Maternal serum retinol, 25(OH)D and 1,25(OH)2D concentrations during pregnancy and peak bone mass and trabecular bone score in adult offspring at 26-year follow-up


Autoři: Chandima N. D. Balasuriya aff001;  Tricia L. Larose aff001;  Mats P. Mosti aff001;  Kari Anne I. Evensen aff001;  Geir W. Jacobsen aff005;  Per M. Thorsby aff007;  Astrid Kamilla Stunes aff001;  Unni Syversen aff001
Působiště autorů: Department of Clinical and Molecular Medicine, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, NTNU, Trondheim, Norway aff001;  Department of Endocrinology, St. Olavs Hospital, Trondheim University Hospital, Trondheim, Norway aff002;  K.G. Jebsen Center for Genetic Epidemiology, Department of Public Health and Nursing, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, NTNU, Trondheim, Norway aff003;  St. Olavs Hospital, Trondheim University Hospital, Trondheim, Norway aff004;  Department of Public Health and Nursing, Norwegian University of Science and Technology, NTNU, Trondheim, Norway aff005;  Department of Physiotherapy, Trondheim Municipality, Trondheim, Norway aff006;  Hormone Laboratory, Department of Medical biochemistry, Oslo University Hospital Aker Hospital, Oslo, Norway aff007
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222712

Souhrn

Background

Vitamin A and D deficiency is prevalent in pregnant women worldwide. Both vitamins are involved in fetal skeletal development. A positive association between maternal vitamin D levels and offspring bone mineral density (BMD) at adulthood has been observed. The impact of maternal vitamin A status in pregnancy on offspring peak bone mass remains unclear.

Method and findings

Forty-one mother-child pairs were recruited from a population-based prospective cohort study in Trondheim, Norway, where pregnant women were followed from gestational week 17. Their term-born infants were followed from birth (1986–88). Regression analyses were performed for vitamin A (retinol), 25-hydroxyvitamin D [25(OH)D] and 1,25-dihydroxyvitamin D [1,25(OH)2D] in maternal serum (gestational weeks 17, 33, 37) and cord blood. Offspring BMD and spine trabecular bone score (TBS), a measure of bone quality, were analyzed by dual x-ray absorptiometry at 26 years. Average levels during pregnancy of retinol, 25(OH)D and 1,25(OH)2D were 1.66 (0.32) μmol/L, 59.0 (20.6) nmol/L, and 251.3 (62.4) pmol/L, respectively. 1,25(OH)2D levels were similar in those with 25(OH)D levels <30 and >75 nmol/L. After adjustment for maternal age, BMI, smoking, and education, and offspring birth weight, maternal serum retinol was positively associated with offspring spine BMD [mean change 30.8 (CI 7.6, 54.0) mg/cm2 per 0.2 μmol/L retinol], and with offspring TBS, although non-significant (p = 0.08). No associations were found between maternal 25(OH)D and 1,25(OH)2D levels and offspring bone parameters. Vitamin levels in cord blood were not associated with offspring BMD or TBS.

Conclusions

This is the first study to show an association between maternal vitamin A status and offspring peak bone mass. Our findings may imply increase future risk for osteoporotic fracture in offspring of mothers with suboptimal vitamin A level. No associations were observed between 25(OH)D and 1,25(OH)2D and offspring BMD.

Klíčová slova:

Birth weight – Bone fracture – Hip – Pregnancy – Vitamin D – Vitamin D deficiency – Vitamin A – Bone development


Zdroje

1. Cooper C, Westlake S, Harvey N, Javaid K, Dennison E, Hanson M. Review: developmental origins of osteoporotic fracture. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 2006;17(3):337–47. Epub 2005/12/07. doi: 10.1007/s00198-005-2039-5 16331359.

2. Wood CL, Stenson C, Embleton N. The Developmental Origins of Osteoporosis. Current genomics. 2015;16(6):411–8. Epub 2015/12/. doi: 10.2174/1389202916666150817202217 27018386.

3. WHO. Global Prevalence of Vitamin A Deficiency in Populations at Risk 1995–2005. WHO Global Database on Vitamin A Deficiency. World Health Organization; Geneva, Switzerland. 2009.

