EHD-03909; No of Pages 5 Early Human Development xxx (2014) xxx–xxx
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Early Human Development journal homepage: www.elsevier.com/locate/earlhumdev
Effects of pre-feeding oral stimulation on oral feeding in preterm infants: A randomized clinical trial Manon Bache a,⁎, Emmanuelle Pizon b, Julien Jacobs c, Michel Vaillant d, Aline Lecomte e a
Neonatal Intensive Care Unit, Centre Hospitalier de Luxembourg, 4 rue Ernest Barblé, 1210 Luxembourg Service d'Évaluation et de Rééducation Fonctionnelle, Centre Hospitalier de Luxembourg, 4 rue Ernest Barblé, 1210 Luxembourg CRP-Santé, Administration and Center for Health Studies, 1A-B, rue Thomas Edison, L-1445 Strassen, Luxembourg d CRP-Santé, Competences Center for Methodology and Statistics, 1A-B, rue Thomas Edison, L-1445 Strassen, Luxembourg e Centre de Recherche Public de la Santé, CRP-Santé, Administration and Center for Health Studies, 1A-B, rue Thomas Edison, L-1445 Strassen, Luxembourg b c
a r t i c l e
i n f o
Article history: Received 24 June 2013 Received in revised form 23 December 2013 Accepted 31 December 2013 Available online xxxx Keywords: Pre-feeding oral stimulation Preterm infants Breastfeeding Oral feeding
a b s t r a c t Objective: To evaluate the effect of early oral stimulation before the introduction of oral feeding, over the duration of concomitant tube feeding (“transition period”), the length of hospital stay and the breastfeeding rates upon discharge in preterm infants. Study design: Preterm infants born between 26 and 33 weeks gestational age (n = 86), were randomized into an intervention and control group. Infants in the intervention group received an oral stimulation program consisting in stimulation of the oral structures for 15 min at least for 10 days, before introduction of oral feeding. Oral feeding was introduced at 34 weeks GA in both groups. Results: Breastfeeding rates upon discharge were significantly higher in the intervention than in the control group (70% versus 45.6%, p = 0.02). There was no statistical difference between the two groups in terms of the length of the transition period or the length of the hospital stay. The need for prolonged CPAP support (HR = 0.937, p = 0.030) and small size for gestational age at birth (HR = 0.338, p = 0.016) were shown to be risk factors for a prolonged transition period. Conclusion: A pre-feeding oral stimulation program improves breastfeeding rates in preterm infants. The study results suggest that oral stimulation, as used in our specific population, does not shorten the transition period to full oral feeding neither the length of hospital stay. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Oral feeding problems in preterm infants are of growing concern for society: cases of breast-feeding failures often result in delayed hospital discharge, maternal stress and long-term health problems. Sucking and swallowing are present in early foetal life but the coordination of sucking and swallowing and breathing and swallowing is thought not to occur before 32 and 33–34 weeks gestational age (GA) respectively. Even if the coordination of suck–swallow–breathe is not necessary to begin oral feeding, effective and safe oral feeding requires the adequate coordination of sucking, swallowing and respiration so as to avoid aspiration, apnea, bradycardia and oxygen desaturations., [1,10,11,13,20]. At present, in the absence of specific contraindications, oral feeding is commonly introduced at around 33 to 34 weeks GA. Usually, there exists a transition period of combined gavage and oral feeding which lasts days or weeks.
⁎ Corresponding author. E-mail address: [email protected] (M. Bache).
Accelerated maturation of the sucking reflex and earlier readiness for bottle-feeding are reported when preterm neonates are presented with non-nutritive sucking (NNS) opportunities during gavage feeding [4]. Recent evidence points to the fact that the sensory consequences associated with the production of NNS have beneficial effects on oral feeding performance and on the development of specific sucking skills [3,6,15,17,18]. Recent studies have suggested that an oral stimulation program combined with NNS applied to preterm infants for at least 10 days in the period of full gavage feeding can facilitate their oral feeding progress, improve breastfeeding rates among preterm infants and decrease the length of hospital stay, while no particular negative outcomes have been reported in the said studies [2,7–9,16,17,19]. In the present situation of our neonatal intensive care unit (NICU), as in the large majority of NICUs, preterm infants never receive oral stimulation before the introduction of oral feeding. Difficulties in the transition from tube to independent oral feeding are frequently observed, even for infants born after 32 weeks GA. The objective of this study was to evaluate the effect of an oral stimulation program on the length of the transition period in preterm
0378-3782/$ – see front matter © 2014 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.earlhumdev.2013.12.011
Please cite this article as: Bache M, et al, Effects of pre-feeding oral stimulation on oral feeding in preterm infants: A randomized clinical trial, Early Hum Dev (2014), http://dx.doi.org/10.1016/j.earlhumdev.2013.12.011
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M. Bache et al. / Early Human Development xxx (2014) xxx–xxx
infants (primary outcome), on the length of hospital stays and on breastfeeding rates upon discharge (secondary outcomes). 2. Methods In a prospective randomized controlled clinical trial, the effect of pre-feeding oral stimulation on the achievement of full oral nutrition within 15 days from offering oral feeding was investigated. For an expected full-oral-feeding success rate of 95% in the intervention group versus 70% in controls, the minimal sample size needed to allow the detection of a difference between the two groups was 37 patients in each group, with a power of 80% and an alpha level of 5%. A total of 101 preterm infants from the neonatal intensive care unit of the Children's Hospital of the Centre Hospitalier de Luxembourg, Luxembourg, were included, from July 2011 to November 2012. Infants were declared eligible for enrolment if they were born between 26 and 33 weeks GA, as determined by clinical examination and first-trimester ultrasound. Infants were excluded from the study if they presented congenital malformations, severe asphyxia, presence of third- or fourth-degree intracranial haemorrhage, severe periventricular leukomalacia, chronic lung disease, if they suffered from a hospital infection, a necrotising enterocolitis, if they were transferred to another hospital before discharge or died during hospitalisation. The randomized classification of the subjects into an experimental and a control group was performed when they reached 32 weeks GA in the case of infants born within 32 weeks, and at birth in the case of infants born after 32 weeks gestational age. The process was performed using sequential numbers kept in sealed, opaque, non-translucid envelopes. Randomization was stratified based on gestational age ranges (26–27, 28–29, 30–31, 32–33) to ensure a similar gestational age distribution in the two groups. Infants in the interventional group received pre-feeding oral stimulation