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Application of tactile/kinesthetic stimulation in preterm infants: a systematic review ☆, Please cite this article as: Pepino VC, Mezzacappa MA. Application of tactile/kinesthetic stimulation in preterm infants: a systematic review. J Pediatr (Rio J). 2015;91:213-33. ☆☆ ☆☆ Study conducted at Department of Pediatrics, Faculty of Medical Sciences, Universidade Estadual de Campinas (UNICAMP), São Paulo, SP, Brazil

Abstracts

OBJECTIVE:

To verify the methods used by the clinical trials that assessed the effect of tactile/kinesthetic stimulation on weight gain in preterm infants and highlight the similarities and differences among such studies.

SOURCES:

This review collected studies from two databases, PEDro and PubMed, in July of 2014, in addition to bibliographies. Two researchers assessed the relevant titles independently, and then chose which studies to read in full and include in this review by consensus. Clinical trials that studied tactile stimulation or massage therapy whether or not associated with kinesthetic stimulation of preterm infants; that assessed weight gain after the intervention; that had a control group and were composed in English, Portuguese, or Spanish were included.

SUMMARY OF THE FINDINGS:

A total of 520 titles were found and 108 were selected for manuscript reading. Repeated studies were excluded, resulting in 40 different studies. Of these, 31 met all the inclusion criteria. There were many differences in the application of tactile/kinesthetic stimulation techniques among studies, which hindered the accurate reproduction of the procedure. Also, many studies did not describe the adverse events that occurred during stimulation, the course of action taken when such events occurred, and their effect on the outcome.

CONCLUSIONS:

These studies made a relevant contribution towards indicating tactile/kinesthetic stimulation as a promising tool. Nevertheless, there was no standard for application among them. Future studies should raise the level of methodological rigor and describe the adverse events. This may permit other researchers to be more aware of expected outcomes, and a standard technique could be established.

Preterm infants; Massage; Review; Weight gain; Tactile/kinesthetic stimulation


OBJETIVO:

Verificar quais metodologias foram usadas por ensaios clínicos que avaliaram o efeito da estimulação tátil-cinestésica sobre o ganho de peso de neonatos prematuros e destacar as diferenças e semelhanças entre esses estudos.

FONTES DOS DADOS:

Esta análise coletou estudos de duas bases de dados, Pedro e PubMed, em julho de 2014, além de bibliografias. Dois pesquisadores avaliaram os títulos relevantes independentemente e, então, escolheram consensualmente quais estudos seriam lidos completamente e incluídos nesta análise. Foram incluídos os ensaios clínicos que estudaram a estimulação tátil ou a massagem terapêutica associada ou não à estimulação cinestésica em neonatos prematuros e avaliaram o ganho de peso após a intervenção, tiveram um grupo de controle e foram escritos em inglês, português ou espanhol.

SÍNTESE DOS DADOS:

Foram encontrados 520 títulos e foram selecionados 108 para leitura. Os estudos repetidos foram excluídos, o que resultou em 40. Desses, 31 atenderam a todos os critérios de inclusão. Há muitas diferenças na aplicação das técnicas de estimulação tátil-cinestésica entre os estudos, o que prejudica a reprodução precisa do procedimento. Além disso, muitos estudos não descreviam os eventos adversos ocorridos durante a estimulação, o procedimento feito quando esses eventos ocorriam e seu efeito sobre o resultado.

CONCLUSÕES:

Esses estudos fizeram uma contribuição relevante ao incluir a estimulação tátil-cinestésica como uma ferramenta promissora. Contudo, não houve padrão de aplicação entre eles. Estudos futuros podem aumentar o nível do rigor metodológico e descrever os eventos adversos. Isso pode permitir que outros pesquisadores tenham mais ciência do que esperar e assim estabelecer uma técnica padrão.

Neonatos prematuros; Massagem; Análise; Ganho de peso; Estimulação tátil-cinestésica


Introduction

Preterm infants (PI) are exposed daily to many stressors in the neonatal intensive care unit (NICU) inherent to the critical care they need to survive. The manner and intensity of exposure vary according to the individual PI condition and response. It has already been shown that such exposure leads to structural and functional changes in specific areas of the brain, affecting its development,1Smith GC, Gutovich J, Smyser C, Pineda R, Newnham C, Tjoeng TH, et al. Neonatal intensive care unit stress is asso- ciated with brain development in preterm infants. Ann Neurol. 2011;70:541-9.language, and social-emotional and adaptive behavior.2Fernandes LV, Goulart AL, Santos AM, Barros MC, Guerra CC, Kopelman BI. Neurodevelopmental assessment of very low birth weight preterm infants at corrected age of 18-24 months by Bayley III scales. J Pediatr (Rio J). 2012;88:471-8.

Tactile stimulation (TS) or massage therapy (MT), sometimes associated with kinesthetic stimulation (KS), is used in PI along with the standard clinical treatment. TS have been the object of clinical studies since the 1960s,3White JL, Labarba RC. The effects of tactile and kinesthetic stimulation on neonatal development in the premature infant. Dev Psychobiol. 1976;9:569-77.when it was proposed as a means of encouraging PI growth and development.3White JL, Labarba RC. The effects of tactile and kinesthetic stimulation on neonatal development in the premature infant. Dev Psychobiol. 1976;9:569-77. , 4Freedman DG, Boverman H, Freedman N. The effects of kines- thetic stimulation on weight gain and on smiling in premature infants Paper presented at the annual meeting of the American Orthopsychiatric Association. San Francisco; 1966. , 5Hasselmeyer EG. The premature neonate's response to hand- ling. American Nursing Association. 1964;11:15-24. , 6Solkoff N, Weintraub D, Yaffe S, Blasé B. Effects of handling on the subsequent development of premature infants. Dev Psychol. 1969;1:765-9. , 7Kramer M, Chamorro I, Green D, Knudtson F. Extra tactile stim- ulation of the premature infant. Nurs Res. 1975;24:324-34. , 8Solkoff N, Matuszak D. Tactile stimulation and behavioral devel- opment among low-birth weight infants. Child Psychiatry Hum Dev. 1975;6:33-7. , 9Rausch PB. Effects of tactile and kinesthetic stimulation on premature infants. JOGN Nurs. 1981;10:34-7. and 1010 Field TM, Schanberg SM, Scafidi F, Bauer CR, Vega-Lahr N, Garcia R, et al. Tactile/kinesthetic stimulation effects on preterm neonates. Pediatrics. 1986;77:654-8. Additionally, recent studies have shown that interventions such as tactile/kinesthetic stimulation (TKS) have the added benefit of reducing behavioral manifestations of stress.1111 Hernandez-Reif M, Diego M, Field T. Preterm infants show reduced stress behaviors and activity after 5 days of massage therapy. Infant Behav Dev. 2007;30:557-61.

The objective of this systematic review was to verify which methodologies were used by clinical trials that study the effects of some types of TS/MT, whether or not associated with KS, on weight gain of PI. Clinical trials were selected that studied the effects on weight gain, as this is a determinant variable for discharge from the NICU. The differences and similarities between the methods used by the reviewed clinical trials were highlighted in an attempt to improve the methodological quality of future trials.

Methods

Two databases were searched for this systematic review: the Physiotherapy Evidence Database (PEDro)1212 Physiotherapy Evidence Database (PEDro). [cited 17 Jul 2014]. Available from: http://www.pedro.fhs.usyd.edu.au
http://www.pedro.fhs.usyd.edu.au...
and the United States National Library of Medicine of the National Institutes of Health (PubMed).1313 United States National Library of Medicine of the National Institutes of Health. [cited 17 Jul 2014]. Available from: www.ncbi.nlm.nih.gov/pubmed
www.ncbi.nlm.nih.gov/pubmed...
All studies listed on the date of search were accessed.

The PEDro database was searched by specifying the following fields in the advanced search option: therapy (stretching, mobilization, manipulation, massage); subdiscipline (pediatrics), and method (clinical trial).

PubMed was searched using six keyword combinations, as follows:

- Search 1: massage premature newborn

- Search 2: tactile kinesthetic stimulation

premature

- Search 3: tactile stimulation premature

- Search 4: massage premature growth

- Search 5: kinesthetic stimulation premature growth

- Search 6: tactile kinesthetic stimulation premature growth

In addition to these searches, the references of the chosen articles were also checked, and another 12 relevant articles were selected for evaluation.

Inclusion criteria

Two independent researchers preselected the articles according to their titles. In case of doubt, the article was included in the selection process by consensus. The preselected titles were then stored in a file according to the database they were found, and their abstracts or texts were downloaded for assessment. Once downloaded, the articles were thoroughly read to select those that met the inclusion criteria detailed below.

