Impact of emollient therapy for preterm infants in the neonatal period on child neurodevelopment in Bangladesh: an observational cohort study

Gary L Darmstadt, Naila Z Khan, Summer Rosenstock, Humaira Muslima, Monowara Parveen, Wajeeha Mahmood, A S M Nawshad Uddin Ahmed, M A K Azad Chowdhury, Scott Zeger, Samir K Saha, Gary L Darmstadt, Naila Z Khan, Summer Rosenstock, Humaira Muslima, Monowara Parveen, Wajeeha Mahmood, A S M Nawshad Uddin Ahmed, M A K Azad Chowdhury, Scott Zeger, Samir K Saha

Abstract

Background: Topical treatment with sunflower seed oil (SSO) or Aquaphor® reduced sepsis and neonatal mortality in hospitalized preterm infants <33 weeks' gestational age in Bangladesh. We sought to determine whether the emollient treatments improved neurodevelopmental outcomes during early childhood.

Methods: 497 infants were randomized to receive SSO, Aquaphor®, or neither through the neonatal period or hospital discharge. 159 infant survivors were enrolled in the longitudinal follow-up study using a validated Rapid Neurodevelopmental Assessment tool and the Bayley Scales of Infant Development II (BSID II) administered at three-monthly intervals for the first year and thereafter at six-monthly intervals. Lowess smoothing was used to display neurodevelopmental status across multiple domains by age and treatment group, and Generalized Estimating Equations (GEE) were used to compare treatment groups across age points.

Results: 123 children completed at least one follow-up visit. Lowess graphs suggest that lower proportions of children who received massage with either SSO or Aquaphor® had neurodevelopmental delays than control infants in a composite outcome of disabilities. In GEE analysis, infants receiving SSO showed a significant protective effect on the development of fine motor skills [odds ratio (OR) 0.92, 95% confidence interval (CI) 0.86-0.98, p=0.006]. The Psychomotor Development Index (PDI) in the BSID II showed significantly lower disability rates in the Aquaphor group (23.6%) compared to the control (55.2%) (OR 0.21, 95% CI 0.06-0.72, p=0.004).

Conclusions: Emollient massage of very preterm, hospitalized newborn infants improved some child neurodevelopmental outcomes over the first 2 years of follow-up. Findings warrant further confirmatory research.

Trial registration: ClinicalTrials.gov (98-04-21-03-2) under weblink https://ichgcp.net/clinical-trials-registry/NCT00162747.

Keywords: Emollient; Follow-up; Neonatal; Neurodevelopment; Newborn; Preterm.

Conflict of interest statement

The authors have indicated they have no potential conflicts of interest to disclose. The authors have indicated they have no financial relationships relevant to this article to disclose.

Figures

Fig. 1
Fig. 1
Lowess graphs of disability probability for preterm infants followed-up during early childhood in Bangladesh. a Probability of any disability. b Probability of cognitive disability. c Probability of fine motor disability. d Probability of hearing disability. e Probability of speech disability