whereas those in the control group received neither oral stimulation nor a pacifier before or during gavage feeding. The intervention started on infants born within 32 gestational weeks when the patients were stable and tube-fed, receiving more than 100 ml/kg/day of milk. On infants born after 32 weeks, the intervention started immediately after clinical stability was achieved. Respiratory support, either by nasal continuous positive airway pressure (CPAP) or high-flow oxygen therapy (HFT), did not represent an exclusion criterion. The pre-feeding oral stimulation program consisted of a 15-min stimulation program delivered by one of the eight trained nurses or one trained member from the medical staff in accordance with the stimulation program proposed by Fucile, Gisel and Lau [8]. Administrators were trained to deliver the stimulation program to the patients, by a member from the paediatric physical therapies medical staff, before the beginning of the study. A written protocol and an illustrative video of the stimulation program were available at any moment to the participant staff. Regular controls of the protocol administration were performed to assure reliability of the administrators. The stimulation program was administered 15 to 30 min prior to tube feeding, once daily for at least 10 days. The program was stopped when the infants attained more than three oral feedings per day. The program was interrupted if the infants were medically unstable and/or had episodes of desaturation, apnoea and/or bradycardia during the intervention. Tube feeding was initiated when the preterm infants were clinically stable in terms of hemodynamics and had peristalsis according to criteria established by the caretaker staff. Enteral diet progress depended on infants' tolerance and was about 20 ml/kg/day. The change from gavage to oral feeding was initiated at 34 weeks GA, subsequent to the beginning of the oral stimulation program in the intervention group, by breast- or bottle-feeding according to the wishes expressed by the parents. A strict protocol for oral feeding advance in the two groups was defined: on the first day (34 week GA),
one oral feeding dose of five millilitres or one breastfeeding opportunity was given to the infant. If the infant ingested the 5 millilitres in less than 10 min, the dose was doubled on the next day to five millilitres twice a day (or two breastfeeding opportunities). If the infant did not ingest the prescribed volume, the same number of oral feedings was proposed until the entire quantity could be ingested orally. If an infant managed to drink three times five millilitres a day, all the feedings were proposed by bottle and/or breast to this infant on the next day. The remaining quantity of milk was administered by gavage feeding. All the nurses from the NICU, including study participant nurses, were responsible for feeding infants. Full oral feeding was defined as an oral intake of milk ≥150 ml/kg/day, for 3 consecutive days. Breastfeeding in our study was defined as exclusive or partial breastfeeding. Preterm infants on a mixed breast- and bottle-feeding regime were considered as breastfed, because they received the benefits of human milk and of the strong mother-to-child relationship that develops during breastfeeding. To define discharge criteria for patients participating in the study, we used the same criteria as for all preterm infants in our unit: weight N 2000 g, feeding autonomy for more than 3 consecutive days with appropriate weight gain and respiratory autonomy controlled by polysomnography before discharge. The member of the medical staff deciding on infants' discharge was not blinded to group assignment. 2.1. Statistical analysis The time for transition (in days) from full gavage to full oral feeding, from the beginning of oral feeding to full oral feeding, the length of the hospital stay and the breastfeeding rate (in percents) were calculated and compared between the two groups. The Student's t-test and chisquare test (or Fisher's exact test as appropriate) were used, for continuous and categorical variables respectively. The Kaplan–Meier survival technique was applied to the time of transition and the length of the hospital stay. Survival curves were compared using the Wilcoxon test. A Cox proportional hazard model was further used to assess the influence of risk factors such as gestational age ranges, birth weight, respiratory distress syndrome and prolonged intubation periods or the need for prolonged nasal-CPAP therapy, on the relationship between the groups and the time of transition or the length of the hospital stay. Analysis was planned in intention to treat. All tests were two-tailed and results with p-value below 0.05 were considered statistically significant. SAS System version 9.2 was used for statistical analyses. The study was approved by the national research ethics committee and by the neonatal unit where it was performed. Prior free and informed consent were obtained from the parents/guardians of the newborns for their participation in the study. 3. Results Over the whole course of the study, 116 preterm infants with gestational age between 26 and 33 weeks were admitted to the neonatal unit. 101 infants were included in the study protocol. Fifteen infants were excluded: eight presented exclusion criteria and seven had less than 10 stimulation sessions. 86 patients were finally analyzed (40 in the intervention group and 46 in the control group) (see Fig. 1). Preterm infants in the intervention and in the control groups did not differ statistically in terms of demographic or medical characteristics (see Table 1). The 40 infants in the intervention group received 10 or more prefeeding stimulation sessions, with an average of 13 sessions [10–14]. The reasons for the cancelled sessions were mainly transitory medical instability or work overload in the neonatal unit. Three infants had interrupted sessions because of medical instability. 52.5% of the patients in the intervention group versus 45.6% in the control group needed CPAP support between 32 and 34 weeks GA
Please cite this article as: Bache M, et al, Effects of pre-feeding oral stimulation on oral feeding in preterm infants: A randomized clinical trial, Early Hum Dev (2014), http://dx.doi.org/10.1016/j.earlhumdev.2013.12.011
M. Bache et al. / Early Human Development xxx (2014) xxx–xxx
Enrollment
3
Assessed for eligibility (n= 116)
Excluded (n= 15) Not meeting inclusion criteria* (n= 8) Declined to participate (n= 3) Other reasons (n= 4)
Randomized (n= 101)
Allocation Allocated to intervention (n= 54) Received allocated intervention (n= 47)
Allocated to control group (n= 47) Excluded*** (n= 1)
Excluded** (n= 7)
Follow-up Lost to follow-up (n= 0)
Lost to follow-up (n= 0)
Analysis Analysed (n= 40) Excluded from analysis (less than 10 stimulation sessions) (n= 7)
Analysed (n= 46)
* 4 severe chronic lung diseases (CLD), 2 fourth degree intracranial hemorrhages, 1 necrotizing enterocolitis (NEC), 1 congenital malformation ** 1 NEC, 1 severe CLD, 1 sepsis, 4 transfers *** 1 transfer
Fig. 1. Flow diagram (CONSORT 2010).
(p = 0.526). 35% whereas 21.7% needed high-flow oxygen therapy during this period (p = 0.172). In these patients, the pre-feeding stimulation was performed during a 15-min CPAP or HFT interruption,
Table 1 Neonatal characteristics.