The present review included all clinical trials that studied the provision of TS or MT, whether or not associated with KS, for PI in the NICU, assessed PI weight gain after the intervention, had a control group that did not receive any intervention in addition to the standard treatment provided by the NICU, and were composed in English, Portuguese, or Spanish.

Results

A total of 508 articles were found in the two abovementioned databases. Seventeen articles were fully read among the 206 articles found in the PEDro database, of which eight met the inclusion criteria. The first search on PubMed resulted in 126 titles, of which 30 were selected and 18 met the inclusion criteria. The second search on PubMed resulted in 16 titles, of which ten were selected and eight met the inclusion criteria. The third search on PubMed resulted in 86 titles, of which 14 were selected and ten met the inclusion criteria. The fourth search on PubMed resulted in 49 titles, of which 23 were selected and 16 met the inclusion criteria. The fifth search on PubMed resulted in 14 titles, of which nine were selected and six met the inclusion criteria. The sixth search on PubMed resulted in 11 titles, of which eight were selected and five met the inclusion criteria.

However, another 12 titles found in the references of the articles that met the inclusion criteria were analyzed, and of these, four were included, five were excluded, and three were not found. Table 1 shows the titles and where they were found.

Table 1.
Descriptions of the included studies.

In summary, 520 titles were found; the repeated studies were eliminated, resulting in 31 that met the inclusion criteria of the present review (Table 1).

TS/MT was done in many different ways,3White JL, Labarba RC. The effects of tactile and kinesthetic stimulation on neonatal development in the premature infant. Dev Psychobiol. 1976;9:569-77. , 9Rausch PB. Effects of tactile and kinesthetic stimulation on premature infants. JOGN Nurs. 1981;10:34-7. , 1010 Field TM, Schanberg SM, Scafidi F, Bauer CR, Vega-Lahr N, Garcia R, et al. Tactile/kinesthetic stimulation effects on preterm neonates. Pediatrics. 1986;77:654-8. , 1414 Mathai S, Fernandez A, Mondkar J, Kanbur W. Effects of tactile- kinesthetic stimulation in preterms: a controlled trial. Indian Pediatr. 2001;38:1091-8. , 1515 Ferber SG, Kuint J, Weller A, Feldman R, Dollberg S, Arbel E, et al. Massage therapy by mothers and trained profession- als enhances weight gain in preterm infants. Early Hum Dev. 2002;67:37-45. , 1616 Mendes EW, Procianoy RS. Massage therapy reduces hospital stay and occurrence of late-onset sepsis in very preterm neonates. J Perinatol. 2008;28:815-20. , 1717 Gonzalez AP, Vasquez-Mendoza G, García-Vela A, Guzmán-Ramirez A, Salazar-Torres M, Romero-Gutierrez G. Weight gain in preterm infants following parent-administered Vimala massage: a randomized controlled trial. Am J Perinatol. 2009;26:247-52. and 1818 Fucile S, Gisel EG. Sensorimotor interventions improve growth and motor function in preterm infants. Neonatal Netw. 2010;29:359-66. and the most of the studies did not provide a detailed description of how to proceed during the stimulation if adverse events occur, nor of the possible effects of these events on the outcomes.

Analysis of the techniques used by different studies showed that older studies, such as Solkoff et al.,6Solkoff N, Weintraub D, Yaffe S, Blasé B. Effects of handling on the subsequent development of premature infants. Dev Psychol. 1969;1:765-9. Kramer et al.,7Kramer M, Chamorro I, Green D, Knudtson F. Extra tactile stim- ulation of the premature infant. Nurs Res. 1975;24:324-34. and Solkoff & Matuszak8Solkoff N, Matuszak D. Tactile stimulation and behavioral devel- opment among low-birth weight infants. Child Psychiatry Hum Dev. 1975;6:33-7. did not specify which parts of the body were stimulated or how often. The pressure used during the intervention and its duration varied greatly between these studies.

White & Labarba3White JL, Labarba RC. The effects of tactile and kinesthetic stimulation on neonatal development in the premature infant. Dev Psychobiol. 1976;9:569-77. were the first to combine TS and KS. In 1981, Rausch9Rausch PB. Effects of tactile and kinesthetic stimulation on premature infants. JOGN Nurs. 1981;10:34-7. divided TKS into three phases of five minutes each and applied TKS only when the PI were awake, without changing their position in the incubator. Both Lee1919 Lee HK. The effect of infant massage on weight gain, physio- logical and behavioral responses in premature infants. Taehan Kanho Hakhoe Chi. 2005;35:1451-60. and Ferreira & Bergamasco2020 Ferreira AM, Bergamasco NH. Behavioral analysis of preterm neonates included in a tactile and kinesthetic stimulation pro- gram during hospitalization. Rev Bras Fisioter. 2010;14:141-8.followed these procedures. Rausch9Rausch PB. Effects of tactile and kinesthetic stimulation on premature infants. JOGN Nurs. 1981;10:34-7. suggested that new studies should provide the intervention for at least ten days, because weight gain increased after this period. Rausch's9Rausch PB. Effects of tactile and kinesthetic stimulation on premature infants. JOGN Nurs. 1981;10:34-7. study was the first to show significantly faster weight gain in PI submitted to TKS and to describe the technique used in detail.

Scafidi et al. 2121 Scafidi FA, Field TM, Schanberg SM, Bauer CR, Vega Lahr N, Garcia R, et al. Effects of tactile/kinesthetic stimulation on the clinical course and sleep/wake behavior of preterm neonates. Infant Behav Dev. 1986;9:91-105. standardized the three five-minute phases proposed by Rausch9Rausch PB. Effects of tactile and kinesthetic stimulation on premature infants. JOGN Nurs. 1981;10:34-7. into prone TS + supine KS + prone TS. Fourteen of the 31 studies that met the inclusion criteria for the present review used the technique described by Field et al. 1010 Field TM, Schanberg SM, Scafidi F, Bauer CR, Vega-Lahr N, Garcia R, et al. Tactile/kinesthetic stimulation effects on preterm neonates. Pediatrics. 1986;77:654-8. in 1986; 11 of the 14 were conducted by Field's team1010 Field TM, Schanberg SM, Scafidi F, Bauer CR, Vega-Lahr N, Garcia R, et al. Tactile/kinesthetic stimulation effects on preterm neonates. Pediatrics. 1986;77:654-8. , 2121 Scafidi FA, Field TM, Schanberg SM, Bauer CR, Vega Lahr N, Garcia R, et al. Effects of tactile/kinesthetic stimulation on the clinical course and sleep/wake behavior of preterm neonates. Infant Behav Dev. 1986;9:91-105. , 2222 Field T, Scafidi F, Schanberg S. Massage of preterm new- borns to improve growth and development. Paediatric Nursing. 1987;13:385-7. , 2323 Scafidi F, Field T, Schanberg S, Bauer C, Tucci K, Roberts J, et al. Massage stimulates growth in preterm infants: a replication. Infant Behav Dev. 1990;13:167-88. , 2424 Field T, Schanberg S. Massage alters growth and catecholamine production in preterm newborns. In: Field T, Brazelton TB, edit- ors. Advances in Touch. Skillman, NJ: Johnson & Johnson; 1990. p. 96-104. , 2525 Wheeden A, Scafidi FA, Field T, Ironson G, Valdeon C, Bandstra E. Massage effects on cocaine-exposed preterm neonates. J Dev Behav Pediatr. 1993;14:318-22. , 2626 Scafidi FA, Field T, Schanberg SM. Factors that predict which preterm infants benefit most from massage therapy. J Dev Behav Pediatr. 1993;14:176-80. , 2727 Dieter JN, Field T, Hernandez-Reif M, Emory EK, Redzepi M. Stable preterm infants gain more weight and sleep less after five days of massage therapy. J Pediatr Psychol. 2003;28:403-11. , 2828 Diego MA, Field T, Hernandez-Reif M. Vagal activity, gastric motility, and weight gain in massaged preterm neonates. J Pedi- atr. 2005;147:50-5. , 2929 Diego MA, Field T, Hernandez-Reif M, Deeds O, Ascencio A, Begert G. Preterm infant massage elicits consistent increases in vagal activity and gastric motility that are associated with greater weight gain. Acta Paediatr. 2007;96:1588-91. and 3030 Field T, Diego M, Hernandez-Reif M, Dieter JN, Kumar AM, Schanberg S, et al. Insulin and insulin-like growth factor-1 increased in preterm neonates following massage therapy. J Dev Behav Pediatr. 2008;29:463-6. in the same institution and three were performed by other researchers, namely Lee,1919 Lee HK. The effect of infant massage on weight gain, physio- logical and behavioral responses in premature infants. Taehan Kanho Hakhoe Chi. 2005;35:1451-60.Massaro et al.,3131 Massaro AN, Hammad TA, Jazzo B, Aly H. Massage with kines- thetic stimulation improves weight gain in preterm infants. J Perinatol. 2009;29:352-7. and Ang et al. 3232 Ang JY, Lua JL, Mathur A, Thomas R, Asmar BI, Savasan S, et al. A randomized placebo-controlled trial of massage ther- apy on the immune system of preterm infants. Pediatrics. 2012;130:e1549-58. The intervention was usually performed after the first feeding in the morning. In 1990, Field & Schanberg2424 Field T, Schanberg S. Massage alters growth and catecholamine production in preterm newborns. In: Field T, Brazelton TB, edit- ors. Advances in Touch. Skillman, NJ: Johnson & Johnson; 1990. p. 96-104. provided the intervention at the beginning of three consecutive hours, after the midday feeding.

