Effect of an oral stimulation program on sucking skill maturation of preterm infants

Effect of an oral stimulation program on sucking skill maturation of preterm infants

Fucile, S

This study assessed the effect of an oral stimulation program on the maturation of sucking skills of preterm infants. Thirty-two preterm infants (13 males, 19 females), appropriate size for gestational age (gestational age at birth 28 wks, SD 1.2wks; birth weight 1002g, SD 251g), were randomly placed into experimental and control groups. The experimental group received a daily 15-minute oral stimulation program, consisting of stroking the peri- and intra-oral structures, for 10 days before the start of oral feedings. Sucking measures were monitored with a specially-designed nipple-bottle apparatus. Results indicate that the experimental group achieved full oral feedings 7 days sooner than the control group, and demonstrated greater overall intake (%), rate of milk transfer (mL/min), and amplitude of the expression component of sucking (mmHg). There was no difference in sucking stage maturation, sucking frequency, and amplitude of the suction component of sucking. Endurance, defined as ability to sustain the same sucking stage, sucking burst duration, and suction and expression amplitudes throughout a feeding session, was not significantly different between the two groups. The stimulation program enhanced the expression component of sucking, resulting in better oral feeding performance.

It is well established that the survival of preterm infants has greatly increased over the last 20 years (Guyer et al. 1999, Kramer et al 2000, Jadcherla and Shaker 2001). However, oral feeding difficulties are one of the most frequently encountered problems in preterm infants (Comrie and Helm 1997, Lau and Hurst 1999, Jadcherla and Shaker 2001). One reason for a prolonged length of stay in hospital for preterm infants is the failure to complete oral feedings safely and successfully (Schanler et al. 1999). Discharge criteria for preterm infants include medical stability, ability to attain full oral feeding, minimal weight gain of 15g/kg/day, and temperature self-regulation (American Academy of Pediatrics 1998).

Feeding specialists use various intervention techniques to facilitate the oral feeding process of preterm infants. One of the most common strategies used consists of sensorimotor input, such as cheek/chin support, oral, tactile, kinesthetic, auditory, and vestibular, and/or visual stimulation (Einarsson-Backes et al. 1993, Gaebler and Hanzlik 1996, Hill et al. 2000, Fucile et al. 2002, White-Traut et al. 2002). Some of these intervention strategies have been shown to be effective. For instance, cheek/chin support during an oral feeding session increased volume intake (Einarsson-Backes et al. 1993); an oral stimulation program consisting of stroking the oral structures, provided before or after the introduction of oral feeding, led to earlier attainment of full oral feeding, greater weight gain, and earlier hospital discharge (Gaebler and Hanzlik 1996, Fucile et al. 2002); an auditory-tactile-visual-vestibular program accelerated the transition from tube to full oral feeding and shortened the length of hospitalization (White-Traut et al. 2002). These studies demonstrated that sensorimotor interventions have beneficial effects on the oral feeding performance of preterm infants. However, it is unclear which components of sucking were enhanced.

Safe and efficient oral feeding in infants necessitates the coordination of sucking, swallowing, and breathing (Gryboski 1969, Bu’Lock et al. 1990). Nutritive sucking is described as the intake of fluid from either the alternation of suction and expression or expression only (Lau et al. 1997). Suction is the negative intraoral pressure generated by lowering the tongue and jaw, and closure of the naso-pharynx to draw milk out (Dubignon and Campbell 1969, Lau et al. 1997). Expression is the stripping/compression of the nipple between the tongue and the hard palate to eject milk (Dubignon and Campbell 1969, Lau et al. 1997, Waterland et al. 1998). The majority of oral feeding strategies are aimed at improving oral feeding performance by enhancing sucking skills. However, to the authors’ knowledge, few studies have investigated the direct benefits of these interventions on the components of sucking of preterm infants.

In an earlier study we described the clinical outcomes observed following a specific oral stimulation program, administered before the start of oral feedings (Fucile et al. 2002). Following this intervention, the transition from tube to full oral feeding was accelerated by 1 week. This was associated with greater overall intake (volume taken/volume prescribed, %) and rate of milk transfer (mL/min). The present study was a continuation of this earlier work. Its purpose was to identify the sucking components that may have contributed to the observed clinical improvement. It was hypothesized that the oral stimulation program would: (1) accelerate the maturation of the sucking pattern; (2) enhance sucking frequency; (3) improve the amplitudes of suction and expression; and (4) increase endurance.