Gestation age at birth (weeks) Gestation age distribution 26–29 + 6 GA 30–31 + 6 GA 32–33 + 6 GA Birth weight (g) Apgar score 5 min Sex Male Female Inborn Parity ≥1 SGA RDS Intubation Duration of intubation (h) CPAP Duration of CPAP (h) High flow oxygen Duration of HFT (h) Previous breastfeeding
Intervention group (n = 40)
Control group (n = 46)
p
31.4 ± 1.5
31.3 ± 1.7
0.812
7 (17.5) 14 (35.0) 19 (47.5) 1560.0 ± 403.1 8.2 ± 1.2
9 (19.6) 13 (28.3) 24 (52.2) 1582.0 ± 350.7 8.3 ± 1.1
0.798
25 (62.5) 15 (37.5) 34 (85.0) 21 (52.5) 10 (25.0) 20 (50.0) 7 (17.5) 5.1 ± 18.5 30 (75.0) 123.3 ± 195.0 16 (40.0) 70.7 ± 128.4 17 (42.5)
25 (54.4) 21 (45.6) 39 (84.8) 25 (54.4) 7 (15.2) 19 (41.3) 13 (28.3) 5.0 ± 15.8 36 (78.3) 135.8 ± 225.1 18 (39.1) 49.6 ± 117.6 19 (41.3)
0.445
Results are presented as means ± SD, or frequencies (percentages).
0.788 0.543
0.978 0.864 0.256 0.419 0.239 0.272 0.721 0.658 0.934 0.642 0.911
without any respiratory support if tolerated or with high-flow oxygen nasal cannula if necessary. Gestational age, days of life and weight at introduction of oral feeding and at full oral feeding were not statistically different between the two groups. The intervention group did not differ from the control group in terms of duration between full gavage diet and full oral feeding, duration between introduction of oral feeding and full oral feeding (“transition period”), or in length of hospital stay (see Table 2). The breastfeeding rate in the intervention group was significantly higher than in the control group (see Table 2). Breastfeeding included exclusively breastfeeding (10 infants in the stimulated group versus seven infants in the control group), partial breastfeeding completed with mother's milk by bottle (15 versus 8 infants) or partial breastfeeding completed with formula milk (three versus six infants). Four patients in the intervention group and seven in the control group were fed mother's milk given by bottle-feeding only. These patients were not considered as breastfed for the purpose of the statistical analysis. The remaining number of infants did only receive formula milk by bottle (8 versus 18 infants). The Cox proportional hazard model showed no difference between the two groups in terms of length of transition period (HR = 0.875, p = 0.558). Differences were found for gestational age, infants born SGA and CPAP duration (see Table 3). Infants born SGA statistically presented prolonged transition periods from the beginning of oral feeding to full oral feeding (HR = 0.338, p = 0.016) and an increased duration by 1 day of CPAP support extended the transition period (HR = 0.937, p = 0.030).
Please cite this article as: Bache M, et al, Effects of pre-feeding oral stimulation on oral feeding in preterm infants: A randomized clinical trial, Early Hum Dev (2014), http://dx.doi.org/10.1016/j.earlhumdev.2013.12.011
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M. Bache et al. / Early Human Development xxx (2014) xxx–xxx
Table 2 Results of study variables for the two groups.
Weight at introduction to oral feeding (g) Gestation age at introduction to oral feeding (weeks) Days of life at introduction to oral feeding (days) Weight at full oral feeding (g) Gestation age at full oral feeding (weeks) Days of life at full oral feeding (days) Duration between full gavage diet and full oral feeding (days) Duration between introduction to oral feeding and 1 oral feeding (days) Duration between introduction to oral feeding and 3 oral feeding (days) Duration between introduction to oral feeding and full oral feeding (days) Length of hospital stay (days) Partial and/or full breastfeeding at discharge
Intervention group (n = 40)
Control group (n = 46)
p
1886.3 ± 324.3 34.0 ± 0.1 18.5 ± 10.8 2386.3 ± 311.2 36.4 ± 1.3 35.3 ± 14.5 25.5 ± 12.5 1.8 ± 2.9 4.6 ± 3.9 16.9 ± 9.2 45.7 ± 16.8 28 (70.0)
1884.8 ± 288.1 34.0 ± 0.1 19.1 ± 12.2 2354.6 ± 253.3 36.3 ± 1.0 35.1 ± 13.8 24.9 ± 12.0 1.7 ± 2.7 4.9 ± 3.5 16.0 ± 6.9 42.5 ± 15.1 21 (45.6)
0.982 0.714 0.806 0.604 0.709 0.938 0.846 0.897 0.737 0.625 0.358 0.023
Results are presented as means ± SD, or frequencies (percentages).
4. Discussion The results of the present study show that oral pre-feeding stimulation can increase the breastfeeding rate in preterm infants born between 26 and 33 weeks GA. The development of the sucking ability on the mother's breast may be enhanced by oral stimulation, which appears to account for why a greater number of infants in the intervention group could be fed by breast upon discharge. However, breastfeeding in a neonatal unit not only requires the ability for the preterm infant to suck on the mother's breast, but also several factors involving the mother. Therefore, a second explanation for these results lies in that mothers in the intervention group showed higher motivation to breastfeed their babies. On seeing their babies receive the oral stimulation for several days and progress in their sucking behaviour over time, they became aware of their competences. This type of positive experience can reassure worried or exhausted mothers and instil in them renewed courage to continue breastfeeding, which is often complicated and frustrating during the hospitalization of a preterm infant. In our study, the stimulation program did not lead to a decreased length of the hospital stay or to an acceleration of the transition from gavage feeding to full oral feeding. These findings differ from those of other studies for several reasons [8,9,14,19]. In most of the other studies, preterm infants were only fed by bottle during the transition period [8,9,14]. The higher rate of breastfeeding at discharge in our intervention group seems to indicate that more infants in that group were introduced to oral feeding directly on their mother's breast. Nipple feeding is easier to manage for a preterm infant than sucking on the breast, which requires more physical effort. Given the higher breastfeeding rate in the intervention group, we came to the conclusion that the transition period in this group was not shorter than in
Table 3 Risk factors associated with a prolonged transition period (proportional Cox hazard model). Hazard ratio Stimulation GA
Birth weight (g) SGA RDS Intubation (days) CPAP (days) HTF (days)
No Yes 26–29 + 6 30–31 + 6 32–33 + 6 No Yes No Yes
1 0.875 2.657 2.345 1 1.001 1 0.338 1 0.612 0.940 0.937 1.022
95% CL
p value
0.560 0.976 1.278
1.367 7.232 4.306
0.558 0.056 0.006
0.999
1.002
0.327
0.141
0.815
0.016
0.355 0.648 0.884 0.962
1.054 1.364 0.994 1.086
0.077 0.745 0.030 0.483
Hazard ratios greater than one indicate lowered transition periods.
