Effect of an oralstimulation programon sucking skillmaturation of preterm infants

S Fucile MSc OT(C);EG Gisel PhD OTR, McGill University, School of Physical andOccupational Therapy, Montreal, Quebec, Canada;C Lau* PhD, Baylor College of Medicine, Department ofPediatrics, Section of Neonatology, Houston, Texas, USA.

*Correspondence to last author at Baylor College ofMedicine, Department of Pediatrics, Section of Neonatology, One Baylor Plaza, Houston, TX 77030, USA.E-mail: clau@bcm.tmc.edu

This study assessed the effect of an oral stimulation programon the maturation of sucking skills of preterm infants. Thirty-two preterm infants (13 males, 19 females), appropriate sizefor gestational age (gestational age at birth 28 wks, SD1.2wks; birthweight 1002g, SD 251g), were randomly placedinto experimental and control groups. The experimental groupreceived a daily 15-minute oral stimulation program,consisting of stroking the peri- and intra-oral structures, for10 days before the start of oral feedings. Sucking measureswere monitored with a specially-designed nipple-bottleapparatus. Results indicate that the experimental groupachieved full oral feedings 7 days sooner than the controlgroup, and demonstrated greater overall intake (%), rate ofmilk transfer (mL/min), and amplitude of the expressioncomponent of sucking (mmHg). There was no difference insucking stage maturation, sucking frequency, and amplitudeof the suction component of sucking. Endurance, defined asability to sustain the same sucking stage, sucking burstduration, and suction and expression amplitudes throughout afeeding session, was not significantly different between thetwo groups. The stimulation program enhanced theexpression component of sucking, resulting in better oralfeeding performance.

It is well established that the survival of preterm infants hasgreatly increased over the last 20 years (Guyer et al. 1999,Kramer et al 2000, Jadcherla and Shaker 2001). However, oralfeeding difficulties are one of the most frequently encounteredproblems in preterm infants (Comrie and Helm 1997, Lau andHurst 1999, Jadcherla and Shaker 2001). One reason for a pro-longed length of stay in hospital for preterm infants is the fail-ure to complete oral feedings safely and successfully (Schanleret al. 1999). Discharge criteria for preterm infants include med-ical stability, ability to attain full oral feeding, minimal weightgain of 15g/kg/day, and temperature self-regulation (AmericanAcademy of Pediatrics 1998).

Feeding specialists use various intervention techniques tofacilitate the oral feeding process of preterm infants. One of themost common strategies used consists of sensorimotor input,such as cheek/chin support, oral, tactile, kinesthetic, auditory,and vestibular, and/or visual stimulation (Einarsson-Backes etal. 1993, Gaebler and Hanzlik 1996, Hill et al. 2000, Fucile et al.2002, White-Traut et al. 2002). Some of these interventionstrategies have been shown to be effective. For instance,cheek/chin support during an oral feeding session increasedvolume intake (Einarsson-Backes et al. 1993); an oral stimula-tion program consisting of stroking the oral structures, providedbefore or after the introduction of oral feeding, led to earlierattainment of full oral feeding, greater weight gain, and earlierhospital discharge (Gaebler and Hanzlik 1996, Fucile et al.2002); an auditory–tactile–visual–vestibular program accel-erated the transition from tube to full oral feeding and short-ened the length of hospitalization (White-Traut et al. 2002).These studies demonstrated that sensorimotor interventionshave beneficial effects on the oral feeding performance ofpreterm infants. However, it is unclear which components ofsucking were enhanced.

Safe and efficient oral feeding in infants necessitates thecoordination of sucking, swallowing, and breathing (Gryboski1969, Bu’Lock et al. 1990). Nutritive sucking is described as theintake of fluid from either the alternation of suction and expres-sion or expression only (Lau et al. 1997). Suction is the negativeintraoral pressure generated by lowering the tongue and jaw,and closure of the naso-pharynx to draw milk out (Dubignonand Campbell 1969, Lau et al. 1997). Expression is the strip-ping/compression of the nipple between the tongue and thehard palate to eject milk (Dubignon and Campbell 1969, Lau etal. 1997, Waterland et al. 1998). The majority of oral feedingstrategies are aimed at improving oral feeding performance byenhancing sucking skills. However, to the authors’ knowledge,few studies have investigated the direct benefits of these inter-ventions on the components of sucking of preterm infants.

