Electroencephalographic activity of preterm infants is increased by family nurture intervention: A randomized controlled trial in the NICU

Clinical Neurophysiology

Volumn 125, Issue 4, 2014, Pages 675-684

  Welch, Martha G ^a,b   Myers, Michael M ^a,b   Grieve, Philip G ^a,c   Isler, Joseph R ^a   Fifer, William P ^a,b   Sahni, Rakesh ^a   Hofer, Myron A ^a,b   Austin, Judy ^d   Ludwig, Robert J ^a   Stark, Raymond I ^a  

^a Columbia University College of Physicians and Surgeons ^*  (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^c Department of Earth and Environmental Sciences   (United States)

^d Department of Medicine   (United States)

Author keywords

Brain maturation; EEG; Maternal separation; Mother infant intervention; Premature birth

Indexed keywords

ARTICLE; BIRTH WEIGHT; BRAIN FUNCTION; BRAIN MATURATION; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPH ELECTRODE; ELECTROENCEPHALOGRAPHY; EMOTIONALITY; FAMILY NURTURE INTERVENTION; FAMILY THERAPY; FEMALE; FRONTAL CORTEX; GESTATIONAL AGE; HUMAN; INTERPERSONAL COMMUNICATION; KANGAROO CARE; MAJOR CLINICAL STUDY; MALE; MATERNAL DEPRIVATION; MOTHER CHILD RELATION; NERVE CELL DIFFERENTIATION; NEWBORN; NEWBORN INTENSIVE CARE; PREMATURE LABOR; PREMATURITY; PRIORITY JOURNAL; SLEEP; TEMPORAL LOBE; BRAIN; CHILD; CONTROLLED STUDY; INFANT; MOTHER; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL; TREATMENT OUTCOME;

BRAIN; CHILD; ELECTROENCEPHALOGRAPHY; FEMALE; GESTATIONAL AGE; HUMANS; INFANT; INFANT, NEWBORN; INFANT, PREMATURE; INTENSIVE CARE UNITS, NEONATAL; MALE; MOTHER-CHILD RELATIONS; MOTHERS; SLEEP; TREATMENT OUTCOME;

EID: 84896725887     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2013.08.021     Document Type: Article

References (76)

