Breastfeeding improves dynamic reorganization of functional connectivity in preterm infants: a temporal brain network study

Substantial evidences have shown the benefits of breastfeeding to infants in terms of better nutrition and neurodevelopmental outcome. However, the relationship between brain development and feeding in preterm infants, who are physiologically and developmentally immature at birth, is only beginning to be quantitatively assessed, coinciding with the recent advent of neuroimaging techniques. In the current work, we studied a sample of 50 preterm infants-born between 29 and 33 weeks (32.20 ± 0.89 weeks) of gestational age, where 30 of them were breastfed and the remaining 20 were formula-fed. Resting-state functional magnetic resonance imaging (fMRI) was recorded around term-equivalent age (40.00 ± 1.31 weeks, range 39-44 weeks) using a 1.5-T scanner under sedation condition. Temporal brain networks were estimated by the correlation of sliding time-window time courses among regions of a predefined atlas. Through our newly introduced temporal efficiency approach, we examined, for the first time, the 3D spatiotemporal architecture of the temporal brain network. We found prominent temporal small-world properties in both groups, suggesting the arrangement of dynamic functional connectivity permits effective coordination of various brain regions for efficient information transfer over time at both local and global levels. More importantly, we showed that breastfed preterm infants exhibited greater temporal global efficiency in comparison with formula-fed preterm infants. Specifically, we found localized elevation of temporal nodal properties in the right temporal gyrus and bilateral caudate. Taken together, these findings provide new evidence to support the notion that breast milk promotes early brain development and cognitive function, which may have neurobiological and public health implications for parents and pediatricians.Breastfeeding has long been recognized to have beneficial effect on early neurodevelopment in infants. However, the influence of breastfeeding on reorganization of functional connectivity in preterm infants are largely unknown. To this end, we utilized our recently developed temporal brain network analysis framework to investigate the dynamic reorganization of brain functional connectivity in preterm infants fed with breast milk. We found that beyond an optimal temporal small-world topology, breastfed preterm infants exhibited improved network efficiency at both global and regional levels in comparisons with those of formula-fed infants. Graphical abstract: Breastfeeding has long been recognized to have beneficial effect on early neurodevelopment in infants. However, the influence of breastfeeding on reorganization of brain functional connectivity in preterm infants are largely unknown. To this end, we utilized our recently developed temporal brain network analysis framework to investigate the dynamic reorganization of functional connectivity in preterm infants fed with breast milk. We found that beyond an optimal temporal small-world topology, breastfed preterm infants exhibited improved network efficiency at both global and regional levels in comparisons with those of formula-fed infants.

[1]  Bruce N. Ames,et al.  Is docosahexaenoic acid, an n−3 long-chain polyunsaturated fatty acid, required for development of normal brain function? An overview of evidence from cognitive and behavioral tests in humans and animals , 2005 .

[2]  P. Guesnet,et al.  Docosahexaenoic acid (DHA) and the developing central nervous system (CNS) - Implications for dietary recommendations. , 2011, Biochimie.

[3]  Jonathan D. Power,et al.  The Development of Human Functional Brain Networks , 2010, Neuron.

[4]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[5]  M. Greicius,et al.  Persistent default‐mode network connectivity during light sedation , 2008, Human brain mapping.

[6]  D. Gadian,et al.  The Effect of Early Human Diet on Caudate Volumes and IQ , 2008, Pediatric Research.

[7]  Yu Chen,et al.  Temporal efficiency evaluation and small-worldness characterization in temporal networks , 2016, Scientific Reports.

[8]  Danielle S. Bassett,et al.  Dynamic graph metrics: Tutorial, toolbox, and tale , 2017, NeuroImage.

[9]  David Borsook,et al.  Resting-State Functional Connectivity in the Infant Brain: Methods, Pitfalls, and Potentiality , 2017, Front. Pediatr..

[10]  Jonathan O'Muircheartaigh,et al.  Breastfeeding and early white matter development: A cross-sectional study , 2013, NeuroImage.

[11]  Scott K Holland,et al.  Factors Determining Success of Awake and Asleep Magnetic Resonance Imaging Scans in Nonsedated Children , 2014, Neuropediatrics.

