed by Healthy Menopausal Women: A 6-Month Randomized Controlled Trial Assessing the Interactions between Doses, Baseline Vitamin D Status, and Seasonality. J Am Coll Nutr, 37:34-43.
32. Grønborg IM, Tetens I, Andersen EW, et al (2019). Effect of vitamin D fortified foods on bone markers and muscle strength in women of Pakistani and Danish origin living in Denmark: a randomised controlled trial. Nutr J, 18:82.
33. Grønborg IM, Tetens I, Christensen T, et al (2020). Vitamin D-fortified foods improve wintertime vitamin D status in women of Danish and Pakistani origin living in Denmark: a randomized controlled trial. Eur J Nutr, 59:741-753.
34. Daly RM, Bass S, Nowson C (2006). Long-term effects of calcium–vitamin-D3-fortified milk on bone geometry and strength in older men. Bone, 39:946-953.
35. Kukuljan S, Nowson CA, Sanders KM, et al (2011). Independent and combined effects of calcium-vitamin D3 and exercise on bone structure and strength in older men: an 18-month factorial design randomized controlled trial. J Clin Endocrinol Metab, 96:955-963.
36. Xueqin D, Zhu K, Trube A, et al (2004). School-milk intervention trial enhances growth and bone mineral accretion in Chinese girls aged 10–12 years in Beijing. Br J Nutr, 92:159-168.
37. Zhu K, Du X, Cowell CT, et al (2005). Effects of school milk intervention on cortical bone accretion and indicators relevant to bone metabolism in Chinese girls aged 10–12 y in Beijing. Am J Clin Nutr, 81:1168-1175.
38. Rich-Edwards JW, Ganmaa D, Kleinman K, et al (2011). Randomized trial of fortified milk and supplements to raise 25-hydroxyvitamin D concentrations in schoolchildren in Mongolia. Am J Clin Nutr, 94:578-584.
39. Khadgawat R, Marwaha R, Garg M, et al (2013). Impact of vitamin D fortified milk supplementation on vitamin D status of healthy school children aged 10–14 years. Osteoporos Int, 24:2335-2343.
40. Neyestani T, Hajifaraji M, Omidvar N, et al (2014). Calcium‐vitamin D‐fortified milk is as effective on circulating bone biomarkers as fortified juice and supplement but has less acceptance: a randomised controlled school‐based trial. J Hum Nutr Diet, 27:606-616.
41. Brett NR, Lavery P, Agellon S, et al (2016). Dietary vitamin D dose-response in healthy children 2 to 8 y of age: a 12-wk randomized controlled trial using fortified foods. Am J Clin Nutr, 103:144-152.
42. Brett NR, Parks CA, Lavery P, et al (2018). Vitamin D status and functional health outcomes in children aged 2–8 y: a 6-mo vitamin D randomized controlled trial. Am J Clin Nutr, 107:355-364.
43. Lu J, Pan H, Hu X, et al (2019). Effects of milk powder intervention on bone mineral density and indicators related to bone metabolism in Chinese adolescents. Osteoporos Int, 30:2231-2239.
44. Fisk CM, Theobald HE, Sanders TA (2012). Fortified malted milk drinks containing low-dose ergocalciferol and cholecalciferol do not differ in their capacity to raise serum 25-hydroxyvitamin D concentrations in healthy men and women not exposed to UV-B. J Nutr, 142:1286-1290.
45. Johnson J, Mistry V, Vukovich M, et al (2005). Bioavailability of vitamin D from fortified process cheese and effects on vitamin D status in the elderly. J Dairy Sci, 88:2295-2301.
46. Neyestani TR, Nikooyeh B, Kalayi A, et al (2015). A vitamin D-calcium-fortified yogurt drink decreased serum PTH but did not affect osteocalcin in subjects with type 2 diabetes. Int J Vitam Nutr Res, 85:61-69.