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

158 Developmental Medicine & Child Neurology 2005, 47: 158–162

Oral Stimulation and Sucking Skill Maturation S Fucile et al. 159

MethodPARTICIPANTS

All participants were recruited from the Neonatal IntensiveCare Unit at Texas Children’s Hospital, Houston, Texas. Thestudy was approved by the Institutional Review Board forHuman Subjects Research of Baylor College of Medicine andAffiliated Hospitals. Informed parental consent was obtainedbefore participants’ entry into the study, following consulta-tion with the attending physician.

A total of 32 preterm infants (13 males, 19 females) partici-pated in the study. Infants were enrolled if they were: (1) bornbetween 26 and 29 weeks’ gestational age as determined byobstetric ultrasound and clinical examination – in instanceswhere there was a discrepancy between the two methods, ges-tational age as determined by the clinical examination wasselected; (2) of appropriate size for gestational age; (3) receiv-ing tube feedings; and (4) without chronic medical complica-tions, including bronchopulmonary dysplasia, intraventricularhemorrhages grades III and IV (Papile et al. 1978), periventric-ular leukomalacia, necrotizing enterocolitis, and congenitalanomalies (e.g. oral, heart, etc.).

PROCEDURE

A randomized trial was carried out. Infants in the experimen-tal group received a non-nutritive oral stimulation programand those in the control group received a sham stimulationprogram. Both interventions were started before the start oforal feedings, 48 hours following discontinuation of nasalcontinuous positive airway pressure, and were administeredonce per day for 10 consecutive days, 15 to 30 minutes beforea tube feeding.

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

The oral stimulation program consisted of stroking the peri-oral and intraoral structures for 15 minutes. Specific details ofthe 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 aroundthe isolette to ensure that caregivers and families were blindedto the assigned treatment (experimental vs sham). The infantwas positioned supine in the isolette and the intervention wasprovided only if the infant was in an optimal behavioral state,i.e. drowsy to quiet alert (stages 3 and 4 of the Preterm InfantsBehavior Scale from the Newborn Individualized Develop-mental Care and Assessment Program; NIDCAP; Als 1995). Thesham stimulation program consisted of the same researcherplacing her hands in the isolette for 15 minutes withouttouching the infant.

OUTCOME MEASURES

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

Clinical outcomes included number of days to transitionfrom 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 suckingpattern, sucking frequency, and amplitudes of suction andexpression. Sucking pattern maturation was assessed using thesucking stage scale developed by Lau and colleagues (2000).This is a 5-point scale that characterizes the developmentalstages of the sucking pattern based on the presence/absenceand rhythmicity of the suction and expression components.Sucking frequency (number of suction or expression peaksper second) and suction and expression amplitudes (mmHg),were calculated from sucking recordings obtained using a nip-ple-bottle apparatus described in a previous study (Lau et al.1997). A modification was made to the system to allow forthe simultaneous recording of both the suction and expres-sion amplitudes. The suction component was monitoredfrom a Mikro-tip sensor transducer (Model SPR-524, Miller

Table I: Participant characteristics and clinical outcomes of oral feeding performance

Infant characteristics Experimental Control pa

and clinical outcomes (n=16) (n=16)

Gestational age Mean (SD) wk 28.2 (1.3) 28.1 (1.1)Range 26.4–29.9 26.0–29.7

Birthweight Mean (SD) g 1044 (260) 959 (244)Range 740–1500 560–1300

Sex distributionMale 7 6 Female 9 10

Apgar (5 min) 2b 2

Nr days to reach full oral feeding Mean (SD) 11 (4) 18 (7) 0.005Range 5–19 9–30

1 to 2 oral feedings/day

Overall intake Mean (SD) % 80 (30) 50 (30) 0.01Range 19–100 10–100

Rate of milk transfer Mean (SD) mL/min 1.6 (0.7) 0.9 (0.6) 0.02Range 0.5–3.2 0.3–1.7