[12]  Anastasios Bezerianos,et al.  Disrupted Functional Brain Connectivity and Its Association to Structural Connectivity in Amnestic Mild Cognitive Impairment and Alzheimer’s Disease , 2014, PloS one.

[13]  Michael Breakspear,et al.  Towards a statistical test for functional connectivity dynamics , 2015, NeuroImage.

[14]  John H. Gilmore,et al.  Functional Connectivity of the Infant Human Brain , 2016, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[15]  H. Lagercrantz,et al.  The functional architecture of the infant brain as revealed by resting-state fMRI. , 2011, Cerebral cortex.

[16]  Dinggang Shen,et al.  Resting-state functional MRI studies on infant brains: A decade of gap-filling efforts , 2019, NeuroImage.

[17]  Peter Fransson,et al.  Resting-state networks in the infant brain , 2007, Proceedings of the National Academy of Sciences.

[18]  E M H Khedr,et al.  Neural maturation of breastfed and formula‐fed infants , 2004, Acta paediatrica.

[19]  Martine Vrijheid,et al.  Breastfeeding, Long-Chain Polyunsaturated Fatty Acids in Colostrum, and Infant Mental Development , 2011, Pediatrics.

[20]  R. Kahn,et al.  The Neonatal Connectome During Preterm Brain Development , 2014, Cerebral cortex.

[21]  Deanne K. Thompson,et al.  Breast Milk Feeding, Brain Development, and Neurocognitive Outcomes: A 7-Year Longitudinal Study in Infants Born at Less Than 30 Weeks' Gestation. , 2016, The Journal of pediatrics.

[22]  Leonardo L. Gollo,et al.  Time-resolved resting-state brain networks , 2014, Proceedings of the National Academy of Sciences.

[23]  Betty R. Vohr,et al.  Persistent Beneficial Effects of Breast Milk Ingested in the Neonatal Intensive Care Unit on Outcomes of Extremely Low Birth Weight Infants at 30 Months of Age , 2007, Pediatrics.

[24]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[25]  Peter Fransson,et al.  Spontaneous Brain Activity in the Newborn Brain During Natural Sleep—An fMRI Study in Infants Born at Full Term , 2009, Pediatric Research.

[26]  G. Gratton,et al.  Combining structural and functional neuroimaging data for studying brain connectivity: a review. , 2008, Psychophysiology.

[27]  D. Spatz,et al.  The relationship of brain development and breastfeeding in the late-preterm infant. , 2012, Journal of pediatric nursing.

[28]  Edward T. Bullmore,et al.  On the use of correlation as a measure of network connectivity , 2012, NeuroImage.

[29]  Alan Lucas,et al.  Impact of Breast Milk on Intelligence Quotient, Brain Size, and White Matter Development , 2010, Pediatric Research.

[30]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[31]  L J Horwood,et al.  Breastfeeding and Later Cognitive and Academic Outcomes , 1998, Pediatrics.

[32]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[33]  Michael S Kramer,et al.  The optimal duration of exclusive breastfeeding: a systematic review. , 2004, Advances in experimental medicine and biology.

[34]  Yu Zhang,et al.  The Human Brainnetome Atlas: A New Brain Atlas Based on Connectional Architecture , 2016, Cerebral cortex.

[35]  Xenophon Papademetris,et al.  Groupwise whole-brain parcellation from resting-state fMRI data for network node identification , 2013, NeuroImage.

[36]  Catie Chang,et al.  Effects of model-based physiological noise correction on default mode network anti-correlations and correlations , 2009, NeuroImage.

[37]  Petter Holme,et al.  Analyzing Temporal Networks in Social Media , 2014, Proceedings of the IEEE.

[38]  V. Calhoun,et al.  The Chronnectome: Time-Varying Connectivity Networks as the Next Frontier in fMRI Data Discovery , 2014, Neuron.

[39]  Alan C. Evans,et al.  Maturation of white matter in the human brain: a review of magnetic resonance studies , 2001, Brain Research Bulletin.