Mathai et al. 1414 Mathai S, Fernandez A, Mondkar J, Kanbur W. Effects of tactile- kinesthetic stimulation in preterms: a controlled trial. Indian Pediatr. 2001;38:1091-8. introduced a new way of providing TKS, as follows: the intervention was done after the morning, midday, and evening feeding in the prone (TS) + supine (TS) + supine (KS) positions, which was repeated by Arora et al. 3333 Arora J, Kumar A, Ramji S. Effect of oil massage on growth and neurobehavior in very low birth weight preterm neonates. Indian Pediatr. 2005;42:1092-100. Like other studies, they also used some type of oil to reduce friction on the PI's skin.1414 Mathai S, Fernandez A, Mondkar J, Kanbur W. Effects of tactile- kinesthetic stimulation in preterms: a controlled trial. Indian Pediatr. 2001;38:1091-8. , 1717 Gonzalez AP, Vasquez-Mendoza G, García-Vela A, Guzmán-Ramirez A, Salazar-Torres M, Romero-Gutierrez G. Weight gain in preterm infants following parent-administered Vimala massage: a randomized controlled trial. Am J Perinatol. 2009;26:247-52. , 3333 Arora J, Kumar A, Ramji S. Effect of oil massage on growth and neurobehavior in very low birth weight preterm neonates. Indian Pediatr. 2005;42:1092-100. , 3434 Kumar J, Upadhyay A, Dwivedi AK, Gothwal S, Jaiswal V, Aggarwal S. Effect of oil massage on growth in preterm neonates less than 1800 g: a randomized control trial. Indian J Pediatr. 2013;80:465-9. and 3535 Abdallah B, Badr LK, Hawwari M. The efficacy of massage on short and long term outcomes in preterm infants. Infant Behav Dev. 2013;36:662-9. In some studies, only the mothers provided KTS.1616 Mendes EW, Procianoy RS. Massage therapy reduces hospital stay and occurrence of late-onset sepsis in very preterm neonates. J Perinatol. 2008;28:815-20. , 3535 Abdallah B, Badr LK, Hawwari M. The efficacy of massage on short and long term outcomes in preterm infants. Infant Behav Dev. 2013;36:662-9. and 3636 Procianoy RS, Mendes EW, Silveira RC. Massage therapy improves neurodevelopment outcome at two years corrected age for very low birth weight infants. Early Hum Dev. 2010;86:7-11.

Ferber et al. 1515 Ferber SG, Kuint J, Weller A, Feldman R, Dollberg S, Arbel E, et al. Massage therapy by mothers and trained profession- als enhances weight gain in preterm infants. Early Hum Dev. 2002;67:37-45. suggested that during the first ten seconds of TS, the caregiver should only rest his hand on the PI, avoiding movements.

Dieter et al. 2727 Dieter JN, Field T, Hernandez-Reif M, Emory EK, Redzepi M. Stable preterm infants gain more weight and sleep less after five days of massage therapy. J Pediatr Psychol. 2003;28:403-11. was the first to provide TKS for only five days, showing that this was enough to increase the rate of weight gain significantly compared with the control group.

Diego et al. 2828 Diego MA, Field T, Hernandez-Reif M. Vagal activity, gastric motility, and weight gain in massaged preterm neonates. J Pedi- atr. 2005;147:50-5. demonstrated that moderate KTS pressure promoted better outcomes than the placebo group who received light KTS pressure. Also, in another time, trained a few therapists and suggested that the technique was effective, regardless of therapist.2929 Diego MA, Field T, Hernandez-Reif M, Deeds O, Ascencio A, Begert G. Preterm infant massage elicits consistent increases in vagal activity and gastric motility that are associated with greater weight gain. Acta Paediatr. 2007;96:1588-91.

Massaro et al. 3131 Massaro AN, Hammad TA, Jazzo B, Aly H. Massage with kines- thetic stimulation improves weight gain in preterm infants. J Perinatol. 2009;29:352-7. tested KTS and TS separately in different groups of infants and found that KTS appears to be better, but the difference was not significant.

Fucile & Gisel1818 Fucile S, Gisel EG. Sensorimotor interventions improve growth and motor function in preterm infants. Neonatal Netw. 2010;29:359-66. used the same trained researcher to provide the intervention and introduced oral stimulation (OS) in addition to KTS. They found that OS did not increase the rate of weight gain and attributed this result to the shorter period dedicated to each intervention, suggesting that the duration of the sensoriomotor input is critical for improving defined outcomes.

Ferreira & Bergamasco2020 Ferreira AM, Bergamasco NH. Behavioral analysis of preterm neonates included in a tactile and kinesthetic stimulation pro- gram during hospitalization. Rev Bras Fisioter. 2010;14:141-8. used gentle techniques with no rigid sequence, only when the PI was awake.

Moyer-Mileur et al. 3737 Moyer-Mileur LJ, Haley S, Slater H, Beachy J, Smith SL. Massage improves growth quality by decreasing body fat deposition in male preterm infants. J Pediatr. 2013;162:490-5. used the Infant Massage USA protocol, but they modified for PI, eliminating massage of the abdomen.

Kumar et al. 3434 Kumar J, Upadhyay A, Dwivedi AK, Gothwal S, Jaiswal V, Aggarwal S. Effect of oil massage on growth in preterm neonates less than 1800 g: a randomized control trial. Indian J Pediatr. 2013;80:465-9. demonstrated that PI who received oil massage soon after birth had less weight loss in the first week, probably due to undetectable water loss through the skin due to blockage of pores and sweat glands. Also, early oil application probably leads to better temperature regulation and less caloric expenditure due to cold stress.

Abdallah et al. 3535 Abdallah B, Badr LK, Hawwari M. The efficacy of massage on short and long term outcomes in preterm infants. Infant Behav Dev. 2013;36:662-9. used TS without KS and did not find greater weight gain, but the pain scores on the Premature Infant Pain Profile were favored in the massaged infants, being lower after the intervention and at discharge, in addition to demonstrating better cognitive scores.

