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Acta Pñdiatr 92: 721±727.


Coordination of suck-swallow and swallow respiration in preterm
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; Children’s 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 Pædiatr 2006; 92: 721–727. 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 1–2 oral feedings/d) and at 6–8
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
Key words: Bottle feeding, nutritive sucking, oral feeding, prematurity, suck-swallow-breathe
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.

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 infant’s 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
(5–10). 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

milk flowed only when the infant was sucking. T2 corresponding to the duration of the respective sucking bursts and B1. This interaction between swallow and respiration has received little attention. Oral feeding was introduced at the discretion of the attending physician.e. The level of milk from a graduated reservoir was continuously adjusted to the level of the infant’s mouth to allow for a self-paced flow. were recruited from the nurseries at Texas Children’s Hospital.e. As such.5 s. in addition to a naso. First. Inasmuch as the nipple chamber was continuously filled. 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. At the beginning of each feeding session. sucking. necrotizing enterocolitis. (18). 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. born between 26 and 29 wk of gestation and appropriate for gestational age as determined by maternal dates and antenatal ultrasonography. Suck-swallow-breathe assessment Because one of our primary goals was to observe feedings as naturally as possible. 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. This approach was selected for three primary reasons. All the infants were offered the type of milk they were receiving normally. chronic lung disease. The two components of sucking. Respiratory effort was monitored via a drum (15 mm diameter) taped in the midline at the thoraco-abdominal junction (14). and was recorded as a biphasic wave with an initial positive or negative pressure change. Full-term infants were followed during their first week and again between 2 to 4 wk of age. Preterm infants were assessed at introduction of oral feeding. As defined by Tarrant et al. any measure relying on nasal airflow to monitor respiration could not be consistently done. Study design The oral feeding performance of infants was monitored in function of rate of milk transfer. The preterm infants (6M. and respiration. Preterm infants swallow at all phases of the respiratory cycle during non-nutritive sucking (13). 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. we allowed the ACTA PÆDIATR 92 (2003) caretakers to select the bottle nipple and determine when to pause for a feeding. major congenital anomalies. Thus. Although the monitoring of respiratory effort may not provide reliable measures such as tidal volume. swallowing. e. that may lead to respiratory imbalance during feeding is the phase of the respiratory cycle when swallowing occurs (5). The preterm infants were treated prophylactically with caffeine citrate until mature control of breathing was demonstrated. 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. i.722 C Lau et al. However. generally no apnea/bradycardia for >2 wk. many of our preterm subjects were receiving oxygen via a nasal cannula. Infants with the following conditions were excluded from the study: intraventricular hemorrhage grades III and IV. 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. with T1. we were concerned that the placement of another piece of equipment to their face. Swallowing was monitored via a small drum held snugly onto the hyoid region as described previously (14). In this study. hydrocephalus. suction and expression. A weighted average was used based on [T1(B1) ‡ T2(B2)]/[T1 ‡ T2]. The bursts to be .g. along with swallowing and respiration were monitored simultaneously (14). These infants were fed ad libitum. Second. 6F). B2 the average of a particular measure within the respective bursts. No encouragement was provided. the hyoid and larynx need to elevate and move anteriorly (15–17). the placement of a nasal thermistor interfered with the work of breathing for infants who were fed through a naso-gastric tube. this measure relates to the changes in lung inflation as measured by chest and abdominal movements. the subjects were able to obtain milk regardless of whether the suction and/or expression component was used (1). when taking 1–2 oral feedings/d and when they reached independent oral feeding (6–8 oral feedings/d). i. Sucking bursts were delineated by periods of pause (no sucking) >1. mother’s milk or preterm formula. recordings of such swallows were confirmed visually. it is unclear when swallowing occurs during nutritive sucking. Third. Swallowing caused an upward movement of the hyoid bone resulting in a pressure change inside the drum. Methods Subjects Twelve “healthy” preterm and 8 full-term infants were studied.or oro-gastric tube and nasal cannula. would impose additional stress. The full-term neonates were healthy and were introduced to oral feeding immediately after birth. it does reliably monitor the changes in chest expansion during respiration.