[40]  Mark E. Bastin,et al.  Early breast milk exposure modifies brain connectivity in preterm infants , 2019, NeuroImage.

[41]  Timothy O. Laumann,et al.  Sources and implications of whole-brain fMRI signals in humans , 2017, NeuroImage.

[42]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[43]  J. Pell,et al.  Meta-analysis of the association between preterm delivery and intelligence. , 2012, Journal of public health.

[44]  Mark W. Woolrich,et al.  Network modelling methods for FMRI , 2011, NeuroImage.

[45]  Yu Chen,et al.  The effects of a mid-task break on the brain connectome in healthy participants: A resting-state functional MRI study , 2017, NeuroImage.

[46]  Dimitri Van De Ville,et al.  The dynamic functional connectome: State-of-the-art and perspectives , 2017, NeuroImage.

[47]  Yufeng Zang,et al.  DPARSF: A MATLAB Toolbox for “Pipeline” Data Analysis of Resting-State fMRI , 2010 .

[48]  Peter Fransson,et al.  From static to temporal network theory: Applications to functional brain connectivity , 2017, Network Neuroscience.

[49]  S. Foster-Cohen,et al.  High Prevalence/Low Severity Language Delay in Preschool Children Born Very Preterm , 2010, Journal of developmental and behavioral pediatrics : JDBP.

[50]  Edward T. Bullmore,et al.  Efficiency and Cost of Economical Brain Functional Networks , 2007, PLoS Comput. Biol..

[51]  Jari Saramäki,et al.  Temporal Networks , 2011, Encyclopedia of Social Network Analysis and Mining.

[52]  Dimitri Van De Ville,et al.  On spurious and real fluctuations of dynamic functional connectivity during rest , 2015, NeuroImage.

[53]  Mark H. Johnson,et al.  Newborns' preferential tracking of face-like stimuli and its subsequent decline , 1991, Cognition.

[54]  John Suckling,et al.  Dynamic Reorganization of Functional Connectivity Reveals Abnormal Temporal Efficiency in Schizophrenia , 2018, Schizophrenia bulletin.

[55]  Betty R. Vohr,et al.  Beneficial Effects of Breast Milk in the Neonatal Intensive Care Unit on the Developmental Outcome of Extremely Low Birth Weight Infants at 18 Months of Age , 2006, Pediatrics.

[56]  Jeffrey S Anderson,et al.  Network anticorrelations, global regression, and phase‐shifted soft tissue correction , 2011, Human brain mapping.

[57]  Ravi S. Menon,et al.  Resting‐state networks show dynamic functional connectivity in awake humans and anesthetized macaques , 2013, Human brain mapping.

[58]  Emma Muñoz-Moreno,et al.  Altered small-world topology of structural brain networks in infants with intrauterine growth restriction and its association with later neurodevelopmental outcome , 2012, NeuroImage.

[59]  T. Cole,et al.  Breast milk and subsequent intelligence quotient in children born preterm , 1992, The Lancet.

[60]  Mark H. Johnson,et al.  The “what” and “where” of object representations in infancy , 2003, Cognition.

[61]  Gehan Roberts,et al.  Executive Function in Adolescents Born <1000 g or <28 Weeks: A Prospective Cohort Study , 2015, Pediatrics.

[62]  Eswar Damaraju,et al.  Tracking whole-brain connectivity dynamics in the resting state. , 2014, Cerebral cortex.

[63]  Bing Wang,et al.  Brain ganglioside and glycoprotein sialic acid in breastfed compared with formula-fed infants. , 2003, The American journal of clinical nutrition.

[64]  Scott K. Holland,et al.  Altered functional network connectivity in preterm infants: antecedents of cognitive and motor impairments? , 2018, Brain Structure and Function.

[65]  Hongkui Jing,et al.  A longitudinal study of differences in electroencephalographic activity among breastfed, milk formula-fed, and soy formula-fed infants during the first year of life. , 2010, Early human development.

[66]  J. Gilmore,et al.  Infant Brain Atlases from Neonates to 1- and 2-Year-Olds , 2011, PloS one.

[67]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.