Weight Status and Visceral Adiposity Mediate the Relation between Exclusive Breastfeeding Duration and Skin Carotenoids in Later Childhood

Ruyu Liu, Caitlyn G Edwards, Corinne N Cannavale, Isabel R Flemming, Morgan R Chojnacki, Ginger E Reeser, Samantha J Iwinski, Lisa M Renzi-Hammond, Naiman A Khan, Ruyu Liu, Caitlyn G Edwards, Corinne N Cannavale, Isabel R Flemming, Morgan R Chojnacki, Ginger E Reeser, Samantha J Iwinski, Lisa M Renzi-Hammond, Naiman A Khan

Abstract

Background: Breastfeeding is associated with healthier weight and nutrient status in early life. However, the impact of breastfeeding on carotenoid status beyond infancy, and the influence of adiposity, are unknown.

Objectives: The aim of the study was to retrospectively investigate the relation between breastfeeding and carotenoid status, and the mediating effect of weight status and adiposity on this relation, among school-age children.

Methods: This was a secondary analysis of baseline data collected from a randomized-controlled clinical trial. Children 7-12 y old (n = 81) were recruited from East-Central Illinois. DXA was used to assess visceral adipose tissue (VAT) and whole-body total fat percentage (%Fat; i.e., whole-body adiposity). Weight was obtained to calculate children's BMI percentiles. Skin carotenoids were assessed via reflection spectroscopy. Macular carotenoids were assessed as macular pigment optical density (MPOD). Dietary, birth, and breastfeeding information was self-reported by parents.

Results: Skin carotenoids were inversely related to %Fat (P < 0.01), VAT (P < 0.01), and BMI percentile (P < 0.01). VAT and BMI percentile significantly mediated this relation between exclusive breastfeeding duration and skin carotenoids, after adjustment for dietary carotenoids, energy intake, and mother education.

Conclusions: Weight status and adipose tissue distribution mediate the positive correlation between exclusive breastfeeding duration and skin carotenoids among children aged 7-12 y. The results indicate the need to support breastfeeding and healthy physical growth in childhood for optimal carotenoid status.This trial was registered at clinicaltrials.gov as NCT03521349.

Keywords: adiposity; adolescents; body mass index; carotenoids; human milk; macular pigment; pediatric; reflection spectroscopy.

© The Author(s) 2021. Published by Oxford University Press on behalf of the American Society for Nutrition.

Figures

FIGURE 1
FIGURE 1
Comparison of mean Veggie Meter scores between subjects split by median exclusive breastfeeding duration (5 mo).
FIGURE 2
FIGURE 2
Results of mediation regression analyses for (A) BMI percentile and (B) VAT without covariates. VAT, visceral adipose tissue.
FIGURE 3
FIGURE 3
Results of mediation regression analyses for (A) BMI percentile and (B) VAT adjusting for total energy intake, total carotenoid intake, and mother education. VAT, visceral adipose tissue.

