The Vulnerable Neonate and the Neonatal Intensive Care Environment
Penny Glass
Technologic advances in care of the sick newborn infant have led to major improvement in mortality rates over the past three decades, especially for the very-low-birth-weight newborn. However, morbidity among survivors remains a significant and ongoing problem. Throughout early childhood, developmental and behavioral differences exist between preterm and healthy full-term infants, even when matched for conceptional age. The preterm infant often shows manifestations of altered brain organization, including disrupted sleep, difficult temperament, hypo- and hypersensitivity to sensory input, prolonged attention to redundant information, inattention to novel stimuli, and poor quality of motor function (1,2,3,4,5). These precursors of learning disabilities and social/emotional problems at school age may occur in more than 50% of Neonatal Intensive Care Unit (NICU) survivors and are not fully explained among preterm infants by either the severity of illness or the subsequent home environment (2). Increasing evidence points to the vulnerability of the immature human brain to pain and stress and to abnormal sensory and social environments. Altogether, this extensive knowledge base supports the ongoing impetus to change the intensive care nursery experience for both the neonate and the family.
In virtually every respect, the NICU is different from the prenatal environment of the fetus and from the home environment of the full-term newborn. The birth of a newborn who requires intensive care is immediately followed by physical separation from the mother and her cohesive protective role, impacting the mother, the infant, and their relationship. The NICU experience includes frequent aversive procedures, excess handling, disturbance of rest, noxious oral stimulation, noise, and bright light. These events and conditions are all sources of stress and physiologic instability. Noxious stimuli disrupt sleep, which can also have biologic consequences for the neonate. Even some medical complications commonly associated with prematurity per se, such as bronchopulmonary dysplasia and necrotizing enterocolitis, may be, in part, stress-related diseases (6).
Appropriate sensory input is essential during maturation. The most vulnerable period occurs during rapid brain growth and neuronal differentiation, which corresponds to 28 to 40 weeks of gestation for the human fetus (7,8,9). Alterations in postnatal brain development have been well demonstrated in the preterm population. It is assumed that for a fetus, the optimal environment is within the womb, and this environment changes as gestation advances. Although it is not practical or feasible to replicate the womb, it provides a point of departure for developing a better sensory, physical, and social environment in the NICU.
The purpose of this chapter is to lend a framework to developmental interventions in the NICU by summarizing the maturation of each sensory system during fetal life and how this relates to the developing neonate in the NICU environment.
▪ NEONATAL SENSORY SYSTEMS
Maturation of all the sensory systems begins during the latter part of embryo gestation. The process is neither unitary nor fixed, in that to some extent, sensory input drives maturation (10). The rate of maturation of each sensory system varies, with the onset of function generally on the following order: tactile, vestibular, gustatory-olfactory, auditory, and visual (11). These sensory systems are also interrelated in a hierarchical manner—stimulation of early maturing senses (e.g., tactile, vestibular) has a positive influence on development of later-maturing ones (e.g., visual) (12). Recent research also indicates that untimely, or precocious, stimulation (e.g., visual) may disrupt the normal maturational process of another sensory system (e.g., auditory) (Philbin MK, Personal communication, 1998).
Tactile System
It is widely known that cortical representation of tactile stimuli is somatotopic and contralateral to the stimulated side. It is also important to note that increased stimulation to an area of the body can alter the pattern of representation in the sensory cortex. Tactile hypersensitivity, or tactile defensive behavior, is described in clinical reports of children with developmental delay, many of whom were born preterm. It is also seen in infants and children who otherwise appear normal. It appears as an overreaction to touch, generally the hands or oral-facial regions. With oral hypersensitivity, the infant may withdraw, gag, or retch when touched, even around the outside of the mouth. Some children are intolerant of normal clothing and even may avoid body contact. Hypersensitivity and hyposensitivity adversely affect parent-infant bonding.
The tactile sense, like the vestibular system, develops very early in fetal life. Receptor cells are present in the perioral region by 8 weeks postconception and spread to all skin and mucosal surfaces by 20 weeks. Response to stroking the lip region occurs first (8 weeks) (13) followed by stimulation of the palmar surface, with most of the body sensitive to touch as early as 15 weeks. The somatosensory cortical pathway is intact by 20 to 24 weeks.
Tactile threshold is very low in the preterm infant, increasing by term. Prior to 30 weeks of gestation, a preterm infant responds with leg withdrawal to a pressure that is 1/3 of the pressure necessary to elicit the same response in a term infant (14). An important, qualitative shift in tactile sensitivity occurs around 32 weeks postconception. Younger preterm infants respond to repeated stimulation with sensitization and diffuse behavioral response, whereas after 32 weeks, infants show habituation to the same stimuli.
