Effect of an oral
greatly increased over the last 20 years (Guyer et al. 1999,
stimulation program
on sucking skill
maturation of
preterm infants
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
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; birthweight 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.
158 Developmental Medicine & Child Neurology 2005, 47: 158162
It is well established that the survival of preterm infants has
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 pro-
longed length of stay in hospital for preterm infants is the fail-
ure to complete oral feedings safely and successfully (Schanler
et al. 1999). Discharge criteria for preterm infants include med-
ical 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 stimula-
tion 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 auditorytactilevisualvestibular 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 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, BuLock et al. 1990). Nutritive sucking is described as the
intake of fluid from either the alternation of suction and expres-
sion 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 strip-
ping/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 inter-
ventions on the components of sucking of preterm infants.
In an earlier study we described the clinical outcomes
observed 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 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 Childrens 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 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) 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, ges-
tational age as determined by the clinical examination was
selected; (2) of appropriate size for gestational age; (3) receiv-
ing tube feedings; and (4) without chronic medical complica-
tions, including bronchopulmonary dysplasia, intraventricular
hemorrhages grades III and IV (Papile et al. 1978), periventric-
ular leukomalacia, necrotizing enterocolitis, and congenital
anomalies (e.g. oral, heart, etc.).
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 nip-
ple-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 expres-
sion amplitudes. The suction component was monitored
from a Mikro-tip sensor transducer (Model SPR-524, Miller
Table I: Participant characteristics and clinical outcomes of
oral feeding performance

PROCEDURE Infant characteristics Experimental Control pa

A randomized trial was carried out. Infants in the experimen- and clinical outcomes (n=16) (n=16)
tal group received a non-nutritive oral stimulation program
Gestational age
and those in the control group received a sham stimulation Mean (SD) wk 28.2 (1.3) 28.1 (1.1)
program. Both interventions were started before the start of Range 26.429.9 26.029.7
oral feedings, 48 hours following discontinuation of nasal Birthweight
continuous positive airway pressure, and were administered Mean (SD) g 1044 (260) 959 (244)
once per day for 10 consecutive days, 15 to 30 minutes before Range 7401500 5601300
a tube feeding. Sex distribution
The initiation and advancement of oral feeding was left to Male 7 6
the discretion of the attending neonatologist. Nurses fed the Female 9 10
infants in their customary fashion with nipples (teats) rou- Apgar (5 min) 2b 2
tinely used in the nursery. Nipple selection was left to the Nr days to reach full oral feeding
Mean (SD) 11 (4) 18 (7) 0.005
nurses discretion. The duration of an oral feeding session Range 519 930
was a maximum of 20 minutes, as per nursery protocol.
Infants sucking skills were monitored twice when they were 1 to 2 oral feedings/day
Overall intake
taking 1 to 2 and 6 to 8 oral feedings per day. Mean (SD) % 80 (30) 50 (30) 0.01
The oral stimulation program consisted of stroking the peri- Range 19100 10100
oral and intraoral structures for 15 minutes. Specific details of Rate of milk transfer
the program can be found in our earlier study (Fucile et al. Mean (SD) mL/min 1.6 (0.7) 0.9 (0.6) 0.02
2002). It was administered by one of the researchers (SF). Range 0.53.2 0.31.7
Before commencing the program, a screen was placed around Postmenstrual age
the isolette to ensure that caregivers and families were blinded Mean (SD) wks 34.8 (1.8) 35.4 (1.6) 0.39
to the assigned treatment (experimental vs sham). The infant Range 31.938.1 32.938.7
was positioned supine in the isolette and the intervention was Weight
Mean (SD) g 1700 (294) 1735 (353) 0.77
provided only if the infant was in an optimal behavioral state,
Range 11452305 12152705
i.e. drowsy to quiet alert (stages 3 and 4 of the Preterm Infants
Behavior Scale from the Newborn Individualized Develop- 6 to 8 oral feedings/day
Overall intake
mental Care and Assessment Program; NIDCAP; Als 1995). The
Mean (SD) % 89 (30) 67 (33) 0.06
sham stimulation program consisted of the same researcher Range 27100 20100
placing her hands in the isolette for 15 minutes without Rate of milk transfer
touching the infant. Mean (SD) mL/min 2.3 (1.0) 1.6 (0.9) 0.08
Range (0.54.0) (0.53.6)
OUTCOME MEASURES Postmenstrual age
Oral feeding performance was assessed as a function of both Mean (SD) wks 36.1 (1.8) 36.9 (1.8) 0.19
clinical outcomes and sucking skills. Infants oral feeding per- Range 32.938.7 33.740.7
formance was followed longitudinally, i.e. when infants were Weight
taking 1 to 2 and 6 to 8 oral feedings per day. Mean (SD) g 1928 (343) 2043 (461) 0.43
Range 12852760 14323470
Clinical outcomes included number of days to transition
from tube to full oral feedings, overall intake (volume taken/ aIndependent t-test; bNumber of infants scoring <7.