the control group, as breastfeeding takes more time to learn than bottle-feeding in preterm infants. A second possible explanation for this result is that our protocol included an oral feeding progression protocol. Oral feeding initiation and progression were not left to the discretion of the attending physician, but followed a strict protocol in both groups. As demonstrated by Pickler et al. [15], a protocol for advancing oral feeding, on the success of the previous feedings, leads to an earlier full oral diet by the development of the sucking ability through feeding opportunities. Our feeding progression program could possibly have understated the effect of the oral stimulation program. We started the intervention on infants characterized as medically stable, even if they still needed respiratory support (CPAP or HFT). In that case, the stimulation was administered during a short CPAP or HFT pause, provided that it was tolerated. For patients under CPAP not tolerating room air without support, HFT nasal cannulas were used during the intervention without disturbing the feasibility of the stimulation movements. A major difference lies between our protocol and those of other studies. The patients in our study, still needing respiratory support between 32 and 34 weeks GA, probably presented higher severity of illness than patients without support in the other studies [8,9,14,16,19]. Even though this is not statistically different, more infants in the intervention group needed CPAP and/or HFT between 32 and 34 weeks GA. This can be one of the reasons why the stimulation program did not show positive effects on transition period and length of stay. Respiratory support can cause sensory deprivation and motor restriction during a critical period of brain development for sucking patterns, by means of tubes, cannulas and tapes placed on the infants' face, and is accountable for a prolonged transition period to oral feeding due to delays in the achievement of feeding milestones [5,12,20]. This is underscored by the results from our Cox proportional hazard regression model, which showed that prolonged CPAP support is a risk factor for an increased length of the transition period. Even if the stimulation program was feasible in the case of infants with nasal cannulas, the fact of being under CPAP or HFT for several hours a day during the intervention period, could have decreased or cancelled the positive effect of this stimulation program, by causing a persistent negative oral experience. In future research, for this type of patients, the length of the oral stimulation period should be considered prolonged after the discontinuation of respiratory support to show a positive effect. Our study presented some methodological limitations. The prefeeding oral stimulation was not systematically administered by the same member of staff. Eight nurses and one member of the medical staff were trained prior to the beginning of the study to administer the stimulation program. Therefore, differences in the administration of the stimulation program cannot be excluded, thereby presenting a potential bias in this study. In addition, the number of pre-feeding
Please cite this article as: Bache M, et al, Effects of pre-feeding oral stimulation on oral feeding in preterm infants: A randomized clinical trial, Early Hum Dev (2014), http://dx.doi.org/10.1016/j.earlhumdev.2013.12.011
M. Bache et al. / Early Human Development xxx (2014) xxx–xxx
stimulation sessions was not exactly the same for all the patients in the intervention group. We hypothesized, as other authors in the literature, that 10 oral stimulation sessions are necessary to have an impact on the oral feeding performance of our patients [8,9,16,19]. To avoid the bias of understating the effect of the oral stimulation in infants with less than 10 stimulation sessions, we chose to not include these patients in the statistical analysis. The blinding of the study proved impossible due to the organization of our relatively small neonatal unit. This constitutes another possible bias in that the same people administered the stimulation program and were responsible for feeding the patients. However, the oral stimulation program proves a positive experience for preterm infants, parents and nurses, without notable negative side effects detected in our or other studies [11]. The stimulation program provided an increased opportunity for caretakers to interact with their patients in a positive and meaningful manner, which considerably differs from their usual tasks often considered very technical and potentially painful for these fragile patients. The program was generally appreciated by participating nurses, patients and parents. Training parents to perform the oral stimulation themselves appears as a real possibility for the future. Parents providing oral stimulation would thus enhance parent–infant interaction and receive the opportunity to participate in the care of their preterm infant, altogether with a positive effect on their development. In conclusion, the present study shows that a pre-feeding oral stimulation program can contribute to the improvement of the breastfeeding rates in preterm infants, even without accelerating the transition period and decreasing the length of the hospital stay. This stimulation program should be considered for all preterm infants with a view of promoting breastfeeding for these fragile patients. Conflict of interest The authors declare no conflict of interest. Acknowledgments The authors would like to thank all the nurses who participated in the study at the Centre Hospitalier de Luxembourg. This study was supported by the Société Luxembourgeoise de Recherche en Pédiatrie (SOLUREP) and the perinatal health monitoring system, implemented at the CRP-Santé, Luxembourg.
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References [1] Amaizu N, Shulman R, Schanler R, Lau C. Maturation of oral feeding skills in preterm infants. Acta Paediatr 2008;97:61–7. [2] Arvedson J, Clark H, Lazarus C, Schooling T, Frymark T. Evidence-based systematic review: effects of oral motor interventions on feeding and swallowing in preterm infants. Am J Speech Lang Pathol 2010;19:321–40. [3] Barlow SM, Finan DS, Lee J, Chu S. Synthetic orocutaneous stimulation entrains preterm infants with feeding difficulties to suck. J Perinatol 2008;28:541–8. [4] Bernbaum JC, Pereira GR, Watkins JB, Peckham GJ. Nonnutritive sucking during gavage feeding enhances growth and maturation in premature infants. Pediatrics Jan 1983;71(1):41–5. [5] Bier JA, Ferguson A, Cho C, Oh W, Vohr BR. The oral motor development of lowbirth-weight infants who underwent orotracheal intubation during the neonatal period. Am J Dis Child Aug 1993;147(8):858–62. [6] 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: F194–200. [7] 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;49:439–44. [8] Fucile S, Gisel E, Lau C. Oral stimulation accelerates the transition from tube to oral feeding in preterm infants. J Pediatr 2002;141:230–6. [9] Fucile S, Gisel EG, Lau C. Effect of an oral stimulation program on sucking skill maturation of preterm infants. Dev Med Child Neurol 2005;47:158–62. [10] 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 Jan 2001;43(1):22–7. [11] Gewolb IH, Vice FL. Maturational changes in the rhythms, patterning, and coordination of respiration and swallow during feeding in preterm and term infants. Dev Med Child Neurol Jul 2006;48(7):589–94. [12] Jadcherla SR, Wang M, Vijayapal AS, Leuthner SR. Impact of prematurity and co-morbidities on feeding milestones in neonates: a retrospective study. J Perinatol Mar 2010;30(3):201–8. [13] Lau C. Oral feeding in the preterm infant. NeoReviews 2006;7:e19–27. [14] Lessen BS. Effect of the premature infant oral motor intervention on feeding progression and length of stay in preterm infants. Adv Neonatal Care Apr 2011;11(2):129–39. [15] Pickler RH, Reyna BA. Effects of non-nutritive sucking on nutritive sucking, breathing, and behavior during bottle feedings of preterm infants. Adv Neonatal Care 2004;4:226–34. [16] Pimenta HP, Moreira ME, Rocha AD, Gomes Jr SC, 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;84:423–7. [17] Pinelli J, Symington A. Non-nutritive sucking for promoting physiologic stability and nutrition in preterm infants. Cochrane Libr 2010(6). [18] Poore M, Zimmerman E, Barlow SM, Wang J, Gu F. Patterned orocutaneous therapy improves sucking and oral feeding in preterm infants. Acta Paediatr 2008;97:920–7. [19] Rocha AD, Moreira ME, Pimenta HP, Ramos JR, Lucena SL. A randomized study of the efficacy of sensory-motor-oral stimulation and non-nutritive sucking in very low birthweight infant. Early Hum Dev 2007;83:385–8. [20] Stumm S, Barlow SM, Estep M, Lee J, Cannon S, Carlson J, Finan D. Respiratory distress syndrome degrades the fine structure of the non-nutritive suck in preterm infants. J Neonatal Nurs 2008;14:9–16.
Please cite this article as: Bache M, et al, Effects of pre-feeding oral stimulation on oral feeding in preterm infants: A randomized clinical trial, Early Hum Dev (2014), http://dx.doi.org/10.1016/j.earlhumdev.2013.12.011
Contents lists available at ScienceDirect
Early Human Development journal homepage: www.elsevier.com/locate/earlhumdev
Effects of pre-feeding oral stimulation on oral feeding in preterm infants: A randomized clinical trial Manon Bache a,⁎, Emmanuelle Pizon b, Julien Jacobs c, Michel Vaillant d, Aline Lecomte e a
Neonatal Intensive Care Unit, Centre Hospitalier de Luxembourg, 4 rue Ernest Barblé, 1210 Luxembourg Service d'Évaluation et de Rééducation Fonctionnelle, Centre Hospitalier de Luxembourg, 4 rue Ernest Barblé, 1210 Luxembourg CRP-Santé, Administration and Center for Health Studies, 1A-B, rue Thomas Edison, L-1445 Strassen, Luxembourg d CRP-Santé, Competences Center for Methodology and Statistics, 1A-B, rue Thomas Edison, L-1445 Strassen, Luxembourg e Centre de Recherche Public de la Santé, CRP-Santé, Administration and Center for Health Studies, 1A-B, rue Thomas Edison, L-1445 Strassen, Luxembourg b c
a r t i c l e
i n f o
Article history: Received 24 June 2013 Received in revised form 23 December 2013 Accepted 31 December 2013 Available online xxxx Keywords: Pre-feeding oral stimulation Preterm infants Breastfeeding Oral feeding
a b s t r a c t Objective: To evaluate the effect of early oral stimulation before the introduction of oral feeding, over the duration of concomitant tube feeding (“transition period”), the length of hospital stay and the breastfeeding rates upon discharge in preterm infants. Study design: Preterm infants born between 26 and 33 weeks gestational age (n = 86), were randomized into an intervention and control group. Infants in the intervention group received an oral stimulation program consisting in stimulation of the oral structures for 15 min at least for 10 days, before introduction of oral feeding. Oral feeding was introduced at 34 weeks GA in both groups. Results: Breastfeeding rates upon discharge were significantly higher in the intervention than in the control group (70% versus 45.6%, p = 0.02). There was no statistical difference between the two groups in terms of the length of the transition period or the length of the hospital stay. The need for prolonged CPAP support (HR = 0.937, p = 0.030) and small size for gestational age at birth (HR = 0.338, p = 0.016) were shown to be risk factors for a prolonged transition period. Conclusion: A pre-feeding oral stimulation program improves breastfeeding rates in preterm infants. The study results suggest that oral stimulation, as used in our specific population, does not shorten the transition period to full oral feeding neither the length of hospital stay. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Oral feeding problems in preterm infants are of growing concern for society: cases of breast-feeding failures often result in delayed hospital discharge, maternal stress and long-term health problems. Sucking and swallowing are present in early foetal life but the coordination of sucking and swallowing and breathing and swallowing is thought not to occur before 32 and 33–34 weeks gestational age (GA) respectively. Even if the coordination of suck–swallow–breathe is not necessary to begin oral feeding, effective and safe oral feeding requires the adequate coordination of sucking, swallowing and respiration so as to avoid aspiration, apnea, bradycardia and oxygen desaturations., [1,10,11,13,20]. At present, in the absence of specific contraindications, oral feeding is commonly introduced at around 33 to 34 weeks GA. Usually, there exists a transition period of combined gavage and oral feeding which lasts days or weeks.
⁎ Corresponding author. E-mail address: [email protected] (M. Bache).
