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A Risk of Sensory Deprivation in the Neonatal Intensive Care Unit

2014; Elsevier BV; Volume: 164; Issue: 6 Linguagem: Inglês

10.1016/j.jpeds.2014.01.072

1097-6833

Alan H. Jobe,

Infant Health and Development

The neonatal intensive care unit (NICU) environment has changed for the better from the 1970s and 1980s when the NICU was congested, noisy, and brightly lit 24 hours a day—a frenetic environment no doubt. Current designs for the NICU as recommended by the Consensus Committee on Recommended Design Standards for Advanced Neonatal Care (2013) emphasize noise and light suppression with space for extended, intimate parental contact, and for parents to "room-in" with the infant.1White R.D. Smith J.A. Shepley M.M. Recommended standards for newborn ICU design, 8th edition.J Perinatol. 2013; 33: S2-S16Crossref PubMed Scopus (144) Google Scholar These designs provide more humane and patient plus parent friendly care, but also greatly increase the floor space and, inevitably, increase cost substantially. The motivations for the design of the new NICU have been guided by concepts of developmental-appropriate care of very preterm infants to minimize stress and optimize neurodevelopmental outcomes.2McAnulty G. Duffy F.H. Kosta S. Weisenfeld N.I. Warfield S.K. Butler S.C. et al.School-age effects of the newborn individualized developmental care and assessment program for preterm infants with intrauterine growth restriction: preliminary findings.BMC Pediatr. 2013; 13: 25Crossref PubMed Scopus (34) Google Scholar The elements of developmental care focus on minimizing stimulation of the infant by limiting noise, sound exposure, and sleep interruptions. In practice, NICU care is anthropomorphized by the NICU staff to environments the adult caretakers think will be optimal for the infant—an intrauterine environment that is generally assumed to be dark, quiet, and without stimulation of the fetus. This perspective results in care strategies such as single rooms for preterm infants that are very quiet, often have low light 24 hours a day, and with an additional blanket over the isolette to further suppress sound and light exposure. Contact with staff is minimized so as to not disturb the infant. Pineda et al3Pineda R.G. Neil J. Dierker D. Smyser C.D. Wallendorf M. Kidokoro H. et al.Alterations in brain structure and neurodevelopmental outcome in preterm infants hospitalized in different NICU environments.J Pediatr. 2013; 164: 52-60.e2Abstract Full Text Full Text PDF PubMed Scopus (230) Google Scholar report that contrary to their hypothesis that single rooms would promote neurodevelopment relative to the ward environment, preterm infants cared for in a ward and evaluated at term had more normal brain structures as assessed by magnetic resonance imaging and better cerebral maturation scores as assessed by electroencephalography than infants cared for in single rooms. Further, when these infants were assessed at 2 years of age, the ward infants had better language and motor scores than the infants cared for in single rooms. How is this outcome possible? Pineda et al hypothesize that the single room, with continuous low light and low sound, and with isolation from stimuli, may result in sensory deprivation to the developing brain. This explanation is strengthened by their demonstration that parental visits tended to be short and infrequent for their parent population.4Pineda R.G. Stransky K.E. Rogers C. Duncan M.H. Smith G.C. Neil J. et al.The single-patient room in the NICU: maternal and family effects.J Perinatol. 2012; 32: 545-551Crossref PubMed Scopus (73) Google Scholar In contrast to this experience, Ortenstrand et al5Ortenstrand A. Westrup B. Brostrom E.B. Sarman I. Akerstrom S. Brune T. et al.The Stockholm Neonatal Family-Centered Care Study: effects on length of stay and infant morbidity.Pediatrics. 