Journal of Pediatric Psychology, Vol. 28, No. 6, 2003, pp. 403-411
© 2003 Society of Pediatric Psychology
Stable Preterm Infants Gain More Weight and Sleep Less after Five Days of Massage Therapy
1 Touch Research Institute, University of Miami School of Medicine, 2 Center for Prenatal Assessment and Human Development, Emory University
All correspondence should be sent to John Dieter, Center for Prenatal Assessment and Human Development, Emory University Briarcliff Campus, Atlanta, Georgia 30306. E-mail: jdieter{at}emory.edu
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Abstract |
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Objective To examine the effects of 5 days of massage therapy on the weight gain and sleep/wake behavior of hospitalized stable preterm infants. Methods Massage therapy (body stroking/passive limb movement for three 15-minute periods per day) was provided to 16 preterm neonates (mean gestational age, 30.1 weeks; mean birth weight, 1359 g), and their weight gain, formula intake, kilocalories, stooling, and sleep/wake behavior were compared with a group of 16 control infants (mean gestational age, 31.1 weeks; mean birth weight, 1421 g). Results The massage group averaged 53% greater daily weight gain than the control group. The massage group spent less time sleeping at the end of 5 treatment days than the control group and more time in the drowsy state. Conclusions Healthy, low-risk preterm infants gained more weight and slept less with just 5 days of massage, in contrast to 10 days in previous studies. Results support the continued use of massage as a cost-effective therapy for medically stable preterm infants.
Key words: preterm infants; massage therapy; weight gain; behavior.
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Introduction |
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Over the last half century, numerous studies have reported that premature birth is associated with neurodevelopmental impairment that is inversely proportional to the gestational age and birth weight of the infant (Bhutta, Cleves, Casey, Cradock, & Anand, 2002
). Early postnatal difficulties include problems with
autonomic nervous system control, behavioral state organization, and attention
(Doussard-Rossevelt, Porges, &
McClenny, 1996; Perlman,
2001). Problems during infancy and early childhood include
auditory and visual deficits as well as delays in cross-modal transformations
and sensorimotor integration (Herrgard,
Karjalainen, Martikainen, & Heinonen, 1995;
Luoma, Herrgard, & Martikainen,
1998; Samson & de Groot,
2001), motor deficits such as abnormal reflexes, diminished
intraoral sucking, hypotonia, impaired postural control and gross motor
coordination, and inferior hand use, as well as difficulties with language
acquisition (Craig, Grealy, & Lee,
2000; Gorga, Stern, Ross,
& Nagler, 1991; Jennische
& Sedin, 1998; van der
Fits, Flikweert, Stremmelaar, Martijn, & Hadders-Algra, 1999).
Longitudinal studies indicate that developmental problems persist into
adolescence and include neuropsychological deficits such as lower IQs, poorer
auditory discrimination, impaired articulation and diminished word fluency,
attention-deficit disorders, and learning disabilities
(Bhutta et al. 2002;
Cherkes-Julkowski, 1998;
Jennische & Sedin, 2001;
Kok, den Ouden, Verloove-Vanhorick, &
Brand, 1998; Lane, Attanasio,
& Huselid, 1994; Tideman,
2000), as well as emotional and behavioral problems such as
hyperactivity, internalizing, and conduct disorders
(Chapieski & Evankovich,
1997; Schothorst & van
Engeland, 1996; Stjernqvist
& Svenningsen, 1999).
Researchers have provided hospitalized preterm infants with various forms
of supplemental stimulation in an effort to enrich the environment of the
neonatal intensive care unit (NICU) or to accelerate development
(Dieter & Emory, 1997;
Feldman & Eidelman, 1998).
One of the most widely studied interventions has been massage therapy
(Vickers, Ohlsson, Lacy, & Horsley,
2000). A number of studies have shown that the 10-day massage
therapy protocol introduced by Field and her colleagues
(1986) promotes weight gain in
preterm infants (Ferber et al.,
2002; Jinon, 1996;
Kuhn et al., 1991;
Scafidi et al., 1990;
Scafidi et al., 1986;
Wheeden et al., 1993). The
average daily weight gain in these studies was 28% to 47% greater in the
massaged groups despite similar formula and caloric intake.
The 10-day massage therapy protocol also alters the distribution of sleep
and awake states. Across studies, the massaged preterm infants spent more time
in active alertness and showed better performance on the Brazelton exam at the
end of the treatment period (Field,
Scafidi, & Schanberg, 1987; Scafidi et al.,
1986,
1990;
Wheeden et al., 1993).
