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Journal of the American College of Nutrition, Vol. 26, No. 4, 356-359 (2007)
Published by the American College of Nutrition

Energy Expenditure in Growing Preterm Infants Receiving Massage Therapy

Sharon Lahat, MD, Francis B. Mimouni, MD, FACN, Gina Ashbel, RN and Shaul Dollberg, MD, FACN

Department of Neonatology, Lis Maternity Hospital, Tel Aviv Sourasky Medical Center, and the Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, ISRAEL

Address reprint requests to: Shaul Dollberg, MD, Department of Neonatology, Lis Maternity Hospital, Tel Aviv Sourasky Medical Center, 6 Weizman Street, Tel Aviv 64239, ISRAEL. E-mail: dollberg{at}tasmc.health.gov.il


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 REFERENCES
 
Objective: Massage therapy has been consistently shown to increase weight gain in preterm infants. The mechanism of this presumed improved metabolic efficiency is unknown. We conducted the following trial to test the hypothesis that massage therapy reduces energy expenditure in growing healthy preterm infants.

Study Design: A prospective, randomized, cross-over design study was conducted in 10 healthy, appropriate weights for gestational age, gavage fed preterm infants. Each infant was studied twice: after a period of either 5 days of massage therapy, or after a period of 5 days without massage therapy. Infants were randomized to 5 days of massage followed by 5 days of no massage (n = 5) or the opposite sequence (n = 5). During the massage therapy period, massage was provided daily for three 15 minute periods at the beginning of each 3 hour period every morning. Metabolic measurements were performed by indirect calorimetry, using the Deltatrac II Metabolic cart.

Results: Energy expenditure was significantly lower in infants after the 5 day massage therapy period (59.6 ± 3.6 Kcal/Kg/ 24 hours) than after the period without (63.1 ± 5.4 Kcal/Kg/ 24 hours) (p = 0.05).

Conclusions: Energy expenditure is significantly lowered by 5 days of massage therapy in metabolically and thermally stable preterm infants. This decrease in energy expenditure may be in part responsible for the enhanced growth caused by massage therapy.

Key words: preterm infants, massage therapy, energy expenditure, weight gain


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 REFERENCES
 
Massage therapy has consistently led to increased weight gain in preterm infants [1–6] and neonates at risk [7–8]. However, the mechanism (s) by which massage might be of benefit is (are) poorly understood. Dieter and Emory [18] have presented a comprehensive theoretical model of how massage therapy might contribute to weight gain and neurobehavioral development. It has been shown that massaged infants do not consume or retain more formula than controls [6]. Thus, the observed increase in weight gain is generally thought to be due to improved conversion of food into growth [9]. The mechanism of this improved metabolic efficiency is unknown and has been suggested by Scaffidi et al to be due to reduced adverse reaction to stress [5]. Paradoxically, research has consistently shown that preterm infants are more active during the administration of massage therapy, as well as during non-stimulation periods. To date, no study has been conducted that examined the impact of massage therapy upon resting energy expenditure in preterm infants.

We conducted the following randomized prospective clinical trial with crossover in order to test the hypothesis that massage therapy reduces resting energy expenditure in growing healthy preterm infants.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 REFERENCES
 
Patients
We studied 10 healthy, growing, consecutively born, appropriate weights for gestational age, gavage fed infants at the postmenstrual age of 29–34 weeks. All infants were clinically and thermally stable, while cared for in either a skin servo controlled incubator (n = 2) or in an infant bassinet (n = 8). At the time of the study they were all tolerating full enteral feedings without significant gastric residuals (>5% of total feed), they were all growing steadily, and had no electrolyte imbalance. No infant had any significant complication of prematurity such as intracranial hemorrhage of any grade, periventricular leukomalacia, necrotizing enterocolitis, supplemental oxygen requirements by 28 days of age or by 36 weeks of postmenstrual age and at least 1 week prior to measurement, active infection, patent ductus arteriosus, or apnea of prematurity. They were all free of congenital anomalies or dysmorphism. Prior to the study and according to our feeding protocol, infants were uniformly bolus fed every 3 hours, either their mother’s breast milk or a preterm infant formula (Similac Special Care, 67 Kcal/100 ml, Ross Laboratories, Columbus, OH). The study was approved by the local Institutional Review Board and written informed consent was obtained from the parents of each infant.

Design
Each infant was studied twice, after a period of either 5 days of massage therapy, or after a period of 5 days without massage therapy. The duration of 5 days was chosen because Dieter et al showed that 5 days of treatment are capable of promoting weight gain. [17]. During both periods, infants were receiving the same formula or breast milk at each study. The sequence in which massage therapy was provided was selected by randomization, in a manner such that 5 infants started with the massage therapy period, while 5 other infants started with the no-massage therapy period. During the massage therapy period, massage was provided daily for three 15 minute periods at the beginning of each 3 hour periods every morning for 5 days as described previously by us [6], and based upon the duration, setting and medium pressure massage described by Field and Dieter [1,17].

Metabolic studies were conducted while the infants were prone and asleep, and at the same time of the morning and noon in all infants. Measurements were stopped during body movements (less than 5% of the time of measurement). During the metabolic study infants were cared for in their own, convective incubator or bassinet and infants were in the incubator or the bassinet for the entire 12 study days. The air temperature in the neonatal intensive care unit during the whole study period was maintained at 21–22.5°C using a central computerized air conditioning system. Air temperature inside the incubator was servo-controlled in order to keep skin temperature over the back at 37°C. Thus both in infants cared for in an incubator, or in a bassinet, the two energy expenditure measurements were made in nearly identical thermal environments.

Measurements
Metabolic measurements were performed by indirect calorimetry, using the Deltatrac II Metabolic monitor (Datex-Ohmeda, Helsinki, Finland). The head of the infant is placed in a transparent hood with an open circuit system that allows continuous measurements of oxygen consumption (VO2) and carbon dioxide production (VCO2) using a constant flow generator. The measurement ranges for both O2 consumption and CO2 production of 5–2000 ml/minute allow measurements in preterm infants with small tidal volumes. Prior to the measurement, the device performs a self-calibration based on independently measured barometric pressure. Additionally, periodic testing for accuracy was performed by alcohol burning according to the manufacturer instructions. This method is safe and allows prolonged measurements while allowing reasonable access to the infant for routine care. Validation studies have shown the technique to give results equivalent to direct measurements [10]. In our hands, the instrument has a consistent intra-assay coefficient of variation of 3%.

Statistical Analysis
The sample size of 10 infants (that is 20 measurements) was chosen empirically as a pilot. Comparison of energy expenditure values between groups was performed using paired t-test. Results are expressed as mean ± SD; a P-value of ≤0.05 was considered significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
REFERENCES
 
Clinical characteristics of the study infants were as follows: there were 5 males and 5 females. Mean birthweight was 1384 ± 441 g; mean gestational age was 32 ± 1.7 weeks; mean chronological age at the time of study was 3.5 ± 2.0 weeks; Five infants out of 10 had previously suffered from RDS; Six out of 10 infants were treated with erythropoietin; and 1 out of the 10 was treated with caffeine for apnea of prematurity during the entire study period. Energy expenditure was significantly lower in infants after the 5 day massage therapy period (59.6 ± 3.6 Kcal/Kg/ 24 hours) than after the period without (63.1 ± 5.4 Kcal/Kg/ 24 hours) (p = 0.05). There was no significant difference in weight gain per weight at the time of the metabolic study (17 ± 3.7 grams per kg weight per day during the massage period vs. 15 ± 3.0 grams per day at the no-massage therapy period) (p = 0.2). In multiple regression analysis, the sequence of massage therapy did not affect the lowering effect of massage on energy expenditure.


   DISCUSSION
 
Gentle tactile stimulation of preterm infants ("massage therapy") has been shown to lead to enhanced growth [1–8]. In their pioneering study, Field et al showed that infants who were randomized to tri-daily routine massage therapy gained 47% more weight than control infants randomized to standard care [1]. This observation has been confirmed by other trials, including ours [6]. The exact mechanism of this effect of tactile stimulation upon growth is unknown. It has been suggested that a change in vagal tone and the secretion of catecholamines may play a role [11]. Alternatively, tactile stimulation may result in increased production of insulin and gastrin, which may increase intestinal food absorption [12]. Finally, it is theoretically possible that enhanced hGH and IGF-1 production may play a role, since a relative deficiency of both hormones is seen when psychosocial deprivation occurs [13]. To the best of our knowledge, no study has been conducted that examined the effect of massage therapy upon metabolic rates of preterm infants. The mechanism of this improved metabolic efficiency is unknown and has been suggested by Scaffidi et al to be due to reduced adverse reaction to stress [2]. Despite the observation that infants who receive massage therapy appear to be more active and alert [1,14], it is possible that enhanced weight gain may be induced by reduced energy expenditure. We therefore conducted this prospective, randomized clinical trial with cross-over, in order to test the hypothesis that metabolic rate is lowered by massage therapy in growing healthy preterm infants.

Consistent with our hypothesis, we found that energy expenditure is significantly lower in metabolically and thermally stable preterm infants who receive routine massage therapy. Thus it is possible that improved weight gain in infants who receive massage therapy may be, in part due to decreased energy expenditure, and subsequently, increased energy storage. However, we did not find a significant difference in weight gain between the two periods of observation. However, our study was not designed to assess the effect of massage therapy upon growth (an effect studied and confirmed by several studies [1–8]), and was probably underpowered for this matter.

To the best of our knowledge, this study is the only randomized one which measured EE, and its validity is probably enhanced by the crossover design, by which each infant served as its own control. This design allowed us to eliminate eliminates biases related to differences inherent between groups i.e., differences in birthweight, socioeconomic factors, anthropometric measurements, use of caffeine [15], or mode of feeding (gavage versus oral feeding), or type of feeding [16]. However, a limitation of this study resides in its small sample size: such sample size may have clearly induced a higher risk for a type-II error (the risk of not finding an effect of massage therapy when such effect exists). This type of error has a lesser significance since in spite of its small sample size, a significant effect of massage therapy was found. In contrast, the small sample size, together with the short period of observation may have led to the fact the we could not find significant differences in weight gain during the study periods. Nevertheless, the mechanism by which massage therapy lowers energy expenditure is unknown, and probably requires additional studies. It may even appear somewhat paradoxical, in that infants who receive massage therapy appear to be more active and alert [1], a fact that should predict increased, rather than decreased energy expenditure. However, increased alertness was observed during the brief periods of massage therapy, while it is theoretically possible that between the periods of massage, infants may have been quieter and pacified, as a long term effect of the massage. Since this was studied neither in Field study [1] nor in ours [6], this could only be a working hypothesis for a further study. However, there was no impact of the massage therapy 5 days after it was stopped, in that energy expenditure was nearly identical after 5 days without massage, regardless of the sequence to which the child had been assigned.

In summary, we conclude from our study that energy expenditure is significantly lowered by 5 days of massage therapy in metabolically and thermally stable preterm infants. We speculate that this decrease in energy expenditure may be in part responsible for the enhanced growth caused by massage therapy.

Received April 22, 2005. Accepted July 11, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 REFERENCES
 

  1. Field TM, Schanberg SM, Scafidi F, Bauer CR, Vega-Lahr N, Garcia R: Tactile-kinesthetic stimulation effects on preterm neonates. Pediatrics77 :654 –658,1986 .[Abstract/Free Full Text]
  2. Scafidi F, Field T, Schanberg S, Bauer C, Tucci K, Roberts J: Massage stimulates growth in preterm infants: a replication. Infant Behav Dev13 :167 –188,1990 .[Medline]
  3. De-Roiste A, Bushnell IWR: Tactile stimulation: short and long-term benefits for preterm infants. Br J Dev Psychol41 :41 –53,1996 .
  4. Ottenbacher KJ, Muller L, Brandt D, Heintzelman A, Hojem P, Sharp P: The effectiveness of tactile stimulation as a form of early interaction: a quantitative evaluation. J Dev Behav Pediatr8 :68 –76,1987 .[Medline]
  5. Scafidi F, Field T, Schanberg SM: Factors that predict which preterm infants benefit most from massage therapy. J Dev Behav Pediatr14 :176 –180,1993 .[Medline]
  6. Ferber SG, Kuint J, Weller A, Feldman R, Dollberg S, Arbel E, Kohelet D: Massage therapy by mothers and trained professionals enhances weight gain in preterm infants. Early Hum Dev67 :37 –45,2002 .[Medline]
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  9. Vickers A, Ohlsson A, Lacy JB, Horsle: Massage for promoting growth and development of preterm and/or low birth-weight infants. Cochrane Database Syst Rev2 : CD000390,2004 .
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  11. Acolet D, Modi N, Giannakoulopoulos X, Bond C, Weg W, Clow A, Glover V: Changes in plasma cortisol and catecholamine concentrati ons in response to massage in preterm infants. Arch Dis Child68 :29 –31,1993 .[Abstract/Free Full Text]
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This Article
Right arrow Abstract Freely available
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Right arrow Articles by Lahat, S.
Right arrow Articles by Dollberg, S.
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Right arrow Articles by Lahat, S.
Right arrow Articles by Dollberg, S.

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