Maternal vitamin D status and the relationship with neonatal anthropometric and childhood neurodevelopmental outcomes: Results from the Seychelles child development nutrition study

Nutrients

Volumn 9, Issue 11, 2017, Pages

  Laird, Eamon ^a   Thurston, Sally W ^b   van Wijngaarden, Edwin ^b   Shamlaye, Conrad F ^c   Myers, Gary J ^b   Davidson, Philip W ^b   Watson, Gene E ^b   McSorley, Emeir M ^d   Mulhern, Maria S ^d   Yeates, Alison J ^d   Ward, Mary ^d   McNulty, Helene ^d   Strain, J J ^d  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^c MINISTRY OF HEALTH   (Seychelles)

^d UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

Birth; Childhood; Health; Neurodevelopment; Pregnancy; Vitamin D

Indexed keywords

25 HYDROXYVITAMIN D; VITAMIN D; 25-HYDROXYVITAMIN D; BIOLOGICAL MARKER;

ADULT; ANTHROPOMETRY; ARTICLE; AUDITORY COMPREHENSION TEST; BIRTH WEIGHT; CHILD; CHILD BEHAVIOR CHECKLIST; CHILD DEVELOPMENT; DISEASE ASSOCIATION; FEMALE; FINGER TAPPING TEST; GESTATIONAL AGE; HEAD CIRCUMFERENCE; HUMAN; KAUFMAN BRIEF INTELLIGENCE TEST; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; MATERNAL NUTRITION; MATERNAL SERUM; MENTAL DISEASE; NEWBORN; NORMAL HUMAN; NUTRITIONAL STATUS; OUTCOME ASSESSMENT; PEDIATRIC REVIEW OF CHILDRENS ENVIRONMENTAL SUPPORT AND STIMULATION; PRESCHOOL LANGUAGE SCALE; SCORING SYSTEM; VERBAL ABILITY SCORE; VITAMIN SUPPLEMENTATION; WOODCOCK-JOHNSON SCHOLASTIC ACHIEVEMENT TEST; AGE; ANALOGS AND DERIVATIVES; ANATOMY AND HISTOLOGY; BLOOD; CHILD BEHAVIOR; COGNITION; GROWTH, DEVELOPMENT AND AGING; HEAD; INFANT; MALE; MULTIVARIATE ANALYSIS; NERVOUS SYSTEM; NUTRITION; PREGNANCY; PRESCHOOL CHILD; SEASON; SEYCHELLES; STATISTICAL MODEL; SUNLIGHT;

ADULT; AGE FACTORS; BIOMARKERS; BIRTH WEIGHT; CHILD BEHAVIOR; CHILD DEVELOPMENT; CHILD, PRESCHOOL; COGNITION; FEMALE; HEAD; HUMANS; INFANT; INFANT, NEWBORN; LINEAR MODELS; MALE; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MULTIVARIATE ANALYSIS; NERVOUS SYSTEM; NUTRITION SURVEYS; NUTRITIONAL STATUS; PREGNANCY; SEASONS; SEYCHELLES; SUNLIGHT; VITAMIN D;

EID: 85034430852     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu9111235     Document Type: Article

References (65)

