Slower postnatal growth is associated with delayed cerebral cortical maturation in preterm newborns

Science Translational Medicine

Volumn 5, Issue 168, 2013, Pages

  Vinall, Jillian ^a,b   Grunau, Ruth E ^a,b,c   Brant, Rollin ^a,b   Chau, Vann ^a,b,c   Poskitt, Kenneth J ^a,b   Synnes, Anne R ^a,b,c   Miller, Steven P ^a,b,d  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c BC Children's and Women's Hospitals   (Canada)

^d HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BODY HEIGHT; BODY WEIGHT; BRAIN CORTEX; BRAIN HEMORRHAGE; BRAIN MATURATION; CEREBELLUM HEMORRHAGE; DIFFUSION TENSOR IMAGING; DISEASE ASSOCIATION; FEMALE; FRACTIONAL ANISOTROPY; GESTATIONAL AGE; HEAD CIRCUMFERENCE; HUMAN; IMAGE ANALYSIS; INFECTION; MAJOR CLINICAL STUDY; MALE; NECROTIZING ENTEROCOLITIS; NEUROIMAGING; NEWBORN; OUTCOME ASSESSMENT; PATENT DUCTUS ARTERIOSUS; POSTNATAL GROWTH; PREMATURITY; PRIORITY JOURNAL; SEX; SEX DIFFERENCE; WHITE MATTER INJURY; ANISOTROPY; BIRTH WEIGHT; CEPHALOMETRY; DIFFUSION WEIGHTED IMAGING; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; PATHOLOGY;

CORTICOSTEROID;

ADRENAL CORTEX HORMONES; ANISOTROPY; BIRTH WEIGHT; CEPHALOMETRY; CEREBRAL CORTEX; DIFFUSION MAGNETIC RESONANCE IMAGING; GROWTH AND DEVELOPMENT; HUMANS; INFANT, NEWBORN; PREMATURE BIRTH;

EID: 84872546142     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3004666     Document Type: Article

References (58)