Postmenstrual age Mean (SD) wks 34.8 (1.8) 35.4 (1.6) 0.39Range 31.9–38.1 32.9–38.7

Weight Mean (SD) g 1700 (294) 1735 (353) 0.77Range 1145–2305 1215–2705

6 to 8 oral feedings/day

Overall intake Mean (SD) % 89 (30) 67 (33) 0.06Range 27–100 20–100

Rate of milk transfer Mean (SD) mL/min 2.3 (1.0) 1.6 (0.9) 0.08Range (0.5–4.0) (0.5–3.6)

Postmenstrual age Mean (SD) wks 36.1 (1.8) 36.9 (1.8) 0.19Range 32.9–38.7 33.7–40.7

Weight Mean (SD) g 1928 (343) 2043 (461) 0.43Range 1285–2760 1432–3470

aIndependent t-test; bNumber of infants scoring <7.

Instruments, Houston, TX, USA) inserted through a catheterflush with the tip of the nipple. The expression component wasmonitored via another Mikro-tip sensor inserted through asilastic catheter to 0.5cm from the tip of the nipple. This systemused nipples routinely used in the nurseries. A weighted aver-age for all sucking measures was calculated from two suckingbursts occurring within the first and last 5 minutes of an oralfeeding session. The weighted averages were computed usingthe following formula: [T1(B1)+T2 (B2)]/ [T1+T2], with T1,T2, corresponding to the duration (in seconds) of the respec-tive sucking bursts, and B1, B2 relating to the average value of aparticular measure within the respective sucking bursts. Thetwo sucking bursts analyzed were selected on the basis thattheir duration and stage of sucking were representative of allthe sucking bursts occurring during these two time peri-ods. Sucking bursts were delineated by periods of pause≥1.5 seconds.

To the authors’ knowledge, there is no objective measureof endurance. Thus, we speculated that infants’ endurancewould be reflected by their ability to maintain the same stage ofsucking, sucking burst duration, and amplitudes of suctionand/or expression throughout a feeding session. Hence, acomparison of each of these outcomes during the first and last5 minutes of the oral feeding session was used as a measure ofendurance.

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

STATISTICAL ANALYSIS

To assess the maturational level of sucking pattern and suck-ing frequency, paired and independent t-tests were used tocompare within- and between-group differences respec-tively, at 1 to 2 and 6 to 8 oral feedings/day. The non-para-

metric Wilcoxon Median test was used to compare the amp-litudes of the expression and suction components due toskewed distribution of these two measures. For the assessmentof endurance, a paired t-test was used to compare the stages ofsucking, sucking burst duration, and amplitudes of suctionand expression during the first and last 5 minutes of the oralfeeding session. Significance was set at 0.05.

ResultsBaseline characteristics of the 32 infants are summarized inTable I. Both groups were appropriate size for gestational ageand comparable for gestational age, birthweight, sex distribu-tion, and Apgar scores at 5 minutes. Table I demonstrates thatinfants in the experimental group achieved full oral feedings 7days sooner than the control group (p=0.005). The experi-mental group demonstrated significantly greater overallintake and rate of milk transfer at 1 to 2 oral feedings/day(p=0.01 and p=0.02 respectively). However, there was no dif-ference between each group in postmenstrual age and weightat this time point.

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

Both groups had similar sucking frequency at the two timepoints (p≥0.06). The sucking frequency for the experimen-tal group was 2.3 (SD 0.2) and 1.1 (SD 0.2) at 1 to 2 and 6 to 8oral feedings/day respectively. For the control group, it was2.6 (SD 0.5) and 1.3 (SD 0.3) at these two time points. Bothgroups demonstrated a significant decrease in sucking fre-quency over time (p≤0.001).

At the 1 to 2 oral feedings/day, the amplitude of the expres-sion component in the experimental infants was significantlygreater than that of the control counterparts (p=0.0003). At6 to 8 oral feedings/day, both groups had similar suction andexpression amplitudes (Table II). There was no differencewithin 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 anychanges in the stage of sucking, amplitudes of suction andexpression, or sucking burst duration between the first andlast 5 minutes of the oral feeding sessions monitored.