Accelerated maturation of the sucking reflex and earlier readiness for bottle-feeding are reported when preterm neonates are presented with non-nutritive sucking (NNS) opportunities during gavage feeding [4]. Recent evidence points to the fact that the sensory consequences associated with the production of NNS have beneficial effects on oral feeding performance and on the development of specific sucking skills [3,6,15,17,18]. Recent studies have suggested that an oral stimulation program combined with NNS applied to preterm infants for at least 10 days in the period of full gavage feeding can facilitate their oral feeding progress, improve breastfeeding rates among preterm infants and decrease the length of hospital stay, while no particular negative outcomes have been reported in the said studies [2,7–9,16,17,19]. In the present situation of our neonatal intensive care unit (NICU), as in the large majority of NICUs, preterm infants never receive oral stimulation before the introduction of oral feeding. Difficulties in the transition from tube to independent oral feeding are frequently observed, even for infants born after 32 weeks GA. The objective of this study was to evaluate the effect of an oral stimulation program on the length of the transition period in preterm
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Please cite this article as: Bache M, et al, Effects of pre-feeding oral stimulation on oral feeding in preterm infants: A randomized clinical trial, Early Hum Dev (2014), http://dx.doi.org/10.1016/j.earlhumdev.2013.12.011
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M. Bache et al. / Early Human Development xxx (2014) xxx–xxx
infants (primary outcome), on the length of hospital stays and on breastfeeding rates upon discharge (secondary outcomes). 2. Methods In a prospective randomized controlled clinical trial, the effect of pre-feeding oral stimulation on the achievement of full oral nutrition within 15 days from offering oral feeding was investigated. For an expected full-oral-feeding success rate of 95% in the intervention group versus 70% in controls, the minimal sample size needed to allow the detection of a difference between the two groups was 37 patients in each group, with a power of 80% and an alpha level of 5%. A total of 101 preterm infants from the neonatal intensive care unit of the Children's Hospital of the Centre Hospitalier de Luxembourg, Luxembourg, were included, from July 2011 to November 2012. Infants were declared eligible for enrolment if they were born between 26 and 33 weeks GA, as determined by clinical examination and first-trimester ultrasound. Infants were excluded from the study if they presented congenital malformations, severe asphyxia, presence of third- or fourth-degree intracranial haemorrhage, severe periventricular leukomalacia, chronic lung disease, if they suffered from a hospital infection, a necrotising enterocolitis, if they were transferred to another hospital before discharge or died during hospitalisation. The randomized classification of the subjects into an experimental and a control group was performed when they reached 32 weeks GA in the case of infants born within 32 weeks, and at birth in the case of infants born after 32 weeks gestational age. The process was performed using sequential numbers kept in sealed, opaque, non-translucid envelopes. Randomization was stratified based on gestational age ranges (26–27, 28–29, 30–31, 32–33) to ensure a similar gestational age distribution in the two groups. Infants in the interventional group received pre-feeding oral stimulation whereas those in the control group received neither oral stimulation nor a pacifier before or during gavage feeding. The intervention started on infants born within 32 gestational weeks when the patients were stable and tube-fed, receiving more than 100 ml/kg/day of milk. On infants born after 32 weeks, the intervention started immediately after clinical stability was achieved. Respiratory support, either by nasal continuous positive airway pressure (CPAP) or high-flow oxygen therapy (HFT), did not represent an exclusion criterion. The pre-feeding oral stimulation program consisted of a 15-min stimulation program delivered by one of the eight trained nurses or one trained member from the medical staff in accordance with the stimulation program proposed by Fucile, Gisel and Lau [8]. Administrators were trained to deliver the stimulation program to the patients, by a member from the paediatric physical therapies medical staff, before the beginning of the study. A written protocol and an illustrative video of the stimulation program were available at any moment to the participant staff. Regular controls of the protocol administration were performed to assure reliability of the administrators. The stimulation program was administered 15 to 30 min prior to tube feeding, once daily for at least 10 days. The program was stopped when the infants attained more than three oral feedings per day. The program was interrupted if the infants were medically unstable and/or had episodes of desaturation, apnoea and/or bradycardia during the intervention. Tube feeding was initiated when the preterm infants were clinically stable in terms of hemodynamics and had peristalsis according to criteria established by the caretaker staff. Enteral diet progress depended on infants' tolerance and was about 20 ml/kg/day. The change from gavage to oral feeding was initiated at 34 weeks GA, subsequent to the beginning of the oral stimulation program in the intervention group, by breast- or bottle-feeding according to the wishes expressed by the parents. A strict protocol for oral feeding advance in the two groups was defined: on the first day (34 week GA),
one oral feeding dose of five millilitres or one breastfeeding opportunity was given to the infant. If the infant ingested the 5 millilitres in less than 10 min, the dose was doubled on the next day to five millilitres twice a day (or two breastfeeding opportunities). If the infant did not ingest the prescribed volume, the same number of oral feedings was proposed until the entire quantity could be ingested orally. If an infant managed to drink three times five millilitres a day, all the feedings were proposed by bottle and/or breast to this infant on the next day. The remaining quantity of milk was administered by gavage feeding. All the nurses from the NICU, including study participant nurses, were responsible for feeding infants. Full oral feeding was defined as an oral intake of milk ≥150 ml/kg/day, for 3 consecutive days. Breastfeeding in our study was defined as exclusive or partial breastfeeding. Preterm infants on a mixed breast- and bottle-feeding regime were considered as breastfed, because they received the benefits of human milk and of the strong mother-to-child relationship that develops during breastfeeding. To define discharge criteria for patients participating in the study, we used the same criteria as for all preterm infants in our unit: weight N 2000 g, feeding autonomy for more than 3 consecutive days with appropriate weight gain and respiratory autonomy controlled by polysomnography before discharge. The member of the medical staff deciding on infants' discharge was not blinded to group assignment. 2.1. Statistical analysis The time for transition (in days) from full gavage to full oral feeding, from the beginning of oral feeding to full oral feeding, the length of the hospital stay and the breastfeeding rate (in percents) were calculated and compared between the two groups. The Student's t-test and chisquare test (or Fisher's exact test as appropriate) were used, for continuous and categorical variables respectively. The Kaplan–Meier survival technique was applied to the time of transition and the length of the hospital stay. Survival curves were compared using the Wilcoxon test. A Cox proportional hazard model was further used to assess the influence of risk factors such as gestational age ranges, birth weight, respiratory distress syndrome and prolonged intubation periods or the need for prolonged nasal-CPAP therapy, on the relationship between the groups and the time of transition or the length of the hospital stay. Analysis was planned in intention to treat. All tests were two-tailed and results with p-value below 0.05 were considered statistically significant. SAS System version 9.2 was used for statistical analyses. The study was approved by the national research ethics committee and by the neonatal unit where it was performed. Prior free and informed consent were obtained from the parents/guardians of the newborns for their participation in the study. 3. Results Over the whole course of the study, 116 preterm infants with gestational age between 26 and 33 weeks were admitted to the neonatal unit. 101 infants were included in the study protocol. Fifteen infants were excluded: eight presented exclusion criteria and seven had less than 10 stimulation sessions. 86 patients were finally analyzed (40 in the intervention group and 46 in the control group) (see Fig. 1). Preterm infants in the intervention and in the control groups did not differ statistically in terms of demographic or medical characteristics (see Table 1). The 40 infants in the intervention group received 10 or more prefeeding stimulation sessions, with an average of 13 sessions [10–14]. The reasons for the cancelled sessions were mainly transitory medical instability or work overload in the neonatal unit. Three infants had interrupted sessions because of medical instability. 52.5% of the patients in the intervention group versus 45.6% in the control group needed CPAP support between 32 and 34 weeks GA
Please cite this article as: Bache M, et al, Effects of pre-feeding oral stimulation on oral feeding in preterm infants: A randomized clinical trial, Early Hum Dev (2014), http://dx.doi.org/10.1016/j.earlhumdev.2013.12.011
M. Bache et al. / Early Human Development xxx (2014) xxx–xxx
Enrollment
3
Assessed for eligibility (n= 116)
Excluded (n= 15) Not meeting inclusion criteria* (n= 8) Declined to participate (n= 3) Other reasons (n= 4)
Randomized (n= 101)
Allocation Allocated to intervention (n= 54) Received allocated intervention (n= 47)
Allocated to control group (n= 47) Excluded*** (n= 1)
Excluded** (n= 7)
Follow-up Lost to follow-up (n= 0)
Lost to follow-up (n= 0)
Analysis Analysed (n= 40) Excluded from analysis (less than 10 stimulation sessions) (n= 7)
Analysed (n= 46)
* 4 severe chronic lung diseases (CLD), 2 fourth degree intracranial hemorrhages, 1 necrotizing enterocolitis (NEC), 1 congenital malformation ** 1 NEC, 1 severe CLD, 1 sepsis, 4 transfers *** 1 transfer
Fig. 1. Flow diagram (CONSORT 2010).
