Acta Pdiatr 92: 721727.

2003

Coordination of suck-swallow and swallow respiration in preterm

infants
C Lau1,2, EO Smith1 and RJ Schanler1,2,3
Department of Pediatrics1, Baylor College of Medicine, Houston, Texas; Section of Neonatology2, Baylor College of Medicine, Houston,
Texas; Childrens Nutrition Research Center3, Baylor College of Medicine, Houston, Texas

Lau C, Smith EO, Schanler RJ. Coordination of suck-swallow and swallow respiration in preterm
infants. Acta Pdiatr 2006; 92: 721727. Stockholm. ISSN 0803-5253
Safe oral feeding of infants necessitates the coordination of suck-swallow-breathe. Healthy fullterm infants demonstrate such skills at birth. But, preterm infants are known to have difficulty in
the transition from tube to oral feeding. Aim: To examine the relationship between suck and
swallow and between swallow and breathe. It is hypothesized that greater milk transfer results
from an increase in bolus size and/or swallowing frequency, and an improved swallow-breathe
interaction. Methods: Twelve healthy preterm (<30 wk of gestation) and 8 full-term infants were
recruited. Sucking (suction and expression), swallowing, and respiration were recorded simultaneously when the preterm infants began oral feeding (i.e. taking 12 oral feedings/d) and at 68
oral feedings/d. The full-term infants were similarly monitored during their first and 2nd to 4th
weeks. Rate of milk transfer (ml/min) was used as an index of oral feeding performance. Sucking
and swallowing frequencies (#/min), average bolus size (ml), and suction amplitude (mmHg) were
measured. Results: The rate of milk transfer in the preterm infants increased over time and was
correlated with average bolus size and swallowing frequency. Average bolus size was not
correlated with swallowing frequency. Bolus size was correlated with suction amplitude, whereas
the frequency of swallowing was correlated with sucking frequency. Preterm infants swallowed
preferentially at different phases of respiration than those of their full-term counterparts.
Conclusion: As feeding performance improved, sucking and swallowing frequency, bolus size,
and suction amplitude increased. It is speculated that feeding difficulties in preterm infants are
more likely to result from inappropriate swallow-respiration interfacing than suck-swallow
interaction.
Key words: Bottle feeding, nutritive sucking, oral feeding, prematurity, suck-swallow-breathe
coordination
Chantal Lau, Department of Pediatrics/Neonatology, Baylor College of Medicine, 1 Baylor Plaza,
Houston TX-77030, USA (Tel. 1 713 7986 710, fax. 1 713 7987 187, e-mail. clau@bcm.tmc.edu)

Oral feeding in infants needs to be efficient to preserve

energy for growth, safe to avoid aspiration, and not
jeopardize respiratory status. This is possible if suck,
swallow, and respiration are properly coordinated. The
majority of full-term infants are born with such skills,
but this is not the case for preterm infants. With the
increased survival of preterm infants, there is now the
realization that feeding difficulty is a major milestone
that these infants need to overcome. The inability to
feed orally is one of the most frequent reasons for the
delayed hospital discharge of preterm infants (1).
Coordination of suck-swallow-breathe is a function
of the infants ability to suck efficiently and swallow
rapidly as the boluses are formed in order to minimize
the duration of airflow interruption. Studies in healthy
preterm infants have demonstrated that sucking skills
improve over time (2, 3). Although swallowing difficulties are common in these infants, the swallowing
2003 Taylor & Francis. ISSN 0803-5253

process has not been studied to the same extent as

sucking. The adaptability of the swallowing process
to adjust to changing variables, such as bolus size, is
necessary to ensure a safe and swift swallow (4). There
is ample evidence to show that during oral feeding
respiration is disrupted, e.g. ventilation and tidal
volume are decreased and apneic episodes are increased
(510). These respiratory changes are not attributed to
sucking per se, as they are not observed during nonnutritive sucking, but rather to factors such as interruption of airflow during swallowing (7, 8, 10). It has been
speculated that control of nutritive sucking necessitates
appropriate feedback afferents to the sucking center
from the mechanoreceptors in and around the oral
region (11, 12). Indeed, the coordination of suck,
swallow, and respiration would necessitate that these
three functions adapt rapidly to their continuously
changing and respective environment. Another factor
DOI 10.1080/08035250310002407