1. R. E. Grunau, M. F. Whitfield, T. B. Fay, Psychosocial and academic characteristics of extremely low birth weight (≤800 g) adolescents who are free of major impairment compared with term-born control subjects. Pediatrics 114, e725-e732 (2004). (Pubitemid 41754906)
2. A. R. Synnes, S. Anson, A. Arkesteijn, A. Butt, R. E. Grunau, M. Rogers, M. F. Whitfield, School entry age outcomes for infants with birth weight ≤800 grams. J. Pediatr. 157, 989-994.e1 (2010).
3. A. Lind, M. Korkman, L. Lehtonen, H. Lapinleimu, R. Parkkola, J. Matomäki, L. Haataja; PIPARI Study Group, Cognitive and neuropsychological outcomes at 5 years of age in preterm children born in the 2000s. Dev. Med. Child Neurol. 53, 256-262 (2011).
4. M. Damodaram, L. Story, E. Kulinskaya, M. Rutherford, S. Kumar, Early adverse perinatal complications in preterm growth-restricted fetuses. Aust. N. Z. J. Obstet. Gynaecol. 51, 204-209 (2011).
5. S. L. Bonifacio, H. C. Glass, V. Chau, J. I. Berman, D. Xu, R. Brant, A. J. Barkovich, K. J. Poskitt, S. P. Miller, D. M. Ferriero, Extreme premature birth is not associated with impaired development of brain microstructure. J. Pediatr. 157, 726-732.e1 (2010).
6. J. Dubois, M. Benders, C. Borradori-Tolsa, A. Cachia, F. Lazeyras, R. Ha-Vinh Leuchter, S. V. Sizonenko, S. K. Warfield, J. F. Mangin, P. S. Hüppi, Primary cortical folding in the human newborn: An early marker of later functional development. Brain 131, 2028-2041 (2008).
7. P. B. Toft, H. Leth, P. B. Ring, B. Peitersen, H. C. Lou, O. Henriksen, Volumetric analysis of the normal infant brain and in intrauterine growth retardation. Early Hum. Dev. 43, 15-29 (1995).
8. C. B. Tolsa, S. Zimine, S. K. Warfield, M. Freschi, A. Sancho Rossignol, F. Lazeyras, S. Hanquinet, M. Pfizenmaier, P. S. Huppi, Early alteration of structural and functional brain development in premature infants born with intrauterine growth restriction. Pediatr. Res. 56, 132-138 (2004). (Pubitemid 38808554)
9. N. Padilla, C. Falcón, M. Sanz-Cortés, F. Figueras, N. Bargallo, F. Crispi, E. Eixarch, A. Arranz, F. Botet, E. Gratacós, Differential effects of intrauterine growth restriction on brain structure and development in preterm infants: A magnetic resonance imaging study. Brain Res. 1382, 98-108 (2011).
10. E. Eixarch, D. Batalle, M. Illa, E. Muñoz-Moreno, A. Arbat-Plana, I. Amat-Roldan, F. Figueras, E. Gratacós, Neonatal neurobehavior and diffusion MRI changes in brain reorganization due to intrauterine growth restriction in a rabbit model. PLoS One 7, e31497 (2012).
11. R. A. Ehrenkranz, N. Younes, J. A. Lemons, A. A. Fanaroff, E. F. Donovan, L. L. Wright, V. Katsikiotis, J. E. Tyson, W. Oh, S. Shankaran, C. R. Bauer, S. B. Korones, B. J. Stoll, D. K. Stevenson, L. A. Papile, Longitudinal growth of hospitalized very low birth weight infants. Pediatrics 104, 280-289 (1999). (Pubitemid 29362137)
12. D. K. Steward, K. F. Pridham, Growth patterns of extremely low-birth-weight hospitalized preterm infants. J. Obstet. Gynecol. Neonatal Nurs. 31, 57-65 (2002).
13. D. C. Wilson, P. Cairns, H. L. Halliday, M. Reid, G. McClure, J. A. Dodge, Randomised controlled trial of an aggressive nutritional regimen in sick very low birthweight infants. Arch. Dis. Child. Fetal Neonatal Ed. 77, F4-F11 (1997). (Pubitemid 28201620)
14. S. P. Miller, D. M. Ferriero, C. Leonard, R. Piecuch, D. V. Glidden, J. C. Partridge, M. Perez, P. Mukherjee, D. B. Vigneron, A. J. Barkovich, Early brain injury in premature newborns detected with magnetic resonance imaging is associated with adverse early neurodevelopmental outcome. J. Pediatr. 147, 609-616 (2005). (Pubitemid 41598332)
15. L. J. Woodward, P. J. Anderson, N. C. Austin, K. Howard, T. E. Inder, Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. N. Engl. J. Med. 355, 685-694 (2006).
16. N. Marlow, D. Wolke, M. A. Bracewell, M. Samara; EPICure Study Group, Neurologic and developmental disability at six years of age after extremely preterm birth. N. Engl. J. Med. 352, 9-19 (2005). (Pubitemid 40075676)
17. R. A. Ehrenkranz, A. M. Dusick, B. R. Vohr, L. L. Wright, L. A. Wrage, W. K. Poole, Growth in the neonatal intensive care unit influences neurodevelopmental and growth outcomes of extremely low birth weight infants. Pediatrics 117, 1253-1261 (2006). (Pubitemid 46071519)
18. R. Rathbone, S. J. Counsell, O. Kapellou, L. Dyet, N. Kennea, J. Hajnal, J. M. Allsop, F. Cowan, A. D. Edwards, Perinatal cortical growth and childhood neurocognitive abilities. Neurology 77, 1510-1517 (2011).
19. Y. Gozzo, B. Vohr, C. Lacadie, M. Hampson, K. H. Katz, J. Maller-Kesselman, K. C. Schneider, B. S. Peterson, N. Rajeevan, R. W. Makuch, R. T. Constable, L. R. Ment, Alterations in neural connectivity in preterm children at school age. Neuroimage 48, 458-463 (2009).
20. S. M. Doesburg, U. Ribary, A. T. Herdman, S. P. Miller, K. J. Poskitt, A. Moiseev, M. F. Whitfield, A. Synnes, R. E. Grunau, Altered long-range alpha-band synchronization during visual shortterm memory retention in children born very preterm. Neuroimage 54, 2330-2339 (2011).
21. P. Mukherjee, J. H. Miller, J. S. Shimony, J. V. Philip, D. Nehra, A. Z. Snyder, T. E. Conturo, J. J. Neil, R. C. McKinstry, Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. AJNR Am. J. Neuroradiol. 23, 1445-1456 (2002). (Pubitemid 35154982)
22. A. R. deIpolyi, P. Mukherjee, K. Gill, R. G. Henry, S. C. Partridge, S. Veeraraghavan, H. Jin, Y. Lu, S. P. Miller, D. M. Ferriero, D. B. Vigneron, A. J. Barkovich, Comparing microstructural and macrostructural development of the cerebral cortex in premature newborns: Diffusion tensor imaging versus cortical gyration. Neuroimage 27, 579-586 (2005). (Pubitemid 41139930)
23. R. C. McKinstry, A. Mathur, J. H. Miller, A. Ozcan, A. Z. Snyder, G. L. Schefft, C. R. Almli, S. I. Shiran, T. E. Conturo, J. J. Neil, Radial organization of developing preterm human cerebral cortex revealed by non-invasive water diffusion anisotropy MRI. Cereb. Cortex 12, 1237-1243 (2002). (Pubitemid 35396961)
24. M. Marín-Padilla, Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: A unifying theory. J. Comp. Neurol. 321, 223-240 (1992).
25. L. Mrzljak, H. B. Uylings, I. Kostovic, C. G. Van Eden, Prenatal development of neurons in the human prefrontal cortex: I. A qualitative Golgi study. J. Comp. Neurol. 271, 355-386 (1988).
26. I. Kostovic, P. Rakic, Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J. Comp. Neurol. 297, 441-470 (1990). (Pubitemid 20222635)
27. I. Kostovic, N. Jovanov-Milosevic, The development of cerebral connections during the first 20-45 weeks' gestation. Semin. Fetal Neonatal Med. 11, 415-422 (2006). (Pubitemid 44666590)
28. R. L. Sidman, P. Rakic, Neuronal migration, with special reference to developing human brain: A review. Brain Res. 62, 1-35 (1973).
29. A. Drobyshevsky, S. K. Song, G. Gamkrelidze, A. M. Wyrwicz, M. Derrick, F. Meng, L. Li, X. Ji, B. Trommer, D. J. Beardsley, N. L. Luo, S. A. Back, S. Tan, Developmental changes in diffusion anisotropy coincide with immature oligodendrocyte progression and maturation of compound action potential. J. Neurosci. 25, 5988-5997 (2005). (Pubitemid 40911430)
30. G. A. Lodygensky, K. Rademaker, S. Zimine, M. Gex-Fabry, A. F. Lieftink, F. Lazeyras, F. Groenendaal, L. S. de Vries, P. S. Huppi, Structural and functional brain development after hydrocortisone treatment for neonatal chronic lung disease. Pediatrics 116, 1-7 (2005).
31. V. Chau, R. Brant, K. J. Poskitt, E. W. Tam, A. Synnes, S. P. Miller, Postnatal infection is associated with widespread abnormalities of brain development in premature newborns. Pediatr. Res. 71, 274-279 (2012).
32. J. Dubois, M. Benders, A. Cachia, F. Lazeyras, R. Ha-Vinh Leuchter, S. V. Sizonenko, C. Borradori-Tolsa, J. F. Mangin, P. S. Hüppi, Mapping the early cortical folding process in the preterm newborn brain. Cereb. Cortex 18, 1444-1454 (2008). (Pubitemid 351769801)
33. V. Chau, K. J. Poskitt, D. E. McFadden, T. Bowen-Roberts, A. Synnes, R. Brant, M. A. Sargent, W. Soulikias, S. P. Miller, Effect of chorioamnionitis on brain development and injury in premature newborns. Ann. Neurol. 66, 155-164 (2009).
34. T. E. Inder, P. S. Huppi, S. Warfield, R. Kikinis, G. P. Zientara, P. D. Barnes, F. Jolesz, J. J. Volpe, Periventricular white matter injury in the premature infant is followed by reduced cerebral cortical gray matter volume at term. Ann. Neurol. 46, 755-760 (1999). (Pubitemid 29518137)
35. T. E. Inder, S. K. Warfield, H. Wang, P. S. Hüppi, J. J. Volpe, Abnormal cerebral structure is present at term in premature infants. Pediatrics 115, 286-294 (2005). (Pubitemid 43193809)
36. L. A. Papile, J. Burstein, R. Burstein, H. Koffler, Incidence and evolution of subependymal and intraventricular hemorrhage: A study of infants with birth weights less than 1,500 gm. J. Pediatr. 92, 529-534 (1978). (Pubitemid 8293290)
37. E. Adams, V. Chau, K. J. Poskitt, R. E. Grunau, A. Synnes, S. P. Miller, Tractography-based quantitation of corticospinal tract development in premature newborns. J. Pediatr. 156, 882-888, 888.e1 (2010).
38. M. Tolcos, E. Bateman, R. O'Dowd, R. Markwick, K. Vrijsen, A. Rehn, S. Rees, Intrauterine growth restriction affects the maturation of myelin. Exp. Neurol. 232, 53-65 (2011).