(p = 0.526). 35% whereas 21.7% needed high-flow oxygen therapy during this period (p = 0.172). In these patients, the pre-feeding stimulation was performed during a 15-min CPAP or HFT interruption,
Table 1 Neonatal characteristics.
Gestation age at birth (weeks) Gestation age distribution 26–29 + 6 GA 30–31 + 6 GA 32–33 + 6 GA Birth weight (g) Apgar score 5 min Sex Male Female Inborn Parity ≥1 SGA RDS Intubation Duration of intubation (h) CPAP Duration of CPAP (h) High flow oxygen Duration of HFT (h) Previous breastfeeding
Intervention group (n = 40)
Control group (n = 46)
p
31.4 ± 1.5
31.3 ± 1.7
0.812
7 (17.5) 14 (35.0) 19 (47.5) 1560.0 ± 403.1 8.2 ± 1.2
9 (19.6) 13 (28.3) 24 (52.2) 1582.0 ± 350.7 8.3 ± 1.1
0.798
25 (62.5) 15 (37.5) 34 (85.0) 21 (52.5) 10 (25.0) 20 (50.0) 7 (17.5) 5.1 ± 18.5 30 (75.0) 123.3 ± 195.0 16 (40.0) 70.7 ± 128.4 17 (42.5)
25 (54.4) 21 (45.6) 39 (84.8) 25 (54.4) 7 (15.2) 19 (41.3) 13 (28.3) 5.0 ± 15.8 36 (78.3) 135.8 ± 225.1 18 (39.1) 49.6 ± 117.6 19 (41.3)
0.445
Results are presented as means ± SD, or frequencies (percentages).
0.788 0.543
0.978 0.864 0.256 0.419 0.239 0.272 0.721 0.658 0.934 0.642 0.911
without any respiratory support if tolerated or with high-flow oxygen nasal cannula if necessary. Gestational age, days of life and weight at introduction of oral feeding and at full oral feeding were not statistically different between the two groups. The intervention group did not differ from the control group in terms of duration between full gavage diet and full oral feeding, duration between introduction of oral feeding and full oral feeding (“transition period”), or in length of hospital stay (see Table 2). The breastfeeding rate in the intervention group was significantly higher than in the control group (see Table 2). Breastfeeding included exclusively breastfeeding (10 infants in the stimulated group versus seven infants in the control group), partial breastfeeding completed with mother's milk by bottle (15 versus 8 infants) or partial breastfeeding completed with formula milk (three versus six infants). Four patients in the intervention group and seven in the control group were fed mother's milk given by bottle-feeding only. These patients were not considered as breastfed for the purpose of the statistical analysis. The remaining number of infants did only receive formula milk by bottle (8 versus 18 infants). The Cox proportional hazard model showed no difference between the two groups in terms of length of transition period (HR = 0.875, p = 0.558). Differences were found for gestational age, infants born SGA and CPAP duration (see Table 3). Infants born SGA statistically presented prolonged transition periods from the beginning of oral feeding to full oral feeding (HR = 0.338, p = 0.016) and an increased duration by 1 day of CPAP support extended the transition period (HR = 0.937, p = 0.030).
Please cite this article as: Bache M, et al, Effects of pre-feeding oral stimulation on oral feeding in preterm infants: A randomized clinical trial, Early Hum Dev (2014), http://dx.doi.org/10.1016/j.earlhumdev.2013.12.011
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M. Bache et al. / Early Human Development xxx (2014) xxx–xxx
Table 2 Results of study variables for the two groups.
Weight at introduction to oral feeding (g) Gestation age at introduction to oral feeding (weeks) Days of life at introduction to oral feeding (days) Weight at full oral feeding (g) Gestation age at full oral feeding (weeks) Days of life at full oral feeding (days) Duration between full gavage diet and full oral feeding (days) Duration between introduction to oral feeding and 1 oral feeding (days) Duration between introduction to oral feeding and 3 oral feeding (days) Duration between introduction to oral feeding and full oral feeding (days) Length of hospital stay (days) Partial and/or full breastfeeding at discharge
Intervention group (n = 40)
Control group (n = 46)
p
1886.3 ± 324.3 34.0 ± 0.1 18.5 ± 10.8 2386.3 ± 311.2 36.4 ± 1.3 35.3 ± 14.5 25.5 ± 12.5 1.8 ± 2.9 4.6 ± 3.9 16.9 ± 9.2 45.7 ± 16.8 28 (70.0)
1884.8 ± 288.1 34.0 ± 0.1 19.1 ± 12.2 2354.6 ± 253.3 36.3 ± 1.0 35.1 ± 13.8 24.9 ± 12.0 1.7 ± 2.7 4.9 ± 3.5 16.0 ± 6.9 42.5 ± 15.1 21 (45.6)
0.982 0.714 0.806 0.604 0.709 0.938 0.846 0.897 0.737 0.625 0.358 0.023
Results are presented as means ± SD, or frequencies (percentages).