Furthermore, the massaged preterm infants were discharged between 3 and 6 days
sooner than control infants, accounting for lower hospital costs.
The first 10-day massage study by Field and colleagues
(1986) suggested that the
weight gain advantage for the massage group first emerged after 5 days of
treatment. The goal of the current study was to examine the effects of 5 days
of massage therapy on the weight gain and sleep/awake behavior of preterm
infants. Showing that an abbreviated protocol is beneficial warrants the
continued use of massage therapy for hospitalized preterm infants who are
being discharged earlier from intermediate care nurseries and at lighter
weights.
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Method |
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Participants
Participating infants were recruited from a large inner-city hospital. Preterm infants were eligible for participation if: (a) their gestational age (GA) was between 25 and 34 weeks as assessed by an evaluation at delivery of passive tone and physical maturity (i.e., Dubowitz score) and as documented by prenatal medical records; (b) their birth weight was between 750 and 1600 g; (c) their birth weight was appropriate for their gestational age (AGA). Discrepancies between pre- and postnatal information regarding GA were ruled in favor of the decision made after birth by the attending neonatologist.
Infants with medical conditions primarily related to immaturity, such as respiratory distress syndrome, hya-line membrane disease, apnea, elevated bilirubin, and mild hypoglycemia and hypocalcemia, were not excluded. All of the infants in the study graduated from the NICU to the intermediate care nursery and had received comparable courses of treatment including oxygen and phototherapy, antibiotics, and intravenous/gavage feedings (see Table I). Preterm infants were specifically excluded if: (a) they exhibited genetic anomalies, congenital heart malformations, and/or central nervous system dysfunction; (b) they were HIV-positive; (c) there was a history of maternal drug use (by drug screen); (d) they required surgery; (e) there was any evidence of intraventricular hemorrhage on ultrasound examination; or (f) they were breast-fed. Those few infants who were breast-fed were excluded so that daily kilocalorie intake could be accurately calculated.
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A computer program (Dubin,
1990) was used to conduct a power analysis for two independent
groups based on the between-group means and standard deviations of the Field
et al. (1986) study. Findings
suggested 6 participants per group were necessary for 95% power to detect the
effect of massage therapy on weight gain (p = .01, two-tail). We
increased the group size to allow for potential attrition and to have a
reasonable participants-to-variables ratio.
Prior to recruitment, informed consent was obtained from the parents and the attending physician. The study had full institutional review board approval from the university's school of medicine. We attempted to recruit all infants who fulfilled the inclusion/exclusion criteria. The ratio of available to assigned infants was roughly 4 to 1. It was our experience that informed consent was usually obtained if the study was discussed with parents when they visited the unit. That so few infants were successfully recruited reflected primarily a failure to obtain written informed consent because of the relative scarcity of parental visits. We do not believe that health status played a role in whether parents agreed to provide consent, since all of the infants were medically stable and in the final stage of their hospital stay at time of recruitment.
A random stratification procedure was used to assign infants to either the massage therapy group (n = 16) or the control group (n = 16). All infants were medically stable and were not receiving IV fluids, oxygen, phototherapy, antibiotics, or gavage feeds at the start of the study.
On average, infants were approximately 3 weeks old at assignment. All were born to mothers of lower socioeconomic status. There were 11 (68.75%) male infants in the massage therapy group and 9 male infants (56.25%)in the control group. Nine massage infants were African American (56.25%), 5 were Hispanic (31.25%), and 2 were white (12.50%). Ten control infants were African American (62.50%), 5 were Hispanic (31.25%), and 1 was white (6.25%).
Measures and Procedure
The massage therapy protocol used by Field et al.
(1986) was also used for this
study. Massage therapy was begun on the day following study assignment, and it
was continued for 5 consecutive days. As in previous studies, the first
15-minute massage occurred approximately one hour after the morning feeding,
the second about one half hour after the midday feeding, and the third
approximately 45 minutes after the completion of the second stimulation
period.
Each treatment session consisted of 5 minutes of tactile stimulation, followed by 5 minutes of kinesthetic stimulation, and concluded with another 5-minute period of tactile stimulation. The therapist warmed his/her hands prior to the start of treatment and remained silent during the 15-minute interval.
During tactile stimulation, the infant was placed prone and was given moderate pressure stroking with the flats of the fingers of both hands. Five one-minute intervals, consisting of six 10-second periods of stroking, were applied to the following body regions: (a) from the top of the infant's head, down the back of the head to the neck and back to the top of the head; (b) from the back of the neck across the shoulders and back to the neck; (c) from the upper back down to the buttocks and returning to the upper back (contact with the spine was avoided); (d) simultaneously on both legs from the hips to the feet and back to the hips; (e) both arms simultaneously from the shoulders to the wrists to the shoulders.
For the kinesthetic phase, the infant was placed in a supine position. Each of the five one-minute segments consisted of six passive flexion/extension movements lasting approximately 10 seconds each. These "bicycling-like" movements of the limbs occurred in the following sequence: (a) right arm, (b) left arm, (c) right leg, (d) left leg, and (e) both legs simultaneously.
During massage therapy, the infant's reaction to stimulation was monitored continuously for signs of adverse events. Furthermore, intermediate care nursery personnel (i.e., physicians, nurses, and staff) were in constant attendance. Behavioral observation focused on the occurrence of signs of distress (e.g., yawning, finger splaying, crying), and physiologic reaction was monitored through heart rate and respiration rate. Because significant behavioral distress (e.g., crying) often leads to physiologic overreactivity in preterm infants, physiologic measures were used to assess adverse treatment responses. At the sign of physiologic distress (i.e., heart rate greater than 200 bpm), massage was discontinued for 15 seconds, or until a return to baseline levels was observed. Massage was then resumed. Auditory alarms warned of excessive physiologic reactivity. The occurrence of five periods of physiologic overreactivity was arbitrarily chosen as the criterion for discontinuing an infant from the study. No infant who received massage therapy needed to discontinue participation due to an adverse treatment response. Furthermore, no infant in either group experienced any significant medical complications during the course of participation.
Due to recent changes in the intermediate care nursery, preterm infants are discharged earlier following their transfer from the NICU. Therefore, the formal assessment of massage therapy effects was limited to 5 treatment days. The majority of the infants were discharged immediately after completing the study or shortly thereafter. This earlier discharge policy prohibited any direct comparison between 5 and 10 treatment days or an evaluation of the lasting effects of massage therapy after its conclusion.
Obstetric and postnatal complications were summarized on the Obstetric and
the Postnatal Complications Scale comprised of items related to pregnancy,
birth, and postnatal events (Littman &
Parmelee, 1978). Higher scores are optimal on both measures.
Nursing notes were examined daily for weight gain, volumetric input, number of bowel movements, and medications. Kilocalories (i.e., cc/kg/d) were calculated each day using the standard formula based on the day's volumetric intake and caloric content of the formula. Formula caloric content was prescribed by each infant's attending physician and remained constant throughout participation. Chi-square analysis revealed no group difference on the number of infants receiving 20 or 24 calories per ounce formula.
Daily weight gain was measured in the early morning by nurses on the preceding night shift. Group assignment was not documented in the infants' charts, in an effort to conceal participation. Regardless, it was likely that some nurses knew which infants were enrolled in the study and to which condition they were assigned. It has been our experience that such knowledge has little effect on how the infants are treated during their time in the study. None of the enrolled infants received supplemental rocking from hospital volunteers.
During each day of participation, the number of family visits was documented. Family visits usually consisted of the parent(s) holding and feeding the infant. The two groups did not differ on the frequency of family visits.
Observations of sleep/awake patterns are useful for studying the
neurobehavioral organization and development of both preterm and full-term
infants. Research indicates that during the preterm period, there is a
significant decrease in active sleep and a significant increase in quiet sleep
and quiet and active waking, as well as greater temporal organization of
sleep/awake patterns (Holditch-Davis & Edwards,
1998a,
1998b;
Ingersoll & Thoman,
1999).
Sleep/awake behaviors were coded via live observations at the same time
(i.e., between the morning and midday feeds) on the preassignment and last
days of the study. We used the same approach established by Field and
colleagues for their previous massage therapy studies (e.g., Scafidi et al.,
1986,
1990). Observations are
designed to be representative of the daytime behavioral organization of
preterms residing in the intermediate care nursery. With the exception of
early evening (when the majority of parental visits occur), the nursery's
schedule is quite consistent given that preterm infants receive
around-the-clock care. That both observations occurred at the same time of day
controlled for the potential effects that circadian rhythm or environmental
factors (e.g., reduced lighting at night) have on preterm infant behavior.
Furthermore, Day 5 observations occurred approximately 90 minutes after the
day's first massage, thus allowing sufficient time for any immediate treatment
effects on behavior to subside.
A standardized behavior coding system was used that included the following
states: (1) non-REM sleep; (2) active sleep without REM; (3) REM sleep; (4)
drowsy; (5) quiet alert; (6) active alert; (7) crying
(Thoman, 1975). The 30-minute
observations were recorded on a laptop computer using a program that records
the percent time (% time) the infant spent in each behavior state. Observers
were trained to 85% interrater.
In order to increase statistical power, the sleep/awake behavior states were combined as follows: (a) sleep, including States 1, 2, and 3; (b) awake, comprising States 5, 6, and 7; (c) quiet, consisting of States 1, 4, and 5; and (d) active, including States 2, 6, and 7. Because of the transitional quality of drowsiness, that state was excluded from the sleep/wake categories but was included in the quiet category. Since REM sleep can occur with or without motor activity, that state was excluded from the quiet or active categories.
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Results |
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Data analyses revealed no differences between groups on sex or ethnicity. Furthermore, the two groups did not differ in hospital treatment course or on the assignment day variables (see Tables I and III).
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A repeated-measures analysis of variance (massage therapy vs. control) yielded a significant group main effect for weight gain, F(1, 30) = 13.91, p = .001 (see Figure 1). On average, the massage therapy group (M = 48.7 g, SD = 36.9) gained 26 g more per day than the control group (M = 22.7 g, SD = 12.2). Univariate tests revealed that the massage therapy group gained significantly more weight than the control group on the first [F(1, 30) = 4.64, p = .04] and fourth [F(1, 30) = 6.48, p =.02] days of participation. Daily formula and kilocalorie intake, number of bowel movements, and number of family visits did not differ across groups (see Table II).
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Examination of the distribution of total weight gain values across both conditions revealed one statistical outlier in the massage therapy group (z = +3.59) and one in the control group (z = -2.20). Removal of the outliers and reanalysis failed to yield any statistically significant changes to the uncorrected findings.
A repeated-measures multivariate analysis of variance (massage therapy vs. control) yielded a significant group by day effect for state organization from the first to the last day of participation, F(3, 28) = 3.21, p =.04 (see Table III). Univariate tests revealed that the massage therapy group spent less time sleeping on the last day than the control group (M % time: 53.0, SD = 37.7 vs. 81.1, SD = 34.5), F(1, 30) = 4.81, p =.04. Post hoc analysis of the seven constituent states revealed that the massage therapy group spent more time in the drowsy state than the control group (M % time: 16.8, SD = 19.3 vs. 2.5, SD = 3.8), F(1, 30) = 8.45, p =.007 (see Table IV).
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Discussion |
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These findings support previous studies showing that massage therapy promotes weight gain and alters the distribution of sleep/awake states in preterm neonates. Those receiving massage showed a 53% greater average daily weight gain compared with the control infants. The massaged preterms in the current study showed a greater daily weight gain with just 5 days of massage, in contrast to the 10 days in prior studies.
As in previous investigations, the current study found no significant
differences between the massage therapy and control groups on formula or
kilocalorie intake. Using an animal model, Uvnas-Moberg, Widstrom, Marchini,
and Winberg (1987) proposed
that tactile stimulation heightens vagal activity, which stimulates the
release of food absorption hormones that facilitate weight gain. Field and
Schanberg (1995) evaluated
this model in human preterms and found that massage therapy increased vagal
tone and was associated with a 62% rise in insulin release. Currently, we are
examining the effects of preterm infant massage therapy on insulin-like growth
factor I and oxytocin, two peptide hormones that play a role in weight gain
and may be stimulated through heightened vagal activity.
In the previous 10-day studies, the massage therapy groups spent more time
in the awake and active states (e.g., Scafidi et al.,
1986,
1990). Five days of massage
therapy also led to a significant reduction in sleep states and an increase in
drowsiness. The reduction in sleep noted in the massage group can be viewed as
a positive effect. A recent treatment model suggests that once preterm infants
are medically stable, supplemental stimulation should be initiated to promote
the preterm infant's engagement with caregivers and the environment
(Dieter & Emory, 1997).
Along with the statistically significant increase in drowsiness, trends shown
by the massage therapy infants may reflect acceleration in the developmental
course of sleep/wake patterns in preterm infants (see
Table IV). A larger sample is
needed to confirm whether 5 days of massage therapy promotes the development
and organization of sleep/wake patterns in preterms. A comparison with 10
treatment days would be useful to determine the dose-response relationship
between massage therapy and behavioral state development.
Since the early findings of Levine
(1959,
1960;
Levine & Mullins, 1966),
animal studies have shown that supplemental stimulation or environmental
enrichment accelerates development. The "handling" paradigm has
been widely applied in these investigations. Studies consist of the
experimenter separating the animal from its mother and holding it for a period
of time. Handled rats have been shown to demonstrate less fear in novel
situations, greater exploratory behavior, better performance during stressful
challenges, lower emotional reactivity, greater weight gain, and even superior
cognitive, learning, and memory performance in old age (e.g.,
Ader, Friedman, Grota, & Schaefer,
1968; Fernandez-Teruel,
Escorihuela, Driscoll, Tobena, & Battig, 1991;
Gonzalez, Rodriguez Echandia, Cabrera,
Foscolo, & Fracchia, 1990;
Meaney, Aitken, Bhatnagar, van Berkel,
& Sapolsky, 1988). Studies have also shown that handled rats
secrete less corticosterone in adulthood than do nonhandled rats, exhibit
permanent increases in hippocampal glucocorticoid receptors, and show lower
levels of corticotropin-releasing factor and plasma adrenocorticotropin
following stressful challenges (e.g.,
Meaney et al. 1988;
Meaney, Aitken, Sharma, Viau, &
Sarrieau, 1989; Meaney,
Aitken, & Sapolsky, 1987;
Plotsky & Meaney, 1993).
Many of the effects of handling on animals appear similar to those observed in
human preterm infants receiving massage, including greater weight gain, fewer
stress signs, and superior performance on challenging neurobehavioral
examinations. Therefore, procedures such as massage therapy may in-oculate the
preterm infant against stress and promote general adaptation, presumably
through their impact on the hypothalamic-pituitary-adrenal axis. While
preliminary findings suggest that massage therapy reduces cortisol levels in
human preterm infants (Acolet et al.,
1993), further investigations are needed to support the validity
of the animal model.
Regardless of positive research findings, massage therapy has not been
widely adopted on NICUs (only 38% of nurseries use massage, based on a recent
national survey [Field, in
press]).This reflects a "minimal touch" policy that
still is maintained by many neonatologists and NICU staff
(Morrow, Field, Scafidi, Roberts, &
Eisen, 1991). The frequently cited study by Long, Alistair,
Philip, and Lucey (1980), who
observed that procedures such as feedings, diaper changes, and examinations
were sometimes associated with significant decreases in transcutaneous oxygen
saturation (tcPO2), is often used to support this minimal touch
policy. The widespread acceptance of this view has hindered the introduction
of procedures that are beyond standard nursery care.
Despite continuing controversy regarding the safety of massaging preterm
infants, at least nine studies have demonstrated the safety of massage therapy
for grower nursery infants, including Morrow and colleagues
(1991), who reported that
preterm infants exhibited clinically safe tcPO2 levels across
massage therapy sessions. Infants in the current study were closely monitored
during massage therapy. None exhibited notable physiologic overreactivity and
no infant was dropped from the study due to adverse events.
With regard to clinical guidelines, massage therapy may start whenever the preterm infant is deemed medically stable by the attending physician. Thereafter, the individual response of the infant to massage therapy should guide the course of treatment. We are currently enrolling infants who are between 1000 and 1100 g at time of recruitment. Some of these infants are even lighter at birth. Infants may be residing in either the NICU or grower nursery. Infants residing in the NICU no longer have main lines for IV feeds and antibiotics since that would prohibit administration of the standardized protocol.
Although the 5-day/weight gain results of this study require replication, they support the continued use of massage as a cost-effective therapy for grower nursery preterm infants. That the promotion of weight gain was so rapid suggests that the dose-response ratio may be lower than previously thought.
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Acknowledgments |
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The authors thank the neonates who participated in this study. This research was supported by Johnson & Johnson funds. Individuals also received funding, including an NRSA 1 F31 MH11161-01 (NIMH) and NARSAD Young Investigator Award to Dr. Dieter, an NIMH Research Scientist Award #MH00331 to Dr. Field, Grant RO-1 AT 00370 (NIH/NCCAM) to Dr. Hernandez-Reif, and Grant RO-1 HD28382 to Dr. Emory.
Received April 15, 2002; revision received September 10, 2002; revision received December 2, 2002; accepted December 3, 2002
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