References

    1. Johnson EJ. The role of carotenoids in human health. Nutr Clin Care. 2002;5:56–65.
    1. Parker RS. Absorption, metabolism, and transport of carotenoids. FASEB J. 1996;10(5):542–51.
    1. Walk AM, Edwards CG, Baumgartner NW, Chojnacki MR, Covello AR, Reeser GE, Hammond BR, Renzi-Hammond LM, Khan NA. The role of retinal carotenoids and age on neuroelectric indices of attentional control among early to middle-aged adults. Front Aging Neurosci. 2017;9:183.
    1. Saint S, Renzi-Hammond L, Khan N, Hillman C, Frick J, Hammond B. The macular carotenoids are associated with cognitive function in preadolescent children. Nutrients. 2018;10(2):193.
    1. Ermakov IV, Sharifzadeh M, Ermakova M, Gellermann W. Resonance Raman detection of carotenoid antioxidants in living human tissue. J Biomed Opt. 2005;10(6):064028.
    1. Stahl W, Sies H. Carotenoids and flavonoids contribute to nutritional protection against skin damage from sunlight. Mol Biotechnol. 2007;37(1):26–30.
    1. Hammond BR, Ciulla TA, Snodderly DM. Macular pigment density is reduced in obese subjects. Invest Ophthalmol Vis Sci. 2002;43(1):47–50.
    1. Scarmo S, Henebery K, Peracchio H, Cartmel B, Lin H, Ermakov IV, Gellermann W, Bernstein PS, Duffy VB, Mayne ST. Skin carotenoid status measured by resonance Raman spectroscopy as a biomarker of fruit and vegetable intake in preschool children. Eur J Clin Nutr. 2012;66(5):555–60.
    1. Suzuki K, Inoue T, Hioki R, Ochiai J, Kusuhara Y, Ichino N, Osakabe K, Hamajima N, Ito Y. Association of abdominal obesity with decreased serum levels of carotenoids in a healthy Japanese population. Clin Nutr. 2006;25(5):780–9.
    1. Yan J, Liu L, Zhu Y, Huang G, Wang PP. The association between breastfeeding and childhood obesity: a meta-analysis. BMC Public Health. 2014;14:1267.
    1. Ortega-García JA, Kloosterman N, Alvarez L, Tobarra-Sánchez E, Cárceles-Álvarez A, Pastor-Valero R, López-Hernández FA, Sánchez-Solis M, Claudio L. Full breastfeeding and obesity in children: a prospective study from birth to 6 years. Child Obes. 2018;14(5):327–37.
    1. Gibson LA, Alava MH, Kelly MP, Campbell MJ. The effects of breastfeeding on childhood BMI: a propensity score matching approach. J Public Health (Oxf). 2017;39(4):e152–60.
    1. O'Tierney PF, Barker DJP, Osmond C, Kajantie E, Eriksson JG. Duration of breast-feeding and adiposity in adult life. J Nutr. 2009;139(2):422S–5S.
    1. Andersen LF, Jacobs DR, Gross MD, Schreiner PJ, Dale Williams O, Lee D-H. Longitudinal associations between body mass index and serum carotenoids: the CARDIA study. Br J Nutr. 2006;95(2):358–65.
    1. Ribaya-Mercado JD, Maramag CC, Tengco LW, Blumberg JB, Solon FS. Relationships of body mass index with serum carotenoids, tocopherols and retinol at steady-state and in response to a carotenoid-rich vegetable diet intervention in Filipino schoolchildren. Biosci Rep. 2008;28(2):97–106.
    1. Meinke MC, Lauer A, Taskoparan B, Gersonde I, Lademann J, Darvin ME. Influence on the carotenoid levels of skin arising from age, gender, body mass index in smoking/non-smoking individuals. Free Radic Antioxid. 2011;1(2):15–20.
    1. Burke JD, Curran Celentano J, Lariviere C, Gowdy-Johnson B. Macular pigment optical density (MPOD) profiles and body mass index in adults. Invest Ophthalmol Vis Sci. 2002;43(13):2543.
    1. Hales CM, Fryar CD, Carroll MD, Freedman DS, Ogden CL. Trends in obesity and severe obesity prevalence in US youth and adults by sex and age, 2007-2008 to 2015-2016. JAMA. 2018;319(16):1723–5.
    1. Ermakov IV, Ermakova M, Sharifzadeh M, Gorusupudi A, Farnsworth K, Bernstein PS, Stookey J, Evans J, Arana T, Tao-Lew Let al. . Optical assessment of skin carotenoid status as a biomarker of vegetable and fruit intake. Arch Biochem Biophys. 2018;646:46–54.
    1. Ermakov IV, Gellermann W. Dermal carotenoid measurements via pressure mediated reflection spectroscopy. J Biophoton. 2012;5(7):559–70.
    1. Wooten BR, Hammond BR, Land RI, Snodderly DM. A practical method for measuring macular pigment optical density. Invest Ophthalmol Vis Sci. 1999;40(11):2481–9.