Regression analyses were used to assess the correlation existing between the various oral-feeding outcomes.8  2. Data analyses A paired t-test was used to compare the following measures within groups at the two time periods: rate of milk transfer.7  1. Sucking frequency consisted of the rate of suction/expression or expression depending upon whether the infants used the mature or immature sucking pattern. The six swallow-respiration interfacings we defined for this study are presented in Fig. Pharyngeal swallows may begin at the start of inspiration/end expiration. The Friedman test was Table 1. sucking frequency (number of sucking/min). Apneic swallow runs were defined as swallows occurring when respiration stopped for 2 s.6  9. we are equating start of inspiration with end of expiration and end expiration with start of inspiration. Insofar as a sucking burst rarely lasted in the minute range in preterm infants. sucking and swallowing frequency. 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. Full-term Preterm 8 4/4 39. The start of the pharyngeal phase of a swallow was defined by the first pressure peak change recorded from the swallow drum. position 4: Sw during exhalation. position 3: Sw at end of inspiration/start expiration. Characteristics of subjects.1  1. suction amplitude. and swallowing frequency (number of swallows/min). position 2: Sw during inhalation.1 (37–40) 3564  568 (2642–4603) Birth (–) 6.6  1.5  3. at the end of inspiration/start of expiration. position 6: Sw episodes when respiration is stopped for 2 s (apneic swallow run). respectively.6  6. the independent t-test was used.1) 44.6  12.8 (34. This categorization primarily aims at identifying high/low lung volume and presence/ absence of airflow. when a swallow interrupted the inspiratory phase. Schematic representation of swallow-respiratory interfacings.8) . The volume thus measured was divided by the number of swallows during that same time period. average bolus size (ml/swallow). at any time during the inspiratory and expiratory phases. Owing to the limitations of our methodology. Position 1: swallow (Sw) at start of inspiration/end expiration. The following variables were calculated: rate of milk transfer (ml/min) over the entire feeding session.5 (–) 12 6/6 26. Average bolus size (ml/swallow) was calculated from readings taken from the graduated milk reservoir every 1 to 2 min.Oral feeding and the preterm infant ACTA PÆDIATR 92 (2003) 723 Fig.2) 63. this measure was calculated from the readings taken closest in time to the sucking bursts being analyzed. To compare the performance between preterm and full-term infants. 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). The rate of occurrence of each swallowrespiration interfacing was calculated also based on a weighted average as described above.3 (–) 20.7 (26–29) 1019  18 (727–1340) 42  9 (33. and during apneic swallow runs.5 (36. The phases of the respiratory cycle when this occurred defined the swallow-respiration interfacings. 1. 1.0  1. average bolus size. position 5: Sw interrupting inspiration. average suction amplitude (mm Hg).

respectively) and between swallowing and sucking frequency (p < 0. Rate of milk transfer. Preterm (1–2 PO/d) Preterm (6–8 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. the order of such occurrence remained similar. the occurrence of apneic swallow runs was significantly more frequent than swallowing during the other phases of respiration.b 7. The increased bolus size may be indicative of improved adaptability of the swallowing process with maturity. the full-term group.20  0.b p < 0. i. the infants were able to swallow larger volumes and/or the improved efficacy of their sucking skills allowed for an increased volume per suck. However. However.81.0  2. average bolus size.001. The suction amplitude averaged over time was significantly lower in the preterm vs. i. but the occurrence of apneic swallow runs and swallowing during inhalation was no longer significant.07c 118  42c p-values between symbols: d p < 0.6c 0.27.63 and 0.e. the percentage rate of occurrence of swallow-respiration interfacing was different from that of preterm infants. an increase over time was observed within the preterm but not the full-term group. r = 0. Insofar as sucking and swallowing frequencies were similar within groups. used to determine whether the percentage occurrence of swallow-respiration interfacings was a random event for each group of infants at each time period. When the infants progressed to 6–8 oral feedings/d. whereas their full-term counterparts did not (Table 2). these infants relied less on apneic swallow runs. respectively).24  0. swallowing occurred more swiftly as a result of improved coordination of the swallowing musculature.001.e p < 0.14  0. Average bolus size was not correlated with swallowing or sucking frequency (p > 0. In addition. Preterm infants had significantly smaller bolus size than their full-term counterparts (Table 2).1  1. c. but the rate of occurrence was different from swallows that occurred during inhalation. During their first week of life.436).0  4.08 107. Preterm (T1) Rate of milk transfer (ml/min) Average bolus size (ml) Suction amplitude (mmHg) 2. this difference was no longer prominent by 2–4 wk of age. at both time points.3  1.1e 7.07 130  34. Results Characteristics of preterm and full-term infants are presented in Table 1. The percentage rate of occurrence of each swallowrespiration interfacing for each group of infants was not a random event (p  0. For the preterm infants. 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 (1–2). The average bolus size was similar within groups. exhalation and interruption of inspiration.6 0. Sucking and swallowing frequencies of preterm and fullterm infants. full-term (combined).2  1. It has been hypothesized that oral feeding is optimal when a 1:1:1 . ACTA PÆDIATR 92 (2003) Table 2.12  0. r = 0.01). There was a 1:1 suck:swallow ratio in both groups at both time periods.73 and 0. As with the rate of transfer. The average bolus size and swallowing frequency were significantly correlated with rate of milk transfer at both time periods in preterm infants (p  0.e a.8d a Preterm (T2) Full-term (1st wk) Full-term (>2 wk) Preterm combined Full-term combined 4. The Wilcoxon signed rank test was used to test for significance between interfacings within group and time.3  0.06c 53  54c 7.15  0. 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). the percentage occurrence of apneic swallow runs was not significantly different from swallows at the start and end of inspiration (p = 0.3b 0.e.9 0.01 vs.77).07 69. a. preterm infants demonstrated a significant increase over time in suction amplitude.724 C Lau et al.059). 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. The increase in swallowing frequency may result from the maturation of the swallowing reflex. For full-term infants. thus confirming our hypothesis.001.0  23.3  47.3 3. these measures were averaged over the two time points for each group.0 0. the patterns were similar with the exception of the apneic swallow runs.2  61d.9c 0. and suction amplitude of preterm and full-term infants. Table 4 shows the interfacings as they occurred in decreasing order of frequency for each group of infants at each time period. During the two time points monitored.22  0.05.01. As they matured. there was a significant relationship between average bolus size and Table 3.03. suction amplitude (p  0. Preterm infants demonstrated lower frequencies than the full-term infants for both measures (Table 3). r = 0.06 28.

