Patterned frequency-modulated oral stimulation in preterm infants: A multicenter randomized controlled trial

Dongli Song, Priya Jegatheesan, Suhas Nafday, Kaashif A Ahmad, Jonathan Nedrelow, Mary Wearden, Sheri Nemerofsky, Sunshine Pooley, Diane Thompson, Daniel Vail, Tania Cornejo, Zahava Cohen, Balaji Govindaswami, Dongli Song, Priya Jegatheesan, Suhas Nafday, Kaashif A Ahmad, Jonathan Nedrelow, Mary Wearden, Sheri Nemerofsky, Sunshine Pooley, Diane Thompson, Daniel Vail, Tania Cornejo, Zahava Cohen, Balaji Govindaswami

Abstract

Objective: To evaluate the effect of patterned, frequency-modulated oro-somatosensory stimulation on time to full oral feeds in preterm infants born 26-30 weeks gestation.

Study design: This is a multicenter randomized controlled trial. The experimental group (n = 109) received patterned, frequency-modulated oral stimulation via the NTrainer system through a pulsatile pacifier and the control group (n = 101) received a non-pulsatile pacifier. Intent-to-treat analysis (n = 210) was performed to compare the experimental and control groups and the outcomes were analyzed using generalized estimating equations. Time-to-event analyses for time to reach full oral feeds and length of hospital stay were conducted using Cox proportional hazards models.

Results: The experimental group had reduction in time to full oral feeds compared to the control group (-4.1 days, HR 1.37 (1.03, 1.82) p = 0.03). In the 29-30 weeks subgroup, infants in the experimental group had a significant reduction in time to discharge (-10 days, HR 1.87 (1.23, 2.84) p < 0.01). This difference was not observed in the 26-28 weeks subgroup. There was no difference in growth, mortality or morbidities between the two groups.

Conclusions: Patterned, frequency-modulated oro-somatosensory stimulation improves feeding development in premature infants and reduces their length of hospitalization.

Trial registration: ClinicalTrials.gov NCT01158391.

Conflict of interest statement

DT was an employee of Innara Health, Inc. during the second half of the study period. DT coordinated the clinical trial conducted at the five participating centers, monitored the progress of the study and critically reviewed the manuscript. The other authors have no conflicts of interest to disclose. DT is an employee of a Venture consulting LLC. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

Figures

Fig 1. CONSORT flowchart—study subject eligibility and…
Fig 1. CONSORT flowchart—study subject eligibility and enrollment.
Fig 2. Intervention sessions.
Fig 2. Intervention sessions.
(A) The NTrainer pulses are patterned as 6-cycle bursts followed by 2-second pause periods. (B) An experimental session: three 3-minute PFOS epochs and two 5.5-minute non-stimulation epochs; a control session: a 20 minute no pulse period. PFOS: patterned and frequency-modulated oro-somatosensory stimulation.
Fig 3. Oral feeding advance protocol.
Fig 3. Oral feeding advance protocol.
Fig 4. Kaplan-Meier curves for time to…
Fig 4. Kaplan-Meier curves for time to reach full oral feeds and length of stay.

