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01-03-2021 | Original Contribution

Higher maternal plasma β-cryptoxanthin concentration is associated with better cognitive and motor development in offspring at 2 years of age

Authors: Jun S. Lai, Shirong Cai, Bee Lan Lee, Keith M. Godfrey, Peter D. Gluckman, Lynette P. Shek, Fabian Yap, Kok Hian Tan, Yap Seng Chong, Choon Nam Ong, Michael J. Meaney, Anne Rifkin-Graboi, Birit F. P. Broekman, Mary F. F. Chong

Published in: European Journal of Nutrition | Issue 2/2021

Abstract

Purpose

Current literature on the roles of α-, β-carotene and β-cryptoxanthin in neurocognitive function has largely focused on preventing cognitive decline in older people, and less on neuro-development in children. We examined the relations of maternal plasma carotenoids concentrations with offspring cognitive development up to age 4.5 years in the Growing Up in Singapore Towards healthy Outcomes mother–offspring cohort study.

Methods

Maternal plasma α-, β-carotene and β-cryptoxanthin concentrations at delivery were determined by ultra-performance liquid chromatography. Children’s cognition was assessed at ages 2 (Bayley Scales of Infant and Toddler Development) and 4.5 (Kaufman Brief Intelligence Test) years. Associations were examined in 419 mother–offspring pairs using linear regressions adjusting for key confounders.

Results

Median and interquartile range of maternal plasma concentrations (mg/L) were: α-carotene 0.052 (0.032, 0.081), β-carotene 0.189 (0.134, 0.286), and β-cryptoxanthin 0.199 (0.123, 0.304). In 2 years old children, higher maternal carotenoids [per standard deviation (SD) log-concentration] were positively associated with neurocognitive functions: β-cryptoxanthin with higher scores in cognitive [β = 0.18, (0.08, 0.28) SD], receptive language [β = 0.17 (0.07, 0.27) SD], fine motor [β = 0.16 (0.05, 0.26) SD], and gross motor [β = 0.16 (0.06, 0.27) SD] scales; β-carotene with higher cognitive score [β = 0.17 (0.05, 0.29) SD]. No significant associations were observed with neurocognitive functions at age 4.5 years.

Conclusion

Our study provides novel data suggesting a potential role of prenatal carotenoids, particularly β-cryptoxanthin, on early offspring cognitive and motor development. Whether the prenatal influences sustain beyond early childhood requires further investigation in longer term studies.

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Clark CA, Pritchard VE, Woodward LJ (2010) Preschool executive functioning abilities predict early mathematics achievement. Dev Psychol 46(5):1176–1191. https://doi.org/10.1037/a0019672CrossRefPubMed

Peet ED, McCoy DC, Danaei G, Ezzati M, Fawzi W, Jarvelin M-R, Pillas D, Fink G (2015) Early Childhood development and schooling attainment: longitudinal evidence from british, finnish and philippine birth cohorts. PLoS ONE 10(9):e0137219. https://doi.org/10.1371/journal.pone.0137219CrossRefPubMedPubMedCentral

Ross CE, Wu C-l (1995) The links between education and health. Am Sociol Rev 60(5):719–745. https://doi.org/10.2307/2096319CrossRef

Ross CE, Mirowsky J (1999) Refining the association between education and health: the effects of quantity, credential, and selectivity. Demography 36(4):445–460CrossRef

Crichton GE, Bryan J, Murphy KJ (2013) Dietary antioxidants, cognitive function and dementia—a systematic review. Plant Foods Hum Nutr 68(3):279–292. https://doi.org/10.1007/s11130-013-0370-0CrossRefPubMed

Rafnsson SB, Dilis V, Trichopoulou A (2013) Antioxidant nutrients and age-related cognitive decline: a systematic review of population-based cohort studies. Eur J Nutr 52(6):1553–1567. https://doi.org/10.1007/s00394-013-0541-7CrossRefPubMed

Wallace TC (2018) A comprehensive review of eggs, choline, and lutein on cognition across the life-span. J Am Coll Nutr 37(4):269–285. https://doi.org/10.1080/07315724.2017.1423248CrossRefPubMed

Johnson EJ (2014) Role of lutein and zeaxanthin in visual and cognitive function throughout the lifespan. Nutr Rev 72(9):605–612. https://doi.org/10.1111/nure.12133CrossRefPubMed

Vishwanathan R, Kuchan MJ, Sen S, Johnson EJ (2014) Lutein and preterm infants with decreased concentrations of brain carotenoids. J Pediatr Gastroenterol Nutr 59(5):659–665. https://doi.org/10.1097/MPG.0000000000000389CrossRefPubMed

10.