1. McGrath, J. Does ‘imprinting’ with low prenatal vitamin D contribute to the risk of various adult disorders? Med. Hypotheses 2001, 56, 367–371.
2. Hutchison, F.N.; Bell, N.H. Osteomalacia and rickets. Semin. Nephrol. 1992, 12, 127–145.
3. Karras, S.N.; Fakhoury, H.; Muscogiuri, G.; Grant, W.B.; van den Ouweland, J.M.; Colao, A.M.; Kosta, K. Maternal vitamin D levels during pregnancy and neonatal health: Evidence to date and clinical implications. Ther. Adv. Musculoskelet. Dis. 2016, 8, 124–135.
4. Marya, R.K.; Rathee, S.; Lata, V.; Mudgil, S. Effects of vitamin D supplementation in pregnancy. Gynecol. Obstet. Investig. 1981, 12, 155–161.
5. Mannion, C.A.; Gray-Donald, K.; Koski, K.G. Association of low intake of milk and vitamin D during pregnancy with decreased birth weight. CMAJ 2006, 174, 1273–1277.
6. Bodnar, L.M.; Catov, J.M.; Zmuda, J.M.; Cooper, M.E.; Parrott, M.S.; Roberts, J.M.; Marazita, M.L.; Simhan, H.N. Maternal serum 25-hydroxyvitamin D concentrations are associated with small-for-gestational age births in white women. J. Nutr. 2010, 140, 999–1006.
7. Chen, Y.H.; Fu, L.; Hao, J.H.; Yu, Z.; Zhu, P.; Wang, H.; Xu, Y.Y.; Zhang, C.; Tao, F.B.; Xu, D.X. Maternal vitamin D deficiency during pregnancy elevates the risks of small for gestational age and low birth weight infants in Chinese population. J. Clin. Endocrinol. Metab. 2015, 100, 1912–1919.
8. Javaid, M.K.; Crozier, S.R.; Harvey, N.C.; Gale, C.R.; Dennison, E.M.; Boucher, B.J.; Arden, N.K.; Godfrey, K.M.; Cooper, C. Maternal vitamin D status during pregnancy and childhood bone mass at age 9 years: A longitudinal study. Lancet 2006, 367, 36–43.
9. Prentice, A.; Jarjou, L.; Goldberg, G.R.; Bennett, J.; Cole, T.J.; Schoenmakers, I. Maternal plasma 25-hydroxyvitamin D concentration and birthweight, growth and bone mineral accretion of Gambian infants. Acta Paediatr. 2009, 98, 1360–1362.
10. Farrant, H.J.; Krishnaveni, G.V.; Hill, J.C.; Boucher, B.J.; Fisher, D.J.; Noonan, K.; Osmond, C.; Veena, S.R.; Fall, C.H. Vitamin D insufficiency is common in Indian mothers but is not associated with gestational diabetes or variation in newborn size. Eur. J. Clin. Nutr. 2009, 63, 646–652.
11. Morales, E.; Guxens, M.; Llop, S.; Rodriguez-Bernal, C.L.; Tardon, A.; Riano, I.; Ibarluzea, J.; Lertxundi, N.; Espada, M.; Rodriguez, A.; et al. Circulating 25-hydroxyvitamin D3 in pregnancy and infant neuropsychological development. Pediatrics 2012, 130, e913–e920.
12. Whitehouse, A.J.; Holt, B.J.; Serralha, M.; Holt, P.G.; Kusel, M.M.; Hart, P.H. Maternal serum vitamin D levels during pregnancy and offspring neurocognitive development. Pediatrics 2012, 129, 485–493.
13. Whitehouse, A.J.; Holt, B.J.; Serralha, M.; Holt, P.G.; Hart, P.H.; Kusel, M.M. Maternal vitamin D levels and the autism phenotype among offspring. J. Autism Dev. Disord. 2013, 43, 1495–1504.
14. Zhu, P.; Tong, S.L.; Hao, J.H.; Tao, R.X.; Huang, K.; Hu, W.B.; Zhou, Q.F.; Jiang, X.M.; Tao, F.B. Cord blood vitamin D and neurocognitive development are nonlinearly related in toddlers. J. Nutr. 2015, 145, 1232–1238.