Discussion

Tactile stimulation has the advantages of being noninvasive, inexpensive, and safe, as was demonstrated by Livingston et al. 3838 Livingston K, Beider S, Kant AJ, Gallardo CC, Joseph MH, Gold JI. Touch and massage for medically fragile infants. Evid Based Complement Alternat Med. 2009;6:473-82. based on physiological stability and no change in agitation/pain scores of the infants receiving massage. The majority of the clinical trials studied herein (20 of the 31 studies)3White JL, Labarba RC. The effects of tactile and kinesthetic stimulation on neonatal development in the premature infant. Dev Psychobiol. 1976;9:569-77. , 1010 Field TM, Schanberg SM, Scafidi F, Bauer CR, Vega-Lahr N, Garcia R, et al. Tactile/kinesthetic stimulation effects on preterm neonates. Pediatrics. 1986;77:654-8. , 1414 Mathai S, Fernandez A, Mondkar J, Kanbur W. Effects of tactile- kinesthetic stimulation in preterms: a controlled trial. Indian Pediatr. 2001;38:1091-8. , 1515 Ferber SG, Kuint J, Weller A, Feldman R, Dollberg S, Arbel E, et al. Massage therapy by mothers and trained profession- als enhances weight gain in preterm infants. Early Hum Dev. 2002;67:37-45. , 1717 Gonzalez AP, Vasquez-Mendoza G, García-Vela A, Guzmán-Ramirez A, Salazar-Torres M, Romero-Gutierrez G. Weight gain in preterm infants following parent-administered Vimala massage: a randomized controlled trial. Am J Perinatol. 2009;26:247-52. , 1818 Fucile S, Gisel EG. Sensorimotor interventions improve growth and motor function in preterm infants. Neonatal Netw. 2010;29:359-66. , 1919 Lee HK. The effect of infant massage on weight gain, physio- logical and behavioral responses in premature infants. Taehan Kanho Hakhoe Chi. 2005;35:1451-60. , 2121 Scafidi FA, Field TM, Schanberg SM, Bauer CR, Vega Lahr N, Garcia R, et al. Effects of tactile/kinesthetic stimulation on the clinical course and sleep/wake behavior of preterm neonates. Infant Behav Dev. 1986;9:91-105. , 2222 Field T, Scafidi F, Schanberg S. Massage of preterm new- borns to improve growth and development. Paediatric Nursing. 1987;13:385-7. , 2323 Scafidi F, Field T, Schanberg S, Bauer C, Tucci K, Roberts J, et al. Massage stimulates growth in preterm infants: a replication. Infant Behav Dev. 1990;13:167-88. , 2424 Field T, Schanberg S. Massage alters growth and catecholamine production in preterm newborns. In: Field T, Brazelton TB, edit- ors. Advances in Touch. Skillman, NJ: Johnson & Johnson; 1990. p. 96-104. , 2525 Wheeden A, Scafidi FA, Field T, Ironson G, Valdeon C, Bandstra E. Massage effects on cocaine-exposed preterm neonates. J Dev Behav Pediatr. 1993;14:318-22. , 2626 Scafidi FA, Field T, Schanberg SM. Factors that predict which preterm infants benefit most from massage therapy. J Dev Behav Pediatr. 1993;14:176-80. , 2727 Dieter JN, Field T, Hernandez-Reif M, Emory EK, Redzepi M. Stable preterm infants gain more weight and sleep less after five days of massage therapy. J Pediatr Psychol. 2003;28:403-11. , 2828 Diego MA, Field T, Hernandez-Reif M. Vagal activity, gastric motility, and weight gain in massaged preterm neonates. J Pedi- atr. 2005;147:50-5. , 2929 Diego MA, Field T, Hernandez-Reif M, Deeds O, Ascencio A, Begert G. Preterm infant massage elicits consistent increases in vagal activity and gastric motility that are associated with greater weight gain. Acta Paediatr. 2007;96:1588-91. , 3030 Field T, Diego M, Hernandez-Reif M, Dieter JN, Kumar AM, Schanberg S, et al. Insulin and insulin-like growth factor-1 increased in preterm neonates following massage therapy. J Dev Behav Pediatr. 2008;29:463-6. , 3131 Massaro AN, Hammad TA, Jazzo B, Aly H. Massage with kines- thetic stimulation improves weight gain in preterm infants. J Perinatol. 2009;29:352-7. , 3232 Ang JY, Lua JL, Mathur A, Thomas R, Asmar BI, Savasan S, et al. A randomized placebo-controlled trial of massage ther- apy on the immune system of preterm infants. Pediatrics. 2012;130:e1549-58. and 3434 Kumar J, Upadhyay A, Dwivedi AK, Gothwal S, Jaiswal V, Aggarwal S. Effect of oil massage on growth in preterm neonates less than 1800 g: a randomized control trial. Indian J Pediatr. 2013;80:465-9. described a significantly benefit on weight gain in the PI group that received the TS/TKS. This information places TS as a promising adjunctive tool in addressing PI in the NICU. Some of the studies did not assess the data statistically; part of them justified this because of small sample size.6Solkoff N, Weintraub D, Yaffe S, Blasé B. Effects of handling on the subsequent development of premature infants. Dev Psychol. 1969;1:765-9. , 7Kramer M, Chamorro I, Green D, Knudtson F. Extra tactile stim- ulation of the premature infant. Nurs Res. 1975;24:324-34. and 8Solkoff N, Matuszak D. Tactile stimulation and behavioral devel- opment among low-birth weight infants. Child Psychiatry Hum Dev. 1975;6:33-7.

Some correlations have been suggested to justify the faster weight gain of PI submitted to TKS, such as greater vagal stimulation and gastric activity,2828 Diego MA, Field T, Hernandez-Reif M. Vagal activity, gastric motility, and weight gain in massaged preterm neonates. J Pedi- atr. 2005;147:50-5. and 2929 Diego MA, Field T, Hernandez-Reif M, Deeds O, Ascencio A, Begert G. Preterm infant massage elicits consistent increases in vagal activity and gastric motility that are associated with greater weight gain. Acta Paediatr. 2007;96:1588-91. relationship with energy intake,3White JL, Labarba RC. The effects of tactile and kinesthetic stimulation on neonatal development in the premature infant. Dev Psychobiol. 1976;9:569-77. , 1010 Field TM, Schanberg SM, Scafidi F, Bauer CR, Vega-Lahr N, Garcia R, et al. Tactile/kinesthetic stimulation effects on preterm neonates. Pediatrics. 1986;77:654-8. , 1515 Ferber SG, Kuint J, Weller A, Feldman R, Dollberg S, Arbel E, et al. Massage therapy by mothers and trained profession- als enhances weight gain in preterm infants. Early Hum Dev. 2002;67:37-45. , 1717 Gonzalez AP, Vasquez-Mendoza G, García-Vela A, Guzmán-Ramirez A, Salazar-Torres M, Romero-Gutierrez G. Weight gain in preterm infants following parent-administered Vimala massage: a randomized controlled trial. Am J Perinatol. 2009;26:247-52. , 2222 Field T, Scafidi F, Schanberg S. Massage of preterm new- borns to improve growth and development. Paediatric Nursing. 1987;13:385-7. , 2323 Scafidi F, Field T, Schanberg S, Bauer C, Tucci K, Roberts J, et al. Massage stimulates growth in preterm infants: a replication. Infant Behav Dev. 1990;13:167-88. , 2424 Field T, Schanberg S. Massage alters growth and catecholamine production in preterm newborns. In: Field T, Brazelton TB, edit- ors. Advances in Touch. Skillman, NJ: Johnson & Johnson; 1990. p. 96-104. , 2525 Wheeden A, Scafidi FA, Field T, Ironson G, Valdeon C, Bandstra E. Massage effects on cocaine-exposed preterm neonates. J Dev Behav Pediatr. 1993;14:318-22. , 2626 Scafidi FA, Field T, Schanberg SM. Factors that predict which preterm infants benefit most from massage therapy. J Dev Behav Pediatr. 1993;14:176-80. , 2727 Dieter JN, Field T, Hernandez-Reif M, Emory EK, Redzepi M. Stable preterm infants gain more weight and sleep less after five days of massage therapy. J Pediatr Psychol. 2003;28:403-11. , 2828 Diego MA, Field T, Hernandez-Reif M. Vagal activity, gastric motility, and weight gain in massaged preterm neonates. J Pedi- atr. 2005;147:50-5. , 2929 Diego MA, Field T, Hernandez-Reif M, Deeds O, Ascencio A, Begert G. Preterm infant massage elicits consistent increases in vagal activity and gastric motility that are associated with greater weight gain. Acta Paediatr. 2007;96:1588-91. , 3030 Field T, Diego M, Hernandez-Reif M, Dieter JN, Kumar AM, Schanberg S, et al. Insulin and insulin-like growth factor-1 increased in preterm neonates following massage therapy. J Dev Behav Pediatr. 2008;29:463-6. , 3131 Massaro AN, Hammad TA, Jazzo B, Aly H. Massage with kines- thetic stimulation improves weight gain in preterm infants. J Perinatol. 2009;29:352-7. and 3939 Benavides-González H, Rivera-Rueda MA, Ibarra-Reyes MP, Flores-Tamez ME, Fragoso-Ramirez A, Morán-Martínez N, et al. Effects of early multimodal stimulation on preterm newborn infants. Bol Med Hosp Infant Mex. 1989;46:789-95. sleep-wake behavior and behavioral scales,6Solkoff N, Weintraub D, Yaffe S, Blasé B. Effects of handling on the subsequent development of premature infants. Dev Psychol. 1969;1:765-9. , 7Kramer M, Chamorro I, Green D, Knudtson F. Extra tactile stim- ulation of the premature infant. Nurs Res. 1975;24:324-34. , 8Solkoff N, Matuszak D. Tactile stimulation and behavioral devel- opment among low-birth weight infants. Child Psychiatry Hum Dev. 1975;6:33-7. , 1010 Field TM, Schanberg SM, Scafidi F, Bauer CR, Vega-Lahr N, Garcia R, et al. Tactile/kinesthetic stimulation effects on preterm neonates. Pediatrics. 1986;77:654-8. , 1414 Mathai S, Fernandez A, Mondkar J, Kanbur W. Effects of tactile- kinesthetic stimulation in preterms: a controlled trial. Indian Pediatr. 2001;38:1091-8. , 1919 Lee HK. The effect of infant massage on weight gain, physio- logical and behavioral responses in premature infants. Taehan Kanho Hakhoe Chi. 2005;35:1451-60. , 2020 Ferreira AM, Bergamasco NH. Behavioral analysis of preterm neonates included in a tactile and kinesthetic stimulation pro- gram during hospitalization. Rev Bras Fisioter. 2010;14:141-8. , 2121 Scafidi FA, Field TM, Schanberg SM, Bauer CR, Vega Lahr N, Garcia R, et al. Effects of tactile/kinesthetic stimulation on the clinical course and sleep/wake behavior of preterm neonates. Infant Behav Dev. 1986;9:91-105. , 2222 Field T, Scafidi F, Schanberg S. Massage of preterm new- borns to improve growth and development. Paediatric Nursing. 1987;13:385-7. , 2323 Scafidi F, Field T, Schanberg S, Bauer C, Tucci K, Roberts J, et al. Massage stimulates growth in preterm infants: a replication. Infant Behav Dev. 1990;13:167-88. , 2424 Field T, Schanberg S. Massage alters growth and catecholamine production in preterm newborns. In: Field T, Brazelton TB, edit- ors. Advances in Touch. Skillman, NJ: Johnson & Johnson; 1990. p. 96-104. , 2525 Wheeden A, Scafidi FA, Field T, Ironson G, Valdeon C, Bandstra E. Massage effects on cocaine-exposed preterm neonates. J Dev Behav Pediatr. 1993;14:318-22. , 2626 Scafidi FA, Field T, Schanberg SM. Factors that predict which preterm infants benefit most from massage therapy. J Dev Behav Pediatr. 1993;14:176-80. , 2727 Dieter JN, Field T, Hernandez-Reif M, Emory EK, Redzepi M. Stable preterm infants gain more weight and sleep less after five days of massage therapy. J Pediatr Psychol. 2003;28:403-11. , 3636 Procianoy RS, Mendes EW, Silveira RC. Massage therapy improves neurodevelopment outcome at two years corrected age for very low birth weight infants. Early Hum Dev. 2010;86:7-11. and 3939 Benavides-González H, Rivera-Rueda MA, Ibarra-Reyes MP, Flores-Tamez ME, Fragoso-Ramirez A, Morán-Martínez N, et al. Effects of early multimodal stimulation on preterm newborn infants. Bol Med Hosp Infant Mex. 1989;46:789-95. serum insulin and IGF-1 levels,3030 Field T, Diego M, Hernandez-Reif M, Dieter JN, Kumar AM, Schanberg S, et al. Insulin and insulin-like growth factor-1 increased in preterm neonates following massage therapy. J Dev Behav Pediatr. 2008;29:463-6. and 3737 Moyer-Mileur LJ, Haley S, Slater H, Beachy J, Smith SL. Massage improves growth quality by decreasing body fat deposition in male preterm infants. J Pediatr. 2013;162:490-5. and use of oil.3333 Arora J, Kumar A, Ramji S. Effect of oil massage on growth and neurobehavior in very low birth weight preterm neonates. Indian Pediatr. 2005;42:1092-100. , 4040 Vaivre-Douret L, Oriot D, Blossier P, Py A, Kasolter-Péré M, Zwang J. The effect of multimodal stimulation and cuta- neous application of vegetable oils on neonatal development in preterm infants: a randomized controlled trial. Child Care Health Dev. 2009;35:96-105. and 4141 Sankaranarayanan K, Mondkar JA, Chauhan MM, Mascarenhas BM, Mainkar AR, Salvi RY. Oil massage in neonates: an open ran- domized controlled study of coconut versus mineral oil. Indian Pediatr. 2005;42:877-84. The results found by Diego et al. 2828 Diego MA, Field T, Hernandez-Reif M. Vagal activity, gastric motility, and weight gain in massaged preterm neonates. J Pedi- atr. 2005;147:50-5. and Field et al. 4242 Field T, Diego MA, Hernandez-Reif M, Deeds O, Figuereido B. Moderate versus light pressure massage therapy leads to greater weight gain in preterm infants. Infant Behav Dev. 2006;29:574-8. on the effects of mild and moderate pressure showed that moderate pressure provided greater vagal stimulation. Diego et al. 2929 Diego MA, Field T, Hernandez-Reif M, Deeds O, Ascencio A, Begert G. Preterm infant massage elicits consistent increases in vagal activity and gastric motility that are associated with greater weight gain. Acta Paediatr. 2007;96:1588-91. also found greater gastric motility among the PI who were stimulated with moderate pressure and suggested that greater gastric activity may explain their faster weight gain. Field et al. 4242 Field T, Diego MA, Hernandez-Reif M, Deeds O, Figuereido B. Moderate versus light pressure massage therapy leads to greater weight gain in preterm infants. Infant Behav Dev. 2006;29:574-8. added that the group of PI stimulated with moderate pressure were more relaxed, characterized by their lower heart rates and by the assessment of their wake and sleep status, and behavior, as recommended by the Thomas Scale of 1975.2121 Scafidi FA, Field TM, Schanberg SM, Bauer CR, Vega Lahr N, Garcia R, et al. Effects of tactile/kinesthetic stimulation on the clinical course and sleep/wake behavior of preterm neonates. Infant Behav Dev. 1986;9:91-105. They then suggested that the more relaxed state of the PI resulted in lower energy expenditure, which would then result in faster weight gain. This was confirmed by Lahat et al.,4343 Lahat S, Mimouni FB, Ashbel G, Dollberg S. Energy expenditure in growing preterm infants receiving massage therapy. J Am Coll Nutr. 2007;26:356-9. who used indirect calorimetry to show that a group of PI submitted to stimulation had lower energy expenditure.