References

    1. Delaney AL, Arvedson JC. Development of swallowing and feeding: prenatal through first year of life. Dev Disabil Res Rev. 2008;14(2):105–17. 10.1002/ddrr.16
    1. da Costa SP, van den Engel-Hoek L, Bos AF. Sucking and swallowing in infants and diagnostic tools. Journal of perinatology. 2008;28(4):247–57. 10.1038/sj.jp.7211924
    1. Barlow SM. Oral and respiratory control for preterm feeding. Current opinion in otolaryngology & head and neck surgery. 2009;17(3):179–86.
    1. Foster JP, Psaila K, Patterson T. Non-nutritive sucking for increasing physiologic stability and nutrition in preterm infants. Cochrane Database Syst Rev. 2016;10:CD001071 10.1002/14651858.CD001071.pub3
    1. Bakewell-Sachs S, Medoff-Cooper B, Escobar GJ, Silber JH, Lorch SA. Infant functional status: the timing of physiologic maturation of premature infants. Pediatrics. 2009;123(5):e878–86. 10.1542/peds.2008-2568
    1. Lau C. Development of infant oral feeding skills: what do we know? Am J Clin Nutr. 2016. February;103(2):616S–21S 10.3945/ajcn.115.109603
    1. Bingham PM. Deprivation and dysphagia in premature infants. Journal of child neurology. 2009;24(6):743–9. 10.1177/0883073808329530
    1. Browne JV, Ross ES. Eating as a neurodevelopmental process for high-risk newborns. Clinics in perinatology. 2011;38(4):731–43. 10.1016/j.clp.2011.08.004
    1. American Academy of Pediatrics Coommittee on Fetus and Newborn. Hospital discharge of the high-risk neonate. Pediatrics. 2008;122(5):1119–26. 10.1542/peds.2008-2174
    1. Pagliaro CL, Bühler KE, Ibidi SM, Limongi SC. Dietary transition difficulties in preterm infants: critical literature review. J Pediatr (Rio J). 2016;92(1):7–14.
    1. Mizuno K, Ueda A. Neonatal feeding performance as a predictor of neurodevelopmental outcome at 18 months. Developmental medicine and child neurology. 2005;47(5):299–304.
    1. Medoff-Cooper B, Shults J, Kaplan J. Sucking behavior of preterm neonates as a predictor of developmental outcomes. Journal of developmental and behavioral pediatrics. 2009;30(1):16–22. 10.1097/DBP.0b013e318196b0a8
    1. Crapnell TL, Woodward LJ, Rogers CE, Inder TE, Pineda RG. Neurodevelopmental profile, growth, and psychosocial environment of preterm infants with difficult feeding behavior at age 2 years. The Journal of pediatrics. 2015;167(6):1347–53. 10.1016/j.jpeds.2015.09.022
    1. Adams-Chapman I, Bann CM, Vaucher YE, Stoll BJ. Association between feeding difficulties and language delay in preterm infants using Bayley Scales of Infant Development-Third Edition. The Journal of pediatrics. 2013;163(3):680–5.e1-3. 10.1016/j.jpeds.2013.03.006
    1. Malas K, Trudeau N, Chagnon M, McFarland DH. Feeding-swallowing difficulties in children later diagnosed with language impairment. Developmental medicine and child neurology. 2015;57(9):872–9. 10.1111/dmcn.12749
    1. Als H. Lester BM, Brazelton TB. Dynamics of the behavioral organization of the premature infant: A theoretical perspective In: Infants Born at risk: Field TM, Sostek AM, Goldberg S, Shauman HH, editors. New York: Spectrum Publication; 1979. Pp. 173–193.
    1. Als H. Curr Opin Pediatr. Developmental care in the newborn intensive care unit. Curr Opin Pediatr. 1998. April;10(2):138–42.
    1. Harding C. An evaluation of the benefits of non-nutritive sucking for premature infants as described in the literature. Arch Dis Child. 2009. August;94(8):636–40 10.1136/adc.2008.144204
    1. Greene Z ODC, Walshe M. Oral stimulation for promoting oral feeding in preterm infants. Cochrane Database Syst Rev. 2016:74.
    1. Bingham PM, Abassi S, Sivieri E. A pilot study of milk odor effect on nonnutritive sucking by premature newborns. Archives of pediatrics & adolescent medicine. 2003;157(1):72–75.