4. Bastos Maia S, Rolland Souza AS, Costa Caminha MdF, Lins da Silva S, Callou Cruz RdSBL, Carvalho Dos Santos C, et al. Vitamin A and Pregnancy: A Narrative Review. Nutrients. 2019;11(3):681. doi: 10.3390/nu11030681 30909386.

5. Palacios C, Gonzalez L. Is vitamin D deficiency a major global public health problem? The Journal of steroid biochemistry and molecular biology. 2014;144 Pt A:138–45. Epub 2013/11/19. doi: 10.1016/j.jsbmb.2013.11.003 24239505; PubMed Central PMCID: PMC4018438.

6. Spiro A, Buttriss JL. Vitamin D: An overview of vitamin D status and intake in Europe. Nutrition bulletin. 2014;39(4):322–50. Epub 2015/01/31. doi: 10.1111/nbu.12108 25635171; PubMed Central PMCID: PMC4288313.

7. Gustafsson MK, Romundstad PR, Stafne SN, Helvik AS, Stunes AK, Morkved S, et al. Alterations in the vitamin D endocrine system during pregnancy: A longitudinal study of 855 healthy Norwegian women. PloS one. 2018;13(4):e0195041. Epub 2018/04/12. doi: 10.1371/journal.pone.0195041 29641551; PubMed Central PMCID: PMC5895009.

8. Blomhoff R, Blomhoff HK. Overview of retinoid metabolism and function. Journal of neurobiology. 2006;66(7):606–30. Epub 2006/05/12. doi: 10.1002/neu.20242 16688755.

9. Niemeier A, Niedzielska D, Secer R, Schilling A, Merkel M, Enrich C, et al. Uptake of postprandial lipoproteins into bone in vivo: impact on osteoblast function. Bone. 2008;43(2):230–7. Epub 2008/06/10. doi: 10.1016/j.bone.2008.03.022 18538644.

10. Soprano DR, Qin P, Soprano KJ. Retinoic acid receptors and cancers. Annual review of nutrition. 2004;24:201–21. Epub 2004/06/11. doi: 10.1146/annurev.nutr.24.012003.132407 15189119.

11. Conaway HH, Henning P, Lerner UH. Vitamin a metabolism, action, and role in skeletal homeostasis. Endocrine reviews. 2013;34(6):766–97. Epub 2013/05/31. doi: 10.1210/er.2012-1071 23720297.

12. See AW, Kaiser ME, White JC, Clagett-Dame M. A nutritional model of late embryonic vitamin A deficiency produces defects in organogenesis at a high penetrance and reveals new roles for the vitamin in skeletal development. Dev Biol. 2008;316(2):171–90. Epub 2008/03/07. doi: 10.1016/j.ydbio.2007.10.018 18321479.

13. Handel MN, Moon RJ, Titcombe P, Abrahamsen B, Heitmann BL, Calder PC, et al. Maternal serum retinol and beta-carotene concentrations and neonatal bone mineralization: results from the Southampton Women's Survey cohort. The American journal of clinical nutrition. 2016;104(4):1183–8. Epub 2016/09/16. doi: 10.3945/ajcn.116.130146 27629051; PubMed Central PMCID: PMC5039809.

14. Zhang J, Chalmers MJ, Stayrook KR, Burris LL, Wang Y, Busby SA, et al. DNA binding alters coactivator interaction surfaces of the intact VDR-RXR complex. Nature structural & molecular biology. 2011;18(5):556–63. Epub 2011/04/12. doi: 10.1038/nsmb.2046 21478866; PubMed Central PMCID: PMC3087838.

15. Elder CJ, Bishop NJ. Rickets. The Lancet. 2014;383(9929):1665–76. https://doi.org/10.1016/S0140-6736(13)61650-5

16. Kovacs CS. Maternal Mineral and Bone Metabolism During Pregnancy, Lactation, and Post-Weaning Recovery. Physiol Rev. 2016;96(2):449–547. Epub 2016/02/19. doi: 10.1152/physrev.00027.2015 26887676.

17. Hollis BW, Johnson D, Hulsey TC, Ebeling M, Wagner CL. Vitamin D supplementation during pregnancy: double-blind, randomized clinical trial of safety and effectiveness. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research. 2011;26(10):2341–57. Epub 2011/06/28. doi: 10.1002/jbmr.463 21706518; PubMed Central PMCID: PMC3183324.