References

    1. Liu L, Oza S, Hogan D, Perin J, Rudan I, Lawn JE, Cousens S, Mathers C, Black RE. Global, regional, and national causes of child mortality in 2000-13, with projections to inform post-2015 priorities: an updated systematic analysis. Lancet. 2015;385(9966):430–440. doi: 10.1016/S0140-6736(14)61698-6.
    1. Dammann O, Leviton A, Gappa M, Dammann CE. Lung and brain damage in preterm newborns, and their association with gestational age, prematurity subgroup, infection/inflammation and long term outcome. BJOG. 2005;112(Suppl 1):4–9. doi: 10.1111/j.1471-0528.2005.00576.x.
    1. Stjernqvist K, Svenningsen NW. Ten-year follow-up of children born before 29 gestational weeks: health, cognitive development, behavior and school achievement. Acta Paediatr. 1999;88(5):557–562. doi: 10.1111/j.1651-2227.1999.tb00175.x.
    1. Wolke D, Meyer R. Cognitive status, language attainment, and prereading skills of 6-year-old very preterm children and their peers: the Bavarian Longitudinal Study. Dev Med Child Neurol. 1999;4:94–109. doi: 10.1017/S0012162299000201.
    1. Taylor H, Klein N, Minich N, Hack M. Middle-school-age outcomes in children with very low birth weight. Child Dev. 2000;71:1495–1511. doi: 10.1111/1467-8624.00242.
    1. Conley D, Bennett N. Comment: outcomes in young adulthood for very-low-birth weight infants. New Engl J Med. 2002;347:141–143. doi: 10.1056/NEJM200207113470214.
    1. Lawn JE, Blencowe H, Darmstadt GL, Bhutta ZA. Beyond newborn survival: the world you are born into determines your risk of disability-free survival. Pediatr Res. 2013;74(Suppl 1):1–3. doi: 10.1038/pr.2013.202.
    1. Luu TM, Rehman Mian MO, Nuyt AM. Long-term impact of preterm birth: neurodevelopmental and physical health outcomes. Clin Perinatol. 2017;44(2):305–314. doi: 10.1016/j.clp.2017.01.003.
    1. Spittle A, Orton J, Anderson PJ, Boyd R, Doyle LW. Early developmental intervention programmes provided post hospital discharge to prevent motor and cognitive impairment in preterm infants. Cochrane Database Syst Rev. 2015;(11):CD005495. 10.1002/14651858.CD005495.pub4.
    1. Conley D, Bennett NG. Is biology destiny? Birth weight and life chances. Am Sociol Rev. 2000;65(3):458–467. doi: 10.2307/2657467.
    1. Lawn JE, Blencowe H, Oza S, You D, Lee AC, Waiswa P, Lalli M, Bhutta Z, Barros AJ, Christian P, Mathers C, Cousens SN, Lancet Every Newborn Study Group Progress, priorities, and potential beyond survival. Lancet. 2014;384(9938):189–205. doi: 10.1016/S0140-6736(14)60496-7.
    1. Khan NZ, Ahmed HM, Parveen M, Bhattacharya M, Begum N, Chowdhury S, Jahan M, Darmstadt GL. Neurodevelopmental outcomes of preterm infants in Bangladesh. Pediatrics. 2006;118(1):280–289. doi: 10.1542/peds.2005-2014.
    1. Leib SA, Benfield G, Guidubaldi J. Effects of early intervention and stimulation on the preterm infant. Pediatrics. 1980;66:83–89.
    1. Maulik PK, Darmstadt GL. Community-based interventions to optimize early childhood development in low resource settings. J Perinatol. 2009;29(8):531–542. doi: 10.1038/jp.2009.42.
    1. Darmstadt GL, Sutton P. Preterm birth and neurodevelopment: a review of outcomes and recommendations for early identification and cost-effective interventions. J Trop Pediatr. 2013;59(4):258–265. doi: 10.1093/tropej/fmt012.
    1. Hernandez-Reif M, Field T. Preterm infants benefit from early interventions. In: Osofsky J, Fitzgerald H, editors. WAIMH Handbook of Infant Mental Health. New York: Wiley; 2000. pp. 296–325.
    1. Black MM, Walker SP, Fernald LCH, Andersen CT, DiGirolamo AM, Lu C, McCoy D, Fink G, Shawar YR, Shiffman J, Devercelli AE, Wodon QT, Vargas-Barón E, Grantham-McGregor S, Lancet Early Childhood Development Series Steering Committee Early childhood development coming of age: science through the life course. Lancet. 2016;389(10064):77–90. doi: 10.1016/S0140-6736(16)31389-7.