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

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 aver-
age 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 respec-
tive 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 peri-
ods. 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 suck-
ing frequency, paired and independent t-tests were used to
compare within- and between-group differences respec-
tively, at 1 to 2 and 6 to 8 oral feedings/day. The non-para-
5
4 changes in the stage of sucking, amplitudes of suction and
Stages of sucking
3 There was no difference in terms of behavioral state, num-
2
1
0 feeding performance in preterm infants following a specific
12 68
Oral feedings per day
Figure 1: Sucking stages at 12 and 68 oral feedings/day
(mean, SD). , experimental group; , control group.
160 Developmental Medicine & Child Neurology 2005, 47: 158162
metric Wilcoxon Median test was used to compare the amp-
litudes 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 distribu-
tion, 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 experi-
mental 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 dif-
ference between each group in postmenstrual age and weight
at 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
(p0.36). 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 (p0.35).
Both groups had similar sucking frequency at the two time
points (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 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 fre-
quency over time (p0.001).
At the 1 to 2 oral feedings/day, the amplitude of the expres-
sion 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
expression, or sucking burst duration between the first and
last 5 minutes of the oral feeding sessions monitored.
ber of episodes of apnea, bradycardia or oxygen desatura-
tions, or breastfeeding sessions between the two groups.
Discussion
Sensorimotor strategies are widely used to enhance the oral
feeding performance of preterm infants. However, the mech-
anism by which the improvement of sucking skills is mediated
is not yet understood. This study investigated the contribu-
tion of sucking components towards the improvement of oral
non-nutritive oral stimulation program. It has been suggested
that 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 or
lack of endurance (BuLock 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 ampli-
tudes 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 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 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 matu-
ration/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.

Table II: Suction and expression amplitudes at 12 and 68 oral feedings per day

Sucking/Expression amplitudes Experimental Control pa

12 oral feedings/day
Suction amplitude, mean (SD) mmHg 31.9 (39.4)a 27.6 (21.4) 0.47
Range 1.0116.9 1.276.5
Expression amplitude, mean (SD) mmHg 32.9 (36.6) 7.9 (9.03) 0.0003
Range 1.0126.7 1.330.9
68 oral feedings/day
Suction amplitude, mean (SD) mmHg 38.9 (25.2) 38.5 (26.5) 0.36
Range 9.898.1 9.197.4
Expression amplitude, mean (SD) mmHg 12.4 (8.8) 9.7 (9.4) 0.10
Range 0.129.1 0.126.9
aWilcoxon median test.

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) 0.39
Range 25 24 25 24
Sucking burst duration, mean (SD) s 39.9 (69.9) 27.6 (27.4) 0.47 16.7 (18.2) 16.8 (15.3) 0.98
Range 6.3261.6 5.6122.4 (4.226.5) 3.062.6
Suction amplitude, mean (SD) mmHg 35.5 (42.0) 44.8 (32.3) 0.74 28.9 (21.9) 23.2 (33.4) 0.59
Range 0.6167.4 0.6116.9 (0.465.9) 3.7124.4
Expression amplitude, mean (SD) mmHg 24.0 (27.0) 35.4 (47.0) 0.41 9.5 (11.4) 5.8 (7.6) 0.31
Range 0.6110.0 7.4161.2 0.534.8 0.228.1
68 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) 0.15
Range 25 35 25 25
Sucking burst duration, mean (SD) s 26.7 (22.0) 20.2 (11.41) 0.32 13.6 (6.96) 10.2 (71.2) 0.24
Range 7.491.1 6.246.4 4.325.9 4.239.2
Suction amplitude, mean (SD) mmHg 41.8 (27.2) 39.6 (28.2) 0.84 40.6 (28.1) 34.9 (26.9) 0.58
Range 7.783.9 7.2108.7 8.489.2 8.4107.9
Expression amplitude, mean (SD) mmHg 11.9 (10.0) 13.7 (10.2) 0.64 9.1 (9.1) 9.4 (12.5) 0.95
Range 1.028.5 1.035.3 0.227.6 0.143.9
aPaired t-tests.

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


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 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 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 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 both
groups 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 be
an indication that infants in both groups were not fatigued.
However, endurance during oral feeding is a complex phe-
nomenon involving not only the infants ability to sustain a par-
ticular sucking pattern, but also their ability to maintain a
consistent behavioral state, respiratory rate, and oxygen satu-
ration 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, bec-
ause 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 addi-
tional interventions aimed at facilitating the development of
other skills involved in oral feeding, such as enhancing the
suction component, behavioral state, and respiratory con-
trol, may be of great importance in order to develop more
efficacious 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 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 Sant
du Qubec graduate student scholarship #3651, #002056, and
#99062 and the National Institute of Child Health and Human
Development (R01-HD28140).
162 Developmental Medicine & Child Neurology 2005, 47: 158162
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