1. Als H., Duffy F.H., McAnulty G., Butler S.C., Lightbody L., Kosta S., et al. NIDCAP improves brain function and structure in preterm infants with severe intrauterine growth restriction. J Perinatol 2012, 32:797-803.
2. Als H., Duffy F.H., McAnulty G.B., Rivkin M.J., Vajapeyam S., Mulkern R.V., et al. Early experience alters brain function and structure. Pediatrics 2004, 113:846-857.
3. Als H., Lawhon G., Duffy F.H., McAnulty G.B., Gibes-Grossman R., Blickman J.G. Individualized developmental care for the very low-birth-weight preterm infant. Medical and neurofunctional effects. JAMA 1994, 272:853-858.
4. Baron I.S., Kerns K.A., Muller U., Ahronovich M.D., Litman F.R. Executive functions in extremely low birth weight and late-preterm preschoolers: effects on working memory and response inhibition. Child Neuropsychol 2012, 18:586-599.
5. Benasich A.A., Gou Z., Choudhury N., Harris K.D. Early cognitive and language skills are linked to resting frontal gamma power across the first 3years. Behav Brain Res 2008, 195:215-222.
6. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 1995, 57:289-300.
7. Buehler D.M., Als H., Duffy F.H., McAnulty G.B., Liederman J. Effectiveness of individualized developmental care for low-risk preterm infants: behavioral and electrophysiologic evidence. Pediatrics 1995, 96:923-932.
8. Caldji C., Hellstrom I.C., Zhang T.Y., Diorio J., Meaney M.J. Environmental regulation of the neural epigenome. FEBS Lett 2011, 585(13):2049-2058.
9. Clapp W.C., Hamm J.P., Kirk I.J., Teyler T.J. Translating long-term potentiation from animals to humans: a novel method for noninvasive assessment of cortical plasticity. Biol Psychiatry 2012, 71:496-502.
10. Coe C.L., Rosenberg L.T., Levine S. Effect of maternal separation on the complement system and antibody responses in infant primates. Int J Neurosci 1988, 40:289-302.
11. Conde-Agudelo A., Belizan J.M., Diaz-Rossello J. Kangaroo mother care to reduce morbidity and mortality in low birthweight infants. Cochrane Database Syst Rev 2011, CD002771.
12. Dawson G., Frey K., Panagiotides H., Yamada E., Hessl D., Osterling J. Infants of depressed mothers exhibit atypical frontal electrical brain activity during interactions with mother and with a familiar, nondepressed adult. Child Dev 1999, 70:1058-1066.
13. Dawson G., Frey K., Self J., Panagiotides H., Hessl D., Yamada E., et al. Frontal brain electrical activity in infants of depressed and nondepressed mothers: relation to variations in infant behavior. Dev Psychopathol 1999, 11:589-605.
14. DeCasper A.J., Fifer W.P. Of human bonding: newborns prefer their mothers' voices. Science 1980, 208:1174-1176.
15. Delaunay-El Allam M., Marlier L., Schaal B. Learning at the breast: preference formation for an artificial scent and its attraction against the odor of maternal milk. Infant Behav Dev 2006, 29:308-321.
16. Diaz A., Bell M.A. Frontal EEG asymmetry and fear reactivity in different contexts at 10months. Dev Psychobiol 2012, 54:536-545.
17. Feldman R., Weller A., Sirota L., Eidelman A.I. Skin-to-skin contact (Kangaroo care) promotes self-regulation in premature infants: sleep-wake cyclicity, arousal modulation, and sustained exploration. Dev Psychol 2002, 38:194-207.
18. Field T., Diego M., Hernandez-Reif M. Preterm infant massage therapy research: a review. Infant Behav Dev 2010, 33:115-124.
19. Field T., Diego M.A., Hernandez-Reif M., Deeds O., Figuereido B. Moderate versus light pressure massage therapy leads to greater weight gain in preterm infants. Infant Behav Dev 2006, 29:574-578.
20. Fifer W.P., Byrd D.L., Kaku M., Eigsti I.M., Isler J.R., Grose-Fifer J., et al. Newborn infants learn during sleep. Proc Natl Acad Sci USA 2010, 107:10320-10323.
21. Fifer W.P., Moon C.M. The role of mother's voice in the organization of brain function in the newborn. Acta Paediatr 1994, 397(Suppl):86-93.
22. Gou Z., Choudhury N., Benasich A.A. Resting frontal gamma power at 16, 24 and 36months predicts individual differences in language and cognition at 4 and 5years. Behav Brain Res 2011, 220:263-270.
23. Grieve P.G., Isler J.R., Izraelit A., Peterson B.S., Fifer W.P., Myers M.M., et al. EEG functional connectivity in term age extremely low birth weight infants. Clin Neurophysiol 2008, 119:2712-2720.
24. Grieve P.G., Myers M.M., Stark R.I., Housman S., Fifer W.P. Topographic localization of electrocortical activation in newborn and two- to four-month-old infants in response to head-up tilting. Acta Paediatr 2005, 94:1756-1763.