    1. Britto PR, Lye SJ, Proulx K, Yousafzai AK, Matthews SG, Vaivada T, Perez-Escamilla R, Rao N, Ip P, Fernald LCH, MacMillan H, Hanson M, Wachs TD, Yao H, Yoshikawa H, Cerezo A, Leckman JF, Bhutta ZA. Nurturing care: promoting early childhood development. Lancet. 2016;389(10064):91–102. doi: 10.1016/S0140-6736(16)31390-3.
    1. Ottenbacher KJ, Muller L, Brandt D, Heintzelman A, Hojem P, Sharpe P. The effectiveness of tactile stimulation as a form of early intervention: a quantitative evaluation. J Dev Behav Pediatr. 1987;8(2):68–76. doi: 10.1097/00004703-198704000-00002.
    1. Vickers A, Ohlsson A, Lacy JB, Horsley A. Massage for promoting growth and development of preterm and/or low birth-weight infants. Cochrane Database Syst Rev. 2008;(4). 10.1002/14651858.CD000390.pub2.
    1. Dieter J, Field T, Hernandez-Reif M, Emory E, Redzepi M. Stable preterm infants gain more weight and sleep less after five days of massage therapy. J Pediatr Psychol. 2003;28(6):403–411. doi: 10.1093/jpepsy/jsg030.
    1. 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 Dev. 2002;67(1-2):37–45. doi: 10.1016/S0378-3782(01)00249-3.
    1. Lahat S, Mimouni FB, Ashbel G, Dollberg S. Energy expenditure in growing preterm infants receiving massage therapy. J Am Coll Nutr. 2007;26(4):356–359. doi: 10.1080/07315724.2007.10719623.
    1. Scafidi FA, Field TM, Schanberg SM, Bauer CR, Tucci K, Roberts J, Morrow C, Kuhn CM. Massage stimulates growth in preterm infants: a replication. Infant Behav Dev. 1990;13(2):167–188. doi: 10.1016/0163-6383(90)90029-8.
    1. Field T, Scafidi FA, Schanberg S. Massage of preterm newborns to improve growth and development. Pediatr Nurs. 1987;13:385–387.
    1. Scafidi FA, Field T, Schanberg SM. Factors that predict which preterm infants benefit most from massage therapy. J Dev Behav Pediatr. 1993;14(3):176–180. doi: 10.1097/00004703-199306010-00008.
    1. Rice RD. Neurophysiological development in premature neonates following stimulation. Dev Psychol. 1977;13(1):69–76. doi: 10.1037/0012-1649.13.1.69.
    1. Field T, Diego M, Hernandez-Reif M. Preterm infant massage therapy research: a review. Infant Behav Dev. 2010;33(2):115–124. doi: 10.1016/j.infbeh.2009.12.004.
    1. Kulkarni A, Kaushik JS, Gupta P, Sharma H, Agrawal R. Massage and touch therapy in neonates: the current evidence. Indian Pediatr. 2010;47(9):771–6.
    1. Badr LK, Abdallah B, Kahale L. A meta-analysis of preterm infant massage: an ancient practice with contemporary applications. MCN Am J Matern Child Nurs. 2015;40(6):344–358. doi: 10.1097/NMC.0000000000000177.
    1. Trivedi D. Cochrane Review Summary: massage for promoting mental and physical health in typically developing infants under the age of six months. Prim Health Care Res Dev. 2015;16(1):3–4. doi: 10.1017/S1463423614000462.
    1. 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(6):465–469. doi: 10.1007/s12098-012-0869-7.
    1. Wang L, He JL, Zhang XH. The efficacy of massage on preterm infants: a meta-analysis. Am J Perinatol. 2013;30(9):731–738. doi: 10.1055/s-0032-1332801.
    1. Salam RA, Darmstadt GL, Bhutta ZA. Effect of emollient therapy on clinical outcomes in preterm neonates in Pakistan: a randomised controlled trial. Arch Dis Child Fetal Neonatal Ed. 2015;100(3):F210–F215. doi: 10.1136/archdischild-2014-307157.
    1. Salam RA, Das JK, Darmstadt GL, Bhutta ZA. Emollient therapy for preterm newborn infants – evidence from the developing world. BMC Public Health. 2013;13(Suppl 3):S31. doi: 10.1186/1471-2458-13-S3-S31.
    1. Moyer-Mileur L, Luetkemeier M, Boomer L, Chan GM. Effect of physical activity on bone mineralization in premature infants. J Pediatr. 1995;127(4):620–625. doi: 10.1016/S0022-3476(95)70127-3.