15. Eyles, D.W.; Smith, S.; Kinobe, R.; Hewison, M.; McGrath, J.J. Distribution of the vitamin D receptor and 1 alpha-hydroxylase in human brain. J. Chem. Neuroanat. 2005, 29, 21–30.
16. Van Etten, E.; Mathieu, C. Immunoregulation by 1, 25-dihydroxyvitamin D3: Basic concepts. J. Steroid Biochem. Mol. Biol. 2005, 97, 93–101.
17. Almeras, L.; Eyles, D.; Benech, P.; Laffite, D.; Villard, C.; Patatian, A.; Boucraut, J.; Mackay-Sim, A.; McGrath, J.; Féron, F. Developmental vitamin D deficiency alters brain protein expression in the adult rat: Implications for neuropsychiatric disorders. Proteomics 2007, 7, 769–780.
18. Holick, M.F. Vitamin D: Importance in the prevention of cancers, type 1 diabetes, heart disease, and osteoporosis. Am. J. Clin. Nutr. 2004, 79, 362–371.
19. Webb, A.R. Who, what, where and when-influences on cutaneous vitamin D synthesis. Prog. Biophys. Mol. Biol. 2006, 92, 17–25.
20. Laird, E.; Ward, M.; McSorley, E.; Strain, J.J.; Wallace, J. Vitamin D and bone health; potential mechanisms. Nutrients 2010, 2, 693–724.
21. Holden, J.M.; Lemar, L.E.; Exler, J. Vitamin D in foods: Development of the US Department of Agriculture database. Am. J. Clin. Nutr. 2008, 87, 1092S–1096S.
22. Harnack, L.J.; Steffrn, L.; Zhou, X.; Luepker, R.V. Trends in vitamin D intake from food sources among adults in the Minneapolis-St Paul, MN, Metropolitan Area, 1980–82 through 2007–2009. J. Am. Diet. Assoc. 2011, 111, 1329–1334.
23. Holmes, V.A.; Barnes, M.S.; Alexander, H.D.; McFaul, P.; Wallace, J.M. Vitamin D deficiency and insufficiency in pregnant women: A longitudinal study. Br. J. Nutr. 2009, 102, 876–881.
24. O’Riordan, M.N.; Kiely, M.; Higgins, J.R.; Cashman, K.D. Prevalence of sub-optimal vitamin D status during pregnancy. Ir. Med. J. 2008, 101, 242–243.
25. Bodnar, L.M.; Catov, J.M.; Simhan, H.N.; Holick, M.F.; Powers, R.W.; Roberts, J.M. Maternal vitamin D deficiency increases the risk of pre-enclampsia. J. Clin. Endocrinol. Metab. 2007, 92, 3517–3522.
26. Wagner, C.L.; Hollis, B.W.; Kotsa, K.; Fakhoury, H.; Karras, S.N. Vitamin D administration during pregnancy as prevention for pregnancy, neonatal and postnatal complications. Rev. Endocr. Metab. Disord. 2017, 18, 1–6.
27. Amrein, K.; Quraishi, S.A.; Litonjua, A.A.; Gibbons, F.K.; Pieber, T.R.; Camargo, C.A., Jr.; Giovannucci, E.; Christopher, K.B. Evidence for a U-shaped relationship between pre-hospital vitamin D status and mortality: A cohort study. J. Clin. Endocrinol. Metab. 2014, 99, 1461–1469.
28. Bleicher, K.; Cumming, R.G.; Naganathan, V.; Blyth, F.M.; Le Couteur, D.G.; Handelsman, D.J.; Waite, L.M.; Seibel, M.J. U-shaped association between serum 25-hydroxyvitamin D and fracture risk in older men: Results from the prospective population-based CHAMP study. J. Bone Miner. Res. 2014, 29, 2024–2031.
29. Durup, D.; Jorgensen, H.L.; Christensen, J.; Tjønneland, A.; Olsen, A.; Halkjær, J.; Lind, B.; Heegaard, A.M.; Schwarz, P. A reverse J-shaped association between serum 25-hydroxyvitamin D and cardiovascular disease mortality-the CopD-study. J. Clin. Endocrinol. Metab. 2015, 100, 2339–2346.