There was no difference in terms of behavioral state, num-ber of episodes of apnea, bradycardia or oxygen desatura-tions, or breastfeeding sessions between the two groups.

DiscussionSensorimotor strategies are widely used to enhance the oralfeeding performance of preterm infants. However, the mech-anism by which the improvement of sucking skills is mediatedis not yet understood. This study investigated the contribu-tion of sucking components towards the improvement of oralfeeding performance in preterm infants following a specificnon-nutritive oral stimulation program. It has been suggestedthat infants’ overall intake and rate of milk transfer are indica-tors not only of their oral-motor skills, and ability to coordi-nate sucking, swallowing, and breathing, but also of fatigue orlack of endurance (Bu’Lock et al. 1990, Lau and Schanler

160 Developmental Medicine & Child Neurology 2005, 47: 158–162

Figure 1: Sucking stages at 1–2 and 6–8 oral feedings/day

(mean, SD). ■■ , experimental group; ■ , control group.

Oral feedings per day

1–2 6–8

Sta

ges

of s

ucki

ng

5

4

3

2

1

0

1996). Thus, we postulated that the improved oral feedingperformance demonstrated by the experimental group maybe due to enhanced sucking skills, such as a more maturesucking pattern, increased sucking frequency, greater ampli-tudes of suction and/or expression, and increased endurance.

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

There was no difference in sucking frequency between thetwo groups (hypothesis 2). Therefore, the increased volumeintake in the experimental group cannot be attributed to fastersucking frequency as shown in previous studies (Sameroff1968, Jain et al. 1987). Furthermore, contrary to other studies,we observed a decrease in sucking frequency over time (Kronet al. 1967, Medoff-Cooper et al. 1993). This may be due to

different methods of measuring sucking frequency. Unlike ear-lier monitoring devices, our nipple-bottle apparatus differenti-ates between the suction and expression components. Thus,we measured sucking frequency by the number of suctionpeaks when the sucking pattern comprised of the alternationof suction/expression, and by the number of expression peakswhen only expression was present.

The oral stimulation program enhanced the expressionamplitude but not that of the suction component (hypothesis3). It is conceivable that the intervention accelerated the matu-ration/coordination of the muscles (e.g. tongue, jaw) used forexpression more than those implicated for the generation ofsuction, leading to a more efficient stripping action of thetongue. Further studies are needed to verify this speculation.Contrary to one of our earlier studies, we did not find anincrease in suction amplitude as infants progressed from 1 to8 oral feedings/day (Lau et al. 2000). This may be explainedby the different flow systems used. In our earlier study, a milkreservoir open to the atmosphere was used which eliminatedthe vacuum build-up that naturally occurs in bottles as infantssuck. However, in the present study, regular bottles were used.

Oral Stimulation and Sucking Skill Maturation S Fucile et al. 161

Table III: Sucking measures at first and last 5 minutes of oral feeding sessions

Sucking measures Experimental pa Control pa

1st 5 min Last 5 min 1st 5 min Last 5 min

1– 2 oral feedings/day

Stage of sucking, mean (SD) 3.3 (0.8)a 3.3 (0.8) 0.83 3.2 (0.8) 2.9 (0.9) 0.39Range 2–5 2–4 2–5 2–4

Sucking burst duration, mean (SD) s 39.9 (69.9) 27.6 (27.4) 0.47 16.7 (18.2) 16.8 (15.3) 0.98Range 6.3–261.6 5.6–122.4 (4.2–26.5) 3.0–62.6

Suction amplitude, mean (SD) mmHg –35.5 (42.0) –44.8 (32.3) 0.74 –28.9 (21.9) –23.2 (33.4) 0.59Range 0.6–167.4 0.6–116.9 (0.4–65.9) 3.7–124.4

Expression amplitude, mean (SD) mmHg 24.0 (27.0) 35.4 (47.0) 0.41 9.5 (11.4) 5.8 (7.6) 0.31Range 0.6–110.0 7.4–161.2 0.5–34.8 0.2–28.1

6–8 oral feedings/day

Stage of sucking, mean (SD) 3.5 (0.7) 3.5 (0.7) 0.90 3.5 (0.8) 3.1 (0.6) 0.15Range 2–5 3–5 2–5 2–5