    1. Arora J, Kumar A, Ramji S. Effect of oil massage on growth and neurobehavior in very low birth weight preterm neonates. Indian Pediatr. 2005;42:1092–1100.
    1. Vaivre-Douret L, Oriot D, Blossier P, Py A, Kasolter-Péré M, Zwang J. The effect of multimodal stimulation and cutaneous application of vegetable oils on neonatal development in preterm infants: a randomized controlled trial. Child Care Health Dev. 2009;35(1):96–105. doi: 10.1111/j.1365-2214.2008.00895.x.
    1. Bhatia S. Traditional childbirth practices: implications for a rural MCH program. Stud Fam Plan. 1981;12(2):66–75. doi: 10.2307/1966274.
    1. Iyengar SD, Bhakoo ON. Prevention of neonatal hypothermia in Himalayan villages. Trop Geogr Med. 1991;43(3):293–296.
    1. Ahmed ASMNU, Saha SK, Chowdhury MAKA, Law P, Black RE, Santosham M, Darmstadt GL. Acceptability of oil massage with skin barrier enhancing emollients in young neonates in Bangladesh. J Health Popul Nutr. 2007;25:236–240.
    1. Mullany LC, Darmstadt GL, Khatry SK, Tielsch JM. Traditional massage of newborns in Nepal: implications for trials of improved practice. J Trop Pediatr. 2005;51(2):82–86. doi: 10.1093/tropej/fmh083.
    1. Darmstadt GL, Saha SK. Neonatal oil massage. Indian Pediatr. 2003;40(11):1098–1099.
    1. Darmstadt GL, Saha SK. Traditional practice of oil massage of neonates in Bangladesh. J Health Popul Nutr. 2002;20:175–179.
    1. Duffy JL, Ferguson RM, Darmstadt GL. Opportunities for improving, adapting and introducing emollient therapy and improved newborn skin care practices in Africa. J Trop Pediatr. 2012;58(2):88–95. doi: 10.1093/tropej/fmr039.
    1. Darmstadt GL, Badrawi N, Law PA, Alam A, Ahmed S, Husein MH, Winch P, Santosham M, Gipson R. Topical therapy with sunflower seed oil prevents nosocomial infections and mortality in premature babies in Egypt: a randomized, controlled clinical trial. Pediatr Infect Dis J. 2004;23(8):719–725. doi: 10.1097/01.inf.0000133047.50836.6f.
    1. Darmstadt GL, Saha SK, Ahmed ASMNU, Chowdhury MAKA, Law PA, Ahmed S, Alam MA, Black RE, Santosham M. Effect of topical treatment with skin barrier-enhancing emollients on nosocomial infections in preterm infants in Bangladesh: a randomized controlled trial. Lancet. 2005;365(9464):1039–1045. doi: 10.1016/S0140-6736(05)71140-5.
    1. Darmstadt GL, Saha SK, Ahmed ASMNU, Ahmed S, Chowdhury MAKA, Law P, Rosenberg RE, Black RE, Santosham M. Effect of skin barrier therapy on neonatal mortality rates in preterm infants in Bangladesh: a randomized, controlled, clinical trial. Pediatrics. 2008;121(3):522–529. doi: 10.1542/peds.2007-0213.
    1. Darmstadt GL, Saha SK, Ahmed ASMNU, Choi Y, Chowdhury MAKA, Law PA, Ahmed S. Effect of topical emollient treatment of preterm neonates in Bangladesh on invasion of pathogens into the bloodstream. Pediatr Res. 2007;61(5, Part 1):588–593. doi: 10.1203/pdr.0b013e3180459f75.
    1. Prottey C, Hartop PJ, Press M. Correction of the cutaneous manifestation s of essential fatty acid deficiency in man by application of sunflower seed oil to the skin. J Invest Dermatol. 1975;64(4):228–234. doi: 10.1111/1523-1747.ep12510667.
    1. Fallah R, Akhavan Karbasi S, Golestan M, Fromandi M. Sunflower oil versus no oil moderate pressure massage leads to greater increases in weight in preterm neonates who are low birth weight. Early Hum Dev. 2013;89(9):769–772. doi: 10.1016/j.earlhumdev.2013.06.002.
    1. Taheri PA, Goudarzi Z, Shariat M, Nariman S, Matin EN. The effect of a short course of moderate pressure sunflower oil massage on the weight gain velocity and length of NICU stay in preterm infants. Infant Behav Dev. 2018;50:22–27. doi: 10.1016/j.infbeh.2017.11.002.
    1. Jabraeile M, Rasooly AS, Farshi MR, Malakouti J. Effect of olive oil massage on weight gain in preterm infants: a randomized controlled clinical trial. Niger Med J. 2016;57(3):160–163. doi: 10.4103/0300-1652.184060.
    1. Li Z, Zhong Q, Tang L. A meta-analysis of the efficacy and safety of using oil massage to promote infant growth. J Pediatr Nurs. 2016;31(5):e313–e322. doi: 10.1016/j.pedn.2016.04.003.
    1. Saedi R, Ghorbani Z, Shapouri MA. The effect of massage with medium-chain triglyceride oil on weight gain in premature neonates. Acta Med Iran. 2015;53(2):134–138.
    1. Lefevre A, Shilcutt SD, Saha SK, Ahmed ASMNU, Ahmed S, Chowdhury MAKA, Law PA, Black RE, Santosham M, Darmstadt GL. Cost effectiveness of skin barrier enhancing emollients among preterm neonates in Bangladesh. Bull World Health Organ. 2010;88(2):104–112. doi: 10.2471/BLT.08.058230.
    1. Dubowitz L, Dubowitz V, Goldberg C. Clinical assessment of gestational age in the newborn infant. J Pediatr. 1970;77(1):1–10. doi: 10.1016/S0022-3476(70)80038-5.
    1. Ballard J, Khoury J, Wedig K, Wang L, Ellers-Walsman B, Lipp R. New Ballard Score, expanded to include extremely premature infants. J Pediatr. 1991;119(3):417–423. doi: 10.1016/S0022-3476(05)82056-6.
    1. Rosenberg RE, Ahmed S, Ahmed ASMNU, Saha SK, Chowdhury MAKA, Black RE, Santosham M, Darmstadt GL. Determining gestational age in a low-resource setting: validity of last menstrual period. J Health Popul Nutr. 2009;27:332–338.
    1. Khan NZ, Muslima H, Begum D, Shilpi AB, Akhter S, Bilkis K, Begum N, Parveen M, Ferdous S, Morshed R, Batra M, Darmstadt GL. Validation of rapid neurodevelopmental assessment instrument for under-two-year-old children in Bangladesh. Pediatrics. 2010;125(4):e755–e762. doi: 10.1542/peds.2008-3471.
    1. World Health Organization . International Classification of Functioning, Disability and Health. Geneva: World Health Organization; 2001.
    1. Bayley N, Psychological Corporation . Bayley Scales of Infant Development. New York: Psychological Corp; 1969.
    1. Parveen M, Rahman S, Islam S, Zaman S, Hamadani J, Khan N. Adaptation of items of bayley scales of infant development-II (BSID-II) suitable for Bangladeshi infants. Dhaka Univ J Biological Sci. 2014;23(2):187–195. doi: 10.3329/dujbs.v23i2.20099.
    1. Thorndike RL, Hagen EP, Sattler JM. The Stanford-Binet Intelligence Scale. 4. Chicago: Riversham Publishing Company; 1986.
    1. Sultana N, Huq S, Khan M. Adaptation of the five nonverbal subtests of Stanford-Binet Intelligence Scale Fifth Edition for use in urban Bangladesh. Int J Soc Sci. 2012;5(1):45–62.
    1. Reynell J. The Reynell-Zinkin Scales. Developmental scales for young visually handicapped children: part i mental development. Windsor: NFER-Nelson Publishing Co; 1981.
    1. Cleveland W. Robust locally weighted regression and smoothing scatterplots. J Am Stat Assoc. 1979;74(368):829–836. doi: 10.1080/01621459.1979.10481038.
    1. Zeger S, Liang K, Albert P. Models for longitudinal data: a generalized estimating equation approach. Biometrics. 1988;44(4):1049–1060. doi: 10.2307/2531734.
    1. Cameron CE, Brock LL, Murrah WM, Bell LH, Worzalla SL, Grissmer D, Morrison FJ. Fine motor skills and executive function both contribute to kindergarten achievement. Child Dev. 2012;83(4):1229–1244. doi: 10.1111/j.1467-8624.2012.01768.x.
    1. Grissmer D, Grimm KJ, Aiyer SM, Murrah WM, Steele JS. Fine motor skills and early comprehension of the world: two new school readiness indicators. Dev Psychol. 2010;46(5):1008–1017. doi: 10.1037/a0020104.
    1. Field T. Preterm infant massage therapy studies: an American approach. Semin Neonatol. 2002;7(6):487–494. doi: 10.1053/siny.2002.0153.
    1. Abdallah B, Badr LK, Hawwari M. The efficacy of massage on short and long term outcomes in preterm infants. Infant Behav Dev. 2013;36(4):662–669. doi: 10.1016/j.infbeh.2013.06.009.

Source: PubMed

Sponsorit ja yhteistyökumppanit

Sairaudet

Huumeiden interventiot

3
Tilaa