47. Moreira-Lucas TS, Duncan AM, Rabasa-Lhoret R, et al (2016). Effect of Vitamin D Fortified Cheese on Oral Glucose Tolerance in Individuals Exhibiting Marginal Vitamin D Status and an Increased Risk for Developing Type 2 Diabetes: A Double-Blind, Randomized Placebo-Controlled Clinical Trial. Faseb J, 30:917.1-917.1.
48. Nikooyeh B, Neyestani TR, Zahedirad M, et al (2016). Vitamin D-fortified bread is as effective as supplement in improving vitamin D status: a randomized clinical trial. J Clin Endocrinol Metab, 101:2511-2519.
49. Salehi S, Sadeghi F, Akhlaghi M, et al (2018). Vitamin D3-fortified milk did not affect glycemic control, lipid profile, and anthropometric measures in patients with type 2 diabetes, a triple-blind randomized clinical trial. Eur J Clin Nutr, 72:1083-1092.
50. Boonen S, Lips P, Bouillon R, et al (2007). Need for additional calcium to reduce the risk of hip fracture with vitamin D supplementation: evidence from a comparative metaanalysis of randomized controlled trials. J Clin Endocrinol Metab, 92:1415-1423.
51. Papadimitropoulos E, Shea B, Wells GA, et al (1997). Vitamin D with or without calcium for treating osteoporosis in postmenopausal women. Cochrane Database Syst Rev, 4: CD000519.
52. Lips P (2001). Vitamin D deficiency and secondary hyperparathyroidism in the elderly: consequences for bone loss and fractures and therapeutic implications. Endocr Rev, 22:477-501.
53. Kuehn BM (2012). USPSTF: Taking vitamin D and calcium doesn’t prevent fractures in older women. JAMA, 308:225-226.
54. Baroncelli GI, Bertelloni S, Ceccarelli C, et al (2000). Bone turnover in children with vitamin D deficiency rickets before and during treatment. Acta Paediatr, 89:513-8.
55. Seibel M (2000). Molecular markers of bone turnover: biochemical, technical and analytical aspects. Osteoporos Int, 11 Suppl 6:S18-29.
56. Calvo MS, Eyre DR, Gundberg CM (1996). Molecular basis and clinical application of biological markers of bone turnover. Endocr Rev, 17:333-368.
57. Sukumar D, Shapses S, Schneider S (2015). Vitamin D supplementation during short-term caloric restriction in healthy overweight/obese older women: effect on glycemic indices and serum osteocalcin levels. Mol Cell Endocrinol, 410:73-77.
58. Je SH, Joo N-S, Choi B-h, et al (2011). Vitamin K supplement along with vitamin D and calcium reduced serum concentration of undercarboxylated osteocalcin while increasing bone mineral density in Korean postmenopausal women over sixty-years-old. J Korean Med Sci, 26:1093-1098.
59. Von Hurst P, Stonehouse W, Kruger M, Coad J (2010). Vitamin D supplementation suppresses age-induced bone turnover in older women who are vitamin D deficient. J Steroid Biochem Mol Biol, 121:293-296.
60. Martinez M, Del Campo M, Sanchez-Cabezudo M, et al (1994). Relations between calcidiol serum levels and bone mineral density in postmenopausal women with low bone density. Calcif Tissue Int, 55:253-256.
61. Khaw K-T, Sneyd M-J, Compston J (1992). Bone density parathyroid hormone and 25-hydroxyvitamin D concentrations in middle aged women. BMJ, 305:273-277.
62. Chapuy M, Schott A, Garnero P, et al (1996). Healthy elderly French women living at home have secondary hyperparathyroidism and high bone turnover in winter. EPIDOS Study Group. J Clin Endocrinol Metab, 81:1129-1133.
63. Jehle PM, Schulten K, Schulz W, et al (2003). Serum levels of insulin-like growth factor (IGF)-I and IGF binding protein (IGFBP)-1 to -6 and their relationship to bone metabolism in osteoporosis patients. Eur J Intern Med, 14:32-38.