Sucking burst duration, mean (SD) s 26.7 (22.0) 20.2 (11.41) 0.32 13.6 (6.96) 10.2 (71.2) 0.24Range 7.4–91.1 6.2–46.4 4.3–25.9 4.2–39.2

Suction amplitude, mean (SD) mmHg –41.8 (27.2) –39.6 (28.2) 0.84 –40.6 (28.1) –34.9 (26.9) 0.58Range 7.7–83.9 7.2–108.7 8.4–89.2 8.4–107.9

Expression amplitude, mean (SD) mmHg 11.9 (10.0) 13.7 (10.2) 0.64 9.1 (9.1) 9.4 (12.5) 0.95Range 1.0–28.5 1.0–35.3 0.2–27.6 0.1–43.9

aPaired t-tests.

Table II: Suction and expression amplitudes at 1–2 and 6–8 oral feedings per day

Sucking/Expression amplitudes Experimental Control pa

1–2 oral feedings/day

Suction amplitude, mean (SD) mmHg –31.9 (39.4)a –27.6 (21.4) 0.47Range 1.0–116.9 1.2–76.5

Expression amplitude, mean (SD) mmHg 32.9 (36.6) 7.9 (9.03) 0.0003Range 1.0–126.7 1.3–30.9

6–8 oral feedings/day

Suction amplitude, mean (SD) mmHg –38.9 (25.2) –38.5 (26.5) 0.36Range 9.8–98.1 9.1–97.4

Expression amplitude, mean (SD) mmHg 12.4 (8.8) 9.7 (9.4) 0.10Range 0.1–29.1 0.1–26.9

aWilcoxon median test.

162 Developmental Medicine & Child Neurology 2005, 47: 158–162

Thus, negative pressure accumulated in the bottle. We havespeculated that this built-up negative pressure opposes thesuction force exerted by the infant and decreases not only theamplitude of their suction, but also their sucking efficiency(Lau and Schanler 2000). Large variations were noted for bothsuction and expression amplitudes in each group. This couldnot be attributed to infants’ varying maturity because there wasno difference in postmenstrual age and weight between bothgroups at 1 to 2 and 6 to 8 oral feedings/day. It has been sug-gested that these large variations are normal and reflect indi-vidual differences in ability to coordinate sucking, swallowing,and breathing, different levels of fatigue, and other behavioralcharacteristics (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 end-urance than the control group because of the increased prac-tice opportunities obtained through the intervention program(hypothesis 4). This was not observed. Instead, infants in bothgroups were able to sustain the same level of sucking stage,expression and suction amplitudes, and sucking burst dura-tion at the start and end of the oral feeding session. This may bean indication that infants in both groups were not fatigued.However, endurance during oral feeding is a complex phe-nomenon involving not only the infant’s ability to sustain a par-ticular sucking pattern, but also their ability to maintain aconsistent behavioral state, respiratory rate, and oxygen satu-ration throughout an oral feeding session. Thus comparingrate of milk transfer during the first and last 5 minutes of thefeeding session may be a better indicator of endurance, bec-ause milk transfer is influenced by all these factors as well asinfants’ fatigue (Lau and Schanler 1996).

This study has provided evidence that a non-nutritive oralstimulation program that facilitated the development of theexpression component of sucking can enhance oral feedingperformance. However, the expression component is justone of many factors involved in the achievement of safe andsuccessful oral feeding. Therefore, the development of addi-tional interventions aimed at facilitating the development ofother skills involved in oral feeding, such as enhancing thesuction component, behavioral state, and respiratory con-trol, may be of great importance in order to develop moreefficacious feeding intervention strategies.

In conclusion, we have demonstrated that oral stimula-tion programs can advance the maturation of specific suck-ing skills. This supports the notion that the development ofsucking is not only an inborn conditioned reflex dependentupon neurophysiological maturation, but that it can also beenhanced 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 datacollection, and M Abrahamovicz PhD for his statistical assistance.This study was supported by the Fonds de la Recherche en Santédu Québec graduate student scholarship #3651, #002056, and#99062 and the National Institute of Child Health and HumanDevelopment (R01-HD28140).

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