30. Pan, P.; Jin, D.H.; Chatterjee-Chakraborty, M.; Halievski, K.; Lawson, D.; Remedios, D.; Smetka, C.; Pinto, V.; Parra, E.; Fleming, A.S. The effects of vitamin D3 during pregnancy and lactation on offspring physiology and behavior in sprague-dawley rats. Dev. Psychobiol. 2014, 56, 12–22.
31. Rayco-Solon, P.; Fulford, A.J.; Prentice, A.M. Differential effects of seasonality on preterm birth and intrauterine growth restriction in rural Africans. Am. J. Clin. Nutr. 2005, 81, 134–139.
32. McNeil, S.A.; Dodds, L.A.; Fell, D.B.; Allen, V.M.; Halperin, B.A.; Steinhoff, M.C.; MacDonald, N.E. Effect of respiratory hospitalization during pregnancy on infant outcomes. Am. J. Obstet. Gynecol. 2011, 204, S54–S57.
33. Davidson, P.W.; Strain, J.J.; Myers, G.J.; Thurston, S.W.; Bonham, M.P.; Shamlaye, C.F.; Stokes-Riner, A.; Wallace, J.M.; Robson, P.J.; Duffy, E.M.; et al. Neurodevelopmental effects of maternal nutritional status and exposure to methylmercury from eating fish during pregnancy. Neurotoxicology 2008, 29, 767–775.
34. Strain, J.J.; Davidson, P.W.; Bonham, M.P.; Duffy, E.M.; Stokes-Riner, A.; Thurston, S.W.; Wallace, J.M.; Robson, P.J.; Shamlaye, C.F.; Georger, L.A.; et al. Associations of maternal long-chain polyunsaturated fatty acids, methyl mercury, and infant development in the Seychelles Child Development Nutrition Study. Neurotoxicology 2008, 29, 776–782.
35. Bonham, M.; Duffy, E.; Wallace, J.; Robson, P.J.; Myers, G.J.; Davidson, P.W.; Clarkson, T.W.; Shamlaye, C.F.; Strain, J.J. Habitual fish consumption does not prevent a decrease in LCPUFA status in pregnant women (The Seychelles child development nutrition study). Prostaglandins Leukot. Essent. Fat. Acids 2008, 78, 343–350.
36. Institute of Medicine. Dietary Reference Intakes for Calcium and Vitamin D; The National Academies Press: Washington, DC, USA, 2011.
37. Watson, G.E.; van Wijngaarden, E.; Love, T.M.T.; Duffy, E.M.; Bonham, M.P.; Mulhern, M.S.; Yeates, A.J.; Davidson, P.W.; Shamlaye, C.F.; Strain, J.J.; et al. Neurodevelopmental outcomes at 5 years in children exposed prenatally to maternal dental amalgam: The Seychelles Child Development Nutrition Study. Neurotoxicol. Teratol. 2013, 39, 57–62.
38. Bischoff-Ferrari, H.A. Optimal serum 25-hydroxyvitamin D levels for multiple health outcomes. Adv. Exp. Med. Biol. 2014, 810, 500–525.
39. Darling, A.L.; Rayman, M.P.; Steer, C.D.; Golding, J.; Lanham-New, S.A.; Bath, S.C. Association between maternal vitamin D status in pregnancy and neurodevelopmental outcomes in childhood: Results from the Avon Longitudinal Study of Parents and Children (ALSPAC). Br. J. Nutr. 2017, 117, 1682–1692.
40. Strøm, M.; Halldorsson, T.I.; Hansen, S.; Granström, C.; Maslova, E.; Petersen, S.B.; Cohen, A.S.; Olsen, S.F. Vitamin D measured in maternal serum and offspring neurodevelopmental outcomes: A prospective study with long-term follow-up. Ann. Nutr. Metab. 2014, 64, 254–261.