Regarding energy intake, some studies have shown that stimulated infants have higher daily weight gain.1010 Field TM, Schanberg SM, Scafidi F, Bauer CR, Vega-Lahr N, Garcia R, et al. Tactile/kinesthetic stimulation effects on preterm neonates. Pediatrics. 1986;77:654-8. , 1717 Gonzalez AP, Vasquez-Mendoza G, García-Vela A, Guzmán-Ramirez A, Salazar-Torres M, Romero-Gutierrez G. Weight gain in preterm infants following parent-administered Vimala massage: a randomized controlled trial. Am J Perinatol. 2009;26:247-52. , 2222 Field T, Scafidi F, Schanberg S. Massage of preterm new- borns to improve growth and development. Paediatric Nursing. 1987;13:385-7. , 2323 Scafidi F, Field T, Schanberg S, Bauer C, Tucci K, Roberts J, et al. Massage stimulates growth in preterm infants: a replication. Infant Behav Dev. 1990;13:167-88. , 2525 Wheeden A, Scafidi FA, Field T, Ironson G, Valdeon C, Bandstra E. Massage effects on cocaine-exposed preterm neonates. J Dev Behav Pediatr. 1993;14:318-22. , 2626 Scafidi FA, Field T, Schanberg SM. Factors that predict which preterm infants benefit most from massage therapy. J Dev Behav Pediatr. 1993;14:176-80. , 2727 Dieter JN, Field T, Hernandez-Reif M, Emory EK, Redzepi M. Stable preterm infants gain more weight and sleep less after five days of massage therapy. J Pediatr Psychol. 2003;28:403-11. , 2828 Diego MA, Field T, Hernandez-Reif M. Vagal activity, gastric motility, and weight gain in massaged preterm neonates. J Pedi- atr. 2005;147:50-5. , 3131 Massaro AN, Hammad TA, Jazzo B, Aly H. Massage with kines- thetic stimulation improves weight gain in preterm infants. J Perinatol. 2009;29:352-7. , 3232 Ang JY, Lua JL, Mathur A, Thomas R, Asmar BI, Savasan S, et al. A randomized placebo-controlled trial of massage ther- apy on the immune system of preterm infants. Pediatrics. 2012;130:e1549-58. and 3939 Benavides-González H, Rivera-Rueda MA, Ibarra-Reyes MP, Flores-Tamez ME, Fragoso-Ramirez A, Morán-Martínez N, et al. Effects of early multimodal stimulation on preterm newborn infants. Bol Med Hosp Infant Mex. 1989;46:789-95. Other studies recorded stooling frequency and found that it increased significantly, together with an increased formula intake on days 6-10.9Rausch PB. Effects of tactile and kinesthetic stimulation on premature infants. JOGN Nurs. 1981;10:34-7. Rausch9Rausch PB. Effects of tactile and kinesthetic stimulation on premature infants. JOGN Nurs. 1981;10:34-7. suggested that increased stooling was a consequence of higher formula intake. On the other hand, Scafidi et al. 2323 Scafidi F, Field T, Schanberg S, Bauer C, Tucci K, Roberts J, et al. Massage stimulates growth in preterm infants: a replication. Infant Behav Dev. 1990;13:167-88.found that the frequency of stooling decreased, even when daily weight gain increased. White Labarba3White JL, Labarba RC. The effects of tactile and kinesthetic stimulation on neonatal development in the premature infant. Dev Psychobiol. 1976;9:569-77. reported that the amount of formula consumed per feeding increased while the number of daily feedings decreased, which the authors attributed to the nursery routine: PI who did not consume the entire serving were fed more often. Other studies that reported faster weight gain did not find significant differences in energy intake.