Walk AM, Khan NA, Barnett SM, Raine LB, Kramer AF, Cohen NJ, Moulton CJ, Renzi-Hammond LM, Hammond BR, Hillman CH (2017) From neuro-pigments to neural efficiency: the relationship between retinal carotenoids and behavioral and neuroelectric indices of cognitive control in childhood. Int J Psychophysiol 118:1–8. https://doi.org/10.1016/j.ijpsycho.2017.05.005CrossRefPubMedPubMedCentral

11.

Saint SE, Renzi-Hammond LM, Khan NA, Hillman CH, Frick JE, Hammond BR (2018) The macular carotenoids are associated with cognitive function in preadolescent children. Nutrients 10(2). doi: 10.3390/nu10020193

12.

Cheatham CL, Sheppard KW (2015) Synergistic effects of human milk nutrients in the support of infant recognition memory: an observational study. Nutrients 7(11):9079–9095. https://doi.org/10.3390/nu7115452CrossRefPubMedPubMedCentral

13.

Bohn T (2012) Provitamin a carotenoids: Occurrence, intake and bioavailability. In: Preedy VR (ed) Vitamin A and carotenoids: chemistry, analysis, function and effects. Royal Society of Chemistry, Cambridge, pp 142–161CrossRef

14.

Chen K, Zhang X, Wei XP, Qu P, Liu YX, Li TY (2009) Antioxidant vitamin status during pregnancy in relation to cognitive development in the first two years of life. Early Hum Dev 85(7):421–427CrossRef

15.

Liu Y, Chen Q, Wei X, Chen L, Zhang X, Chen K, Chen J, Li T (2015) Relationship between perinatal antioxidant vitamin and heavy metal levels and the growth and cognitive development of children at 5 years of age. Asia Pac J Clin Nutr 24(4):650–658PubMed

16.

Zhang X, Chen K, Wei XP, Qu P, Liu YX, Chen J, Li TY (2009) Perinatal vitamin A status in relation to neurodevelopmental outcome at two years of age. Int J Vitam Nutr Res 79(4):238–249CrossRef

17.

Cicero AFG, Colletti A (2017) Effects of carotenoids on health: are all the same? Results from clinical trials. Curr Pharm Des 23(17):2422–2427. https://doi.org/10.2174/1381612823666170207095459CrossRefPubMed

18.

Renzi-Hammond L, Bovier E, Fletcher L, Miller L, Mewborn C, Lindbergh C, Baxter J, Hammond B (2017) Effects of a lutein and zeaxanthin intervention on cognitive function: a randomized, double-masked, placebo-controlled trial of younger healthy adults. Nutrients 9(11):1246CrossRef

19.

Buonocore G, Tataranno ML, Perrone S (2011) Oxidative stress in fetal and neonatal brain development. Pediatr Res 70:118. https://doi.org/10.1038/pr.2011.343CrossRef

20.

Prof W, Sies H (2001) Effects of carotenoids and retinoids on gap junctional communication. BioFactors (Oxford, England) 15:95–98. https://doi.org/10.1002/biof.5520150209CrossRef

21.

Zielinska MA, Hamulka J, Grabowicz-Chądrzyńska I, Bryś J, Wesolowska A (2019) Association between breastmilk LC PUFA, carotenoids and psychomotor development of exclusively breastfed infants. Int J Environ Res Public Health 16(7):1144CrossRef

22.

Johnson EJ, Vishwanathan R, Johnson MA, Hausman DB, Davey A, Scott TM, Green RC, Miller LS, Gearing M, Woodard J, Nelson PT, Chung H-Y, Schalch W, Wittwer J, Poon LW (2013) Relationship between serum and brain carotenoids, α-tocopherol, and retinol concentrations and cognitive performance in the oldest old from the georgia centenarian study. J Aging Res 2013:951786. https://doi.org/10.1155/2013/951786CrossRefPubMedPubMedCentral

23.

Hu P, Bretsky P, Crimmins EM, Guralnik JM, Reuben DB, Seeman TE (2006) Association between serum beta-carotene levels and decline of cognitive function in high-functioning older persons with or without apolipoprotein E 4 alleles: MacArthur studies of successful aging. J Gerontol A Biol Sci Med Sci 61(6):616–620CrossRef

24.

Grodstein F, Kang JH, Glynn RJ, Cook NR, Gaziano JM (2007) A randomized trial of beta carotene supplementation and cognitive function in men: the physicians' health study II. Arch Intern Med 167(20):2184–2190. https://doi.org/10.1001/archinte.167.20.2184CrossRefPubMed

25.

Rinaldi P, Polidori MC, Metastasio A, Mariani E, Mattioli P, Cherubini A, Catani M, Cecchetti R, Senin U, Mecocci P (2003) Plasma antioxidants are similarly depleted in mild cognitive impairment and in Alzheimer's disease. Neurobiol Aging 24(7):915–919CrossRef

26.