722

C Lau et al.

that may lead to respiratory imbalance during feeding is

the phase of the respiratory cycle when swallowing
occurs (5). This interaction between swallow and
respiration has received little attention. Preterm infants
swallow at all phases of the respiratory cycle during
non-nutritive sucking (13). However, it is unclear when
swallowing occurs during nutritive sucking.
In this study, we hypothesized that the improvement
in oral feeding performance over time in healthy
preterm infants results from an increase in bolus size
and/or swallowing frequency and an improved swallowbreathe interaction.

Methods
Subjects
Twelve healthy preterm and 8 full-term infants were
studied. The preterm infants (6M, 6F), born between 26
and 29 wk of gestation and appropriate for gestational
age as determined by maternal dates and antenatal
ultrasonography, were recruited from the nurseries at
Texas Childrens Hospital. Infants with the following
conditions were excluded from the study: intraventricular hemorrhage grades III and IV, necrotizing
enterocolitis, hydrocephalus, major congenital anomalies, chronic lung disease. The preterm infants were
treated prophylactically with caffeine citrate until
mature control of breathing was demonstrated, i.e.
generally no apnea/bradycardia for >2 wk. Oral feeding
was introduced at the discretion of the attending
physician. Advancement of oral feeding was based on
an adequate daily weight gain (15 g kg 1 d 1) and the
ability of the infant to finish all the assigned feedings the
previous day. The full-term neonates were healthy and
were introduced to oral feeding immediately after birth.
These infants were fed ad libitum. All the infants were
offered the type of milk they were receiving normally,
e.g. mothers milk or preterm formula. The Baylor
College of Medicine Institutional Review Board for
Human Research approved this study and informed
consent was obtained from the parents following
consultation with the attending physicians.
Study design
The oral feeding performance of infants was monitored
in function of rate of milk transfer, sucking, swallowing,
and respiration. Preterm infants were assessed at
introduction of oral feeding, when taking 12 oral
feedings/d and when they reached independent oral
feeding (68 oral feedings/d). Full-term infants were
followed during their first week and again between 2 to
4 wk of age.
Suck-swallow-breathe assessment
Because one of our primary goals was to observe
feedings as naturally as possible, we allowed the

ACTA PDIATR 92 (2003)

caretakers to select the bottle nipple and determine

when to pause for a feeding. The two components of
sucking, suction and expression, along with swallowing
and respiration were monitored simultaneously (14).
The level of milk from a graduated reservoir was
continuously adjusted to the level of the infants mouth
to allow for a self-paced flow, i.e. milk flowed only
when the infant was sucking. No encouragement was
provided. Inasmuch as the nipple chamber was continuously filled, the subjects were able to obtain milk
regardless of whether the suction and/or expression
component was used (1). Swallowing was monitored
via a small drum held snugly onto the hyoid region as
described previously (14). Swallowing caused an
upward movement of the hyoid bone resulting in a
pressure change inside the drum, and was recorded as a
biphasic wave with an initial positive or negative
pressure change. We used this initial peak pressure
deflection as a marker of the start of the pharyngeal
phase of a swallow because to protect the larynx, the
hyoid and larynx need to elevate and move anteriorly
(1517). Thus, the initial movement of the hyoid was
felt to be an appropriate marker of the time at which
airflow is halted for the passage of a bolus. At the
beginning of each feeding session, recordings of such
swallows were confirmed visually. Respiratory effort
was monitored via a drum (15 mm diameter) taped in
the midline at the thoraco-abdominal junction (14). As
defined by Tarrant et al. (18), this measure relates to the
changes in lung inflation as measured by chest and
abdominal movements. This approach was selected for
three primary reasons. First, many of our preterm
subjects were receiving oxygen via a nasal cannula.
As such, any measure relying on nasal airflow to
monitor respiration could not be consistently done.
Second, the placement of a nasal thermistor interfered
with the work of breathing for infants who were fed
through a naso-gastric tube. Third, we were concerned
that the placement of another piece of equipment to
their face, in addition to a naso- or oro-gastric tube and
nasal cannula, would impose additional stress. Although
the monitoring of respiratory effort may not provide
reliable measures such as tidal volume, it does reliably
monitor the changes in chest expansion during respiration.
Oral feeding outcomes
Sucking and swallowing measures were computed from
an average of 2 sucking bursts occurring within the first
and last 2 min of the monitored sessions to account for
performance decreases as the infant fatigued. A
weighted average was used based on [T1(B1)
T2(B2)]/[T1 T2], with T1, T2 corresponding to the
duration of the respective sucking bursts and B1, B2
the average of a particular measure within the respective bursts. Sucking bursts were delineated by
periods of pause (no sucking) >1.5 s. The bursts to be