Method

PARTICIPANTS

All participants were recruited from the Neonatal Intensive Care Unit at Texas Children’s Hospital, Houston, Texas. The study was approved by the Institutional Review Board for Human Subjects Research of Baylor College of Medicine and Affiliated Hospitals. Informed parental consent was obtained before participants’ entry into the study, following consultation with the attending physician.

A total of 32 preterm infants (13 males, 19 females) participated in the study. Infants were enrolled if they were: (1) born between 26 and 29 weeks’ gestational age as determined by obstetric ultrasound and clinical examination – in instances where there was a discrepancy between the two methods, gestational age as determined by the clinical examination was selected; (2) of appropriate size for gestational age; (3) receiving tube feedings; and (4) without chronic medical complications, including bronchopulmonary dysplasia, intraventricular hemorrhages grades III and IV (Papile et al. 1978), periventricular leukomalacia, necrotizing enterocolitis, and congenital anomalies (e.g. oral, heart, etc.).

PROCEDURE

A randomized trial was carried out. Infants in the experimental group received a non-nutritive oral stimulation program and those in the control group received a sham stimulation program. Both interventions were started before the start of oral feedings, 48 hours following discontinuation of nasal continuous positive airway pressure, and were administered once per day for 10 consecutive days, 15 to 30 minutes before a tube feeding.

The initiation and advancement of oral feeding was left to the discretion of the attending neonatologist. Nurses fed the infants in their customary fashion with nipples (teats) routinely used in the nursery. Nipple selection was left to the nurses’ discretion. The duration of an oral feeding session was a maximum of 20 minutes, as per nursery protocol. Infants’ sucking skills were monitored twice when they were taking 1 to 2 and 6 to 8 oral feedings per day.

The oral stimulation program consisted of stroking the perioral and intraoral structures for 15 minutes. Specific details of the program can be found in our earlier study (Fucile et al. 2002). It was administered by one of the researchers (SF). Before commencing the program, a screen was placed around the isolette to ensure that caregivers and families were blinded to the assigned treatment (experimental vs sham). The infant was positioned supine in the isolette and the intervention was provided only if the infant was in an optimal behavioral state, i.e. drowsy to quiet alert (stages 3 and 4 of the Preterm Infants Behavior Scale from the Newborn Individualized Developmental Care and Assessment Program; NIDCAP; Als 1995). The sham stimulation program consisted of the same researcher placing her hands in the isolette for 15 minutes without touching the infant.

OUTCOME MEASURES

Oral feeding performance was assessed as a function of both clinical outcomes and sucking skills. Infants’ oral feeding performance was followed longitudinally, i.e. when infants were taking 1 to 2 and 6 to 8 oral feedings per day.

Clinical outcomes included number of days to transition from tube to full oral feedings, overall intake (volume taken/ volume prescribed, %) and rate of milk transfer (mL/min; Fucile et al. 2002).

Sucking skills included the maturational level of the sucking pattern, sucking frequency, and amplitudes of suction and expression. Sucking pattern maturation was assessed using the sucking stage scale developed by Lau and colleagues (2000). This is a 5-point scale that characterizes the developmental stages of the sucking pattern based on the presence/absence and rhythmicity of the suction and expression components. Sucking frequency (number of suction or expression peaks per second) and suction and expression amplitudes (mmHg), were calculated from sucking recordings obtained using a nipple-bottle apparatus described in a previous study (Lau et al. 1997). A modification was made to the system to allow for the simultaneous recording of both the suction and expression amplitudes. The suction component was monitored from a Mikro-tip sensor transducer (Model SPR-524, Miller Instruments, Houston, TX, USA) inserted through a catheter flush with the tip of the nipple. The expression component was monitored via another Mikro-tip sensor inserted through a silastic catheter to 0.5cm from the tip of the nipple. This system used nipples routinely used in the nurseries. A weighted average for all sucking measures was calculated from two sucking bursts occurring within the first and last 5 minutes of an oral feeding session. The weighted averages were computed using the following formula: [T1(B1)+T2 (B2)]/ [T1+T2], with T1, T2, corresponding to the duration (in seconds) of the respective sucking bursts, and B1, B2 relating to the average value of a particular measure within the respective sucking bursts. The two sucking bursts analyzed were selected on the basis that their duration and stage of sucking were representative of all the sucking bursts occurring during these two time periods. Sucking bursts were delineated by periods of pause ≥ 1.5 seconds.