    1. Yildiz A, Arikan D, Gözüm S, Taştekın A, Budancamanak I. The effect of the odor of breast milk on the time needed for transition from gavage to total oral feeding in preterm infants. J Nurs Scholarsh. 2011;43(3):265–273. 10.1111/j.1547-5069.2011.01410.x
    1. Chorna OD, Slaughter JC, Wang L, Stark AR, Maitre NL. A pacifier-activated music player with mother's voice improves oral feeding in preterm infants. Pediatrics. 2014;133(3):462–468. 10.1542/peds.2013-2547
    1. Yildiz A, Arikan D. The effects of giving pacifiers to premature infants and making them listen to lullabies on their transition period for total oral feeding and sucking success. J Clin Nurs. 2012;21(5–6):644–656. 10.1111/j.1365-2702.2010.03634.x
    1. Zimmerman E, Barlow SM. The effects of vestibular stimulation rate and magnitude of acceleration on central pattern generation for chest wall kinematics in preterm infants. J Perinatol. 2012;32(8):614–620. 10.1038/jp.2011.177
    1. White-Traut RC, Nelson MN, Silvestri JM, Vasan U, Littau S, Meleedy-Rey et al. Effect of auditory, tactile, visual, and vestibular intervention on length of stay, alertness, and feeding progression in preterm infants. Dev Med Child Neurol. 2002;44(2):91–97.
    1. Tian X, Yi LJ, Zhang L, et al. Oral Motor Intervention Improved the Oral Feeding in Preterm Infants: Evidence Based on a Meta-Analysis With Trial Sequential Analysis. Medicine (Baltimore). 2015;94(31):e1310 10.1097/MD.0000000000001310
    1. McCain GC. Promotion of preterm infant nipple feeding with nonnutritive sucking. J Pediatr Nurs. 1995. February;10(1):3–8 10.1016/S0882-5963(05)80093-4
    1. Fucile S, Gisel EG, Lau C. Effect of an oral stimulation program on sucking skill maturation of preterm infants. Dev Med Child Neurol. 2005. March;47(3):158–62.
    1. Fucile S, Gisel EG, McFarland DH, Lau C. Oral and non-oral sensorimotor interventions enhance oral feeding performance in preterm infants. Dev Med Child Neurol. 2011. September;53(9):829–835. 10.1111/j.1469-8749.2011.04023.x
    1. Boiron M, Da Nobrega L, Roux S, Henrot A, Saliba E. Effects of oral stimulation and oral support on non-nutritive sucking and feeding performance in preterm infants. Dev Med Child Neurol. 2007. June;49(6):439–44. 10.1111/j.1469-8749.2007.00439.x
    1. Zhang Y, Lyu T, Hu X, Shi P, Cao Y, Latour JM. Effect of nonnutritive sucking and oral stimulation on feeding performance in preterm infants: a randomized controlled trial. Pediatr Crit Care Med. 2014;15(7):608–614. 10.1097/PCC.0000000000000182
    1. Lau C, Smith EO. Interventions to improve the oral feeding performance of preterm infants. Acta Paediatr. 2012. July;101(7):e269–74. 10.1111/j.1651-2227.2012.02662.x
    1. Harding C, Frank L, Van Someren V, Hilari K 3, Botting N. How does non-nutritive sucking support infant feeding? Infant Behav Dev. 2014. November;37(4):457–64. 10.1016/j.infbeh.2014.05.002
    1. Boiron M, Da Nobrega L, Roux S, Henrot A, Saliba E. Effects of oral stimulation and oral support on non-nutritive sucking and feeding performance in preterm infants. Dev Med Child Neurol. 2007. June;49(6):439–44. 10.1111/j.1469-8749.2007.00439.x
    1. Bragelien R, Røkke W, Markestad T. Stimulation of sucking and swallowing to promote oral feeding in premature infants. Acta Paediatr. 2007. October;96(10):1430–2. 10.1111/j.1651-2227.2007.00448.x
    1. Barlow SM, Finan DS, Lee J, Chu S. Synthetic orocutaneous stimulation entrains preterm infants with feeding difficulties to suck. Journal of perinatology: official journal of the California Perinatal Association. 2008;28(8):541–8.
    1. Poore M, Zimmerman E, Barlow SM, Wang J, Gu F. Patterned orocutaneous therapy improves sucking and oral feeding in preterm infants. Acta Paediatr. 2008;97(7):920–7. 10.1111/j.1651-2227.2008.00825.x