Classic studies (15) have demonstrated the profound importance of contact comfort for normal development. In parallel fashion, preterm infants seek and maintain contact with a physical object in their incubator, and more so if the tactile source contains rhythmic stimulation (16).
Early Fetal Experience
The fetus is housed in a thermoneutral, fluid-filled space that is a source of cutaneous input from the entire body surface. Fetal movement provides tactile self-stimulation and, perhaps even more importantly, often evokes a contingent maternal response. As term approaches and the intrauterine space becomes more constraining, the normal posture of flexion facilitates hand-mouth, skin-to-skin, and body-on-body tactile feedback. The effect is progressive, gradually changing throughout gestation. After a normal term birth, a ventral-to-ventral position is preferred by both mother and infant, with touch followed by slow stroking (17). Traditionally, the infant is then swaddled and held. Human proximity is universal under normal circumstances.
Touch and Handling in the NICU
The type and frequency of tactile stimulation imposed on a sick newborn in the NICU would be overwhelming even for a healthy adult. They may be handled by more than 10 different nurses in the course of a month, in addition to physicians, occupational or physical therapists, laboratory and x-ray technicians, and the
parents. Handling occurs more often among the sickest infants, typically is related to procedures, generally is disturbing, and often is painful. Sleep has important biologic and immunologic consequences (18,19) and may be disrupted by frequent intrusions. In addition, excess handling may have other negative physiologic consequences, such as effects on blood pressure, cerebral blood flow, and oxygen saturation.
parents. Handling occurs more often among the sickest infants, typically is related to procedures, generally is disturbing, and often is painful. Sleep has important biologic and immunologic consequences (18,19) and may be disrupted by frequent intrusions. In addition, excess handling may have other negative physiologic consequences, such as effects on blood pressure, cerebral blood flow, and oxygen saturation.
More benign manipulations, such as those that occur during neurodevelopmental assessment, are associated with elevated cortisol levels (20,21). It is not clear whether this is a response to the assessment itself or to stress associated with crying, but handling per se appears stressful even for a stable preterm infant.
Tactile Intervention in the NICU
The two general approaches to tactile intervention in the NICU provide either a reduction of general handling or a provision of planned touch experiences. Touch may be pressure alone from an adult’s open palm at rest, or may include stroking. The neonates may be acutely ill or medically stable. These distinctions are important.
As part of an individualized approach to developmental care of acutely ill preterm infants, Als and colleagues (22) provided a model of minimal handling and clustering of routine procedures, in addition to positioning devices and techniques to improve postural flexion. Their approach triggered a significant change in the role of the nurse, to that of a caregiver.
More specific to the tactile modality, Jay (23) evaluated the effects of gentle touch for 12-minute periods four times a day on acutely ill preterm infants. This intervention consisted of hands on contact, but no stroking or manipulating, and was associated with a lower required fraction of inspired oxygen (FIO2) after 5 days compared to a similar nonintervention group.
A different approach has been successful employed by Field et al., and Scafidi et al., with preterm infants who were beyond their acute phase, stable, and growing (24,25). The treatment involved infant massage (i.e., stroking and passive limb movement). Compared to nonintervention groups, the massaged infants showed greater weight gain (on the same amount of formula), spent more time awake, showed better performance on the Brazelton neonatal assessment, were discharged home 6 days sooner, and had better performance on developmental assessment at 8 months past term.
Although the overall effects of the tactile interventions have been positive, the response of individual infants is variable, and the timing of the intervention may be less than optimal when protocols are used. An unintended response, such as oxygen desaturation, may occur during the intervention or afterward, and may not be adequately monitored. Individual differences also exist among caregivers. Teaching the parent a gradual approach, which begins early with steady/hands-on, is likely to have additional benefit in terms of bonding and helps to encourage the parenting role during visits.
Soft swaddling and soft clothing provide tactile input in a more sustained fashion and are more widely accepted. Early swaddling should provide a loose boundary for the limbs, rather than the more traditional firm swaddling. The use of swaddling in the NICU is necessary if the parent is to retain that option at home as a means of calming and supporting sleep. Swaddling is difficult to reinitiate after a period when the infant is unswaddled. Once discharged home, NICU parents are apt to place their baby prone to sleep because they sleep longer, in spite of the “Back to Sleep” teaching and literature that is made available.
Nonnutritive Sucking
Nonnutritive sucking (NNS) is an important oral-tactile intervention that supports both feeding and behavioral regulation. It represents an early endogenous rhythm and manifestation of sensorimotor integration (26), is reported to occur in the fetus (27), and is observed in the preterm newborn prior to 28 weeks of gestation. The number of sucks per burst increases with maturation, whereas the duration of burst remains fairly stable.