    1. Renzi LM, Dengler MJ, Puente A, Miller LS, Hammond BR. Relationships between macular pigment optical density and cognitive function in unimpaired and mildly cognitively impaired older adults. Neurobiol Aging. 2014;35(7):1695–9.
    1. McCorkle SM, Raine LB, Hammond BR, Renzi-Hammond L, Hillman CH, Khan NA. Reliability of heterochromatic flicker photometry in measuring macular pigment optical density among preadolescent children. Foods. 2015;4(4):594–604.
    1. CDC . BMI percentile calculator for child and teen. [Internet]. Atlanta, GA: CDC; 2020. [Cited 2019 July 9]. Available from: .
    1. Goran MI, Driscoll P, Johnson R, Nagy TR, Hunter G. Cross-calibration of body-composition techniques against dual-energy X-ray absorptiometry in young children. Am J Clin Nutr. 1996;63(3):299–305.
    1. CDC . Clinical growth charts. [Internet]. Hyattsville, MD: National Center for Health Statistics; 2017. [Cited 2019 July 30]. Available from:.
    1. Fenton TR, Kim JH. A systematic review and meta-analysis to revise the Fenton growth chart for preterm infants. BMC Pediatr. 2013;13:59.
    1. Chojnacki MR, Holscher HD, Balbinot AR, Raine LB, Biggan JR, Walk AM, Kramer AF, Cohen NJ, Hillman CH, Khan NA. Relations between mode of birth delivery and timing of developmental milestones and adiposity in preadolescence: a retrospective study. Early Hum Dev. 2019;129:52–9.
    1. Preacher KJ, Kelley K. Effect size measures for mediation models: quantitative strategies for communicating indirect effects. Psychol Methods. 2011;16(2):93–115.
    1. Preacher KJ, Hayes AF. Contemporary approaches to assessing mediation in communication research. In: Hayes AF, Slater MD, Snyder LBeditors. The SAGE sourcebook of advanced data analysis methods for communication research. Thousand Oaks, CA: Sage Publications, Inc; 2014. p. 13–54.
    1. Aguilar SS, Wengreen HJ, Lefevre M, Madden GJ, Gast J. Skin carotenoids: a biomarker of fruit and vegetable intake in children. J Acad Nutr Diet. 2014;114(8):1174–80.
    1. Hayes AF. Communication monographs beyond Baron and Kenny: statistical mediation analysis in the new millennium. Commun Monogr. 2009;76(4):408–20.
    1. Ogden CL, Li Y, Freedman DS, Borrud LG, Flegal KM. Smoothed percentage body fat percentiles for U.S. children and adolescents 1999–2004. [Internet]. Natl Health Stat Report. 2011;43(9). [Cited 2019 July 30]. Available from: .
    1. American Psychological Association . Appendix 2. Estimated calorie needs per day, by age, sex, and physical activity level. 2015–2020 Dietary Guidelines. [Internet]. Washington (DC): US Department of Health and Human Services; 2015. [Cited 2019 July 30]. Available from:.
    1. Erdman JW Jr, Bierer TL, Gugger ET. Absorption and transport of carotenoids. Ann N Y Acad Sci. 1993;691:76–85.
    1. Bovier ER, Lewis RD, Hammond BR. The relationship between lutein and zeaxanthin status and body fat. Nutrients. 2013;5(3):750–7.
    1. Hassevoort KM, Khazoum SE, Walker JA, Barnett SM, Raine LB, Hammond BR, Renzi-Hammond LM, Kramer AF, Khan NA, Hillman CHet al. . Macular carotenoids, aerobic fitness, and central adiposity are associated differentially with hippocampal-dependent relational memory in preadolescent children. J Pediatr. 2017;183:108–14.e1.
    1. Zheng W, Zhang Z, Jiang K, Zhu J, He G, Ke B. Macular pigment optical density and its relationship with refractive status and foveal thickness in Chinese school-aged children. Curr Eye Res. 2013;38(1):168–73.
    1. Marseglia L, Manti S, D'Angelo G, Nicotera A, Parisi E, Di Rosa G, Gitto E, Arrigo T. Oxidative stress in obesity: a critical component in human diseases. Int J Mol Sci. 2014;16:378–400.
    1. Trieschmann M, Beatty S, Nolan JM, Hense HW, Heimes B, Austermann U, Fobker M, Pauleikhoff D. Changes in macular pigment optical density and serum concentrations of its constituent carotenoids following supplemental lutein and zeaxanthin: the LUNA study. Exp Eye Res. 2007;84(4):718–28.
    1. Hammond BR Jr, Johnson EJ, Russell RM, Krinsky NI, Yeum K-J, Edwards RB, Snodderly DM. Dietary modification of human macular pigment density. Invest Ophthalmol Vis Sci. 1997;38(9):1795–801.