64. O'Connor KG, Tobin JD, Harman SM, et al (1998). Serum levels of insulin-like growth factor-I are related to age and not to body composition in healthy women and men. J Gerontol A Biol Sci Med Sci, 53:M176-82.
2. Emadzadeh M, Rashidmayvan M, Sahebi R, et al (2020). The effect of vitamin D fortified products on anthropometric indices: A systematic review and meta-analysis. Complement Ther Clin Pract, 41:101242.
3. Emadzadeh M, Sahebi R, Khedmatgozar H, et al (2020). A systematic review and meta‐analysis of the effect of Vitamin D‐fortified food on glycemic indices. Biofactors, 46(4):502-513.
4. Tangestani H, Djafarian K, Emamat H, et al (2020). Efficacy of vitamin D fortified foods on bone mineral density and serum bone biomarkers: A systematic review and meta-analysis of interventional studies. Crit Rev Food Sci Nutr, 60(7):1094-1103.
5. Jafari T, Faghihimani E, Feizi A, Iraj B, et al (2016). Effects of vitamin D-fortified low fat yogurt on glycemic status, anthropometric indexes, inflammation, and bone turnover in diabetic postmenopausal women: A randomised controlled clinical trial. Clin Nutr, 35:67-76.
6. Moulas AN, Vaiou M (2018). Vitamin D fortification of foods and prospective health outcomes. J Biotechnol, 285:91-101.
7. Vasikaran S, Eastell R, Bruyere O, et al (2011). Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards. Osteoporos Int, 22:391-420.
8. Heshmat R, Mohammad K, Majdzadeh S, et al (2008). Vitamin D deficiency in Iran: A multi-center study among different urban areas. Iran J Public Health, 37(Supple 2):72-78.
9. Pilz S, März W, Cashman KD, et al (2018). Rationale and plan for vitamin D food fortification: a review and guidance paper. Front Endocrinol (Lausanne), 9:373.
10. Moher D, Liberati A, Tetzlaff J, Altman DG (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med, 151:264-269.
11. Jadad AR, Moore RA, Carroll D, et al (1996). Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials, 17:1-12.
12. Lundh A, Gøtzsche PC (2008). Recommendations by Cochrane Review Groups for assessment of the risk of bias in studies. BMC Med Res Methodol, 8:22.
13. Mostafai R, Mohammadi R, Nachvak SM, et al (2018). Fortified yogurt with vitamin D as a cost-effective food to prevent diabetes: A randomized double-blind clinical trial. J Funct Foods, 42:137-145.
14. Mazidi M, Gao H-K, Rezaie P, Ferns GA (2016). The effect of ginger supplementation on serum C-reactive protein, lipid profile and glycaemia: a systematic review and meta-analysis. Food Nutr Res, 60:32613.
15. Mazidi M, Rezaie P, Karimi E, Kengne AP (2017). The effects of bile acid sequestrants on lipid profile and blood glucose concentrations: a systematic review and meta-analysis of randomized controlled trials. Int J Cardiol, 227:850-857.
16. Zein H, Tran VL-H, Abdelmotaleb Ghazy A, et al (2015). How to extract data from graphs using plot digitizer or Getdata graph digitizer. Technical Report.
17. Borenstein M, Hedges L, Higgins J, Rothstein H (2005). “Comprehensive meta analysis Version 2”Biostat. https://www.meta-analysis.com/downloads/Meta-Analysis-Manual.pdf
18. Keane EM, Rochfort A, Cox J, et al (1992). Vitamin-D-fortified liquid milk–a highly effective method of vitamin D administration for house-bound and institutionalised elderly. Gerontology, 38:280-284.
19. Moschonis G, Manios Y (2006). Skeletal site-dependent response of bone mineral density and quantitative ultrasound parameters following a 12-month dietary intervention using dairy products fortified with calcium and vitamin D: the Postmenopausal Health Study. Br J Nutr, 96:1140-1148.
20. Manios Y, Moschonis G, Trovas G, Lyritis GP (2007). Changes in biochemical indexes of bone metabolism and bone mineral density after a 12-mo dietary intervention program: the Postmenopausal Health Study. Am J Clin Nutr, 86:781-789.