Bolduc FV, Lau A, Rosenfelt CS, Langer S, Wang N, Smithson L, Lefebvre D, Alexander RT, Dickson CT, Li L, Becker AB, Subbarao P, Turvey SE, Pei J, Sears MR, Mandhane PJ, Investigators CS (2016) Cognitive enhancement in infants associated with increased maternal fruit intake during pregnancy: results from a birth cohort study with validation in an animal model. EBioMedicine 8:331–340. https://doi.org/10.1016/j.ebiom.2016.04.025CrossRefPubMedPubMedCentral

27.

O'Sullivan A, Fitzpatrick N, Doyle O (2017) Effects of early intervention on dietary intake and its mediating role on cognitive functioning: a randomised controlled trial. Public Health Nutr 20(1):154–164. https://doi.org/10.1017/S1368980016001877CrossRefPubMed

28.

Soh S-E, Tint MT, Gluckman PD, Godfrey KM, Rifkin-Graboi A, Chan YH, Stünkel W, Holbrook JD, Kwek K, Chong Y-S, Saw SM, Group tGS (2014) Cohort Profile: Growing Up in Singapore Towards healthy Outcomes (GUSTO) birth cohort study. Int J Epidemiol 43 (5):1401-1409. doi:10.1093/ije/dyt125

29.

Lee BL, Ong CN (2009) Comprehensive high-performance liquid chromatographic method for the measurements of lipophilic antioxidants in human plasma. J Chromatogr A 1216(15):3131–3137. https://doi.org/10.1016/j.chroma.2009.01.101CrossRefPubMed

30.

Bayley N (2006) Bayley scales of infant and toddler development: administration manual, 3rd edn. Psychorp, USA

31.

Kaufman AS, Kaufman NL (2013) Kaufman brief intelligence test, Second Edition. In: Encyclopedia of Special Education. John Wiley & Sons, Inc. doi:10.1002/9781118660584.ese1325

32.

Goh SKY, Tham EKH, Magiati I, Sim L, Sanmugam S, Qiu A, Daniel ML, Broekman BFP, Rifkin-Graboi A (2017) Analysis of item-level bias in the bayley-III language subscales: the validity and utility of standardized language assessment in a multilingual setting. J Speech Lang Hear Res 60(9):2663–2671. https://doi.org/10.1044/2017_jslhr-l-16-0196CrossRefPubMed

33.

Cai S, Pang WW, Low YL, Sim LW, Sam SC, Bruntraeger MB, Wong EQ, Fok D, Broekman BF, Singh L, Richmond J, Agarwal P, Qiu A, Saw SM, Yap F, Godfrey KM, Gluckman PD, Chong YS, Meaney MJ, Kramer MS, Rifkin-Graboi A (2015) Infant feeding effects on early neurocognitive development in Asian children. Am J Clin Nutr 101(2):326–336. https://doi.org/10.3945/ajcn.114.095414CrossRefPubMed

34.

Pang WW, Tan PT, Cai S, Fok D, Chua MC, Lim SB, Shek LP, Chan S-Y, Tan KH, Yap F, Gluckman PD, Godfrey KM, Meaney MJ, Broekman BFP, Kramer MS, Chong Y-S, Rifkin-Graboi A (2019) Nutrients or nursing?. Eur J Nutr, Understanding how breast milk feeding affects child cognition. https://doi.org/10.1007/s00394-019-01929-2CrossRef

35.

Ali H, Hamadani J, Mehra S, Tofail F, Hasan MI, Shaikh S, Shamim AA, Wu LS, West KP Jr, Christian P (2017) Effect of maternal antenatal and newborn supplementation with vitamin A on cognitive development of school-aged children in rural Bangladesh: a follow-up of a placebo-controlled, randomized trial. Am J Clin Nutr 106(1):77–87. https://doi.org/10.3945/ajcn.116.134478CrossRefPubMed

36.

Cox JL, Holden JM, Sagovsky R (1987) Detection of postnatal depression. Development of the 10-item Edinburgh postnatal depression scale. Br J Psychiatry 150:782–786CrossRef

37.

Spielberger CD (1984) State-trait anxiety inventory: a comprehensive bibliography. Consulting Psychologists Press, Palo Alto

38.

Han CY, Colega M, Quah EPL, Chan YH, Godfrey KM, Kwek K, Saw S-M, Gluckman PD, Chong Y-S, Chong MF-F, group obotGs (2015) A healthy eating index to measure diet quality in pregnant women in Singapore: a cross-sectional study. BMC Nutr 1(1):39. https://doi.org/10.1186/s40795-015-0029-3CrossRef

39.

Aris IM, Gandhi M, Cheung YB, Soh SE, Tint MT, Gluckman PD, Lee YS, Yap FK, Chong YS (2014) A new population-based reference for gestational age-specific size-at-birth of Singapore infants. Ann Acad Med Singapore 43(9):439–447PubMed

40.

Herlenius E, Lagercrantz H (2004) Development of neurotransmitter systems during critical periods. Exp Neurol 190(Suppl 1):S8–21. https://doi.org/10.1016/j.expneurol.2004.03.027CrossRefPubMed

41.

Vohr BR, Poggi Davis E, Wanke CA, Krebs NF (2017) Neurodevelopment: the impact of nutrition and inflammation during preconception and pregnancy in low-resource settings. Pediatrics 139(Suppl 1):S38–s49. https://doi.org/10.1542/peds.2016-2828FCrossRefPubMed

42.

Hj F, Mp A, Diane H (2015) The relationship between maternal education and children's academic outcomes: a theoretical framework. J Marriage Family 77(1):60–76. https://doi.org/10.1111/jomf.12156CrossRef

43.

Qiu A, Rifkin-Graboi A, Chen H, Chong YS, Kwek K, Gluckman PD, Fortier MV, Meaney MJ (2013) Maternal anxiety and infants' hippocampal development: timing matters. Transl Psychiatry 3:e306. https://doi.org/10.1038/tp.2013.79CrossRefPubMedPubMedCentral

44.

Burri BJ, La Frano MR, Zhu C (2016) Absorption, metabolism, and functions of β-cryptoxanthin. Nutr Rev 74(2):69–82. https://doi.org/10.1093/nutrit/nuv064CrossRefPubMedPubMedCentral

45.

Burri BJ (2015) Beta-cryptoxanthin as a source of vitamin A. J Sci Food Agric 95(9):1786–1794. https://doi.org/10.1002/jsfa.6942CrossRefPubMed

46.

Turner T, Burri BJ, Jamil KM, Jamil M (2013) The effects of daily consumption of β-cryptoxanthin–rich tangerines and β-carotene–rich sweet potatoes on vitamin A and carotenoid concentrations in plasma and breast milk of Bangladeshi women with low vitamin A status in a randomized controlled trial. Am J Clin Nutr 98(5):1200–1208. https://doi.org/10.3945/ajcn.113.058180CrossRefPubMed

47.

Fox SE, Levitt P, Nelson CA (2010) How the Timing and Quality of Early Experiences Influence the Development of Brain Architecture. Child Dev 81(1):28–40. https://doi.org/10.1111/j.1467-8624.2009.01380.xCrossRefPubMedPubMedCentral

48.

Eriksen H-LF, Kesmodel US, Underbjerg M, Kilburn TR, Bertrand J, Mortensen EL (2013) Predictors of intelligence at the age of 5: family, pregnancy and birth characteristics, postnatal influences, and postnatal growth. PLoS ONE 8(11):e79200. https://doi.org/10.1371/journal.pone.0079200CrossRefPubMedPubMedCentral

49.

Flores-Mendoza CE, Santiago BMC, Andrade DM, Fontes WP, Rodrigues LA, Tuma CAM (2017) Mothers-offspring resemblance in intelligence and its relationship to socioeconomic status. Paidéia (Ribeirão Preto) 27:98–106CrossRef

50.

Cusick SE, Georgieff MK (2016) The role of nutrition in brain development: the golden opportunity of the “first 1000 days”. J Pediatr 175:16–21. https://doi.org/10.1016/j.jpeds.2016.05.013CrossRefPubMedPubMedCentral

51.

Burrows TL, Williams R, Rollo M, Wood L, Garg ML, Jensen M, Collins CE (2015) Plasma carotenoid levels as biomarkers of dietary carotenoid consumption: a systematic review of the validation studies. J Nutr Intermed Metab 2(1):15–64. https://doi.org/10.1016/j.jnim.2015.05.001CrossRef

52.

Ritchie SJ, Tucker-Drob EM (2018) How Much Does Education Improve Intelligence? A Meta-Analysis Psychol Sci 29(8):1358–1369. https://doi.org/10.1177/0956797618774253CrossRefPubMed

Title: Higher maternal plasma β-cryptoxanthin concentration is associated with better cognitive and motor development in offspring at 2 years of age
Authors: Jun S. Lai
Shirong Cai
Bee Lan Lee
Keith M. Godfrey
Peter D. Gluckman
Lynette P. Shek
Fabian Yap
Kok Hian Tan
Yap Seng Chong
Choon Nam Ong
Michael J. Meaney
Anne Rifkin-Graboi
Birit F. P. Broekman
Mary F. F. Chong
Publication date: 01-03-2021
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Nutrition / Issue 2/2021
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI: https://doi.org/10.1007/s00394-020-02277-2

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