41. Gale, C.R.; Robinson, S.M.; Harvey, N.C.; Javaid, M.K.; Jiang, B.; Martyn, C.N.; Godfrey, K.M.; Cooper, C. Maternal vitamin D status during pregnancy and child outcomes. Eur. J. Clin. Nutr. 2008, 62, 68–77.
42. Ong, Y.L.; Quah, P.L.; Tint, M.T.; Aris, I.M.; Chen, L.W.; van Dam, R.M.; Heppe, D.; Saw, S.M.; Godfrey, K.M.; Gluckman, P.D.; et al. The association of maternal vitamin D status with infant birth outcomes, postnatal growth and adiposity in the first 2 years of life in a multi-ethnic Asian population: The Growing Up in Singapore Towards healthy Outcomes (GUSTO) cohort study. Br. J. Nutr. 2016, 116, 621–631.
43. Morales, E.; Rodriguez, A.; Valvi, D.; Iniguez, C.; Esplugues, A.; Vioque, J.; Marina, L.S.; Jimenez, A.; Espada, M.; Dehli, C.R.; et al. Deficit of vitamin D in pregnancy and growth and overweight in the offspring. Int. J. Obes. (London) 2015, 39, 61–68.
44. De-Regil, L.M.; Palacios, C.; Ansary, A.; Kulier, R.; Peña-Rosas, J.P. Vitamin D supplementation for women during pregnancy. Cochrane Database Syst. Rev. 2012, 2, CD008873.
45. Brough, L.; Rees, G.A.; Crawford, M.A.; Morton, R.H.; Dorman, E.K. Effect of multiple-micronutrient supplementation on maternal nutrient status, infant birth weight and gestational age at birth in a low-income, multi-ethnic population. Br. J. Nutr. 2010, 104, 437–445.
46. Hashemipour, S.; Ziaee, A.; Javadi, A.; Movahed, F.; Elmizadeh, K.; Javadi, E.H.; Lalooha, F. Effect of treatment of vitamin D deficiency and insufficiency during pregnancy on fetal growth indices and maternal weight gain: A randomized clinical trial. Eur. J. Obstet. Gynecol. Reprod. Biol. 2014, 172, 15–19.
47. Kalra, P.; Das, V.; Agarwal, A.; Kumar, M.; Ramesh, V.; Bhatia, E.; Gupta, S.; Singh, S.; Saxena, P.; Bhatia, V. Effect of vitamin D supplementation during pregnancy on neonatal mineral homeostasis and anthropometry of the newborn and infant. Br. J. Nutr. 2012, 108, 1052–1058.
48. Lisonkova, S.; Joseph, K.S. Incidence of preeclampsia: Risk factors and outcomes associated with early-versus late-onset disease. Am. J. Obstet. Gynecol. 2013, 209, 544:e1–544:e12.
49. Darling, A.L.; Hart, K.H.; Gibbs, M.A.; Gossiel, F.; Kantermann, T.; Horton, K.; Johnsen, S.; Berry, J.L.; Skene, D.J.; Eastell, R.; et al. Greater seasonal cycling of 25-hydroxyvitamin D is associated with increased parathyroid hormone and bone resorption. Osteoporos. Int. 2014, 25, 933–941.
50. Grant, W.B.; Bhattoa, H.P.; Boucher, B.J. Seasonal variations of U.S. mortality rates: Roles of solar ultraviolet-B doses, vitamin D, gene exp ression, and infections. J. Steroid Biochem. Mol. Biol. 2017, 173, 5–12.
51. Martineau, A.R.; Jolliffe, D.A.; Hooper, R.L.; Greenberg, L.; Aloia, J.F.; Bergman, P.; Dubnov-Raz, G.; Esposito, S.; Ganmaa, D.; Ginde, A.A.; et al. Vitamin D supplementation to prevent acute respiratory tract infections: Systematic review and meta-analysis of individual participant data. BMJ 2017, 356, i6583.
52. Shi, L.; Fatemi, S.H.; Sidwell, R.W.; Patterson, P.H. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J. Neurosci. 2003, 23, 297–302.