    1. Barlow S, Lee J, Wang J, Oder A, Oh H, Hall S, et al. Effects of oral stimulus frequency spectra on the development of non-nutritive suck in preterm infants with respiratory distress syndrome or chronic lung disease, and preterm infants of diabetic mothers. J Neonatal Nurs. 2014;20(4):178–88. 10.1016/j.jnn.2013.10.005
    1. Simpson C, Schanler RJ, Lau C. Early introduction of oral feeding in preterm infants. Pediatrics. 2002;110(3):517–22.
    1. Patel AL, Engstrom JL, Meier PP, Jegier BJ, Kimura RE. Calculating postnatal growth velocity in very low birth weight (VLBW) premature infants. Journal of perinatology. 2009;29(9):618–22. 10.1038/jp.2009.55
    1. Hibbs AM, Black D, Palermo L, Cnaan A, Luan X, Truog WE, et al. Accounting for multiple births in neonatal and perinatal trials: systematic review and case study. J Pediatr. 2010. February;156(2):202–8. 10.1016/j.jpeds.2009.08.049
    1. Carlo WA, Finer NN, Walsh MC, Rich W, Gantz MG, Laptook AR, et al. Target ranges of oxygen saturation in extremely preterm infants. N Engl J Med. 2010. May 27;362(21):1959–69. 10.1056/NEJMoa0911781
    1. Wolff PH. The serial organization of sucking in the young infant. Pediatrics. 1968. December;42(6):943–56
    1. Hack M, Estabrook MM, Robertson SS. Development of sucking rhythm in preterm infants. Early Hum Dev. 1985. July;11(2):133–40.
    1. Hafström M, Kjellmer I. Non-nutritive sucking in the healthy pre-term infant. Early Hum Dev. 2000. November;60(1):13–24.
    1. Lau C, Alagugurusamy R, Schanler RJ, Smith EO, Shulman RJ. Characterization of the developmental stages of sucking in preterm infants during bottle feeding. Acta Paediatr. 2000. July;89(7):846–52.
    1. Lau C, Kusnierczyk I. Dysphagia. 2001 Winter;16(1):58–67. Quantitative evaluation of infant's nonnutritive and nutritive sucking. Dysphagia. 2001 Winter;16(1):58–67.
    1. Barlow SM. Central pattern generation involved in oral and respiratory control for feeding in the term infant. Curr Opin Otolaryngol Head Neck Surg. 2009
    1. Bingham PM, Ashikaga T, Abbasi S. Prospective study of non-nutritive sucking and feeding skills in premature infants. Arch Dis Child Fetal Neonatal Ed. 2010;95(3):F194–200. 10.1136/adc.2009.164186
    1. Mizuno K, Ueda A. The maturation and coordination of sucking, swallowing, and respiration in preterm infants. J Pediatr. 2003;142(1):36–40. 10.1067/mpd.2003.mpd0312
    1. Lau C.Development of Suck and Swallow Mechanisms in Infants. Ann Nutr Metab. 2015;66 Suppl 5:7–14.
    1. Gewolb IH, Vice FL, Schwietzer-Kenney EL, Taciak VL, Bosma JF. Developmental patterns of rhythmic suck and swallow in preterm infants. Dev Med Child Neurol. 2001. January;43(1):22–7.
    1. Gewolb IH, Vice FL. Abnormalities in the coordination of respiration and swallow in preterm infants with bronchopulmonary dysplasia. Dev Med Child Neurol. 2006;48(7):595–599. 10.1017/S0012162206001241
    1. da Costa SP, van der Schans CP, Zweens MJ, Boelema SR, van der Meij E, Boerman MA, et al. Development of sucking patterns in pre-term infants with bronchopulmonary dysplasia. Neonatology. 2010;98(3):268–277. 10.1159/000281106
    1. Jadcherla SR, Wang M, Vijayapal AS, Leuthner SR. Impact of prematurity and co-morbidities on feeding milestones in neonates: a retrospective study. J Perinatol. 2010;30(3):201–208. 10.1038/jp.2009.149
    1. Fucile S, McFarland DH, Gisel EG, Lau C. Oral and nonoral sensorimotor interventions facilitate suck-swallow-respiration functions and their coordination in preterm infants. Early Hum Dev. 2012. June;88(6):345–50. 10.1016/j.earlhumdev.2011.09.007
    1. McCain GC. An evidence-based guideline for introducing oral feeding to healthy preterm infants.Neonatal Netw. 2003. Sep-Oct;22(5):45–50 10.1891/0730-0832.22.5.45
    1. Ludwig SM, Waitzman KA. Changing feeding documentation to reflect infant-driven feeding prctice. Newborn & Infant Nursing Reviews. 2007;7(3):155–60.
    1. McCain GC.Behavioral state activity during nipple feedings for preterm infants. Neonatal Netw. 1997. August;16(5):43–7.