2010; 125: e278-e285Crossref PubMed Scopus (234) Google Scholar reported benefits of family-centered care with single rooms in Scandinavia, but a parent was required to be continually present 24 hours a day to help care for the infant. Of note, although developmental care may benefit infants,2McAnulty G. Duffy F.H. Kosta S. Weisenfeld N.I. Warfield S.K. Butler S.C. et al.School-age effects of the newborn individualized developmental care and assessment program for preterm infants with intrauterine growth restriction: preliminary findings.BMC Pediatr. 2013; 13: 25Crossref PubMed Scopus (34) Google Scholar such benefits are not uniformly reported.6Ohlsson A. Jacobs S.E. NIDCAP: a systematic review and meta-analyses of randomized controlled trials.Pediatrics. 2013; 131: e881-e893Crossref PubMed Scopus (112) Google Scholar Rather than arguing the perceived benefits of the elements of developmental care and single rooms in the NICU, brief reviews of the biology of sound, light, and manual stimulation of preterm infants may be more fruitful. There is extensive literature describing the excessive sound exposures for infants in the NICU, with recommendations from the American Academy of Pediatrics for limiting these exposures.7Noise: a hazard for the fetus and newborn. American Academy of Pediatrics. Committee on Environmental Health.Pediatrics. 1997; 100: 724-727Crossref PubMed Scopus (411) Google Scholar Modern isolettes and ventilators are more quiet than in the past, but the amount of continuous white noise can be substantial and a hazard.8Lasky R.E. Williams A.L. Noise and light exposures for extremely low birth weight newborns during their stay in the neonatal intensive care unit.Pediatrics. 2009; 123: 540-546Crossref PubMed Scopus (114) Google Scholar However, sound exposure is critical for the development of normal speech. The fetal environment is not quiet, although high frequency sounds are filtered out. The human fetus can hear and respond to sounds by 23-24 weeks, and the development of the auditory cortex is critically dependent on the auditory environment from early gestation.9McMahon E. Wintermark P. Lahav A. Auditory brain development in premature infants: the importance of early experience.Ann NY Acad Sci. 2012; 1252: 17-24Crossref PubMed Scopus (106) Google Scholar Deprivation of maternal sounds will interfere with the development of the fetal auditory cortex and interfere with speech and language acquisition. The amount of speech-related brain activity after birth increases with more fetal exposure to speech.10Partanen E. Kujala T. Naatanen R. Liitola A. Sambeth A. Huotilainen M. Learning-induced neural plasticity of speech processing before birth.Proc Natl Acad Sci USA. 2013; 110: 15145-15150Crossref PubMed Scopus (117) Google Scholar Surprisingly, language exposure in utero initiates the fetus to the phonic characteristics of its native language.11Moon C. Lagercrantz H. Kuhl P.K. Language experienced in utero affects vowel perception after birth: a two-country study.Acta Paediatrica. 2013; 102: 156-160Crossref PubMed Scopus (174) Google Scholar However, following very preterm birth, exposure to adult language—maternal or from the NICU staff—was found to be a small percent of the sound exposure.12Caskey M. Stephens B. Tucker R. Vohr B. Importance of parent talk on the development of preterm infant vocalizations.Pediatrics. 2011; 128: 910-916Crossref PubMed Scopus (150) Google Scholar The appropriate emphasis on sound abatement in the new or renovated NICU should be on background noise, alarm noise, and other non-human noises that can startle and disrupt sleep of the preterm.13Kuhn P. Zores C. Langlet C. Escande B. Astruc D. Dufour A. Moderate acoustic changes can disrupt the sleep of very preterm infants in their incubators.Acta Paediatrica. 2013; 102: 949-954Crossref PubMed Scopus (46) Google Scholar However, the focus on noise abatement has morphed into a goal of silence in the NICU with exclusion of staff talk and lively discussions on work rounds. The result may be a severe limitation of the exposure of the vulnerable developing auditory cortex to human voices and sounds that are necessary for language development. This delay in language development for infants in single rooms is just what was observed by the Pineda article.3Pineda R.G. Neil J. Dierker D. Smyser C.D. Wallendorf M. Kidokoro H. et al.Alterations in brain structure and neurodevelopmental outcome in preterm infants hospitalized in different NICU environments.J Pediatr. 