Oral feeding and the preterm infant

ACTA PDIATR 92 (2003)

723

Fig. 1. Schematic representation of swallow-respiratory interfacings. Position 1: swallow (Sw) at start of inspiration/end expiration; position
2: Sw during inhalation; position 3: Sw at end of inspiration/start expiration; position 4: Sw during exhalation; position 5: Sw interrupting
inspiration; position 6: Sw episodes when respiration is stopped for 2 s (apneic swallow run).

analyzed were selected on the basis that their duration

and stage of sucking were representative of all the
sucking bursts occurring during those two time periods.
The following variables were calculated: rate of milk
transfer (ml/min) over the entire feeding session,
average bolus size (ml/swallow), average suction
amplitude (mm Hg), sucking frequency (number of
sucking/min), and swallowing frequency (number of
swallows/min). Average bolus size (ml/swallow) was
calculated from readings taken from the graduated milk
reservoir every 1 to 2 min. Insofar as a sucking burst
rarely lasted in the minute range in preterm infants, this
measure was calculated from the readings taken closest
in time to the sucking bursts being analyzed. The
volume thus measured was divided by the number of
swallows during that same time period. Sucking
frequency consisted of the rate of suction/expression
or expression depending upon whether the infants used
the mature or immature sucking pattern, respectively.
The six swallow-respiration interfacings we defined
for this study are presented in Fig. 1. Owing to the
limitations of our methodology, we are equating start of
inspiration with end of expiration and end expiration
with start of inspiration. This categorization primarily
aims at identifying high/low lung volume and presence/

absence of airflow. Apneic swallow runs were defined

as swallows occurring when respiration stopped for
2 s. The start of the pharyngeal phase of a swallow
was defined by the first pressure peak change recorded
from the swallow drum. The phases of the respiratory
cycle when this occurred defined the swallow-respiration interfacings. Pharyngeal swallows may begin at the
start of inspiration/end expiration, at the end of
inspiration/start of expiration, at any time during the
inspiratory and expiratory phases, when a swallow
interrupted the inspiratory phase, and during apneic
swallow runs. The rate of occurrence of each swallowrespiration interfacing was calculated also based on a
weighted average as described above.
Data analyses
A paired t-test was used to compare the following
measures within groups at the two time periods: rate of
milk transfer, average bolus size, suction amplitude,
sucking and swallowing frequency. To compare the
performance between preterm and full-term infants, the
independent t-test was used. Regression analyses were
used to assess the correlation existing between the
various oral-feeding outcomes. The Friedman test was

Table 1. Characteristics of subjects.

N
M/F
Gestational age (wk)*
Birthweight (g)
Oral feeding introduction (d)
(pma)
Postnatal days at T1
(pma)
Postnatal days at T2
(pma)
*Mean  SD (range).

Full-term

Preterm

8
4/4
39.1  1.1 (3740)
3564  568 (26424603)
Birth
()
6.5  3.3
()
20.6  6.5
()

12
6/6
26.8  2.7 (2629)
1019  18 (7271340)
42  9
(33.6  1.1)
44.6  9.8
(34.0  1.2)
63.6  12.5
(36.7  1.8)

724

C Lau et al.

