Abstract
Breastfeeding has been associated with several short- and long-term health benefits, including positive cognitive and behavioral outcomes. However, the impact of breastfeeding on structural brain development over time remains unclear. We aimed to assess the association between breastfeeding duration in childhood and the developmental trajectory of overall cortical thickness, cortical area, and total intracranial volume during the transition from childhood to early adulthood. Participants included 670 children and adolescents with 1326 MRI scans acquired over 8 years from the Brazilian High-Risk Cohort for Mental Conditions (BHRCS). Breastfeeding was assessed using a questionnaire answered by the parents. Brain measures were estimated using MRI T1-weighted images at three time points, with 3-year intervals. Data were evaluated using generalized additive models adjusted for multiple confounders. We found that a longer breastfeeding duration was directly associated with higher global cortical thickness in the left (edf = 1.0, F = 6.07, p = 0.01) and right (edf = 1.0, F = 4.70, p = 0.03) hemispheres. For the total intracranial volume, we found an interaction between duration of breastfeeding and developmental stage (edf = 1.0, F = 6.81, p = 0.009). No association was found between breastfeeding duration and brain area. Our study suggests that the duration of breastfeeding impacts overall cortical thickness and the development of total brain volume, but not area. This study adds to the evidence on the potential impact of breastfeeding on brain development and provides relevant insights into the mechanisms by which breastfeeding might confer cognitive and mental health benefits.
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References
WHO Collaborative Study Team on the Role of Breastfeeding on the Prevention of Infant Mortality (2000) Effect of breastfeeding on infant and child mortality due to infectious diseases in less developed countries: a pooled analysis. Lancet Lond Engl 355:451–455
Hitchcock NE, Gracey M, Gilmour AI (1985) The growth of breast fed and artificially fed infants from birth to twelve months. Acta Paediatr Scand 74:240–245. https://doi.org/10.1111/j.1651-2227.1985.tb10957.x
Hoefer C, Hardy MC (1929) Later development of breast fed and artifically fed infants: comparison of physical and mental growth. J Am Med Assoc 92:615–619. https://doi.org/10.1001/jama.1929.02700340015006
Anderson JW, Johnstone BM, Remley DT (1999) Breast-feeding and cognitive development: a meta-analysis. Am J Clin Nutr 70:525–535. https://doi.org/10.1093/ajcn/70.4.525
Bernardo H, Cesar V, Organization WH (2013) Long-term effects of breastfeeding: a systematic review. World Health Organization
Horta BL, Bas A, Bhargava SK, Fall CHD, Feranil A, de Kadt J, Martorell R, Richter LM, Stein AD, Victora CG, COHORTS Group (2013) Infant feeding and school attainment in five cohorts from low- and middle-income countries. PLoS ONE 8:e71548. https://doi.org/10.1371/journal.pone.0071548
Horwood LJ, Fergusson DM (1998) Breastfeeding and later cognitive and academic outcomes. Pediatrics 101:E9. https://doi.org/10.1542/peds.101.1.e9
Richards M, Hardy R, Wadsworth MEJ (2002) Long-term effects of breast-feeding in a national birth cohort: educational attainment and midlife cognitive function. Public Health Nutr 5:631–635. https://doi.org/10.1079/PHN2002338
Victora CG, Horta BL, de Mola CL, Quevedo L, Pinheiro RT, Gigante DP, Gonçalves H, Barros FC (2015) Association between breastfeeding and intelligence, educational attainment, and income at 30 years of age: a prospective birth cohort study from Brazil. Lancet Glob Health 3:e199–e205. https://doi.org/10.1016/S2214-109X(15)70002-1
Núñez C, García-Alix A, Arca G, Agut T, Carreras N, Portella MJ, Stephan-Otto C Breastfeeding duration is associated with larger cortical gray matter volumes in children from the ABCD study. J Child Psychol Psychiatry. https://doi.org/10.1111/jcpp.13790
Ou X, Andres A, Pivik RT, Cleves MA, Snow JH, Ding Z, Badger TM (2016) Voxel-based morphometry and fMRI revealed differences in brain gray matter in breastfed and milk formula-fed children. AJNR Am J Neuroradiol 37:713–719. https://doi.org/10.3174/ajnr.A4593