2013; 164: 52-60.e2Abstract Full Text Full Text PDF PubMed Scopus (230) Google Scholar In contrast, the open ward better reflects the fetal environment with human sounds and activities. Although the fetus is in a dark environment in utero, the fetus has a circadian rhythm entrained by maternal hormones.14Rivkees S.A. Emergence and influences of circadian rhythmicity in infants.Clin Perinatol. 2004; 31: 217-228Abstract Full Text Full Text PDF PubMed Scopus (50) Google Scholar The circadian regulator in the brain—the hypothalamic superchiasmatic nuclei—of the very preterm baboon equivalent to about 24-week preterm infants, responds to light with increased metabolism and gene expression.15Hao H. Rivkees S.A. The biological clock of very premature primate infants is responsive to light.Proc Natl Acad Sci USA. 1999; 96: 2426-2429Crossref PubMed Scopus (73) Google Scholar Preterm infants cared for in dimly lighted rooms or day-night lighted rooms develop circadian sleep patterns independent of cycled light.16Mirmiran M. Baldwin R.B. Ariagno R.L. Circadian and sleep development in preterm infants occurs independently from the influences of environmental lighting.Pediat Res. 2003; 53: 933-938Crossref PubMed Scopus (54) Google Scholar, 17Rivkees S.A. Mayes L. Jacobs H. Gross I. Rest-activity patterns of premature infants are regulated by cycled lighting.Pediatrics. 2004; 113: 833-839Crossref PubMed Scopus (106) Google Scholar Nevertheless, development of the visual system requires visual experiences.18Baroncelli L. Braschi C. Spolidoro M. Begenisic T. Sale A. Maffei L. Nurturing brain plasticity: impact of environmental enrichment.Cell death and differentiation. 2010; 17: 1092-1103Crossref PubMed Scopus (194) Google Scholar Sight deprivation interrupts visual development, and environmental enrichment fosters brain plasticity. The fetal mouse eye responds to light with signaling via melanopsin in the fetal retina to induce regression of the hyaloid vasculature and stimulate retinal development by down-regulating vascular endothelial growth factor.19Rao S. Chun C. Fan J. Kofron J.M. Yang M.B. Hegde R.S. et al.A direct and melanopsin-dependent fetal light response regulates mouse eye development.Nature. 2013; 494: 243-246Crossref PubMed Scopus (128) Google Scholar Surprisingly, there is enough light in utero in the mouse to signal melanopsin. This same opsin that is present prior to rod and cone development can signal a light avoidance response in newborn mice.20Johnson J. Wu V. Donovan M. Majumdar S. Renteria R.C. Porco T. et al.Melanopsin-dependent light avoidance in neonatal mice.Proc Natl Acad Sci USA. 2010; 107: 17374-17378Crossref PubMed Scopus (104) Google Scholar Circadian rhythms regulate more than sleep cycles, and there is minimal research to explore other potential effects of light on the preterm infant. Accepting that the fetus has a circadian rhythm and the dark-exposed preterm infant does not, the conservative approach to exposure of the preterm infant to light would be cycling of dim light sufficient for care at night to brighter light during the day. The covering of the isolettes with blankets continuously seems to be questionable because visual development requires light exposure. The biology suggests that judicious light exposure is appropriate until more is known about the effects of light on the preterm infant. Physical stimulation of preterm infants is limited in the NICU today by confining the infants in positional molds and wrapping. But the fetus is intermittently active and responsive to sound stimuli with brisk movements. Much of fetal movement presumably is spontaneous, and the handling of the newborn may be a different stimulus. At the extreme, decreased fetal movements cause muscle contractions. Most caregivers support kangaroo care as of benefit to preterm infants and the parents. Kangaroo care includes substantial tactile stimulation and