    1. Pickler RH1, Frankel HB, Walsh KM, Thompson NM. Effects of nonnutritive sucking on behavioral organization and feeding performance in preterm infants. Nurs Res. 1996. May-Jun;45(3):132–5.
    1. Gill NE, Behnke M, Conlon M, Anderson GC. Nonnutritive sucking modulates behavioral state for preterm infants before feeding. Scand J Caring Sci. 1992;6(1):3–7.
    1. Griffith T1, Rankin K, White-Traut R.The Relationship between behavioral states and oral feeding efficiency in preterm infants. Adv Neonatal Care. 2017. February;17(1):E12–E19. 10.1097/ANC.0000000000000318
    1. White-Traut RC, Berbaum ML, Lessen B, McFarlin B, Cardenas L.Feeding readiness in preterm infants: the relationship between preterm behavioral state and feeding readiness behaviors and efficiency during transition from gavage to oral feeding. MCN Am J Matern Child Nurs. 2005. Jan-Feb;30(1):52–9.
    1. Pimenta HP, Moreira ME, Rocha AD, Gomes SC Jr, Pinto LW, Lucena SL. Effects of non-nutritive sucking and oral stimulation on breastfeeding rates for preterm, low birth weight infants: a randomized clinical trial. J Pediatr (Rio J). 2008. Sep-Oct;84(5):423–7.
    1. Bache M, Pizon E, Jacobs J, Vaillant M, Lecomte A. Effects of pre-feeding oral stimulation on oral feeding in preterm infants: a randomized clinical trial. Early Hum Dev. 2014. March;90(3):125–9. 10.1016/j.earlhumdev.2013.12.011
    1. Kaya V, Aytekin A. Effects of pacifier use on transition to full breastfeeding and sucking skills in preterm infants: a randomised controlled trial. J Clin Nurs. 2017. July;26(13–14):2055–2063. 10.1111/jocn.13617
    1. Say B, Simsek GK, Canpolat FE, Oguz SS. Effects of Pacifier Use on Transition time from gavage to breastfeeding in preterm infants: A randomized controlled trial. Breastfeed Med. 2018. Jul-Aug;13(6):433–437. 10.1089/bfm.2018.0031
    1. Fucile S, Milutinov M, Timmons K, Dow K. Oral Sensorimotor Intervention Enhances Breastfeeding Establishment in Preterm Infants. Breastfeed Med. 2018. September;13(7):473–478. 10.1089/bfm.2018.0014
    1. Trulsson M, Johansson RS. Orofacial mechanoreceptors in humans: encoding characteristics and responses during natural orofacial behaviors. Behav Brain Res. 2002;135(1–2):27–33.
    1. Barlow SM. Mechanical frequency detection thresholds in the human face. Exp Neurol. 1987;96(2):253–61
    1. Barlow SM, Jegatheesan P, Weiss S, Govindaswami B, Wang J, Lee J, et al. Amplitude-integrated EEG and range-EEG modulation associated with pneumatic orocutaneous stimulation in preterm infants. Journal of perinatology. 2014;34(3):213–9. 10.1038/jp.2013.150
    1. Song D, Jegatheesan P, Weiss S, Govindaswami B, Wang J, Lee J, et al. Modulation of EEG spectral edge frequency during patterned pneumatic oral stimulation in preterm infants. Pediatr Res. 2014;75(1–1):85–92. 10.1038/pr.2013.179
    1. Dodrill P, Donovan T, Cleghorn G, McMahon S, Davies PS. Attainment of early feeding milestones in preterm neonates. Journal of perinatology. 2008;28(8):549–55. 10.1038/jp.2008.56
    1. Barlow SM, Lee J, Wang J, Oder A, Hall S, Knox K, et al. Frequency-modulated orocutaneous stimulation promotes non-nutritive suck development in preterm infants with respiratory distress syndrome or chronic lung disease. Journal of perinatology. 2014;34(2):136–42. 10.1038/jp.2013.149
    1. Eichenwald EC, Blackwell M, Lloyd JS, Tran T, Wilker RE, Richardson DK. Inter-neonatal intensive care unit variation in discharge timing: influence of apnea and feeding management. Pediatrics. 2001;108(4):928–33.
    1. Barlow SM, Maron JL, Alterovitz G, Song D, Wilson BJ, Jegatheesan P, et al. Somatosensory modulation of salivary gene expression and oral feeding in preterm infants: fandomized controlled trial. JMIR Res Protoc. 2017;6(6):e113 10.2196/resprot.7712

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe