Estimulación de los niños prematuros Tiffany M. Field , PhD Pediatrics in Review Vol 24 Nº 1 Enero 2003

Almost 2 decades ago, Dr Jerry Lucey, editor of Pediatrics, said the following in a foreword to a book on stimulation of the preterm infant: “The prematurely born infant emerges into a hectic, cold, noisy, and bright environment filled with mysterious equipment and peopled by masked strangers who try to help. Almost everything done to or for the infant is painful, and that pain can certainly be felt, although it cannot be communicated. The infant who must have an endotracheal tube cannot cry and is not fed by mouth for weeks. His or her feet are slashed periodically for blood samples. The infant’s respirator roars away night and day, keeping his or her lungs inflated and sustaining life – but at what price?” In an article on stimulation of preterm infants published in Pediatrics in Review in 1988, we reviewed several studies on calming and growth-enhancing stimulation. The current article reviews studies that basically replicated the investigations reviewed in the 1988 report. The most widely documented forms of supplemental stimulation are nonnutritive sucking, kangaroo care, and massage therapy.

Nonnutritive Sucking

Sucking on the hand is one of the most common behaviors by the fetus and newborn. Indeed, some infants are born with abrasions on their wrists from vigorous sucking in utero. Newborn distress often is followed by handsucking. Nonnutrititive sucking is a

complex behavior involving the coordination of numerous muscle groups to generate rhythmic oral motor patterns (Finan, 1999). Because this behavior is less organized in preterm infants, some nurseries provide pacifiers. Research and anecdotal reports show

that nonnutritive sucking helps calm children across a broad spectrum, from the preterm infant undergoing an uncomfortable procedure to the toddler adapting to an unfamiliar situation. Nonnutritive sucking provides comfort, promotes physiologic organization, and even facilitates growth and development.

Calming, Soothing Effects

One of the first studies on the use of pacifiers for reducing pain was based on the premise that if sucking was incompatible with crying, then crying and its accompanying physiologic disorganization would be reduced when infants were given pacifiers (Field and Goldson, 1984). In this study, preterm infants were given pacifiers during heelsticks. Following pacifier sucking, the infants’ heart and respiratory rates decreased significantly. In a more recent study, nonnutritive sucking during heelsticks reduced the time of crying and heart rate in preterm neonates (Corbo et al, 2000). Although a series of studies by Blass and colleagues (1999) has documented the pain-reducing effects of sucrose and glucose as well as sucrose combined with sucking on a pacifier, a recent study comparing sucrose, glucose, and pacifiers showed that glucose plus a pacifier was the most calming, followed by the the individual uses of pacifier, sucrose, and glucose (Carbajal et al, 1999).

Thus, the analgesic effects of the pacifier are greater than those of either sucrose or glucose alone, and the optimal combination appears to be a pacifier dipped in glucose. Pacifiers also have been shown to reduce crying by 40% during circumcisions (Gunner et al, 1984). Currently, it is not known whether sucking reduces pain associated with aversive procedures and other stress or whether infants’ crying responses to pain diminish simply because sucking is incompatible with crying (Field and Goldson, 1984). Nonnutritive sucking has many of the same benefits for normal term infants, including increased state regu-lation (ability to prolong alert wakefulness without fuss-ing), oxygenation, nutrition, weight gain, and growth. State regulation may be the most frequently noted posi-tive effect of sucking, probably because it facilitates op-timal sleep and feeding states. Woodson and colleagues (1985), for example, noted that following nonnutritive sucking, less time was spent in active sleep states and more time in quiescent states, which probably contributes to more restorative sleep, physiologic organization, and growth. Gill and associates (1992) similarly noted enhanced sleep and reduced restless states following nonnutritive sucking, reporting further that nonnutritive sucking enhanced optimal feeding states. Other investigators have noted decreased crying and restlessness and more optimal feeding states following nonnutritive suck-ing (Dittrichova and Paul, 1982; McCain, 1992). Fortu-nately, fetuses have an instinctive inclination to suck on their own hands as early as 5 months’ gestation, as demonstrated on ultrasonography. During the first day after birth, infants have been observed sucking as much as 30 min/h (Koepke and Barnes, 1982). In a survey on nonnutritive sucking, 89% of parents who introduced pacifiers did so to soothe their infants (Mathur et al, 1990).

The pacifier has also been assumed to help reduce the incidence of sudden infant death syndrome (SIDS). In one study, significantly fewer SIDS infants used a pacifier for the last “reference sleep” (Fleming et al, 1999). In a subsequent study, the risk of SIDS during sleep was postulated to decrease with the use of a pacifier and by conditions facilitating arousals from sleep (Franco et al, 2000). Sleeping infants in this study were exposed to white noise of increasing intensity during rapid eye movement sleep. Infants using pacifiers during sleep had lower auditory arousal thresholds than those who did not use pacifiers during sleep, suggesting that infants who are more easily aroused are better able to organize their sleep states.  

Weight Gain and Shorter Hospital Stay

Nonnutritive sucking has been noted to increase during gavage feedings. In one study, the overall proportion of sucking engagement, the mean duration of sucking burst, the mean number of sucks per burst, and the mean duration of individual sucks within a burst increased markedly during gavage feeding compared with both pretest and posttest periods (Rochat et al, 1997). In a study by Uvnas-Moberg and colleagues (1987), stimu-lation of the oral cavity through breastfeeding or nonnu-tritive sucking increased vagal activity (as measured by heart rate and converted to vagal activity). Increased vagal activity facilitated the release of gastrointestinal food absorption hormones, including gastrin and insulin, which would be expected to facilitate food absorption and weight gain. Increased vagal activity and the release of gastrin, insulin, and glucose may explain the relationship be-tween pacifier sucking and weight gain. Preterm infants given pacifiers during tube feedings gained more weight in several studies. In a study by Field and colleagues (1982), newborns who sucked on pacifiers during tube feedings made the transition to bottle feedings 7 days earlier, were easier to bottle feed, and required less bottle repositioning and encouragement to feed by nurses. The infants using pacifiers also had fewer medical problems (including a lower incidence of necrotizing enterocoli-tis), more rapid weight gain, and a hospital discharge 6 days earlier than those not using pacifiers, leading to a significant hospital cost savings (at that time, $3,000 per baby). At 1 year of age, they continued to show a growth advantage, including greater weight and head circumfer-ence. These findings were confirmed by Anderson and as-sociates (1983) and Birnbaum and colleagues (1983), who conducted the same study but added carmine dye to the formula to follow its progression through the gastro-intestinal tract. When the infants sucked on nipples dur-ing tube feedings, the formula had a faster transit time, suggesting greater feeding efficiency. The neonates who sucked on pacifiers during tube feedings experienced greater weight gain and performed better on the Brazel-ton Neonatal Behavior Assessment Scale. In a review of 19 studies, other positive outcomes of nonnutritive suck-ing included a faster transition from tube to bottle feed-ings and a shorter length of hospital stay (Pinelli and Symington, 2000).

Exploration and Learning

Those who research the infant period have used sucking as a dependent measure in many studies on infant per-ception. For example, infants are noted to prefer their mother’s voice to another woman’s voice as early as 4 hours following birth (DeCasper and Fifer, 1980). Infants in that study sucked harder on a pacifier that turned on a recording of their mother’s voice versus a stranger’s voice. Fetuses also have been noted to suck harder upon hearing their mother’s voice in utero (Moonand Fifer, 1990).  Sucking is secondary to heart rate as the most popular measure for determining a newborn’s ability to discriminate, for example, among different colors, and to learn the musical scale (Gregg, et al 1976). Preterm infants have been noted to suck longer on a

nipple of the suckometer when the odor of maternal human milk was present (Meza et al, 1998). Similarly, the nipple has been used to assess the newborn’s discrimination of speech boundaries. For example, in a study presenting bisyllabic words, newborns discriminated bi-syllabic items with the same phonemic content by the amplitude of their nonnutritive sucking (Christophe et al, 1994). Other investigators have studied the amount of learn-ing that occurs during infant mouth exploration, docu-menting, for example, cross-modal transfer from oral touch to visual discrimination (Pecheux et al, 1988). Newborns offered nipples that had nubby and smooth textures following mouthing with the different textured nipples could discriminate the nipples (Hernandez-Reif et al, 2000; Meltzoff and Borton, 1979). As early as 5 months’ gestation, fetuses explore their hands with their mouths, an action that persists through early infancy, when the mouth explores the hands, fists, thumbs, and fingers, and virtually everything the infant grasps goes into the mouth. The very young infant who has learned mostly through sucking displays this learning by sucking harder on preferred objects.

Kangaroo Care

Kangaroo care is a practice that originated in Bogota, Colombia, in which preterm infants are carried chest-to-chest within their parent’s clothes starting at about 30 weeks’ gestation to provide tactile, kinesthetic, and vestibular stimulation and to transmit heat from the parent’s to the infant’s body. This has evolved into a practice that includes frequent breastfeeding.

Early studies of kangaroo care focused on assessing its safety using physiologic data recorded during kangaroo care versus no kangaroo care in the same infants. Acolet and colleagues (1993) found no significant differences in oxygen saturation, heart rate, and temperature. Subsequent studies addressed the positive benefits of kangaroo care, including immediate changes in physiology, longer-term changes in sleep patterns and activity level, effects on breastfeeding, reduction of undesirable physiologic changes such as apnea and bradycardia, decrease in infec-tions and illness, and subsequent decreased hospital stay. Studies focusing on physiologic changes documented significantly increased skin temperature during both ma-ternal and paternal kangaroo care and an increase in temperature and stability of oxygen consumption in a ample of infants weighing less than 1,500 g (Bauer et al, 1996, 1997). Kangaroo care infants also had less temper-ature variability (Syfrett and Anderson, 1996). Oxygen saturation was notably higher during kangaroo care ver-sus standard care (Blaymore Bier et al, 1996). In another quasi-experimental design using a pretest-posttest com-parison in which neonates served as their own controls, neonates receiving kangaroo care had more stable oxy-gen saturation (Mesmer et al, 1997).

At least two groups of investigators have noted an increase in quiet sleep frequency and reduced activity levels with kangaroo care (Ludington, 1990; Mesmer et al, 1997) that may have contributed to a decreased incidence of physiologic disorganization, including re-duced frequency of apneic episodes and bradycardia. This greater physiologic and behavioral organization also may have contributed to lower cortisol levels and subse-quent fewer infections and illness. For example, Sloan and associates (1994) noted a significantly lower rate of serious illnesses, including lower respiratory tract disor-ders, apnea, aspiration, pneumonia, septicemia, and gen-eral infections, in the kangaroo care compared with the standard care group (5% versus 18%). In addition to a lower incidence of infections, Charpak and colleagues (1997) noted a significantly shorter hospital stay in the kangaroo care babies, especially for those weighing 1,800 g or less.

Kangaroo care also appears to facilitate breastfeeding via reduced breast engorgement, higher milk produc-tion, and a longer duration of lactation (Shiau and Anderson, 1997; Whitelaw and Sleath, 1985). Wahlburg and associates (1990) reported that 90% of mothers in the kangaroo care group continued breastfeeding for the duration of the infant’s hospitalization compared with 61% in the standard care group, with 50% and 11% of the respective groups continuing breastfeeding through at least 1 month after discharge.

Babies who receive kangaroo care have been noted to have a greater mean daily weight gain and an earlier discharge, with a lower hospital care cost (Lima et al, 2000) . In this study, the breastfeeding rate was signifi-cantly higher at discharge and at 1 and 3 months post-discharge. A group in Bogota assessed the differences between hospitals that practiced kangaroo care and those that practiced traditional care (Charpak et al, 1994), noting that newborns in the kangaroo care hospitals had shorter mean durations of hospital stay, less severe infections, and higher breastfeeding rates.

A recent study documented the pain-reducing effects or analgesic effects of kangaroo care following heel lance procedures (Gray et al, 2000). Infants were randomly assigned to being held by their mothers in a whole body or skin-to-skin contact or to a “no intervention group” (swaddled in the crib) during a standard heel lance procedure. Crying and grimacing were reduced by 82% and 65% from baseline levels in the respective groups that were held during the heel lance procedure.

These studies suggest not only the safety of skin-to-skin kangaroo care, but also the immediate positive effects on physiology and the longer-term effects on sleep states, activity level, infections, illness, hospital stay, facilitating effects on breastfeeding, and pain reduction.

Massage Therapy

Another approach for calming babies was introduced by a nurse (Jay, 1982), who simply placed her hands on the backs of babies for 10 min/d for 10 days and docu-mented significant decreases in the oxygen needed by the infants. A simpler measure of the infants’ response to this treatment was the reduction in the nonstartle and startle responses during the study period. Subsequently, several investigators gave preterm infants what they called tactile/kinesthetic stimulation, which later was termed “massage therapy.” Massage therapy was probably a better term because the only tactile stimulation that was effective involved pressure rather than light touch. Lightly stroking (an instinctive reaction to their fragility) appears to be aversive to infants, who do not gain weight (Scafidi et al, 1990).

Before conducting evaluative studies, it was necessary to demonstrate that massage was not a dangerous procedure because published data (Long et al, 1980) showed that simple handling of babies for diaper changes followed by repositioning produced a decrease in Tc PO 2 . This led to the “minimal touch” procedure. When Morrow  and associates (1991) compared Tc PO 2 during massage and the heelstick procedure, they documented an average decrease in Tc PO 2 of about 14 to 16 mm during heelsticks, followed by a return to baseline after the procedure, and a negligible change in Tc PO 2 with massage therapy.

A meta-analysis of data from 19 tactile/kinesthetic stimulation studies revealed that 72% of the massaged infants were positively affected (Ottenbacher et al, 1987). Most of the infants experienced greater weight gain and better performance on developmental tasks. Those studies that did not report significant weight gain had used a light stroking procedure. Infants who gained weight had been given deeper pressure massage, thus stimulating both tactile and pressure receptors.

In one of the studies included in this meta-analysis, Field and colleagues (1986) gave massage therapy to preterm newborns for 45 minutes a day (in doses of three 15-min periods) for 10 days. On average, the infants were delivered 9 weeks preterm, weighed 2 lb, and had received 3 weeks of intensive care treatment before the study. The study was started when the primary goal was to gain weight. The massage therapy sessions had three phases. For the first and last phases, the infants were placed on their stomachs and stroked for five 1-min periods (12 strokes at approximately 5 sec per stroking motion) over each region in the following sequence: a)

from the top of the head to the neck and back to the top of the head; b) from the neck across the shoulders and back to the neck; c) from the neck to the buttocks and back to the neck; d) from the thigh to the foot to the thigh on both legs; and e) from the shoulder to the hand to the shoulder on both arms. This massage was given with moderate pressure because, as already noted, infants showed that they preferred some degree of pressure by squirming, arching their backs, and grimacing when the massage was too light. During the middle phase, the infants’ arms and legs were moved back and forth in a bicycling motion while the infants were lying on their backs.

The massaged infants in this study gained 47% more weight than the nonmassaged infants (even though the groups consumed the same amount of formula). They showed fewer stress behaviors (eg, mouthing, facial grimaces, and clenched fists). They were awake and active more of the time, even though they were expected to sleep more, and they were more alert and responsive to the examiner’s face and voice and showed more organized limb movements on the Brazelton scale. Finally, they were discharged from the hospital 6 days sooner, saving an average of $3,000 in hospital costs per infant.

At 8 months of age, the infants continued to show a weight advantage and had superior performance on the Bayley (1969) mental and motor scales (Field et al, 1987). This longer-term effect was interpreted as being due to greater responsiveness on the Brazelton Neonatal Assessment Scale at discharge, greater weight gain, going home earlier, and having parents who found it easier to respond and to relate to their babies. More positive stimulation from the parents led to better development.

In another study of massage with preterm infants, 33 mother-infant pairs were assigned randomly to one of three groups: control, talking, or interactive (massage and talking) (White-Traut and Nelson, 1988). The in-teractive group was more responsive and easier to feed. The biochemical response to massage among 11 preterm infants included consistent decreases in cortisol levels after massage and decreased skin temperature (Acolet et al, 1993).

Cocaine-exposed preterm infants also have benefited from massage therapy (Wheeden et al, 1993), showing a 28% greater daily weight gain compared with nonmas-saged cocaine-exposed infants, less irritability, fewer medical complications, and more mature motor activity.

Similar findings were noted in a study using massage therapy for newborns exposed to human immunodefi-ciency virus (HIV) (Scafidi and Field, 1997). After 2 weeks of daily massage therapy, infants showed greater weight gain, better performance on the social and motor items on the Brazelton Scale, and fewer stress behaviors than the control infants.

Weight gain has been associated with massage therapy in studies from the Philippines, Korea, and Israel (Jinon, 1996; Goldstein-Feber, 1997) and when using the pre-term massage procedure for only 5 days (Dieter et al, submitted for publication). Among other growth  mea-sures affected positively are length and head circumfer-ence (Lu et al, 1998). Increased bone density also has been demonstrated using absorptiometry (Moyer-Mileur, et al, 1995).

In a recent review of massage therapy for preterm infants, massage improved daily weight gain by an aver-age of 5 g, although no weight gain advantage was noted for light touch (Vickers et al, 2000). Massage also re-duced the average length of neonatal intensive care unit (NICU) stay by 5 days, decreased the incidence of post-natal complications, and enhanced weight at 4 to 6 months.

Despite these positive findings, the mechanism for the massage/weight gain effect remains unknown. Increased intake is unlikely because caloric consumption has not increased. In addition, although the infants were ex-pected to be calmer and less active, thereby saving calo-ries, they actually spent more time awake and active than the control group. These data have been interpreted in the context of the literature on the rat model (Mittleman and Valenstein, 1984) that suggested that exercised rats gain more weight independent of food intake. Studies of malnourished children (Torva et al, 1979) also showed that exercise without any additional food intake resulted in greater weight gain.