25. Grieve P.G., Stark R.I., Isler J.R., Housman S.L., Fifer W.P., Myers M.M. Electrocortical functional connectivity in infancy: response to body tilt. Pediatr Neurol 2007, 37:91-98.
26. Guzzetta A., Baldini S., Bancale A., Baroncelli L., Ciucci F., Ghirri P., et al. Massage accelerates brain development and the maturation of visual function. J Neurosci 2009, 29:6042-6051.
27. Guzzetta A., D'Acunto M.G., Carotenuto M., Berardi N., Bancale A., Biagioni E., et al. The effects of preterm infant massage on brain electrical activity. Dev Med Child Neurol 2011, 53(Suppl. 4):46-51.
28. Hamilton B.E., Hoyert D.L., Martin J.A., Strobino D.M., Guyer B. Annual Summary of Vital Statistics: 2010-2011. Pediatrics 2013.
29. Hane A.A., Fox N.A. Ordinary variations in maternal caregiving influence human infants' stress reactivity. Psychol Sci 2006, 17:550-556.
30. Hane A.A., Henderson H.A., Reeb-Sutherland B.C., Fox N.A. Ordinary variations in human maternal caregiving in infancy and biobehavioral development in early childhood: a follow-up study. Dev Psychobiol 2010, 52:558-567.
31. Hofer M.A. Studies on how early maternal separation produces behavioral change in young rats. Psychosom Med 1975, 37:245-264.
32. Hofer M.A. Hidden regulators in attachment, separation, and loss. Monogr Soc Res Child Dev 1994, 59:192-207.
33. Hofer M.A. On the nature and consequences of early loss. Psychosom Med 1996, 58:570-581.
34. Isler J.R., Garland M., Stark R.I., Grieve P.G. Local coherence oscillations in the EEG during development in the fetal baboon. Clin Neurophysiol 2005, 116:2121-2128.
35. Jensen C.L., Champagne F.A. Epigenetic and neurodevelopmental perspectives on variation in parenting behavior. Parent Sci Pract 2012, 12:202-211.
36. Johnson S., Marlow N. Preterm birth and childhood psychiatric disorders. Pediatr Res 2011, 69:8R-11R.
37. Johnston M.V., Nishimura A., Harum K., Pekar J., Blue M.E. Sculpting the developing brain. Adv Pediatr 2001, 48:1-38.
38. Kaffashi F., Scher M.S., Ludington-Hoe S.M. Loparo KA 2012, A preliminary study. Clin Neurophysiol, An analysis of the kangaroo care intervention using neonatal EEG complexity.
39. Kojima S., Alberts J.R. Warmth from skin-to-skin contact with mother is essential for the acquisition of filial huddling preference in preweanling rats. Dev Psychobiol 2011, 53:813-827.
40. Kuhn C.M., Schanberg S.M. Responses to maternal separation: mechanisms and mediators. Int J Dev Neurosci 1998, 16:261-270.
41. Ludington-Hoe S.M., Johnson M.W., Morgan K., Lewis T., Gutman J., Wilson P.D., et al. Neurophysiologic assessment of neonatal sleep organization: preliminary results of a randomized, controlled trial of skin contact with preterm infants. Pediatrics 2006, 117:e909-e923.
42. Marlier L., Schaal B., Soussignan R. Orientation responses to biological odours in the human newborn. Initial pattern and postnatal plasticity. C R Acad Sci III 1997, 320:999-1005.
43. McAnulty G., Duffy F.H., Butler S., Parad R., Ringer S., Zurakowski D., et al. Individualized developmental care for a large sample of very preterm infants: health, neurobehaviour and neurophysiology. Acta Paediatr 2009, 98:1920-1926.
44. McLaughlin K.A., Fox N.A., Zeanah C.H., Nelson C.A. Adverse rearing environments and neural development in children: the development of frontal electroencephalogram asymmetry. Biol Psychiatry 2011, 70:1008-1015.
45. Meaney M.J., Diorio J., Francis D., Widdowson J., LaPlante P., Caldji C., et al. Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev Neurosci 1996, 18:49-72.
46. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 2001, 24:1161-1192.
47. Moon C.M., Fifer W.P. Evidence of transnatal auditory learning. J Perinatol 2000, 20:S37-S44.
48. Myers M.M., Brunelli S.A., Shair H.N., Squire J.M., Hofer M.A. Relationships between maternal behavior of SHR and WKY dams and adult blood pressures of cross-fostered F1 pups. Dev Psychobiol 1989, 22:55-67.
49. Myers M.M., Brunelli S.A., Squire J.M., Shindeldecker R.D., Hofer M.A. Maternal behavior of SHR rats and its relationship to offspring blood pressures. Dev Psychobiol 1989, 22:29-53.
50. Myers M.M., Fifer W.P., Grose-Fifer J., Sahni R., Stark R.I., Schulze K.F. A novel quantitative measure of Trace-alternant EEG activity and its association with sleep states of preterm infants. Dev Psychobiol 1997, 31:167-174.
51. Myers M.M., Grieve P.G., Izraelit A., Fifer W.P., Isler J.R., Darnall R.A., et al. Developmental profiles of infant EEG: overlap with transient cortical circuits. Clin Neurophysiol 2012, 123:1502-1511.
52. Myers M.M., Stark R.I., Fifer W.P., Grieve P.G., Haiken J., Leung K., et al. A quantitative method for classification of EEG in the fetal baboon. Am J Physiol 1993, 265:R706-R714.