To the authors’ knowledge, there is no objective measure of endurance. Thus, we speculated that infants’ endurance would be reflected by their ability to maintain the same stage of sucking, sucking burst duration, and amplitudes of suction and/or expression throughout a feeding session. Hence, a comparison of each of these outcomes during the first and last 5 minutes of the oral feeding session was used as a measure of endurance.

The following covariates were taken into consideration: behavioral state of the infant at the start and end of the feeding session using the Preterm Infants Behavioral Scale from NID-CAP (Als 1995); episodes of apnea, bradycardia, and oxygen desaturations during the oral feeding session; and infants who received breastfeedings throughout the study.

STATISTICAL ANALYSIS

To assess the maturational level of sucking pattern and sucking frequency, paired and independent t-tests were used to compare within- and between-group differences respectively, at 1 to 2 and 6 to 8 oral feedings/day. The non-parametric Wilcoxon Median test was used to compare the amplitudes of the expression and suction components due to skewed distribution of these two measures. For the assessment of endurance, a paired t-test was used to compare the stages of sucking, sucking burst duration, and amplitudes of suction and expression during the first and last 5 minutes of the oral feeding session. Significance was set at 0.05.

Results

Baseline characteristics of the 32 infants are summarized in Table I. Both groups were appropriate size for gestational age and comparable for gestational age, birthweight, sex distribution, and Apgar scores at 5 minutes. Table I demonstrates that infants in the experimental group achieved full oral feedings 7 days sooner than the control group (p=0.005). The experimental group demonstrated significantly greater overall intake and rate of milk transfer at 1 to 2 oral feedings/day (p=0.01 and p=0.02 respectively). However, there-was no difference between each group in postmenstrual age and weight at this time point.

Figure 1 demonstrates that both groups had similar sucking pattern maturation at 1 to 2 and 6 to 8 oral feedings/day (p≥0.36). Mean stage of sucking for the experimental group was 3.3 (SD 0.6) at 1 to 2 oral feedings/day and 3.5 (SD 0.6) at 6 to 8 oral feedings/day. For the control group, mean stage of sucking was 3.1 (SD 0.8) and 3.4 (SD 0.6) at these two time points. There was no difference within each group over time in the stages of sucking (p≥0.35).

Both groups had similar sucking frequency at the two time points (p≥0.06). The sucking frequency for the experimental group was 2.3 (SD 0.2) and 1.1 (SD 0.2) at 1 to 2 and 6 to 8 oral feedings/day respectively. For the control group, it was 2.6 (SD 0.5) and 1.3 (SD 0.3) at these two time points. Both groups demonstrated a significant decrease in sucking frequency over time (p≤0.001).

At the 1 to 2 oral feedings/day, the amplitude of the expression component in the experimental infants was significantly greater than that of the control counterparts (p=0.0003). At 6 to 8 oral feedings/day, both groups had similar suction and expression amplitudes (Table II). There was no difference within each group over time (1 to 2 vs 6 to 8 feedings/day; p≥0.15) in either the suction or expression amplitudes.

Table III illustrates that neither group demonstrated any changes in the stage of sucking, amplitudes of suction and expression, or sucking burst duration between the first and last 5 minutes of the oral feeding sessions monitored.

There was no difference in terms of behavioral state, number of episodes of apnea, bradycardia or oxygen desaturations, or breastfeeding sessions between the two groups.

Discussion

Sensorimotor strategies are widely used to enhance the oral feeding performance of preterm infants. However, the mechanism by which the improvement of sucking skills is mediated is not yet understood. This study investigated the contribution of sucking components towards the improvement of oral feeding performance in preterm infants following a specific non-nutritive oral stimulation program. It has been suggested that infants’ overall intake and rate of milk transfer are indicators not only of their oral-motor skills, and ability to coordinate sucking, swallowing, and breathing, but also of fatigue or lack of endurance (Bu’Lock et al. 1990, Lau and Schanler 1996). Thus, we postulated that the improved oral feeding performance demonstrated by the experimental group may be due to enhanced sucking skills, such as a more mature sucking pattern, increased sucking frequency, greater amplitudes of suction and/or expression, and increased endurance.

Our results indicate that the intervention program did not enhance sucking pattern maturation (hypothesis 1). This may be due to the criteria used to describe the five stages of sucking. Indeed, the stages are defined by the presence/absence of the expression and suction components, and their rhythmicity (Lau et al. 2000). They do not take into account the amplitudes of the expression and suction. Thus, alterations in magnitude of either suction or expression amplitudes are not reflected in the sucking stages.

There was no difference in sucking frequency between the two groups (hypothesis 2). Therefore, the increased volume intake in the experimental group cannot be attributed to faster sucking frequency as shown in previous studies (Sameroff 1968, Jain et al. 1987). Furthermore, contrary to other studies, we observed a decrease in sucking frequency over time (Kron et al. 1967, Medoff-Cooper et al. 1993). This may be due to different methods of measuring sucking frequency. Unlike earlier monitoring devices, our nipple-bottle apparatus differentiates between the suction and expression components. Thus, we measured sucking frequency by the number of suction peaks when the sucking pattern comprised of the alternation of suction/expression, and by the number of expression peaks when only expression was present.

The oral stimulation program enhanced the expression amplitude but not that of the suction component (hypothesis 3). It is conceivable that the intervention accelerated the maturation/coordination of the muscles (e.g. tongue, jaw) used for expression more than those implicated for the generation of suction, leading to a more efficient stripping action of the tongue. Further studies are needed to verify this speculation. Contrary to one of our earlier studies, we did not find an increase in suction amplitude as infants progressed from 1 to 8 oral feedings/day (Lau et al. 2000). This may be explained by the different flow systems used. In our earlier study, a milk reservoir open to the atmosphere was used which eliminated the vacuum build-up that naturally occurs in bottles as infants suck. However, in the present study, regular bottles were used. Thus, negative pressure accumulated in the bottle. We have speculated that this built-up negative pressure opposes the suction force exerted by the infant and decreases not only the amplitude of their suction, but also their sucking efficiency (Lau and Schanler 2000). Large variations were noted for both suction and expression amplitudes in each group. This could not be attributed to infants’ varying maturity because there was no difference in postmenstrual age and weight between both groups at 1 to 2 and 6 to 8 oral feedings/day. It has been suggested that these large variations are normal and reflect individual differences in ability to coordinate sucking, swallowing, and breathing, different levels of fatigue, and other behavioral characteristics (Medoff-Cooper et al. 1993, Lau et al. 2000).

Based on the measure of endurance defined in our study, we expected the experimental group would have greater endurance than the control group because of the increased practice opportunities obtained through the intervention program (hypothesis 4). This was not observed. Instead, infants in both groups were able to sustain the same level of sucking stage, expression and suction amplitudes, and sucking burst duration at the start and end of the oral feeding session. This may be an indication that infants in both groups were not fatigued. However, endurance during oral feeding is a complex phenomenon involving not only the infant’s ability to sustain a particular sucking pattern, but also their ability to maintain a consistent behavioral state, respiratory rate, and oxygen saturation throughout an oral feeding session. Thus comparing rate of milk transfer during the first and last 5 minutes of the feeding session may be a better indicator of endurance, because milk transfer is influenced by all these factors as well as infants’ fatigue (Lau and Schanler 1996).

This study has provided evidence that a non-nutritive oral stimulation program that facilitated the development of the expression component of sucking can enhance oral feeding performance. However, the expression component is just one of many factors involved in the achievement of safe and successful oral feeding. Therefore, the development of additional interventions aimed at facilitating the development of other skills involved in oral feeding, such as enhancing the suction component, behavioral state, and respiratory control, may be of great importance in order to develop more efficacious feeding intervention strategies.

In conclusion, we have demonstrated that oral stimulation programs can advance the maturation of specific sucking skills. This supports the notion that the development of sucking is not only an inborn conditioned reflex dependent upon neurophysiological maturation, but that it can also be enhanced with practice.

DOI: 10.1017/S0012162205000290

Accepted for publication 16th April 2004.

Acknowledgments

The authors wish to thank all the families for their participation, CE Scheel MD and C Simpson MD for their assistance in the data collection, and M Abrahamovicz PhD for his statistical assistance. This study was supported by the Fonds de la Recherche en Santé du Québec graduate student scholarship #3651, #002056, and #99062 and the National Institute of Child Health and Human Development (R01-HD28140).

References

Als H. (1995) A manual for naturalistic observation of the newborn (preterm and full term infants). In: Goldson E, editor. Nurturing the Premature Infant, Developmental Interventions in the Neonatal Intensive Care Nursery. New York: Oxford University Press. p 77-85.

American Academy of Pediatrics. (1998) Hospital discharge of the high-risk neonate – proposed guidelines (RE9812). Pediatrics 102: 411-417.

Bu’Lock F, Woolridge MW, Baum JD. (1990) Development of co-ordination of sucking, swallowing, and breathing: ultrasound study of term and preterm infants. Dev Med Child Neurol 32: 669-678.

