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

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Abstract

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.

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.

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Funding

This work was supported by the National Natural Science Foundation of China (Grant no. 81801785, 81573516), by the “Hundred Talents Program” of Zhejiang University and by the Fundamental Research Funds for the Central Universities (Grant no. 2019FZJD005 and 2020FZZX001-05). This work was partially supported by the National Key Research and Development Program of China (Grant no. 2016YFC0100300), Natural Science Foundation of Zhejiang Province (Grant no. 491050+N21702), Scientific Research Fund of Zhejiang Provincial Education Department (Grant no. Y201431325), Provincial and Ministerial Joint Construction Major Project of National Health Commission of Zhejiang Province (Grant no. WKJ-ZJ-2008), and Zhejiang Lab (Grant no. 2019KE0AD01).

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    Authors and Affiliations

    1. Department of Radiology, Children’s Hospital, National Clinical Research Center for Child Health, Zhejiang University School of Medicine, Zhejiang, China

      Weiming Niu, Hongxi Zhang, Tianmei Liu, Can Lai & Yu Sun

    2. Department of Nursing, Women’s Hospital, Zhejiang University School of Medicine, Zhejiang, China

      Xinfen Xu

    3. Department of Obstetrics and Gynecology Nursing, Haining Maternal and Child Health Hospital, Zhejiang, China

      Xinfen Xu

    4. Women’s Hospital School of Medicine Zhejiang University Haining Branch, Haining Maternity and Child Health Care Hospital, Zhejiang, China

      Xinfen Xu

    5. Department of Midwifery, Zhejiang Chinese Medical University School of Nursing, Zhejiang, China

      Yao Zhang

    6. Clinical Trial Institute, Children’s Hospital, National Clinical Research Center for Child Health, Zhejiang University School of Medicine, Zhejiang, China

      Shaoqing Ni

    7. Neonatal Intensive Care Unit, Women’s Hospital, Zhejiang University School of Medicine, Zhejiang, China

      Qiufang Li

    8. Department of Biomedical Engineering, Key Laboratory for Biomedical Engineering of Ministry of Education, Zhejiang University, Zhejiang, China

      Yu Sun

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    Niu, W., Xu, X., Zhang, H. et al. Breastfeeding improves dynamic reorganization of functional connectivity in preterm infants: a temporal brain network study. Med Biol Eng Comput 58, 2805–2819 (2020). https://doi.org/10.1007/s11517-020-02244-3

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