    1. Borel P, Grolier P, Mekki N, Boirie Y, Rochette Y, Le Roy B, Alexandre-Gouabau MC, Lairon D, Azais-Braesco V. Low and high responders to pharmacological doses of β-carotene: proportion in the population, mechanisms involved and consequences on β-carotene metabolism. J Lipid Res. 1998;39(11):2250–60.
    1. Li B, Vachali P, Frederick JM, Bernstein PS. Identification of StARD3 as a lutein-binding protein in the macula of the primate retina. Biochemistry. 2011;50(13):2541–9.
    1. Bhosale P, Larson AJ, Frederick JM, Southwick K, Thulin CD, Bernstein PS. Identification and characterization of a Pi isoform of glutathione S-transferase (GSTP1) as a zeaxanthin-binding protein in the macula of the human eye. J Biol Chem. 2004;279(47):49447–54.
    1. Harder T, Bergmann R, Kallischnigg G, Plagemann A. Duration of breastfeeding and risk of overweight: a meta-analysis. Am J Epidemiol. 2005;162(5):397–403.
    1. Pannaraj PS, Li F, Cerini C, Bender JM, Yang S, Rollie A, Adisetiyo H, Zabih S, Lincez PJ, Bittinger Ket al. . Association between breast milk bacterial communities and establishment and development of the infant gut microbiome. JAMA Pediatr. 2017;171(7):647–54.
    1. Kallus SJ, Brandt LJ. The intestinal microbiota and obesity. J Clin Gastroenterol. 2012;46(1):16–24.
    1. Zivkovic AM, German JB, Lebrilla CB, Mills DA. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc Natl Acad Sci U S A. 2011;108(Suppl. 1):4653–8.
    1. Lawson MAE, O'Neill IJ, Kujawska M, Gowrinadh Javvadi S, Wijeyesekera A, Flegg Z, Chalklen L, Hall LJ. Breast milk-derived human milk oligosaccharides promote Bifidobacterium interactions within a single ecosystem. ISME J. 2020;14;635–48.
    1. Safavi M, Farajian S, Kelishadi R, Mirlohi M, Hashemipour M. The effects of synbiotic supplementation on some cardio-metabolic risk factors in overweight and obese children: a randomized triple-masked controlled trial. Int J Food Sci Nutr. 2013;64(6):687–93.
    1. Byrne ML, Schwartz OS, Simmons JG, Sheeber L, Whittle S, Allen NB. Duration of breastfeeding and subsequent adolescent obesity: effects of maternal behavior and socioeconomic status. J Adolesc Health. 2018;62(4):471–9.
    1. Pruszkowska-Przybylska P, Sitek A, Rosset I, Żądzińska E, Sobalska-Kwapis M, Słomka M, Strapagiel D. The association between socioeconomic status, duration of breastfeeding, parental age and birth parameters with BMI, body fat and muscle mass among prepubertal children in Poland. Anthropol Anz. 2019;76(5):409–19.
    1. Heck KE, Braveman P, Cubbin C, Chávez GF, Kiely JL. Socioeconomic status and breastfeeding initiation among California mothers. Public Health Rep. 2006;121(1):51–9.
    1. Rush E, Amoah I, Diep T, Jalili-Moghaddam S. Determinants and suitability of carotenoid reflection score as a measure of carotenoid status. Nutrients. 2020;12(1):113.
    1. Matsumoto M, Suganuma H, Shimizu S, Hayashi H, Sawada K, Tokuda I, Ihara K, Nakaji S. Skin carotenoid level as an alternative marker of serum total carotenoid concentration and vegetable intake correlates with biomarkers of circulatory diseases and metabolic syndrome. Nutrients. 2020;12(6):1825.
    1. Östh M, Öst A, Kjolhede P, Strålfors P. The concentration of β-carotene in human adipocytes, but not the whole-body adipocyte stores, is reduced in obesity. PLoS One. 2014;9(1):e85610.
    1. Chung H-Y, Ferreira ALA, Epstein S, Paiva SAR, Castaneda-Sceppa C, Johnson EJ. Site-specific concentrations of carotenoids in adipose tissue: relations with dietary and serum carotenoid concentrations in healthy adults. Am J Clin Nutr. 2009;90(3):533–9.
    1. Li R, Scanlon KS, Serdula MK. The validity and reliability of maternal recall of breastfeeding practice. Nutr Rev. 2005;63(4):103–10.
    1. Natland ST, Andersen LF, Nilsen TIL, Forsmo S, Jacobsen GW. Maternal recall of breastfeeding duration twenty years after delivery. BMC Med Res Methodol. 2012;12:179.
    1. CDC . Breastfeeding report card. [Internet]. Atlanta, GA: CDC. [Cited 2019 July 23]. Available from: .

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