NNS experience may facilitate important physiologic and behavioral mechanisms that potentially reduce cost of care (28,29). It has a positive effect during gavage feeding by improving gastrointestinal transit time, improving suck pressure and number of sucks per burst, and decreasing sporadic sucks. NNS is associated with earlier onset of bottle feeding, better weight gain, and shorter hospital stays. However, having a pacifier continuously available may not be beneficial and may encourage inappropriate sucking patterns, particularly in the chronically ill neonate.
NNS also serves as a behavioral organizer by increasing quiet/alert state and decreasing motor activity, which in turn facilitates social interaction. In addition, NNS dampens an infant’s behavioral response, but not the cortisol response, after a painful procedure (i.e., heel stick, circumcision) (20,30,31). It is noteworthy, however, that sucking on a pacifier before and during repeated painful procedures may be inappropriate, because aversive conditioning to the pacifier could result. This cautionary note is also included in recent studies showing a similar decreased behavioral response to heel stick during nursing.
Vestibular System
The vestibular system responds to movement and directional changes in gravity. It is situated in the nonauditory labyrinth of the inner ear and connects to the cerebellum, rather than the cortex. Lack of normal vestibular stimulation in a developing organism is thought to affect general neurobehavioral organization (12).
Initial vestibular development is concurrent with auditory development, emanating from the same otocyst early in gestation. The three semicircular canals reach morphologic maturity by 14 weeks postconception and full size by week 20 (10). Response to vestibular stimulation has been observed by 25 weeks (32). The traditional vertex presentation of the fetus at term is thought to result from fetal activity induced in response to vestibular input.
Intrauterine Vestibular Experience
The fetus experiences both contingent and noncontingent vestibular stimulation, which varies during gestation. Fetal movement is first reported by mothers around 16 weeks postconception. After 28 weeks of gestation, with the decrease in the relative amount of amniotic fluid, the movement of the fetus becomes constrained by the more limited physical space. Vestibular experience is thereafter less contingent upon self-activation and more related to normal maternal activity and position change, which often occurs in response to fetal activity. In general, maternal activity level slows as parturition approaches.
After birth, the infant normally is held. Movement is slow, and change of position is gradual, even in the arms of an experienced parent. Thereafter, the infant experiences multiple episodes of slow movement in space and changes of position with each feeding/diapering episode, or when carried from room to room.
Vestibular stimulation per se is typically used to influence state—moving upright to increase arousal, or monotonous side-to-side rocking and parental pacing to induce sleep. More vigorous position changes are usually initiated when an infant is crying. Stimulation in this manner is highly contingent on the infant’s behavior and response, with variation in rate, rhythm, and duration.
Vestibular Experience in the NICU
In the NICU, the infant is typically nursed on a stationary surface, thus vestibular stimulation is limited to efficient manipulation or turning of the neonate by the caregiver and clearly lacks any of the temporal qualities or contingencies that the fetal or typical postnatal environment would have provided. Spontaneous limb
movement is generally diffuse, often unrestricted, and typically disorganizing in its effect. Infants requiring mechanical ventilation experience even less position change.
movement is generally diffuse, often unrestricted, and typically disorganizing in its effect. Infants requiring mechanical ventilation experience even less position change.
Vestibular Intervention in the NICU
Like the tactile sense, the early development of the vestibular system provides a theoretical basis for primary intervention within the NICU environment, but implementation has varied. Initial studies supported the use of an oscillating waterbed or air mattress to reduce apnea of prematurity, improve sleep state organization/alertness, decrease irritability, enhance motor behaviors, and improve somatic growth (33,34,35,36). Importantly, these studies were limited to medically stable preterm infants. A subsequent clinical trial (37) failed to confirm a reduction in apneic episodes or changes in neurobehavioral responses; however, the study cohorts included infants requiring ventilator support. More recent findings have demonstrated a positive effect of vestibular stimulation on apnea and oxygen saturation (38). Thus, it would seem reasonable to consider a trial on an oscillating water bed/air mattress, for an otherwise stable infant with apnea/oxygen desaturations, before assuming that pharmacologic intervention is required.
Other sources of vestibular stimulation, such as swings, hammocks, and rocking/vibrating seats, have not been investigated formally. A rocking chair for an adult belongs at each infant’s bedside. Swings are questionable, given the excessive upright position of the baby and the standard rate of oscillation (too fast and invariant), especially for an infant with a feeding issue. A crib has been devised that provides controlled motion that is designed to be similar to a woman in late pregnancy walking. The rate of oscillation of this crib appears too rapid for a preterm infant, but the device has shown some effect in modulating fussiness in full-term infants. The duration of the motion may be individually controlled and proportionally reduced over time (39).