53. Nosarti C., Reichenberg A., Murray R.M., Cnattingius S., Lambe M.P., Yin L., et al. Preterm birth and psychiatric disorders in young adult life. Arch Gen Psychiatry 2012, 69:E1-E8.
54. Ohlsson A., Jacobs S.E. NIDCAP: a systematic review and meta-analyses of randomized controlled trials. Pediatrics 2013, 131:e881-e893.
55. Park H., Poo M.M. Neurotrophin regulation of neural circuit development and function. Nat Rev Neurosci 2013, 14:7-23.
56. Peterson B.S., Vohr B., Staib L.H., Cannistraci C.J., Dolberg A., Schneider K.C., et al. Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 2000, 284:1939-1947.
57. Pinto-Martin J.A., Levy S.E., Feldman J.F., Lorenz J.M., Paneth N., Whitaker A.H. Prevalence of autism spectrum disorder in adolescents born weighing <2000g. Pediatrics 2011, 128:883-891.
58. Robinson S.R., Kleven G.A., Brumley M.R. Prenatal development of interlimb motor learning in the rat fetus. Infancy 2008, 13:204-228.
59. Sahni R., Schulze K.F., Kashyap S., Ohira-Kist K., Fifer W.P., Myers M.M. Sleeping position and electrocortical activity in low birthweight infants. Arch Dis Child Fetal Neonatal Ed 2005, 90:F311-F315.
60. Sahni R., Schulze K.F., Stefanski M., Myers M.M., Fifer W.P. Methodological issues in coding sleep states in immature infants. Dev Psychobiol 1995, 28:85-101.
61. Sanchez M.M., Ladd C.O., Plotsky P.M. Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev Psychopathol 2001, 13:419-449.
62. Schaal B., Marlier L., Soussignan R. Human foetuses learn odours from their pregnant mother's diet. Chem Senses 2000, 25:729-737.
63. Scher M.S., Ludington-Hoe S., Kaffashi F., Johnson M.W., Holditch-Davis D., Loparo K.A. Neurophysiologic assessment of brain maturation after an 8-week trial of skin-to-skin contact on preterm infants. Clin Neurophysiol 2009, 120:1812-1818.
64. Scher M.S., Steppe D.A., Banks D.L. Prediction of lower developmental performances of healthy neonates by neonatal EEG-sleep measures. Pediatr Neurol 1996, 14:137-144.
65. Shackman A.J., McMenamin B.W., Slagter H.A., Maxwell J.S., Greischar L.L., Davidson R.J. Electromyogenic artifacts and electroencephalographic inferences. Brain Topogr 2009, 22:7-12.
66. Stefanski M., Schulze K., Bateman D., Kairam R., Pedley T.A., Masterson J., et al. A scoring system for states of sleep and wakefulness in term and preterm infants. Pediatr Res 1984, 18:58-62.
67. Sullivan R.M., Brake S.C., Hofer M.A., Williams C.L. Huddling and independent feeding of neonatal rats can be facilitated by a conditioned change in behavioral state. Dev Psychobiol 1986, 19:625-635.
68. Sullivan R.M., Hofer M.A., Brake S.C. Olfactory-guided orientation in neonatal rats is enhanced by a conditioned change in behavioral state. Dev Psychobiol. 1986, 19:615-623.
69. Symington A., Pinelli J. Developmental care for promoting development and preventing morbidity in preterm infants. Cochrane Database Syst Rev 2006, CD001814.
70. Tarullo A.R., Lee J., Gera S., Condon C., Tamura E.K., Grieve P.G., et al. Language development linked to newborn frontal gamma power. Dev Psychobiol 2012, 54:769.
71. Vickers A., Ohlsson A., Lacy J.B., Horsley A. Massage for promoting growth and development of preterm and/or low birth-weight infants. Cochrane Database Syst Rev 2004, CD000390.
72. Welch M.G., Hofer M.A., Brunelli S.A., Stark R.I., Andrews H.F., Austin J., et al. Family nurture intervention (FNI): methods and treatment protocol of a randomized controlled trial in the NICU. BMC Pediatr 2012, 12:14.
73. Welch M.G., Hofer M.A., Stark R.I., Andrews H.F., Austin J., Glickstein S.B., et al. Randomized controlled trial of Family Nurture Intervention in the NICU: Assessments of length of stay, feasibility and safety. BMC Pediatrics 2013, 13:148. 10.1186/1471-2431-13-148.
74. Welch M.G., Northrup R.S., Welch-Horan T.B., Ludwig R.J., Austin C.L., Jacobson J.S. Outcomes of Prolonged Parent-Child Embrace Therapy among 102 children with behavioral disorders. Complement Ther Clin Pract 2006, 12:3-12.
75. Williams I.A., Tarullo A.R., Grieve P.G., Wilpers A., Vignola E.F., Myers M.M., et al. Fetal cerebrovascular resistance and neonatal EEG predict 18-month neurodevelopmental outcome in infants with congenital heart disease. Ultrasound Obstet Gynecol 2012, 40:304-309.
76. Zhang T.Y., Labonte B., Wen X.L., Turecki G., Meaney M.J. Epigenetic mechanisms for the early environmental regulation of hippocampal glucocorticoid receptor gene expression in rodents and humans. Neuropsychopharmacology 2013, 38:111-123.