Along with weight gain, other variables, some mentioned above, have been analyzed after application of TKS in premature. All of the following parameters were analyzed by clinical studies in PI who received TS/MT whether or not associated with KS during their NICU stay: weight gain;3White JL, Labarba RC. The effects of tactile and kinesthetic stimulation on neonatal development in the premature infant. Dev Psychobiol. 1976;9:569-77. , 6Solkoff N, Weintraub D, Yaffe S, Blasé B. Effects of handling on the subsequent development of premature infants. Dev Psychol. 1969;1:765-9. , 7Kramer M, Chamorro I, Green D, Knudtson F. Extra tactile stim- ulation of the premature infant. Nurs Res. 1975;24:324-34. , 8Solkoff N, Matuszak D. Tactile stimulation and behavioral devel- opment among low-birth weight infants. Child Psychiatry Hum Dev. 1975;6:33-7. , 9Rausch PB. Effects of tactile and kinesthetic stimulation on premature infants. JOGN Nurs. 1981;10:34-7. , 1010 Field TM, Schanberg SM, Scafidi F, Bauer CR, Vega-Lahr N, Garcia R, et al. Tactile/kinesthetic stimulation effects on preterm neonates. Pediatrics. 1986;77:654-8. , 1414 Mathai S, Fernandez A, Mondkar J, Kanbur W. Effects of tactile- kinesthetic stimulation in preterms: a controlled trial. Indian Pediatr. 2001;38:1091-8. , 1515 Ferber SG, Kuint J, Weller A, Feldman R, Dollberg S, Arbel E, et al. Massage therapy by mothers and trained profession- als enhances weight gain in preterm infants. Early Hum Dev. 2002;67:37-45. , 1616 Mendes EW, Procianoy RS. Massage therapy reduces hospital stay and occurrence of late-onset sepsis in very preterm neonates. J Perinatol. 2008;28:815-20. , 1717 Gonzalez AP, Vasquez-Mendoza G, García-Vela A, Guzmán-Ramirez A, Salazar-Torres M, Romero-Gutierrez G. Weight gain in preterm infants following parent-administered Vimala massage: a randomized controlled trial. Am J Perinatol. 2009;26:247-52. , 1818 Fucile S, Gisel EG. Sensorimotor interventions improve growth and motor function in preterm infants. Neonatal Netw. 2010;29:359-66. , 1919 Lee HK. The effect of infant massage on weight gain, physio- logical and behavioral responses in premature infants. Taehan Kanho Hakhoe Chi. 2005;35:1451-60. , 2020 Ferreira AM, Bergamasco NH. Behavioral analysis of preterm neonates included in a tactile and kinesthetic stimulation pro- gram during hospitalization. Rev Bras Fisioter. 2010;14:141-8. , 2121 Scafidi FA, Field TM, Schanberg SM, Bauer CR, Vega Lahr N, Garcia R, et al. Effects of tactile/kinesthetic stimulation on the clinical course and sleep/wake behavior of preterm neonates. Infant Behav Dev. 1986;9:91-105. , 2222 Field T, Scafidi F, Schanberg S. Massage of preterm new- borns to improve growth and development. Paediatric Nursing. 1987;13:385-7. , 2323 Scafidi F, Field T, Schanberg S, Bauer C, Tucci K, Roberts J, et al. Massage stimulates growth in preterm infants: a replication. Infant Behav Dev. 1990;13:167-88. , 2424 Field T, Schanberg S. Massage alters growth and catecholamine production in preterm newborns. In: Field T, Brazelton TB, edit- ors. Advances in Touch. Skillman, NJ: Johnson & Johnson; 1990. p. 96-104. , 2525 Wheeden A, Scafidi FA, Field T, Ironson G, Valdeon C, Bandstra E. Massage effects on cocaine-exposed preterm neonates. J Dev Behav Pediatr. 1993;14:318-22. , 2626 Scafidi FA, Field T, Schanberg SM. Factors that predict which preterm infants benefit most from massage therapy. J Dev Behav Pediatr. 1993;14:176-80. , 2727 Dieter JN, Field T, Hernandez-Reif M, Emory EK, Redzepi M. Stable preterm infants gain more weight and sleep less after five days of massage therapy. J Pediatr Psychol. 2003;28:403-11. , 2828 Diego MA, Field T, Hernandez-Reif M. Vagal activity, gastric motility, and weight gain in massaged preterm neonates. J Pedi- atr. 2005;147:50-5. , 2929 Diego MA, Field T, Hernandez-Reif M, Deeds O, Ascencio A, Begert G. Preterm infant massage elicits consistent increases in vagal activity and gastric motility that are associated with greater weight gain. Acta Paediatr. 2007;96:1588-91. , 3030 Field T, Diego M, Hernandez-Reif M, Dieter JN, Kumar AM, Schanberg S, et al. Insulin and insulin-like growth factor-1 increased in preterm neonates following massage therapy. J Dev Behav Pediatr. 2008;29:463-6. , 3131 Massaro AN, Hammad TA, Jazzo B, Aly H. Massage with kines- thetic stimulation improves weight gain in preterm infants. J Perinatol. 2009;29:352-7. , 3232 Ang JY, Lua JL, Mathur A, Thomas R, Asmar BI, Savasan S, et al. A randomized placebo-controlled trial of massage ther- apy on the immune system of preterm infants. Pediatrics. 2012;130:e1549-58. , 3333 Arora J, Kumar A, Ramji S. Effect of oil massage on growth and neurobehavior in very low birth weight preterm neonates. Indian Pediatr. 2005;42:1092-100. , 3434 Kumar J, Upadhyay A, Dwivedi AK, Gothwal S, Jaiswal V, Aggarwal S. Effect of oil massage on growth in preterm neonates less than 1800 g: a randomized control trial. Indian J Pediatr. 2013;80:465-9. , 3535 Abdallah B, Badr LK, Hawwari M. The efficacy of massage on short and long term outcomes in preterm infants. Infant Behav Dev. 2013;36:662-9. , 3636 Procianoy RS, Mendes EW, Silveira RC. Massage therapy improves neurodevelopment outcome at two years corrected age for very low birth weight infants. Early Hum Dev. 2010;86:7-11. , 3737 Moyer-Mileur LJ, Haley S, Slater H, Beachy J, Smith SL. Massage improves growth quality by decreasing body fat deposition in male preterm infants. J Pediatr. 2013;162:490-5. and 3939 Benavides-González H, Rivera-Rueda MA, Ibarra-Reyes MP, Flores-Tamez ME, Fragoso-Ramirez A, Morán-Martínez N, et al. Effects of early multimodal stimulation on preterm newborn infants. Bol Med Hosp Infant Mex. 1989;46:789-95. length of hospital stay;1010 Field TM, Schanberg SM, Scafidi F, Bauer CR, Vega-Lahr N, Garcia R, et al. Tactile/kinesthetic stimulation effects on preterm neonates. Pediatrics. 1986;77:654-8. , 1616 Mendes EW, Procianoy RS. Massage therapy reduces hospital stay and occurrence of late-onset sepsis in very preterm neonates. J Perinatol. 2008;28:815-20. , 1717 Gonzalez AP, Vasquez-Mendoza G, García-Vela A, Guzmán-Ramirez A, Salazar-Torres M, Romero-Gutierrez G. Weight gain in preterm infants following parent-administered Vimala massage: a randomized controlled trial. Am J Perinatol. 2009;26:247-52. , 2020 Ferreira AM, Bergamasco NH. Behavioral analysis of preterm neonates included in a tactile and kinesthetic stimulation pro- gram during hospitalization. Rev Bras Fisioter. 2010;14:141-8. , 2121 Scafidi FA, Field TM, Schanberg SM, Bauer CR, Vega Lahr N, Garcia R, et al. Effects of tactile/kinesthetic stimulation on the clinical course and sleep/wake behavior of preterm neonates. Infant Behav Dev. 1986;9:91-105. , 2323 Scafidi F, Field T, Schanberg S, Bauer C, Tucci K, Roberts J, et al. Massage stimulates growth in preterm infants: a replication. Infant Behav Dev. 1990;13:167-88. , 2424 Field T, Schanberg S. Massage alters growth and catecholamine production in preterm newborns. In: Field T, Brazelton TB, edit- ors. Advances in Touch. Skillman, NJ: Johnson & Johnson; 1990. p. 96-104. , 2828 Diego MA, Field T, Hernandez-Reif M. Vagal activity, gastric motility, and weight gain in massaged preterm neonates. J Pedi- atr. 2005;147:50-5. , 3131 Massaro AN, Hammad TA, Jazzo B, Aly H. Massage with kines- thetic stimulation improves weight gain in preterm infants. J Perinatol. 2009;29:352-7. , 3232 Ang JY, Lua JL, Mathur A, Thomas R, Asmar BI, Savasan S, et al. A randomized placebo-controlled trial of massage ther- apy on the immune system of preterm infants. Pediatrics. 2012;130:e1549-58. , 3535 Abdallah B, Badr LK, Hawwari M. The efficacy of massage on short and long term outcomes in preterm infants. Infant Behav Dev. 2013;36:662-9. , 3737 Moyer-Mileur LJ, Haley S, Slater H, Beachy J, Smith SL. Massage improves growth quality by decreasing body fat deposition in male preterm infants. J Pediatr. 2013;162:490-5. and 3939 Benavides-González H, Rivera-Rueda MA, Ibarra-Reyes MP, Flores-Tamez ME, Fragoso-Ramirez A, Morán-Martínez N, et al. Effects of early multimodal stimulation on preterm newborn infants. Bol Med Hosp Infant Mex. 1989;46:789-95. behavioral responses;6Solkoff N, Weintraub D, Yaffe S, Blasé B. Effects of handling on the subsequent development of premature infants. Dev Psychol. 1969;1:765-9. , 7Kramer M, Chamorro I, Green D, Knudtson F. Extra tactile stim- ulation of the premature infant. Nurs Res. 1975;24:324-34. , 8Solkoff N, Matuszak D. Tactile stimulation and behavioral devel- opment among low-birth weight infants. Child Psychiatry Hum Dev. 1975;6:33-7. , 1010 Field TM, Schanberg SM, Scafidi F, Bauer CR, Vega-Lahr N, Garcia R, et al. Tactile/kinesthetic stimulation effects on preterm neonates. Pediatrics. 1986;77:654-8. , 1414 Mathai S, Fernandez A, Mondkar J, Kanbur W. Effects of tactile- kinesthetic stimulation in preterms: a controlled trial. Indian Pediatr. 2001;38:1091-8. , 1919 Lee HK. The effect of infant massage on weight gain, physio- logical and behavioral responses in premature infants. Taehan Kanho Hakhoe Chi. 2005;35:1451-60. , 2020 Ferreira AM, Bergamasco NH. Behavioral analysis of preterm neonates included in a tactile and kinesthetic stimulation pro- gram during hospitalization. Rev Bras Fisioter. 2010;14:141-8. , 2121 Scafidi FA, Field TM, Schanberg SM, Bauer CR, Vega Lahr N, Garcia R, et al. Effects of tactile/kinesthetic stimulation on the clinical course and sleep/wake behavior of preterm neonates. Infant Behav Dev. 1986;9:91-105. , 2222 Field T, Scafidi F, Schanberg S. Massage of preterm new- borns to improve growth and development. Paediatric Nursing. 1987;13:385-7. , 2323 Scafidi F, Field T, Schanberg S, Bauer C, Tucci K, Roberts J, et al. Massage stimulates growth in preterm infants: a replication. Infant Behav Dev. 1990;13:167-88. , 2525 Wheeden A, Scafidi FA, Field T, Ironson G, Valdeon C, Bandstra E. Massage effects on cocaine-exposed preterm neonates. J Dev Behav Pediatr. 1993;14:318-22. , 2626 Scafidi FA, Field T, Schanberg SM. Factors that predict which preterm infants benefit most from massage therapy. J Dev Behav Pediatr. 1993;14:176-80. , 3636 Procianoy RS, Mendes EW, Silveira RC. Massage therapy improves neurodevelopment outcome at two years corrected age for very low birth weight infants. Early Hum Dev. 2010;86:7-11. and 3939 Benavides-González H, Rivera-Rueda MA, Ibarra-Reyes MP, Flores-Tamez ME, Fragoso-Ramirez A, Morán-Martínez N, et al. Effects of early multimodal stimulation on preterm newborn infants. Bol Med Hosp Infant Mex. 1989;46:789-95. sleep/wake stage;1010 Field TM, Schanberg SM, Scafidi F, Bauer CR, Vega-Lahr N, Garcia R, et al. Tactile/kinesthetic stimulation effects on preterm neonates. Pediatrics. 1986;77:654-8. , 2121 Scafidi FA, Field TM, Schanberg SM, Bauer CR, Vega Lahr N, Garcia R, et al. Effects of tactile/kinesthetic stimulation on the clinical course and sleep/wake behavior of preterm neonates. Infant Behav Dev. 1986;9:91-105. , 2323 Scafidi F, Field T, Schanberg S, Bauer C, Tucci K, Roberts J, et al. Massage stimulates growth in preterm infants: a replication. Infant Behav Dev. 1990;13:167-88. , 2424 Field T, Schanberg S. Massage alters growth and catecholamine production in preterm newborns. In: Field T, Brazelton TB, edit- ors. Advances in Touch. Skillman, NJ: Johnson & Johnson; 1990. p. 96-104. , 2626 Scafidi FA, Field T, Schanberg SM. Factors that predict which preterm infants benefit most from massage therapy. J Dev Behav Pediatr. 1993;14:176-80. and 2727 Dieter JN, Field T, Hernandez-Reif M, Emory EK, Redzepi M. Stable preterm infants gain more weight and sleep less after five days of massage therapy. J Pediatr Psychol. 2003;28:403-11. stress behavior;1111 Hernandez-Reif M, Diego M, Field T. Preterm infants show reduced stress behaviors and activity after 5 days of massage therapy. Infant Behav Dev. 2007;30:557-61. energy expenditure;4343 Lahat S, Mimouni FB, Ashbel G, Dollberg S. Energy expenditure in growing preterm infants receiving massage therapy. J Am Coll Nutr. 2007;26:356-9. body temperature;3White JL, Labarba RC. The effects of tactile and kinesthetic stimulation on neonatal development in the premature infant. Dev Psychobiol. 1976;9:569-77. , 6Solkoff N, Weintraub D, Yaffe S, Blasé B. Effects of handling on the subsequent development of premature infants. Dev Psychol. 1969;1:765-9. , 2121 Scafidi FA, Field TM, Schanberg SM, Bauer CR, Vega Lahr N, Garcia R, et al. Effects of tactile/kinesthetic stimulation on the clinical course and sleep/wake behavior of preterm neonates. Infant Behav Dev. 1986;9:91-105. , 2323 Scafidi F, Field T, Schanberg S, Bauer C, Tucci K, Roberts J, et al. Massage stimulates growth in preterm infants: a replication. Infant Behav Dev. 1990;13:167-88. , 2424 Field T, Schanberg S. Massage alters growth and catecholamine production in preterm newborns. In: Field T, Brazelton TB, edit- ors. Advances in Touch. Skillman, NJ: Johnson & Johnson; 1990. p. 96-104. , 2525 Wheeden A, Scafidi FA, Field T, Ironson G, Valdeon C, Bandstra E. Massage effects on cocaine-exposed preterm neonates. J Dev Behav Pediatr. 1993;14:318-22. , 2626 Scafidi FA, Field T, Schanberg SM. Factors that predict which preterm infants benefit most from massage therapy. J Dev Behav Pediatr. 1993;14:176-80. and 4444 Diego MA, Field T, Hernandez-Reif M. Temperature increases in preterm infants during massage therapy. Infant Behav Dev. 2008;31:149-52. variations in stimulation pressure;4242 Field T, Diego MA, Hernandez-Reif M, Deeds O, Figuereido B. Moderate versus light pressure massage therapy leads to greater weight gain in preterm infants. Infant Behav Dev. 2006;29:574-8. use or non-use of oil;3333 Arora J, Kumar A, Ramji S. Effect of oil massage on growth and neurobehavior in very low birth weight preterm neonates. Indian Pediatr. 2005;42:1092-100. , 4040 Vaivre-Douret L, Oriot D, Blossier P, Py A, Kasolter-Péré M, Zwang J. The effect of multimodal stimulation and cuta- neous application of vegetable oils on neonatal development in preterm infants: a randomized controlled trial. Child Care Health Dev. 2009;35:96-105. and 4141 Sankaranarayanan K, Mondkar JA, Chauhan MM, Mascarenhas BM, Mainkar AR, Salvi RY. Oil massage in neonates: an open ran- domized controlled study of coconut versus mineral oil. Indian Pediatr. 2005;42:877-84. speed of brain maturation;3838 Livingston K, Beider S, Kant AJ, Gallardo CC, Joseph MH, Gold JI. Touch and massage for medically fragile infants. Evid Based Complement Alternat Med. 2009;6:473-82. vagal activity and gastric motility;2828 Diego MA, Field T, Hernandez-Reif M. Vagal activity, gastric motility, and weight gain in massaged preterm neonates. J Pedi- atr. 2005;147:50-5. and 2929 Diego MA, Field T, Hernandez-Reif M, Deeds O, Ascencio A, Begert G. Preterm infant massage elicits consistent increases in vagal activity and gastric motility that are associated with greater weight gain. Acta Paediatr. 2007;96:1588-91. serum insulin and growth factor I levels;3030 Field T, Diego M, Hernandez-Reif M, Dieter JN, Kumar AM, Schanberg S, et al. Insulin and insulin-like growth factor-1 increased in preterm neonates following massage therapy. J Dev Behav Pediatr. 2008;29:463-6. and 3737 Moyer-Mileur LJ, Haley S, Slater H, Beachy J, Smith SL. Massage improves growth quality by decreasing body fat deposition in male preterm infants. J Pediatr. 2013;162:490-5. late-onset sepsis;1616 Mendes EW, Procianoy RS. Massage therapy reduces hospital stay and occurrence of late-onset sepsis in very preterm neonates. J Perinatol. 2008;28:815-20. body fat deposition;3737 Moyer-Mileur LJ, Haley S, Slater H, Beachy J, Smith SL. Massage improves growth quality by decreasing body fat deposition in male preterm infants. J Pediatr. 2013;162:490-5.effect on the immune system;3232 Ang JY, Lua JL, Mathur A, Thomas R, Asmar BI, Savasan S, et al. A randomized placebo-controlled trial of massage ther- apy on the immune system of preterm infants. Pediatrics. 2012;130:e1549-58. and bone formation.4545 Aly H, Moustafa MF, Hassanein SM, Massaro AN, Amer HA, Patel K. Physical activity combined with massage improves bone mineralization in premature infants: a randomized trial. J Peri- natol. 2004;24:305-9. The studies had very similar objectives; that is, to identify the effects of TKS on these parameters and the possible causes of its benefits.