Positioning
The physical position of an infant is a part of the NICU tactile-vestibular experience. In the past, nursing care for sick infants was routinely provided with the infant in supine position and exposed, thus simplifying management, but not optimal for the infant. More recently, management in supine has incorporated small devices to reduce the shoulder and hip abduction effects and to incorporate more natural upper and lower limb flexion, which may have long-term benefits (40). This “nesting” approach has the added effect of visually improving the physical appearance of the infant, an important benefit for both parents and staff.
Prone positioning in the NICU has been strongly supported physiologically, with resulting improved gastric emptying, more quiet sleep, and less crying, in addition to higher PAO2 (41,42,43,44). The evidence suggests that, when possible, the infant with respiratory compromise should be nursed in a prone position, with a slight elevation of the head of the bed. Elevation of the head is particularly important if enteral feedings have been initiated.
The dilemma is that, due to the increased risk for sudden infant death syndrome (SIDS), the prone sleep position is contrary to the recommendation by the American Academy of Pediatrics (AAP). Parents are highly influenced by the manner in which their infant is cared for in the NICU. In spite of the information provided to them prior to NICU discharge about “Back to Sleep,” they are apt to continue to place their infant prone to sleep once home, stating that the baby sleeps better.
Kangaroo Care
Kangaroo care, which evolved primarily in South America in an effort to discharge small or near term infants earlier from hospital, is widely used in Level III NICUs. Traditionally, the infant is clad only in a diaper and “nested,” upright, under the mother’s clothing between her breasts, remaining there according to the mother’s comfort and the infant’s physiologic stability, and feeding on demand. The technique provides familiar, multimodal stimulation: tactile, vestibular, proprioceptive, olfactory, taste, and auditory. Kangaroo care appears to be safe for medically stable larger preterm or full-term infants, in whom it demonstrates the greatest benefits in the facilitation and maintenance of lactation and enhancement of the maternal sense of competency.
More caution should be used with infants who are less than 32 weeks of postconceptual age (PCA) or still requiring mechanical ventilation. The primary consideration should be whether the increased stimulation and additional handling might overstress the immature or sick infant. It is important to note that the vast majority of research reporting the benefits of skin-to-skin contact did not use other forms of holding/cuddling by a parent as a comparison, but compared infants receiving kangaroo care to infants lying stationary in an incubator or crib (45).
Successful kangaroo experience by the mother in the NICU also has a major caveat. Clinical reports have shown that it may encourage prone sleeping on the mother’s chest after discharge home (exhausted parents will tend to also fall asleep), contrary to APA recommendations regarding SIDS prevention.
Chemical Senses
Chemoreceptors include taste and olfaction. Taste receptors are in the taste buds, which are located primarily in the papillae of the tongue but are also found on the soft palate and epiglottis (10,46). Taste stimuli (i.e., sweet, sour, bitter, salt) transmit to the brainstem, and the hypothalamus. Cortical regions are involved in learned taste preferences. Olfactory receptors are located in the lining of the olfactory epithelium in the posterior portion of the nasal passage. The afferent pathway has no cortical projection area but connects directly to the limbic system. Olfaction also is an integral part of infant/maternal attachment and may be as important to maternal bonding with her infant as it is in reverse (47).
Chemoreceptors are well developed within the first trimester (10,46). Taste buds appear around 8 to 9 weeks, and receptors are present by 16 weeks, increasing by term to adult levels. Taste discrimination at term is sufficiently sensitive to detect a 0.1 mol/L concentration of NaCl in water (48). Full-term neonates, even anencephalic infants, demonstrate reliably discriminable facial expressions to sweet, bitter, sour, and salt (49). In a behavior described as “savoring”, normal newborns discriminate between different concentrations of sucrose and even among various sugars (48).
In the fetus, taste receptors are functional by 34 weeks, with a differential behavioral response to distinct tastes injected into the amniotic fluid: increased swallowing with sweeter taste and decreased swallowing with bitter taste (10). By 30 weeks of gestation, preterm infants show stronger sucking in response to glucose, compared to plain water (50). Behavioral response to formula, or breast milk, administered to the tip of the tongue has been documented in preterm infants prior to 28 weeks of gestation (Zorc L, Unpublished doctoral dissertation, 2000).
Stimulation of taste receptors has important implications for early feeding and behavioral regulation. Smotherman and Robinson (51) hypothesized that tastes of milk activate a centrally mediated endogenous opioid system in newborn term infants, consistent with their animal model. Thus, in normal development, the mechanism to support early feeding might very well extend beyond maintenance of chemical or caloric balance and become “feeding to thrive.”
The human olfactory system is composed of four anatomically distinct but integrated subsystems, each of which differentiate very early in gestation and are nearly mature prior to term birth (10,52
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