21. Manios Y, Moschonis G, Panagiotakos DB, et al (2009). Changes in biochemical indices of bone metabolism in post-menopausal women following a dietary intervention with fortified dairy products. J Hum Nutr Diet, 22:156-65.
22. Green TJ, Skeaff CM, Rockell JE (2010). Milk fortified with the current adequate intake for vitamin D (5μg) increases serum 25-hydroxyvitamin D compared to control milk but is not sufficient to prevent a seasonal decline in young women. Asia Pac J Clin Nutr, 19:195-199.
23. Moschonis G, Katsaroli I, Lyritis GP, Manios Y (2010). The effects of a 30-month dietary intervention on bone mineral density: the Postmenopausal Health Study. Br J Nutr, 104:100-107.
24. Manios Y, Moschonis G, Lyritis G (2011). Seasonal variations of vitamin D status in Greek postmenopausal women receiving enriched dairy products for 30 months: the Postmenopausal Health Study. Eur J Clin Nutr, 65:412-4.
25. Tenta R, Moschonis G, Koutsilieris M, Manios Y (2011). Calcium and vitamin D supplementation through fortified dairy products counterbalances seasonal variations of bone metabolism indices: the Postmenopausal Health Study. Eur J Nutr, 50:341-349.
26. Kanellakis S, Moschonis G, Tenta R, et al (2012). Changes in parameters of bone metabolism in postmenopausal women following a 12-month intervention period using dairy products enriched with calcium, vitamin D, and phylloquinone (vitamin K 1) or menaquinone-7 (vitamin K 2): the Postmenopausal Health Study II. Calcif Tissue Int, 90:251-262.
27. Bonjour J-P, Benoit V, Payen F, Kraenzlin M (2013). Consumption of yogurts fortified in vitamin D and calcium reduces serum parathyroid hormone and markers of bone resorption: a double-blind randomized controlled trial in institutionalized elderly women. J Clin Endocrinol Metab, 98:2915-2921.
28. Bonjour J-P, Benoit V, Atkin S, Walrand S (2015). Fortification of yogurts with vitamin D and calcium enhances the inhibition of serum parathyroid hormone and bone resorption markers: A double blind randomized controlled trial in women over 60 living in a community dwelling home. J Nutr Health Aging, 19:563-569.
29. Itkonen ST, Skaffari E, Saaristo P, et al (2016). Effects of vitamin D 2-fortified bread v. supplementation with vitamin D 2 or D 3 on serum 25-hydroxyvitamin D metabolites: an 8-week randomised-controlled trial in young adult Finnish women. Br J Nutr, 115:1232-1239.
30. Tripkovic L, Wilson LR, Hart K, et al (2017). Daily supplementation with 15 μg vitamin D2 compared with vitamin D3 to increase wintertime 25-hydroxyvitamin D status in healthy South Asian and white European women: a 12-wk randomized, placebo-controlled food-fortification trial. Am J Clin Nutr, 106:481-490.
31. Bonjour J-P, Dontot-Payen F, Rouy E, et al (2018). Evolution of Serum 25OHD in Response to Vitamin D3–Fortified Yogurts Consumed by Healthy Menopausal Women: A 6-Month Randomized Controlled Trial Assessing the Interactions between Doses, Baseline Vitamin D Status, and Seasonality. J Am Coll Nutr, 37:34-43.
32. Grønborg IM, Tetens I, Andersen EW, et al (2019). Effect of vitamin D fortified foods on bone markers and muscle strength in women of Pakistani and Danish origin living in Denmark: a randomised controlled trial. Nutr J, 18:82.
33. Grønborg IM, Tetens I, Christensen T, et al (2020). Vitamin D-fortified foods improve wintertime vitamin D status in women of Danish and Pakistani origin living in Denmark: a randomized controlled trial. Eur J Nutr, 59:741-753.