Comrie JD, Helm JM. (1997) Common feeding problems in the intensive care nursery, maturation, organization, evaluation, and management strategies. Semin Speech Lang 18: 239-261.

Dubignon J, Campbell D. (1969) Sucking in the newborn during a feed. J Exp Child Psychol 7: 282-298.

Einarsson-Backes LM, Deitz J, Price R, Glass R, Hays R. (1993) The effect of oral support on sucking efficiency in preterm infants. Am J Occup Ther 48: 490-498.

Fucile S, Gisel E, Lau C. (2002) Oral stimulation accelerates the transition from tube to oral feeding in preterm infants. J Pediatr 141: 230-236.

Gaebler CP, Hanzlik JR. (1996) The effects of a prefeeding stimulation program on preterm infants. Am J Occup Ther 50: 184-192.

Gryboski JD. (1969) Suck and swallow in the premature infant. Pediatrics 43: 96-102.

Guyer B, Hoyert DL, Martin JA, Ventura SJ, MacDorman MF, Strobino DM. (1999) Annual summary of vital statistics – 1998. Pediatrics 104: 1229-1246.

Hill AS, Kurkowski TB, Garcia J. (2000) Oral support measures used in feeding the preterm infant. Nur Res 49: 2-10.

Jain L, Sivieri E, Abbasi S, Bhutani VK. (1987) Energetics and mechanics of nutritive sucking in the preterm and term neonate. Pediatrics 111: 894-898.

Jadcherla SR, Shaker R. (2001) Esophageal and upper esophageal sphincter motor function in babies. Am J Med 111 (Suppl 8A): 64S-68S.

Kramer MS, Demissie K, Yang H, Platt RW, Sauve R, Liston R. (2000) The contribution of mild and moderate preterm birth to infant mortality. Fetal and Infant Health Study Group of the Canadian Perinatal Surveillance System. JAMA 284: 843-849.

Kron RE, Stein M, Goddard KE, Phoenix MD. (1967) Effect of nutrient upon the sucking behavior of newborn infants. Psychosom Med 29: 24-32.

Lau C, Alagugurusamy R, Smith EO, Schanler RJ. (2000) Characterization of the developmental stages of sucking in preterm infants during bottle feeding. Acta Paediatr 89: 846-852.

Lau C, Hurst N. (1999) Oral feeding in infants. Curr Probl Pediatr 29: 105-124.

Lau C, Schanler RJ. (1996) Oral motor function in the neonate. Clin Perinatol 23: 161-178.

Lau C, Schanler RJ. (2000) Oral feeding in premature infants: advantage of a self-paced milk flow. Acta Paediatr 89: 453-459.

Lau C, Sheena H, Shulman RJ, Schanler RJ. (1997) Oral feeding in low birth weight infants. J Pediatr 130: 561-569.

Medoff-Cooper B, Verklan T, Carlson S. (1993) The development of sucking patterns and physiologic correlates in very-low-birth-weight infants. Nurs Res 42: 100-105.

Papile L, Burnstein J, Burnstein R, Kuffler H. (1978) Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1500 grams. J Pediatr 92: 529-534.

Sameroff AJ. (1968) The components of sucking in the human newborn. J Exp Child Psychol 6: 607-623.

Schanler RJ, Shulman RJ, Lau C, Smith O, Heitkemper MM. (1999) Feeding strategies for premature infants: randomized trial of gastrointestinal priming and tube-feeding method. Pediatrics 103: 434-439.

Waterland RA, Berkowitz RI, Stunkard AJ, Stallings VA. (1998) Calibrated-orifice nipples for measurement of infant sucking. J Pediatr 132: 523-526.

White-Traut RC, Nelson MN, Silvestri JM, Vasan U, Littau S, Meleedy-Rey P, Gu G, Patel M. (2002) Effect of auditory, tactile, visual, and vestibular intervention on length of stay, alertness, and feeding progression in preterm infants. Dev Med Child Neurol 44: 91-97.

S Fucile MSc OT(C);

E G Gisel PhD OTR, McGill University, School of Physical and Occupational Therapy, Montreal, Quebec, Canada;

C Lau* PhD, Baylor College of Medicine, Department of Pediatrics, Section of Neonatology, Houston, Texas, USA.

* Correspondence to last author at Baylor College of Medicine, Department of Pediatrics, Section of Neonatology, One Baylor Plaza, Houston, TX 77030, USA.

E-mail: clau@bcm.tmc.edu

Copyright Mac Keith Press Mar 2005

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