18. Zhu K, Whitehouse AJ, Hart PH, Kusel M, Mountain J, Lye S, et al. Maternal vitamin D status during pregnancy and bone mass in offspring at 20 years of age: a prospective cohort study. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research. 2014;29(5):1088–95. Epub 2013/11/06. doi: 10.1002/jbmr.2138 24189972.

19. Javaid MK, Crozier SR, Harvey NC, Gale CR, Dennison EM, Boucher BJ, et al. Maternal vitamin D status during pregnancy and childhood bone mass at age 9 years: a longitudinal study. Lancet. 2006;367(9504):36–43. Epub 2006/01/10. doi: 10.1016/S0140-6736(06)67922-1 16399151.

20. Lawlor DA, Wills AK, Fraser A, Sayers A, Fraser WD, Tobias JH. Association of maternal vitamin D status during pregnancy with bone-mineral content in offspring: a prospective cohort study. Lancet. 2013;381(9884):2176–83. Epub 2013/03/23. doi: 10.1016/S0140-6736(12)62203-X 23518316; PubMed Central PMCID: PMC3691477.

21. Garcia AH, Erler NS, Jaddoe VW, Tiemeier H, van den Hooven EH, Franco OH, et al. 25-hydroxyvitamin D concentrations during fetal life and bone health in children aged 6 years: a population-based prospective cohort study. The lancet Diabetes & endocrinology. 2017. Epub 2017/03/06. doi: 10.1016/s2213-8587(17)30064-5. 28259646.

22. Lim LS, Harnack LJ, Lazovich D, Folsom AR. Vitamin A intake and the risk of hip fracture in postmenopausal women: the Iowa Women's Health Study. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 2004;15(7):552–9. Epub 2004/02/05. doi: 10.1007/s00198-003-1577-y 14760518; PubMed Central PMCID: PMC2020807.

23. Caire-Juvera G, Ritenbaugh C, Wactawski-Wende J, Snetselaar LG, Chen Z. Vitamin A and retinol intakes and the risk of fractures among participants of the Women's Health Initiative Observational Study. The American journal of clinical nutrition. 2009;89(1):323–30. Epub 2008/12/06. doi: 10.3945/ajcn.2008.26451 19056568; PubMed Central PMCID: PMC2715292.

24. Mata-Granados JM, Cuenca-Acevedo R, Luque de Castro MD, Sosa M, Quesada-Gomez JM. Vitamin D deficiency and high serum levels of vitamin A increase the risk of osteoporosis evaluated by Quantitative Ultrasound Measurements (QUS) in postmenopausal Spanish women. Clinical biochemistry. 2010;43(13–14):1064–8. Epub 2010/07/06. doi: 10.1016/j.clinbiochem.2010.06.001 20599880.

25. Mata-Granados JM, Cuenca-Acevedo JR, Luque de Castro MD, Holick MF, Quesada-Gomez JM. Vitamin D insufficiency together with high serum levels of vitamin A increases the risk for osteoporosis in postmenopausal women. Archives of osteoporosis. 2013;8:124. Epub 2013/02/19. doi: 10.1007/s11657-013-0124-5 23417776.

26. Tata JR. Signalling through nuclear receptors. Nature reviews Molecular cell biology. 2002;3(9):702–10. Epub 2002/09/05. doi: 10.1038/nrm914 12209130.

27. Bakketeig LS, Jacobsen GW, Hoffman HJ, Lindmark G, Bergsjo P, Molne K, et al. Pre-pregnancy risk factors for small-for-gestational age births among parous women in Scandinavia. Acta obstetrica et gynecologica Scandinavica. 1993;72:273–9.

28. Kanis JA, McCloskey EV, Johansson H, Oden A, Strom O, Borgstrom F. Development and use of FRAX in osteoporosis. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 2010;21 Suppl 2:S407–13. Epub 2010/05/22. doi: 10.1007/s00198-010-1253-y 20464374.

29. Hans D, Goertzen AL, Krieg MA, Leslie WD. Bone microarchitecture assessed by TBS predicts osteoporotic fractures independent of bone density: the Manitoba study. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research. 2011;26(11):2762–9. Epub 2011/09/03. doi: 10.1002/jbmr.499 21887701.

30. Hyde NK, Brennan-Olsen SL, Wark JD, Hosking SM, Holloway KL, Pasco JA. Maternal vitamin D and offspring trabecular bone score. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 2017. Epub 2017/09/05. doi: 10.1007/s00198-017-4208-8 28868588.

31. Weaver CM, Gordon CM, Janz KF, Kalkwarf HJ, Lappe JM, Lewis R, et al. The National Osteoporosis Foundation's position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 2016;27(4):1281–386. Epub 2016/02/10. doi: 10.1007/s00198-015-3440-3 26856587; PubMed Central PMCID: PMC4791473.

32. Kaiser ME, Merrill RA, Stein AC, Breburda E, Clagett-Dame M. Vitamin A deficiency in the late gastrula stage rat embryo results in a one to two vertebral anteriorization that extends throughout the axial skeleton. Dev Biol. 2003;257(1):14–29. Epub 2003/04/25. doi: 10.1016/s0012-1606(03)00044-7 12710954.

33. De Luca F, Uyeda JA, Mericq V, Mancilla EE, Yanovski JA, Barnes KM, et al. Retinoic acid is a potent regulator of growth plate chondrogenesis. Endocrinology. 2000;141(1):346–53. Epub 1999/12/30. doi: 10.1210/endo.141.1.7283 10614657.

34. Delgado-Calle J, Garmilla P, Riancho JA. Do epigenetic marks govern bone mass and homeostasis? Current genomics. 2012;13(3):252–63. Epub 2012/11/02. doi: 10.2174/138920212800543129 23115526; PubMed Central PMCID: PMC3382279.

35. Bar-El Dadon S, Reifen R. Vitamin A and the epigenome. Critical reviews in food science and nutrition. 2017;57(11):2404–11. Epub 2015/11/14. doi: 10.1080/10408398.2015.1060940 26565606.

36. Green AC, Martin TJ, Purton LE. The role of vitamin A and retinoic acid receptor signaling in post-natal maintenance of bone. J Steroid Biochem Mol Biol. 2016;155(Pt A):135–46. Epub 2015/10/06. doi: 10.1016/j.jsbmb.2015.09.036 26435449.

37. Mattinzoli D, Messa P, Corbelli A, Ikehata M, Zennaro C, Armelloni S, et al. A novel model of in vitro osteocytogenesis induced by retinoic acid treatment. European cells & materials. 2012;24:403–25. Epub 2012/11/20. 23160992.

38. Green AC, Poulton IJ, Vrahnas C, Hausler KD, Walkley CR, Wu JY, et al. RARgamma is a negative regulator of osteoclastogenesis. The Journal of steroid biochemistry and molecular biology. 2015;150:46–53. Epub 2015/03/25. doi: 10.1016/j.jsbmb.2015.03.005 25800721.

39. Fetahu IS, Hobaus J, Kallay E. Vitamin D and the epigenome. Front Physiol. 2014;5:164. Epub 2014/05/09. doi: 10.3389/fphys.2014.00164 24808866; PubMed Central PMCID: PMC4010791.

40. Harvey NC, Sheppard A, Godfrey KM, McLean C, Garratt E, Ntani G, et al. Childhood bone mineral content is associated with methylation status of the RXRA promoter at birth. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research. 2014;29(3):600–7. Epub 2013/08/03. doi: 10.1002/jbmr.2056 23907847; PubMed Central PMCID: PMC3836689.

41. Moon RJ, Harvey NC, Cooper C. ENDOCRINOLOGY IN PREGNANCY: Influence of maternal vitamin D status on obstetric outcomes and the fetal skeleton. European journal of endocrinology. 2015;173(2):R69–83. Epub 2015/04/12. doi: 10.1530/EJE-14-0826 25862787; PubMed Central PMCID: PMC4968635.

42. Cruz S, Matos A, da Cruz SP, Pereira S, Saboya C, Ramalho A. Relationship between the Nutritional Status of Vitamin A per Trimester of Pregnancy with Maternal Anthropometry and Anemia after Roux-en-Y Gastric Bypass. Nutrients. 2017;9(9). Epub 2017/09/09. doi: 10.3390/nu9090989 28885564; PubMed Central PMCID: PMC5622749.