ACTA PDIATR 92 (2003)

Table 2. Rate of milk transfer, average bolus size, and suction amplitude of preterm and full-term infants.
Preterm (T1)
Rate of milk transfer (ml/min)
Average bolus size (ml)
Suction amplitude (mmHg)

2.3  0.9
0.12  0.06
28.0  23.8d
a

Preterm (T2)

Full-term (1st wk) Full-term (>2 wk) Preterm combined Full-term combined

4.2  1.6
0.15  0.07
69.2  61d,e

a,b

7.1  1.3b
0.20  0.07
130  34.1e

7.0  4.0
0.24  0.08
107.3  47.3

3.3  1.6c
0.14  0.06c
53  54c

7.0  2.9c
0.22  0.07c
118  42c

p-values between symbols: d p < 0.05; a,b p < 0.01; c,e p < 0.001.

used to determine whether the percentage occurrence of

swallow-respiration interfacings was a random event for
each group of infants at each time period. The Wilcoxon
signed rank test was used to test for significance
between interfacings within group and time.

Results
Characteristics of preterm and full-term infants are
presented in Table 1. The average rate of milk transfer
over the two time points (combined) was significantly
lower in the preterm than in the full-term infants (Table
2). In addition, an increase over time was observed
within the preterm but not the full-term group. Preterm
infants had significantly smaller bolus size than their
full-term counterparts (Table 2). The average bolus size
was similar within groups. The suction amplitude
averaged over time was significantly lower in the
preterm vs. the full-term group. As with the rate of
transfer, preterm infants demonstrated a significant
increase over time in suction amplitude, whereas their
full-term counterparts did not (Table 2).
Insofar as sucking and swallowing frequencies were
similar within groups, these measures were averaged
over the two time points for each group. Preterm infants
demonstrated lower frequencies than the full-term
infants for both measures (Table 3). There was a 1:1
suck:swallow ratio in both groups at both time periods.
The average bolus size and swallowing frequency were
significantly correlated with rate of milk transfer at both
time periods in preterm infants (p  0.001; r = 0.63 and
0.81, respectively). Average bolus size was not correlated with swallowing or sucking frequency
(p > 0.436). However, at both time points, there was a
significant relationship between average bolus size and
Table 3. Sucking and swallowing frequencies of preterm and fullterm infants.

Preterm (12 PO/d)

Preterm (68 PO/d)
Full-term (<2 wk)
Full-term (>2 wk)
Preterm (combined)
Full-term (combined)

Sucking frequency
(#/min)

Swallowing frequency
(#/min)

45  10
51  18
62  12
57  13
48  14*
59  12

41  11
49  16
56  18
55  13
45  14*
55  15

* p < 0.01 vs. full-term (combined).

suction amplitude (p  0.03, r = 0.73 and 0.27, respectively) and between swallowing and sucking frequency
(p < 0.001; r = 0.77).
The percentage rate of occurrence of each swallowrespiration interfacing for each group of infants was not
a random event (p  0.01). Table 4 shows the interfacings as they occurred in decreasing order of frequency
for each group of infants at each time period. For the
preterm infants, the occurrence of apneic swallow runs
was significantly more frequent than swallowing during
the other phases of respiration. When the infants
progressed to 68 oral feedings/d, the order of such
occurrence remained similar, but the occurrence of
apneic swallow runs and swallowing during inhalation
was no longer significant. For full-term infants, the
percentage rate of occurrence of swallow-respiration
interfacing was different from that of preterm infants.
During the two time points monitored, the patterns were
similar with the exception of the apneic swallow runs.
As they matured, these infants relied less on apneic
swallow runs. During their first week of life, the
percentage occurrence of apneic swallow runs was not
significantly different from swallows at the start and end
of inspiration (p = 0.059), but the rate of occurrence was
different from swallows that occurred during inhalation,
exhalation and interruption of inspiration. However,
this difference was no longer prominent by 24 wk of
age.