Solis-Urra P, Esteban-Cornejo I, Cadenas-Sanchez C, Rodriguez-Ayllon M, Mora-Gonzalez J, Migueles JH, Labayen I, Verdejo-Román J, Kramer AF, Erickson KI, Hillman CH, Catena A, Ortega FB (2019) Early life factors, gray matter brain volume and academic performance in overweight/obese children: the ActiveBrains project. Neuroimage 202:116130. https://doi.org/10.1016/j.neuroimage.2019.116130
Higgins RC, Keller KL, Aruma JC, Masterson TD, Adise S, Fearnbach N, Stein WM, English LK, Fuchs B, Pearce AL (2022) Influence of exclusive breastfeeding on hippocampal structure, satiety responsiveness, and weight status. Matern Child Nutr 18:e13333. https://doi.org/10.1111/mcn.13333
Koshiyama D, Okada N, Ando S, Koike S, Yahata N, Morita K, Sawada K, Morita S, Kawakami S, Kanata S, Fujikawa S, Sugimoto N, Toriyama R, Masaoka M, Araki T, Kano Y, Endo K, Yamasaki S, Nishida A, Hiraiwa-Hasegawa M, Kasai K (2020) Association between duration of breastfeeding based on maternal reports and dorsal and ventral striatum and medial orbital gyrus volumes in early adolescence. Neuroimage 220:117083. https://doi.org/10.1016/j.neuroimage.2020.117083
Kafouri S, Kramer M, Leonard G, Perron M, Pike B, Richer L, Toro R, Veillette S, Pausova Z, Paus T (2013) Breastfeeding and brain structure in adolescence. Int J Epidemiol 42:150–159. https://doi.org/10.1093/ije/dys172
Isaacs EB, Fischl BR, Quinn BT, Chong WK, Gadian DG, Lucas A (2010) Impact of breast milk on intelligence quotient, brain size, and white matter development. Pediatr Res 67:357–362. https://doi.org/10.1203/PDR.0b013e3181d026da
Deoni SCL, Dean DC, Piryatinsky I, O’Muircheartaigh J, Waskiewicz N, Lehman K, Han M, Dirks H (2013) Breastfeeding and early white matter development: a cross-sectional study. Neuroimage 82:77–86. https://doi.org/10.1016/j.neuroimage.2013.05.090
Kar P, Reynolds JE, Grohs MN, Bell RC, Jarman M, Dewey D, Lebel C (2021) Association between breastfeeding during infancy and white matter microstructure in early childhood. Neuroimage 236:118084. https://doi.org/10.1016/j.neuroimage.2021.118084
Sullivan G, Vaher K, Blesa M, Galdi P, Stoye DQ, Quigley AJ, Thrippleton MJ, Norrie J, Bastin ME, Boardman JP (2023) Breast milk exposure is associated with cortical maturation in preterm infants. Ann Neurol 93:591–603. https://doi.org/10.1002/ana.26559
Belfort MB, Anderson PJ, Nowak VA, Lee KJ, Molesworth C, Thompson DK, Doyle LW, Inder TE (2016) Breast milk feeding, brain development, and neurocognitive outcomes: a 7-year longitudinal study in infants born at less than 30 weeks’ gestation. J Pediatr 177:133-139.e1. https://doi.org/10.1016/j.jpeds.2016.06.045
Ottolini KM, Andescavage N, Kapse K, Jacobs M, Limperopoulos C (2020) Improved brain growth and microstructural development in breast milk–fed very low birth weight premature infants. Acta Paediatr 109:1580–1587. https://doi.org/10.1111/apa.15168
Victora CG, Bahl R, Barros AJD, França GVA, Horton S, Krasevec J, Murch S, Sankar MJ, Walker N, Rollins NC, Lancet Breastfeeding Series Group (2016) Breastfeeding in the 21st century: epidemiology, mechanisms, and lifelong effect. Lancet Lond Engl 387:475–490. https://doi.org/10.1016/S0140-6736(15)01024-7
Salum GA, Gadelha A, Pan PM, Moriyama TS, Graeff-Martins AS, Tamanaha AC, Alvarenga P, Valle Krieger F, Fleitlich-Bilyk B, Jackowski A, Sato JR, Brietzke E, Polanczyk GV, Brentani H, de Jesus MJ, Do Rosário MC, Manfro GG, Bressan RA, Mercadante MT, Miguel EC, Rohde LA (2015) High risk cohort study for psychiatric disorders in childhood: rationale, design, methods and preliminary results. Int J Methods Psychiatr Res 24:58–73. https://doi.org/10.1002/mpr.1459
Fischl B (2012) FreeSurfer. Neuroimage 62:774–781. https://doi.org/10.1016/j.neuroimage.2012.01.021
Fischl B, Salat DH, van der Kouwe AJW, Makris N, Ségonne F, Quinn BT, Dale AM (2004) Sequence-independent segmentation of magnetic resonance images. Neuroimage 23(Suppl 1):S69-84. https://doi.org/10.1016/j.neuroimage.2004.07.016
Rosen AFG, Roalf DR, Ruparel K, Blake J, Seelaus K, Villa LP, Ciric R, Cook PA, Davatzikos C, Elliott MA, de La Garza AG, Gennatas ED, Quarmley M, Schmitt JE, Shinohara RT, Tisdall MD, Craddock RC, Gur RE, Gur RC, Satterthwaite TD (2018) Quantitative assessment of structural image quality. Neuroimage 169:407–418. https://doi.org/10.1016/j.neuroimage.2017.12.059