39. C. D. Kroenke, D. C. Van Essen, T. E. Inder, S. Rees, G. L. Bretthorst, J. J. Neil, Microstructural changes of the baboon cerebral cortex during gestational development reflected in magnetic resonance imaging diffusion anisotropy. J. Neurosci. 27, 12506-12515 (2007). (Pubitemid 350127812)
40. S. N. Jespersen, L. A. Leigland, A. Cornea, C. D. Kroenke, Determination of axonal and dendritic orientation distributions within the developing cerebral cortex by diffusion tensor imaging. IEEE Trans. Med. Imaging 31, 16-32 (2012).
41. S. V. Sizonenko, E. J. Camm, J. R. Garbow, S. E. Maier, T. E. Inder, C. E. Williams, J. J. Neil, P. S. Huppi, Developmental changes and injury induced disruption of the radial organization of the cortex in the immature rat brain revealed by in vivo diffusion tensor MRI. Cereb. Cortex 17, 2609-2617 (2007). (Pubitemid 47537820)
42. M. Bisignano, S. Rees, The effects of intrauterine growth retardation on synaptogenesis and mitochondrial formation in the cerebral and cerebellar cortices of fetal sheep. Int. J. Dev. Neurosci. 6, 453-460 (1988).
43. G. B. Samuelsen, B. Pakkenberg, N. Bogdanovic, H. J. Gundersen, J. F. Larsen, N. Graem, H. Laursen, Severe cell reduction in the future brain cortex in human growth-restricted fetuses and infants. Am. J. Obstet. Gynecol. 197, 56.e1-56.e7 (2007).
44. J. L. Smart, J. Dobbing, B. P. Adlard, A. Lynch, J. Sands, Vulnerability of developing brain: Relative effects of growth restriction during the fetal and suckling periods on behavior and brain composition of adult rats. J. Nutr. 103, 1327-1338 (1973).
45. M. K. Georgieff, Nutrition and the developing brain: Nutrient priorities and measurement. Am. J. Clin. Nutr. 85, 614S-620S (2007). (Pubitemid 46220971)
46. P. S. McQuillen, D. M. Ferriero, Perinatal subplate neuron injury: Implications for cortical development and plasticity. Brain Pathol. 15, 250-260 (2005). (Pubitemid 41161182)
47. P. S. McQuillen, R. A. Sheldon, C. J. Shatz, D. M. Ferriero, Selective vulnerability of subplate neurons after early neonatal hypoxia-ischemia. J. Neurosci. 23, 3308-3315 (2003). (Pubitemid 36531972)
48. P. O. Kanold, P. Kara, R. C. Reid, C. J. Shatz, Role of subplate neurons in functional maturation of visual cortical columns. Science 301, 521-525 (2003). (Pubitemid 36900310)
49. R. Villescas, R. Ostwald, H. Morimoto, E. L. Bennett, Effects of neonatal undernutrition and cold stress on behavior and biochemical brain parameters in rats. J. Nutr. 111, 1103-1110 (1981). (Pubitemid 11034752)
50. J. Mourek, W. A. Himwich, J. Myslivecek, D. A. Callison, The role of nutrition in the development of evoked cortical responses in rat. Brain Res. 6, 241-251 (1967).
51. F. J. Seidler, J. M. Bell, T. A. Slotkin, Undernutrition and overnutrition in the neonatal rat: Long-term effects on noradrenergic pathways in brain regions. Pediatr. Res. 27, 191-197 (1990). (Pubitemid 20044541)
52. J. Vinall, S. P. Miller, V. Chau, S. Brummelte, A. R. Synnes, R. E. Grunau, Neonatal pain in relation to postnatal growth in infants born very preterm. Pain 153, 1374-1381 (2012).
53. B. J. Stoll, N. I. Hansen, I. Adams-Chapman, A. A. Fanaroff, S. R. Hintz, B. Vohr, R. D. Higgins; National Institute of Child Health and Human Development Neonatal Research Network, Neurodevelopmental and growth impairment among extremely low-birth-weight infants with neonatal infection. JAMA 292, 2357-2365 (2004). (Pubitemid 39491920)
54. M. J. Bell, J. L. Ternberg, R. D. Feigin, J. P. Keating, R. Marshall, L. Barton, T. Brotherton, Neonatal necrotizing enterocolitis. Therapeutic decisions based upon clinical staging. Ann. Surg. 187, 1-7 (1978).
55. P. S. Hüppi, S. E. Maier, S. Peled, G. P. Zientara, P. D. Barnes, F. A. Jolesz, J. J. Volpe, Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr. Res. 44, 584-590 (1998). (Pubitemid 28447347)
56. S. C. Partridge, P. Mukherjee, R. G. Henry, S. P. Miller, J. I. Berman, H. Jin, Y. Lu, O. A. Glenn, D. M. Ferriero, A. J. Barkovich, D. B. Vigneron, Diffusion tensor imaging: Serial quantitation of white matter tract maturity in premature newborns. Neuroimage 22, 1302-1314 (2004). (Pubitemid 38829219)
57. J. M. Bland, D. G. Altman, Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1, 307-310 (1986). (Pubitemid 16134762)
58. S. Pajevic, C. Pierpaoli, Color schemes to represent the orientation of anisotropic tissues from diffusion tensor data: Application to white matter fiber tract mapping in the human brain. Magn. Reson. Med. 42, 526-540 (1999). (Pubitemid 29416214)