Some studies using only KS obtained results not only in greater weight gain but also in bone mineralization.4646 Moyer-Mileur LJ, Brunstetter V, McNaught TP, Gill G, Chan GM. Daily physical activity program increases bone mineralization and growth in preterm very low birth weight infants. Pediatrics. 2000;106:1088-92. , 4747 Vignochi CM, Miura E, Canani LH. Effects of motor physical ther- apy on bone mineralization in premature infants: a randomized controlled study. J Perinatol. 2008;28:624-31. and 4848 Vignochi CM, Silveira RC, Miura E, Canani LH, Procianoy RS. Physical therapy reduces bone resorption and increases bone formation in preterm infants. Am J Perinatol. 2012;29:573-8. As for TKS with or without KS for bone weight gain analyzed herein, they found that there was no ideal level of stimulation4747 Vignochi CM, Miura E, Canani LH. Effects of motor physical ther- apy on bone mineralization in premature infants: a randomized controlled study. J Perinatol. 2008;28:624-31. or optimal duration, frequency, and type of exercise for bone development.4949 Litmanovitz I, Dolfin T, Arnon S, Regev RH, Nemet D, Eliakim A. Assisted exercise and bone strength in preterm infants. Calcif Tissue Int. 2007;80:39-43. Further evaluation of this intervention (KS) was suggested to indicate for this purpose.5050 Schulzke SM, Trachsel D, Patole SK. Physical activity programs for promoting bone mineralization and growth in preterm infants. Cochrane Database Syst Rev. 2007; (2). CD005387. A more recent study demonstrated a significant improvement in bone formation and decrease of bone resorption, using a more rigorous methodological design.4848 Vignochi CM, Silveira RC, Miura E, Canani LH, Procianoy RS. Physical therapy reduces bone resorption and increases bone formation in preterm infants. Am J Perinatol. 2012;29:573-8.