34. Daly RM, Bass S, Nowson C (2006). Long-term effects of calcium–vitamin-D3-fortified milk on bone geometry and strength in older men. Bone, 39:946-953.
35. Kukuljan S, Nowson CA, Sanders KM, et al (2011). Independent and combined effects of calcium-vitamin D3 and exercise on bone structure and strength in older men: an 18-month factorial design randomized controlled trial. J Clin Endocrinol Metab, 96:955-963.
36. Xueqin D, Zhu K, Trube A, et al (2004). School-milk intervention trial enhances growth and bone mineral accretion in Chinese girls aged 10–12 years in Beijing. Br J Nutr, 92:159-168.
37. Zhu K, Du X, Cowell CT, et al (2005). Effects of school milk intervention on cortical bone accretion and indicators relevant to bone metabolism in Chinese girls aged 10–12 y in Beijing. Am J Clin Nutr, 81:1168-1175.
38. Rich-Edwards JW, Ganmaa D, Kleinman K, et al (2011). Randomized trial of fortified milk and supplements to raise 25-hydroxyvitamin D concentrations in schoolchildren in Mongolia. Am J Clin Nutr, 94:578-584.
39. Khadgawat R, Marwaha R, Garg M, et al (2013). Impact of vitamin D fortified milk supplementation on vitamin D status of healthy school children aged 10–14 years. Osteoporos Int, 24:2335-2343.
40. Neyestani T, Hajifaraji M, Omidvar N, et al (2014). Calcium‐vitamin D‐fortified milk is as effective on circulating bone biomarkers as fortified juice and supplement but has less acceptance: a randomised controlled school‐based trial. J Hum Nutr Diet, 27:606-616.
41. Brett NR, Lavery P, Agellon S, et al (2016). Dietary vitamin D dose-response in healthy children 2 to 8 y of age: a 12-wk randomized controlled trial using fortified foods. Am J Clin Nutr, 103:144-152.
42. Brett NR, Parks CA, Lavery P, et al (2018). Vitamin D status and functional health outcomes in children aged 2–8 y: a 6-mo vitamin D randomized controlled trial. Am J Clin Nutr, 107:355-364.
43. Lu J, Pan H, Hu X, et al (2019). Effects of milk powder intervention on bone mineral density and indicators related to bone metabolism in Chinese adolescents. Osteoporos Int, 30:2231-2239.
44. Fisk CM, Theobald HE, Sanders TA (2012). Fortified malted milk drinks containing low-dose ergocalciferol and cholecalciferol do not differ in their capacity to raise serum 25-hydroxyvitamin D concentrations in healthy men and women not exposed to UV-B. J Nutr, 142:1286-1290.
45. Johnson J, Mistry V, Vukovich M, et al (2005). Bioavailability of vitamin D from fortified process cheese and effects on vitamin D status in the elderly. J Dairy Sci, 88:2295-2301.
46. Neyestani TR, Nikooyeh B, Kalayi A, et al (2015). A vitamin D-calcium-fortified yogurt drink decreased serum PTH but did not affect osteocalcin in subjects with type 2 diabetes. Int J Vitam Nutr Res, 85:61-69.
47. Moreira-Lucas TS, Duncan AM, Rabasa-Lhoret R, et al (2016). Effect of Vitamin D Fortified Cheese on Oral Glucose Tolerance in Individuals Exhibiting Marginal Vitamin D Status and an Increased Risk for Developing Type 2 Diabetes: A Double-Blind, Randomized Placebo-Controlled Clinical Trial. Faseb J, 30:917.1-917.1.
48. Nikooyeh B, Neyestani TR, Zahedirad M, et al (2016). Vitamin D-fortified bread is as effective as supplement in improving vitamin D status: a randomized clinical trial. J Clin Endocrinol Metab, 101:2511-2519.
49. Salehi S, Sadeghi F, Akhlaghi M, et al (2018). Vitamin D3-fortified milk did not affect glycemic control, lipid profile, and anthropometric measures in patients with type 2 diabetes, a triple-blind randomized clinical trial. Eur J Clin Nutr, 72:1083-1092.