4. Discussion The results of the present study show that oral pre-feeding stimulation can increase the breastfeeding rate in preterm infants born between 26 and 33 weeks GA. The development of the sucking ability on the mother's breast may be enhanced by oral stimulation, which appears to account for why a greater number of infants in the intervention group could be fed by breast upon discharge. However, breastfeeding in a neonatal unit not only requires the ability for the preterm infant to suck on the mother's breast, but also several factors involving the mother. Therefore, a second explanation for these results lies in that mothers in the intervention group showed higher motivation to breastfeed their babies. On seeing their babies receive the oral stimulation for several days and progress in their sucking behaviour over time, they became aware of their competences. This type of positive experience can reassure worried or exhausted mothers and instil in them renewed courage to continue breastfeeding, which is often complicated and frustrating during the hospitalization of a preterm infant. In our study, the stimulation program did not lead to a decreased length of the hospital stay or to an acceleration of the transition from gavage feeding to full oral feeding. These findings differ from those of other studies for several reasons [8,9,14,19]. In most of the other studies, preterm infants were only fed by bottle during the transition period [8,9,14]. The higher rate of breastfeeding at discharge in our intervention group seems to indicate that more infants in that group were introduced to oral feeding directly on their mother's breast. Nipple feeding is easier to manage for a preterm infant than sucking on the breast, which requires more physical effort. Given the higher breastfeeding rate in the intervention group, we came to the conclusion that the transition period in this group was not shorter than in
Table 3 Risk factors associated with a prolonged transition period (proportional Cox hazard model). Hazard ratio Stimulation GA
Birth weight (g) SGA RDS Intubation (days) CPAP (days) HTF (days)
No Yes 26–29 + 6 30–31 + 6 32–33 + 6 No Yes No Yes
1 0.875 2.657 2.345 1 1.001 1 0.338 1 0.612 0.940 0.937 1.022
95% CL
p value
0.560 0.976 1.278
1.367 7.232 4.306
0.558 0.056 0.006
0.999
1.002
0.327
0.141
0.815
0.016
0.355 0.648 0.884 0.962
1.054 1.364 0.994 1.086
0.077 0.745 0.030 0.483
Hazard ratios greater than one indicate lowered transition periods.
the control group, as breastfeeding takes more time to learn than bottle-feeding in preterm infants. A second possible explanation for this result is that our protocol included an oral feeding progression protocol. Oral feeding initiation and progression were not left to the discretion of the attending physician, but followed a strict protocol in both groups. As demonstrated by Pickler et al. [15], a protocol for advancing oral feeding, on the success of the previous feedings, leads to an earlier full oral diet by the development of the sucking ability through feeding opportunities. Our feeding progression program could possibly have understated the effect of the oral stimulation program. We started the intervention on infants characterized as medically stable, even if they still needed respiratory support (CPAP or HFT). In that case, the stimulation was administered during a short CPAP or HFT pause, provided that it was tolerated. For patients under CPAP not tolerating room air without support, HFT nasal cannulas were used during the intervention without disturbing the feasibility of the stimulation movements. A major difference lies between our protocol and those of other studies. The patients in our study, still needing respiratory support between 32 and 34 weeks GA, probably presented higher severity of illness than patients without support in the other studies [8,9,14,16,19]. Even though this is not statistically different, more infants in the intervention group needed CPAP and/or HFT between 32 and 34 weeks GA. This can be one of the reasons why the stimulation program did not show positive effects on transition period and length of stay. Respiratory support can cause sensory deprivation and motor restriction during a critical period of brain development for sucking patterns, by means of tubes, cannulas and tapes placed on the infants' face, and is accountable for a prolonged transition period to oral feeding due to delays in the achievement of feeding milestones [5,12,20]. This is underscored by the results from our Cox proportional hazard regression model, which showed that prolonged CPAP support is a risk factor for an increased length of the transition period. Even if the stimulation program was feasible in the case of infants with nasal cannulas, the fact of being under CPAP or HFT for several hours a day during the intervention period, could have decreased or cancelled the positive effect of this stimulation program, by causing a persistent negative oral experience. In future research, for this type of patients, the length of the oral stimulation period should be considered prolonged after the discontinuation of respiratory support to show a positive effect. Our study presented some methodological limitations. The prefeeding oral stimulation was not systematically administered by the same member of staff. Eight nurses and one member of the medical staff were trained prior to the beginning of the study to administer the stimulation program. Therefore, differences in the administration of the stimulation program cannot be excluded, thereby presenting a potential bias in this study. In addition, the number of pre-feeding
Please cite this article as: Bache M, et al, Effects of pre-feeding oral stimulation on oral feeding in preterm infants: A randomized clinical trial, Early Hum Dev (2014), http://dx.doi.org/10.1016/j.earlhumdev.2013.12.011
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stimulation sessions was not exactly the same for all the patients in the intervention group. We hypothesized, as other authors in the literature, that 10 oral stimulation sessions are necessary to have an impact on the oral feeding performance of our patients [8,9,16,19]. To avoid the bias of understating the effect of the oral stimulation in infants with less than 10 stimulation sessions, we chose to not include these patients in the statistical analysis. The blinding of the study proved impossible due to the organization of our relatively small neonatal unit. This constitutes another possible bias in that the same people administered the stimulation program and were responsible for feeding the patients. However, the oral stimulation program proves a positive experience for preterm infants, parents and nurses, without notable negative side effects detected in our or other studies [11]. The stimulation program provided an increased opportunity for caretakers to interact with their patients in a positive and meaningful manner, which considerably differs from their usual tasks often considered very technical and potentially painful for these fragile patients. The program was generally appreciated by participating nurses, patients and parents. Training parents to perform the oral stimulation themselves appears as a real possibility for the future. Parents providing oral stimulation would thus enhance parent–infant interaction and receive the opportunity to participate in the care of their preterm infant, altogether with a positive effect on their development. In conclusion, the present study shows that a pre-feeding oral stimulation program can contribute to the improvement of the breastfeeding rates in preterm infants, even without accelerating the transition period and decreasing the length of the hospital stay. This stimulation program should be considered for all preterm infants with a view of promoting breastfeeding for these fragile patients. Conflict of interest The authors declare no conflict of interest. Acknowledgments The authors would like to thank all the nurses who participated in the study at the Centre Hospitalier de Luxembourg. This study was supported by the Société Luxembourgeoise de Recherche en Pédiatrie (SOLUREP) and the perinatal health monitoring system, implemented at the CRP-Santé, Luxembourg.
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Please cite this article as: Bache M, et al, Effects of pre-feeding oral stimulation on oral feeding in preterm infants: A randomized clinical trial, Early Hum Dev (2014), http://dx.doi.org/10.1016/j.earlhumdev.2013.12.011