A few studies have described the adverse situations that could occur during the procedure and the parameters that should encourage the therapist to interrupt the session.1414 Mathai S, Fernandez A, Mondkar J, Kanbur W. Effects of tactile- kinesthetic stimulation in preterms: a controlled trial. Indian Pediatr. 2001;38:1091-8. , 1818 Fucile S, Gisel EG. Sensorimotor interventions improve growth and motor function in preterm infants. Neonatal Netw. 2010;29:359-66. , 1919 Lee HK. The effect of infant massage on weight gain, physio- logical and behavioral responses in premature infants. Taehan Kanho Hakhoe Chi. 2005;35:1451-60. , 2626 Scafidi FA, Field T, Schanberg SM. Factors that predict which preterm infants benefit most from massage therapy. J Dev Behav Pediatr. 1993;14:176-80. and 3333 Arora J, Kumar A, Ramji S. Effect of oil massage on growth and neurobehavior in very low birth weight preterm neonates. Indian Pediatr. 2005;42:1092-100. Certain signs during the application of the TKS, such as stress or uninterrupted crying for more than 60 seconds,2626 Scafidi FA, Field T, Schanberg SM. Factors that predict which preterm infants benefit most from massage therapy. J Dev Behav Pediatr. 1993;14:176-80. defecation or urination,1414 Mathai S, Fernandez A, Mondkar J, Kanbur W. Effects of tactile- kinesthetic stimulation in preterms: a controlled trial. Indian Pediatr. 2001;38:1091-8. increased heart rate,1919 Lee HK. The effect of infant massage on weight gain, physio- logical and behavioral responses in premature infants. Taehan Kanho Hakhoe Chi. 2005;35:1451-60. and 2727 Dieter JN, Field T, Hernandez-Reif M, Emory EK, Redzepi M. Stable preterm infants gain more weight and sleep less after five days of massage therapy. J Pediatr Psychol. 2003;28:403-11. or heart rate < 100 for 12 seconds and desaturation for more than 30 seconds,1919 Lee HK. The effect of infant massage on weight gain, physio- logical and behavioral responses in premature infants. Taehan Kanho Hakhoe Chi. 2005;35:1451-60. were some of the causes that led the therapists to interrupt the procedure or discontinue the study. Some therapists considered some signs in the 24 hours that preceded the intervention to suspend the procedure, such as fussing, vomiting, growing oxygen demand, frequent episodes of apnea, bradycardia, desaturation, or interventions conducted within the 30 minutes that preceded TKS, such as sight and hearing tests.1818 Fucile S, Gisel EG. Sensorimotor interventions improve growth and motor function in preterm infants. Neonatal Netw. 2010;29:359-66. Arora et al. 3333 Arora J, Kumar A, Ramji S. Effect of oil massage on growth and neurobehavior in very low birth weight preterm neonates. Indian Pediatr. 2005;42:1092-100. separated the adverse situations into temporary interruption and minor problems that neither affected feeding nor required any interruption in the trial.

Despite the information above, the majority of the studies did not mention adverse events and/or did not describe a course of action to deal with adverse events during the intervention. The studies that reported the occurrence of events that required the interruption of the procedure did not indicate how the procedure was resumed; for example, whether it was resumed from the start of the massage routine or whether it was continued from where it had stopped; also, they did not indicate whether the procedure should be resumed on the same day or on the next day, or whether these interruptions could affect weight gain. The clinical trials studied by this review made a relevant contribution to the scope of TS. Nevertheless, adding detailed data highlighted by this review, such as adverse events, would improve methodology and reliability for future studies.

Limitations

This systematic review was performed using two databases, in addition to checking the bibliographic articles of those that met the inclusion criteria; however, the possibility of not having included an article relevant to the topic that could have been found in other databases cannot be ruled out.

Conclusion

Assessment of the methodology of the studies reviewed herein showed that there is no standard for application of TS technique or recommended course of action if adverse events occur during the procedure. The effect of these adverse events that can occur during the TKS procedure may influence the results.

Generally, some kind of benefit associated with TKS, such as faster weight gain, shorter hospital stay, and better behavior, among others, was reported by all studies that used TS or TKS in PI. Nurseries have many stressors and TKS has been shown to be helpful in this context. Therefore, TKS should be considered as a possible therapy to be associated with the standard medical treatment. Even discrete gains in this population can result in long-term benefits. Future studies may raise the level of methodological rigor and describe the adverse events that can occur during the procedure. This may permit other researchers to be more aware of expect outcomes, and a standard TKS technique could be established.

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  • Please cite this article as: Pepino VC, Mezzacappa MA. Application of tactile/kinesthetic stimulation in preterm infants: a systematic review. J Pediatr (Rio J). 2015;91:213-33.
  • ☆☆
    Study conducted at Department of Pediatrics, Faculty of Medical Sciences, Universidade Estadual de Campinas (UNICAMP), São Paulo, SP, Brazil

Data availability

Data citations

United States National Library of Medicine of the National Institutes of Health. [cited 17 Jul 2014]. Available from: www.ncbi.nlm.nih.gov/pubmed

Publication Dates

  • Publication in this collection
    May-Jun 2015

History

  • Received
    19 Sept 2014
  • Accepted
    06 Oct 2014
Sociedade Brasileira de Pediatria Av. Carlos Gomes, 328 cj. 304, CEP: 90480-000 , Tel.: (+55 51) 3108-3328 - Porto Alegre - RS - Brazil
E-mail: assessoria@jped.com.br