increased sound and light exposure relative to the isolette. Another form of stimulation is passive physical activity and massage provided by the staff. Moyer-Mileur et al reported in 1995 and again in 2000 that daily physical activity increased bone mineralization and growth in preterm infants.21Moyer-Mileur L. Luetkemeier M. Boomer L. Chan G.M. Effect of physical activity on bone mineralization in premature infants.J Ped. 1995; 127: 620-625Abstract Full Text Full Text PDF Scopus (111) Google Scholar, 22Moyer-Mileur L.J. Brunstetter V. McNaught T.P. Gill G. Chan G.M. Daily physical activity program increases bone mineralization and growth in preterm very low birth weight infants.Pediatrics. 2000; 106: 1088-1092Crossref PubMed Scopus (144) Google Scholar The loss of bone mineralization in the preterm infant relative to the fetus at equivalent gestational age results in part from the limited ability of clinicians to supply adequate calcium and phosphorus. But environment also matters, and a simple physical therapy program can reduce bone reabsorption and promote bone formation.23Haley S. Beachy J. Ivaska K.K. Slater H. Smith S. Moyer-Mileur L.J. Tactile/kinesthetic stimulation (TKS) increases tibial speed of sound and urinary osteocalcin (U-MidOC and unOC) in premature infants (29-32 weeks PMA).Bone. 2012; 51: 661-666Abstract Full Text Full Text PDF PubMed Scopus (15) Google Scholar, 24Vignochi C.M. Silveira R.C. Miura E. Canani L.H. Procianoy R.S. Physical therapy reduces bone resorption and increases bone formation in preterm infants.Am J Perinatol. 2012; 29: 573-578Crossref PubMed Scopus (26) Google Scholar This physical stimulus might be further augmented with the human voice and a bit of light. Brain plasticity can be optimized by multiple stimuli, and promotion of that plasticity is essential for optimum normal development or to improve outcomes of preterm infants with injured brains.18Baroncelli L. Braschi C. Spolidoro M. Begenisic T. Sale A. Maffei L. Nurturing brain plasticity: impact of environmental enrichment.Cell death and differentiation. 2010; 17: 1092-1103Crossref PubMed Scopus (194) Google Scholar The report by Pineda et al demonstrates adverse neurodevelopmental effects of single room neonatal care and should sound an alarm.3Pineda R.G. Neil J. Dierker D. Smyser C.D. Wallendorf M. Kidokoro H. et al.Alterations in brain structure and neurodevelopmental outcome in preterm infants hospitalized in different NICU environments.J Pediatr. 2013; 164: 52-60.e2Abstract Full Text Full Text PDF PubMed Scopus (230) Google Scholar The study is imperfect in that infants were not randomized to care environments. However, the prospective and extensive assessments have yielded results that seem to be more compelling for risk than some of the benefits attributed to developmental care.6Ohlsson A. Jacobs S.E. NIDCAP: a systematic review and meta-analyses of randomized controlled trials.Pediatrics. 2013; 131: e881-e893Crossref PubMed Scopus (112) Google Scholar My perspective is that it is time for the neonatal community to stop designing neonatal care based on what we think these infants would like (anthropomorphosis) but rather on the biology of what stimuli will optimize neurodevelopment. The preterm newborn is not equivalent to the fetus in metabolic, hormonal, or environmental needs. The biology tells us that neurosensory deprivation clearly is harmful, and is a possible consequence of the single room environment. Stimuli for the preterm seem to be conflated with stress, and too much minimization of stimuli may impair development. However, the converse is also likely true: too much stress will have adverse effects on development. We do not know how much or what type of sound, how much light, or how much physical stimulation in combination will optimize brain development and plasticity at which gestational ages. Parental participation in the care of preterm infants is desirable, as is the suppression of white noise and bright lights. We should use our resources to get answers about how to best optimize brain plasticity for the benefit of our patients.