50. Boonen S, Lips P, Bouillon R, et al (2007). Need for additional calcium to reduce the risk of hip fracture with vitamin D supplementation: evidence from a comparative metaanalysis of randomized controlled trials. J Clin Endocrinol Metab, 92:1415-1423.
51. Papadimitropoulos E, Shea B, Wells GA, et al (1997). Vitamin D with or without calcium for treating osteoporosis in postmenopausal women. Cochrane Database Syst Rev, 4: CD000519.
52. Lips P (2001). Vitamin D deficiency and secondary hyperparathyroidism in the elderly: consequences for bone loss and fractures and therapeutic implications. Endocr Rev, 22:477-501.
53. Kuehn BM (2012). USPSTF: Taking vitamin D and calcium doesn’t prevent fractures in older women. JAMA, 308:225-226.
54. Baroncelli GI, Bertelloni S, Ceccarelli C, et al (2000). Bone turnover in children with vitamin D deficiency rickets before and during treatment. Acta Paediatr, 89:513-8.
55. Seibel M (2000). Molecular markers of bone turnover: biochemical, technical and analytical aspects. Osteoporos Int, 11 Suppl 6:S18-29.
56. Calvo MS, Eyre DR, Gundberg CM (1996). Molecular basis and clinical application of biological markers of bone turnover. Endocr Rev, 17:333-368.
57. Sukumar D, Shapses S, Schneider S (2015). Vitamin D supplementation during short-term caloric restriction in healthy overweight/obese older women: effect on glycemic indices and serum osteocalcin levels. Mol Cell Endocrinol, 410:73-77.
58. Je SH, Joo N-S, Choi B-h, et al (2011). Vitamin K supplement along with vitamin D and calcium reduced serum concentration of undercarboxylated osteocalcin while increasing bone mineral density in Korean postmenopausal women over sixty-years-old. J Korean Med Sci, 26:1093-1098.
59. Von Hurst P, Stonehouse W, Kruger M, Coad J (2010). Vitamin D supplementation suppresses age-induced bone turnover in older women who are vitamin D deficient. J Steroid Biochem Mol Biol, 121:293-296.
60. Martinez M, Del Campo M, Sanchez-Cabezudo M, et al (1994). Relations between calcidiol serum levels and bone mineral density in postmenopausal women with low bone density. Calcif Tissue Int, 55:253-256.
61. Khaw K-T, Sneyd M-J, Compston J (1992). Bone density parathyroid hormone and 25-hydroxyvitamin D concentrations in middle aged women. BMJ, 305:273-277.
62. Chapuy M, Schott A, Garnero P, et al (1996). Healthy elderly French women living at home have secondary hyperparathyroidism and high bone turnover in winter. EPIDOS Study Group. J Clin Endocrinol Metab, 81:1129-1133.
63. Jehle PM, Schulten K, Schulz W, et al (2003). Serum levels of insulin-like growth factor (IGF)-I and IGF binding protein (IGFBP)-1 to -6 and their relationship to bone metabolism in osteoporosis patients. Eur J Intern Med, 14:32-38.
64. O'Connor KG, Tobin JD, Harman SM, et al (1998). Serum levels of insulin-like growth factor-I are related to age and not to body composition in healthy women and men. J Gerontol A Biol Sci Med Sci, 53:M176-82.
| Files | ||
| Issue | Vol 51 No 2 (2022) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v51i2.8681 | |
| Keywords | ||
| Vitamin D Bone density Osteocalcin Parathyroid hormone Insulin-like growth factor I | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Emadzadeh M, Mehdizadeh A, Sharifan P, Khoshakhlagh M, Sahebi R, Sadeghi R, Ferns GA, Ghayour-Mobarhan M. The Effects of Vitamin D Fortified Products on Bone Biomarkers: A Systematic Review and Meta-Analysis. Iran J Public Health. 2022;51(2):278-291.