43. Faure H, Preziosi P, Roussel AM, Bertrais S, Galan P, Hercberg S, et al. Factors influencing blood concentration of retinol, α-tocopherol, vitamin C, and β-carotene in the French participants of the SU.VI.MAX trial. European Journal of Clinical Nutrition. 2006;60(6):706–17. doi: 10.1038/sj.ejcn.1602372 16391586

44. Wu AM, Huang CQ, Lin ZK, Tian NF, Ni WF, Wang XY, et al. The relationship between vitamin A and risk of fracture: meta-analysis of prospective studies. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research. 2014;29(9):2032–9. Epub 2014/04/05. doi: 10.1002/jbmr.2237 24700407.

45. Chen GD, Zhu YY, Cao Y, Liu J, Shi WQ, Liu ZM, et al. Association of dietary consumption and serum levels of vitamin A and beta-carotene with bone mineral density in Chinese adults. Bone. 2015;79:110–5. Epub 2015/06/02. doi: 10.1016/j.bone.2015.05.028 26027509.

46. Holvik K, Ahmed LA, Forsmo S, Gjesdal CG, Grimnes G, Samuelsen SO, et al. No increase in risk of hip fracture at high serum retinol concentrations in community-dwelling older Norwegians: the Norwegian Epidemiologic Osteoporosis Studies. The American journal of clinical nutrition. 2015;102(5):1289–96. Epub 2015/09/18. doi: 10.3945/ajcn.115.110528 26377161.

47. Sommer A, Davidson FR. Assessment and control of vitamin A deficiency: the Annecy Accords. The Journal of nutrition. 2002;132(9 Suppl):2845s–50s. Epub 2002/09/11. doi: 10.1093/jn/132.9.2845S 12221259.

48. McCauley ME, van den Broek N, Dou L, Othman M. Vitamin A supplementation during pregnancy for maternal and newborn outcomes. Cochrane Database Syst Rev. 2015;(10):Cd008666. Epub 2015/10/28. doi: 10.1002/14651858.CD008666.pub3 26503498.

49. Haugen M, Brantsaeter AL, Alexander J, Meltzer HM. Dietary supplements contribute substantially to the total nutrient intake in pregnant Norwegian women. Annals of nutrition & metabolism. 2008;52(4):272–80. Epub 2008/07/23. doi: 10.1159/000146274 18645244; PubMed Central PMCID: PMC2813797.

50. Yakoob MY, Lo CW. Nutrition (Micronutrients) in Child Growth and Development: A Systematic Review on Current Evidence, Recommendations and Opportunities for Further Research. J Dev Behav Pediatr. 2017;38(8):665–79. Epub 2017/07/27. doi: 10.1097/DBP.0000000000000482 28746059.

51. Checkley W, West KP, Wise RA, Baldwin MR, Wu L, LeClerq SC, et al. Maternal Vitamin A Supplementation and Lung Function in Offspring. New England Journal of Medicine. 2010;362(19):1784–94. doi: 10.1056/NEJMoa0907441 20463338.

52. Bastos Maia S, Costa Caminha MF, Lins da Silva S, Rolland Souza AS, Carvalho Dos Santos C, Batista Filho M. The Prevalence of Vitamin A Deficiency and Associated Factors in Pregnant Women Receiving Prenatal Care at a Reference Maternity Hospital in Northeastern Brazil. Nutrients. 2018;10(9). Epub 2018/09/13. doi: 10.3390/nu10091271 30205601; PubMed Central PMCID: PMC6165532.

53. Soliman A, Salama H, Alomar S, Shatla E, Ellithy K, Bedair E. Clinical, biochemical, and radiological manifestations of vitamin D deficiency in newborns presented with hypocalcemia. Indian J Endocrinol Metab. 2013;17(4):697–703. Epub 2013/08/21. doi: 10.4103/2230-8210.113764 23961489; PubMed Central PMCID: PMC3743373.

54. Wirth JP, Petry N, Tanumihardjo SA, Rogers LM, McLean E, Greig A, et al. Vitamin A Supplementation Programs and Country-Level Evidence of Vitamin A Deficiency. Nutrients. 2017;9(3). Epub 2017/03/02. doi: 10.3390/nu9030190 28245571; PubMed Central PMCID: PMC5372853.

55. Thompson PD, Remus LS, Hsieh JC, Jurutka PW, Whitfield GK, Galligan MA, et al. Distinct retinoid X receptor activation function-2 residues mediate transactivation in homodimeric and vitamin D receptor heterodimeric contexts. Journal of molecular endocrinology. 2001;27(2):211–27. Epub 2001/09/21. 11564604.


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