One of the experiments frequently conducted with rats is to remove pups from their mothers, which invari-ably results in diminished growth and decreased levels of ornithine decarboxylase (ODC), a measure of tissue growth, in the brain, heart, and liver, accompanied by a similar decrease in growth hormone (Schanberg and Field, 1987). Using this rat model to explore potential mechanisms for the weight gain associated with massage, these investigators found that the mother rat provides several different forms of stimulation, including pinching of the tails of the rat pups, light stroking, and carrying them. The mother rats spent most of their time tongue-licking the pups to stimulate voiding and defecation. Simulating the tongue-licking with a wet paint brush brought ODC levels back to normal in the brain, heart, and liver. Similarly, growth hormone returned to base-line following heavy stroking with the paint brush. The effects of stroking were contrasted with kinesthetic (rhythmic movement of limbs) and vestibular (spinning on a merry-go-round platform) stimulation. Neither kin-esthetic nor vestibular stimulation were effective in re-turning ODC and growth hormone to normal levels. The more recent discovery of a growth gene that re-sponds to touch suggests a strong genetic influence on the relationship between touching and growth.

A Swedish study (Uvnas-Moberg et al, 1987) on human infants suggested another possible mechanism. Vagal tone increased, with a consequent slowing of heart rate, during feeding. As noted previously, vagal tone also increases during massage. The Swedish study showed that stimulation of the mammary gland or the oral lining of the baby’s mouth increases vagal tone and cat-echolamines and releases gastrointestinal food absorp-tion hormones, such as insulin, gastrin, glucose, and cholecystokinin. A preliminary analysis suggested that insulin levels also increased during infant massage. Thus, stimulation to the mouth, the mammary gland, or other parts of the body can increase vagal tone, which increases the release of insulin and other food absorption hor-mones that can facilitate weight gain.

Cost-effective methods of delivering massage therapy are needed for this to become a common practice in NICUs. Because other hospital personnel have limited time and parents are not always compliant, elderly vol-unteer personnel who often help with feedings and rock-ing were asked to provide the massages in a recent study (Field et al, 1998). They massaged neglected and abused children who resided in a shelter. The study was designed  to measure massage therapy effects on both the children and the volunteer grandparents giving the massage. In this study, the grandparent volunteers reported lower anxiety levels, fewer depression symptoms, less irritability, and an improved mood after giving and after receiv-ing a massage. Their stress hormone levels (cortisol) also decreased. After 1 month of giving or getting the ther-apy, their lifestyle improved, including consuming fewer cups of coffee, having more social contacts, and making fewer trips to the doctor’s office. Somewhat surprisingly, these improvements were greater after 1 month of giving the infant massages than they were after 1 month of receiving massages. Thus, massage therapy is not only effective for infants, but it also helps the adults who are massaging them.

A comparison of entry-into-study weights in the pre-viously described studies suggests that smaller babies benefit more from massage than heavier babies. Three samples of infants whose weights ranged from 1,100 to 1,300 g at study entry gained 21% to 47% more weight than the control groups; infants who weighed almost 1,800 g did not have a greater weight gain following massage therapy. On the other hand, small size may be a contraindication because massage potentially could dis-organize the behavior and physiology of very small in-fants still in medical jeopardy.

Nonnutritive sucking and kangaroo care appear to have been widely adopted, as documented in a recent survey we conducted of 90 United States hospitals (Table). In that survey, 98% of NICUs were using kangaroo care, 97% were using nonnutritive sucking during tube feeding, and 79% were using nonnutritive sucking during heelsticks. Massage therapy was employed in 39% of units. Kangaroo care may have been successfully imple-mented because parents are the therapists. Nonnutritive sucking was cost-effective because of the ease of using a pacifier. Massage therapy may require parents to be therapists, not unlike kangaroo care, and parents may benefit much as the elderly volunteers in the previously described study did.

Summary

Three of the most popular types of stimulation in the NICU (nonnutritive sucking, kangaroo care, and mas-sage therapy) have been researched increasingly over the past few decades. Results suggest that preterm neonates benefit not only from the soothing, calming properties of these forms of simulation, but they conserve energy, can be pacified during painful procedures, and can demonstrate growth gains following this stimulation. These forms of simulation may have a common underlying mechanism that involves enhancement of vagal activity, associated slowing of the infant’s physiology, and an increase in the release of food absorption hormones.

Further research is needed to establish underlying mech-anisms, particularly because such practices rarely are es-tablished in NICUs until the underlying mechanisms are understood. In the interim, the data are sufficiently com-pelling to educate parents about the efficacy of these forms of stimulation.

Survey of Stimulation Infants Receive at United States Hospitals (N _ 90)