Discussion
We observed that increased rate of milk transfer over
time in the preterm infants was significantly correlated
with average bolus size and swallowing frequency, thus
confirming our hypothesis. The increased bolus size
may be indicative of improved adaptability of the
swallowing process with maturity, i.e. the infants were
able to swallow larger volumes and/or the improved
efficacy of their sucking skills allowed for an increased
volume per suck. The latter is supported by the
significant correlation existing between suction amplitude and bolus size and the increased use of suction/
expression with age observed in earlier studies (12).
The increase in swallowing frequency may result from
the maturation of the swallowing reflex, i.e. swallowing
occurred more swiftly as a result of improved coordination of the swallowing musculature. It has been
hypothesized that oral feeding is optimal when a 1:1:1

Oral feeding and the preterm infant

ACTA PDIATR 92 (2003)

725

Table 4. Ranking of the percentage occurrence of the swallow-respiration interfacings in decreasing order of frequency.

Apneic swallow run

(37.2  24.8)
Start inspiration/end expiration
(35.9  22.9)
End inspiration/start expiration
(12.2  9.6)
Inhalationb
(8.7  8.4)
Exhalationb
(3.6  6.1)
Interrupt inspirationb
(2.3  3.6)

>2 wk

! !

Apneic swallow run

(45.5  30)
Inhalation
(22.8  18.3)
Start inspiration/end expiration**
(14.4  18.6)
End inspiration/start expiration**
(13.5  8.7)
Exhalation**
(2.0  4.0)
Interrupt inspiration**
(1.7  2.8)

Apneic swallow run

(52.6  24.7)a
Inhalation*
(21.0  12.7)
Start inspiration/end expiration*
(10.6  10.5)
!
End inspiration/start expiration*
(8.1  8.2)
!
Interrupt inspiration*
(4.6  6.3)
Exhalation*
(3.1  5.6)

Full-term Infants
1st wk

68 oral feedings/d

Preterm Infants
12 oral feedings/d

Start inspiration/end expiration

(33.8  20.1)
End inspiration/start expiration
(23.2  12.9)
Inhalation
(19.4  11.2)
Apneic swallow run
(13.4  11.6)
Exhalation
(6.6  7.4)
Interrupt inspiration
(3.6  6.2)

Mean  SD vs apneic swallow run. b p = 0.036. * p 0.02. ** p  0.05.

or 2:2:1 ratio of suck, swallow, and respiration pattern is

attained (1921). In the present study, the significant
correlation between sucking and swallowing frequencies and their 1:1 ratio suggest that a stable pattern of
coordination had been reached between these two
parameters early on when preterm infants were using
primarily the immature sucking pattern consisting of
expression without suction. This would imply that the
first half of the suck-swallow-breathe relationship was
already attained by the time the infants were introduced
to oral feeding.
The observations made on the swallow-respiration
interfacings show that although infants swallow at all
phases of respiration (13), when full-term and preterm
infants were introduced to oral feeding, swallows
occurred most commonly during apneic swallow runs.
This corroborates the observations made by other
investigators (5, 7, 9, 22). However, with experience
and/or maturation, coordination improves, as reflected
by the decrease in apneic swallow runs observed in both
populations of infants (22). By 68 oral feedings/d,
although still favoring apneic swallow runs, preterm
infants shifted to swallowing more during the inspiratory phase, suggesting improvement in their ability to
breathe and feed orally at the same time. Apneic
swallow runs aside, full-term infants swallowed preferentially at the start of inspiration/end expiration (at
low lung volume), then at end of inspiration/start
expiration (at high lung volume), and during the
inspiratory phase. This is unlike adults, who swallow
primarily during exhalation (23). In studies of full-term
infants it has been observed that swallows occur during
inspiration as well as expiration (2426). This apparent
discrepancy may be due to the different methods used in
monitoring swallowing and respiration. Insofar as we
used the same methodology to monitor these parameters
in both groups of infants, our observation that preterm
infants do not swallow at the same phase of the
respiratory cycle as their full-term counterparts remains
valid.