53. Shi, L.; Smith, S.E.; Malkova, N.; Tse, D.; Su, Y.; Patterson, P.H. Activation of the maternal immune system alters cerebellar development in the offspring. Brain Behav. Immun. 2009, 23, 116–123.
54. Nicolaidou, P.; Hatzistamatiou, Z.; Papadopoulou, A.; Kaleyias, J.; Floropoulou, E.; Lagona, E.; Tsagris, V.; Costalos, C.; Antsaklis, A. Low vitamin D status in mother-newborn pairs in Greece. Calcif. Tissue Int. 2006, 78, 337–342.
55. Luxwolda, M.F.; Kuipers, R.S.; Kema, I.P.; van der Veer, E.; Dijck-Brouwer, D.J.; Muskiet, F.A. Vitamin D status indicators in indigenous populations in East Africa. Eur. J. Nutr. 2013, 52, 1115–1125.
56. Hien, V.T.; Lam, N.T.; Skeaff, C.M.; Todd, J.; McLean, J.M.; Green, T.J. Vitamin D status of pregnant and non-pregnant women of reproductive age living in Hanoi City and the Hai Duong province of Vietnam. Matern. Child Nutr. 2012, 8, 533–539.
57. Charatcharoenwitthaya, N.; Nanthakomon, T.; Somprasit, C.; Chanthasenanont, A.; Chailurkit, L.O.; Pattaraarchachai, J.; Ongphiphadhanakul, B. Maternal vitamin D status, its associated factors and the course of pregnancy in Thai women. Clin. Endocrinol. (Oxford) 2013, 78, 126–133.
58. Figueiredo, A.C.; Trujillo, J.; Freitas-Vilela, A.A.; Franco-Sena, A.B.; Rebelo, F.; Cunha, G.M.; de Castro, M.B.; Farnum, A.; Mokhtar, R.R.; Holick, M.F.; et al. Association between plasma concentrations of vitamin D metabolites and depressive symptoms throughout pregnancy in a prospective cohort of Brazilian women. J. Psychiatr. Res. 2017, 95, 1–8.
59. Bonham, M.P.; Duffy, E.M.; Robson, P.J.; Wallace, J.M.; Myers, G.J.; Davidson, P.W.; Clarkson, T.W.; Shamlaye, C.F.; Strain, J.J.; Livingstone, M.B. Contribution of fish to intakes of micronutrients important for fetal development: A dietary survey of pregnant women in the Republic of Seychelles. Public Health Nutr. 2009, 12, 1312–1320.
60. Lehmann, U.; Gjessing, H.R.; Hirche, F.; Mueller-Belecke, A.; Gudbrandsen, O.A.; Ueland, P.M.; Mellgren, G.; Lauritzen, L.; Lindqvist, H.; Hansen, A.L.; et al. Efficacy of fish intake on vitamin D status: A meta-analysis of randomized controlled trials. Am. J. Clin. Nutr. 2015, 102, 837–847.
61. Dietary Reference Values for Food Energy and Nutrients for the United Kingdom. Report of the Panel on Dietary Reference Values of the Committee on Medical Aspects of Food Policy; Report 41; HMSO: London, UK, 1997.
62. Food Safety Authority of Ireland (FSAI). Recommended Dietary Allowances for Ireland; Government Publications Sales Office: Dublin, Ireland, 1999.
63. Cashman, K.D.; Hill, T.R.; Lucey, A.J.; Taylor, N.; Seamans, K.M.; Muldowney, S.; FitzGerald, A.P.; Flynn, A.; Barnes, M.S.; Horigan, G.; et al. Estimation of the dietary requirement for vitamin D in healthy adults. Am. J. Clin. Nutr. 2008, 88, 1535–1542.
64. McGowan, C.A.; Byrne, J.; Walsh, J.; McAuliffe, F.M. Insufficient vitamin D intakes among pregnant women. Eur. J. Clin. Nutr. 2011, 65, 1076–1078.
65. Jensen, C.B.; Petersen, S.B.; Granström, C.; Maslova, E.; Mølgaard, C.; Olsen, S.F. Sources and determinants of vitamin D intake in Danish pregnant women. Nutrients 2012, 4, 259–272.