Zugman A, Harrewijn A, Cardinale EM, Zwiebel H, Freitag GF, Werwath KE, Bas-Hoogendam JM, Groenewold NA, Aghajani M, Hilbert K, Cardoner N, Porta-Casteràs D, Gosnell S, Salas R, Blair KS, Blair JR, Hammoud MZ, Milad M, Burkhouse K, Phan KL, Schroeder HK, Strawn JR, Beesdo-Baum K, Thomopoulos SI, Grabe HJ, Van der Auwera S, Wittfeld K, Nielsen JA, Buckner R, Smoller JW, Mwangi B, Soares JC, Wu M, Zunta-Soares GB, Jackowski AP, Pan PM, Salum GA, Assaf M, Diefenbach GJ, Brambilla P, Maggioni E, Hofmann D, Straube T, Andreescu C, Berta R, Tamburo E, Price R, Manfro GG, Critchley HD, Makovac E, Mancini M, Meeten F, Ottaviani C, Agosta F, Canu E, Cividini C, Filippi M, Kostić M, Munjiza A, Filippi CA, Leibenluft E, Alberton BAV, Balderston NL, Ernst M, Grillon C, Mujica-Parodi LR, van Nieuwenhuizen H, Fonzo GA, Paulus MP, Stein MB, Gur RE, Gur RC, Kaczkurkin AN, Larsen B, Satterthwaite TD, Harper J, Myers M, Perino MT, Yu Q, Sylvester CM, Veltman DJ, Lueken U, Van der Wee NJA, Stein DJ, Jahanshad N, Thompson PM, Pine DS, Winkler AM (2020) Mega-analysis methods in ENIGMA: the experience of the generalized anxiety disorder working group. Hum Brain Mapp 43:255–277. https://doi.org/10.1002/hbm.25096
Victora CG, Barros FC (2006) Cohort profile: the 1982 Pelotas (Brazil) birth cohort study. Int J Epidemiol 35:237–242. https://doi.org/10.1093/ije/dyi290
Ministério da Saúde (2020) Caderneta da Criança—Menino, 2nd edn
Sørensen Ø, Walhovd KB, Fjell AM (2021) A recipe for accurate estimation of lifespan brain trajectories, distinguishing longitudinal and cohort effects. Neuroimage 226:117596. https://doi.org/10.1016/j.neuroimage.2020.117596
Hedman AM, van Haren NEM, Schnack HG, Kahn RS, Hulshoff Pol HE (2011) Human brain changes across the life span: a review of 56 longitudinal magnetic resonance imaging studies. Hum Brain Mapp 33:1987–2002. https://doi.org/10.1002/hbm.21334
Gogtay N, Thompson PM (2010) Mapping Gray Matter Development: implications for typical development and vulnerability to psychopathology. Brain Cogn 72:6. https://doi.org/10.1016/j.bandc.2009.08.009
Paus T (2005) Mapping brain maturation and cognitive development during adolescence. Trends Cogn Sci 9:60–68. https://doi.org/10.1016/j.tics.2004.12.008
Córdova-Palomera A, Fatjó-Vilas M, Falcón C, Bargalló N, Alemany S, Crespo-Facorro B, Nenadic I, Fañanás L (2015) Birth weight and adult IQ, but not anxious-depressive psychopathology, are associated with cortical surface area: a study in twins. PLoS ONE 10:e0129616. https://doi.org/10.1371/journal.pone.0129616
Skranes J, Løhaugen GCC, Martinussen M, Håberg A, Brubakk A-M, Dale AM (2013) Cortical surface area and IQ in very-low-birth-weight (VLBW) young adults. Cortex J Devoted Study Nerv Syst Behav 49:2264–2271. https://doi.org/10.1016/j.cortex.2013.06.001
Xiang M, Alfvén G, Blennow M, Trygg M, Zetterström R (2000) Long-chain polyunsaturated fatty acids in human milk and brain growth during early infancy. Acta Paediatr Oslo Nor 1992 89:142–147. https://doi.org/10.1080/080352500750028735
Tallima H, El Ridi R (2017) Arachidonic acid: physiological roles and potential health benefits—a review. J Adv Res 11:33–41. https://doi.org/10.1016/j.jare.2017.11.004
Krol KM, Grossmann T (2018) Psychological effects of breastfeeding on children and mothers. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 61:977–985. https://doi.org/10.1007/s00103-018-2769-0
Ratsika A, Codagnone MC, O’Mahony S, Stanton C, Cryan JF (2021) Priming for life: early life nutrition and the microbiota-gut-brain axis. Nutrients 13:423. https://doi.org/10.3390/nu13020423
Funding
This study was financed by with grants from the National Institute of Development Psychiatric for Children and Adolescent (INPD; Grants: CNPq 465550/2014-2, FAPESP 2014/50917-0, and European Research Council [FP7/2007-2013]/Grant 337673, The Medical Research Council-United Kingdom).
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LG and GS conceptualized and designed the study, carried out the initial analyses, drafted the initial manuscript, and critically reviewed and revised the manuscript. DT, LR, EM, PP, AJ and AZ critically reviewed and revised the manuscript. All the authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.
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Grevet, L.T., Teixeira, D.S., Pan, P.M. et al. The association between duration of breastfeeding and the trajectory of brain development from childhood to young adulthood: an 8-year longitudinal study. Eur Child Adolesc Psychiatry (2023). https://doi.org/10.1007/s00787-023-02283-9
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DOI: https://doi.org/10.1007/s00787-023-02283-9