Preterm infants, excluding apneic swallow runs and

in decreasing order of frequency, primarily favored
swallowing during the inspiratory phase, at the start of
inspiration/end expiration, and at end of inspiration/start
expiration. The following explanation is offered to
clarify these events. First, two premises are advanced.
The passage of a bolus from the oral cavity to the
esophagus will follow preferentially the safest path so
as to minimize the risk of aspiration and/or the path of
least resistance in order to conserve energy. As such, the
safest time to swallow would be when there is no
airflow, i.e. at beginning/end of inspiration or beginning/end of expiration. The path of least resistance
would be at a time when the pressure gradient in the
pharyngeal-esophageal region is the lowest. Indeed, to
propel a bolus, an intra-bolus pressure, i.e. the pressure
needed to transport a bolus, needs to be generated by the
aboral piston-like movement of the base of the tongue
(27). Hypopharyngeal contractions that follow the
pharyngeal passage of the bolus are essential in forming
a head of pressure to propel the bolus past the upper
esophageal sphincter (28, 29). Thus, the transport of a
bolus would be facilitated if the pressure gradient in the
pharyngeal-esophageal segment were decreased. Kawasaki and Ogura (29) observed consistently higher
values of this gradient during the expiratory than
inspiratory phase in dogs (60130 cm H2O vs. 5
25 cm H2O, respectively). This is primarily due to the
greater pharyngeal pressure present during expiration
than inspiration. In a similar manner, it is speculated
that this pressure gradient would be greatest when lung
volume is at its highest, i.e. at the end of inspiration/start
expiration, and lowest when lung volume is at its
lowest, i.e. at the beginning of inspiration/end expiration. Therefore, a greater effort would be required to
propel a bolus during expiration and at high lung
volume than during inspiration and at low lung volume.
As preterm infants generate weaker intra-bolus pressures (30), it would be expected that swallowing would
occur preferentially at the lowest lung volume, when

726

C Lau et al.

there is no airflow, when the pharyngeal-esophageal

pressure gradient (i.e. during inhalation) and/or intrathoracic pressure (17) are at their lowest. It is
conceivable also that the suction of air into the lungs
occurring during inspiration may further facilitate the
passage of the bolus down the pharynx (29). This may
explain the higher incidence of aspiration observed in
preterm as compared with full-term infants. For fullterm infants with a more mature pulmonary function
and the ability to generate greater intra-bolus pressures,
swallowing would be expected to occur more frequently
when airflow is halted, with a bias favoring start of
inspiration/end expiration when lung volume is at its
lowest. It is evident that additional studies are needed to
verify the hypothesis advanced herein. The pattern of
swallow-respiratory interfacings observed in infants
may also depend upon the position in which they are
fed.
There is little understanding regarding the oral-motor
skills preterm infants need in order to feed safely and
successfully by mouth. The observations presented here
are a first step towards identifying some of these
components. Two primary elements have been identified. Oral feeding efficiency is improved by increased
bolus size and swallowing frequency. Increases in both
suction amplitude and sucking rate play a part in the
improvement of these two components. The coordination of suck-swallow-breathe that is crucial for safe oral
feeding appears to mature in two stages. Coordination
of suck-swallow already was attained when preterm
infants were introduced to oral feeding. On the other
hand, the coordination of swallow-breathe evolved
more slowly as the infants progressed with oral feeding.
Therefore, improved oral feeding performance is not
only reliant on the development of a mature sucking
pattern, but also on the ability to cope with a larger
bolus size and increased swallowing frequency. The
in-coordination of suck-swallow-breathe commonly
attributed to unsafe oral feeding is most likely the
result of the in-coordination of swallow-breathe. The
data collected in the present study provide a basis for
designing clinical assessments of preterm infants who
are having difficulty with the transition to independent
oral feeding.

Acknowledgements.We express our gratitude to P. Burns, C.

Bryant, E. Newton-Novato, and L. Schwartz for their assistance in
this study. This work was supported by grants from the National
Institute of Child Health and Human Development (R01-HD28140),
the General Clinical Research, Baylor College of Medicine/Texas
Childrens Hospital (M01-RR-00188), National Institutes of Health.
Partial funding was also provided from the USDA/ARS, Childrens
Nutrition Research, and the Department of Pediatrics, Baylor College
of Medicine. The contents of this publication do not necessarily
reflect the views or policies of the USDA, nor does mention of trade
names, commercial products, or organizations imply endorsement by
the US government.

ACTA PDIATR 92 (2003)

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