2) Mean  SD vs apneic swallow run.8  20. needs to be generated by the aboral piston-like movement of the base of the tongue (27). with experience and/or maturation.1  8.3  3. As preterm infants generate weaker intra-bolus pressures (30).1) Interrupt inspirationb (2. the transport of a bolus would be facilitated if the pressure gradient in the pharyngeal-esophageal segment were decreased. the pressure needed to transport a bolus. The following explanation is offered to clarify these events. This apparent discrepancy may be due to the different methods used in monitoring swallowing and respiration. This is unlike adults. b p = 0.9) End inspiration/start expiration (12.e.7  2.8  18.7) Start inspiration/end expiration* (10. a Apneic swallow run (37.3) Exhalation* (3.1) End inspiration/start expiration (23.6) End inspiration/start expiration** (13.4  11. the safest time to swallow would be when there is no airflow.e. suggesting improvement in their ability to breathe and feed orally at the same time. Insofar as we used the same methodology to monitor these parameters in both groups of infants. 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. 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. However.5  8. 22). two premises are advanced.6) Inhalationb (8. it would be expected that swallowing would occur preferentially at the lowest lung volume. then at end of inspiration/start expiration (at high lung volume).e. i. or 2:2:1 ratio of suck. First. i. In studies of full-term infants it has been observed that swallows occur during inspiration as well as expiration (24–26). By 6–8 oral feedings/d.8) Start inspiration/end expiration (35. at beginning/end of inspiration or beginning/end of expiration. As such. * p 0.2  24. swallow. Preterm infants. i. an intra-bolus pressure. respectively).4  11. ** p  0.e.05. at the beginning of inspiration/end expiration. 5– 25 cm H2O.4) Interrupt inspiration (3.Oral feeding and the preterm infant ACTA PÆDIATR 92 (2003) 725 Table 4.0) Interrupt inspiration** (1. 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. to propel a bolus. Therefore.2  9. and respiration pattern is attained (19–21).7) Exhalation** (2. 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. Thus. The observations made on the swallow-respiration interfacings show that although infants swallow at all phases of respiration (13).1  5. and lowest when lung volume is at its lowest.9  22. 9. it is speculated that this pressure gradient would be greatest when lung volume is at its highest. and during the inspiratory phase. although still favoring apneic swallow runs. Kawasaki and Ogura (29) observed consistently higher values of this gradient during the expiratory than inspiratory phase in dogs (60–130 cm H2O vs.8) ! Apneic swallow run (52.036.4) Exhalationb (3. preterm infants shifted to swallowing more during the inspiratory phase. when . and at end of inspiration/start expiration.7  8.6  6.2) ! Interrupt inspiration* (4.6  6.2) Apneic swallow run (13. 7.4  18. This corroborates the observations made by other investigators (5. excluding apneic swallow runs and in decreasing order of frequency.6  6. 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 (28.6  24. primarily favored swallowing during the inspiratory phase.5) ! End inspiration/start expiration* (8.7)a Inhalation* (21. Ranking of the percentage occurrence of the swallow-respiration interfacings in decreasing order of frequency. who swallow primarily during exhalation (23).6  10. coordination improves. at the end of inspiration/start expiration. i. In the present study. 29).0  4.6) >2 wk ! ! Apneic swallow run (45.0  12. Indeed. when full-term and preterm infants were introduced to oral feeding. In a similar manner.6) Full-term Infants 1st wk 6–8 oral feedings/d ! Preterm Infants 1–2 oral feedings/d Start inspiration/end expiration (33. full-term infants swallowed preferentially at the start of inspiration/end expiration (at low lung volume). our observation that preterm infants do not swallow at the same phase of the respiratory cycle as their full-term counterparts remains valid.6) Exhalation (6. Apneic swallow runs aside.5  30) Inhalation (22.02.6  7. The path of least resistance would be at a time when the pressure gradient in the pharyngeal-esophageal region is the lowest. This is primarily due to the greater pharyngeal pressure present during expiration than inspiration.2  12. at the start of inspiration/end expiration.3) Start inspiration/end expiration** (14. as reflected by the decrease in apneic swallow runs observed in both populations of infants (22). swallows occurred most commonly during apneic swallow runs.9) Inhalation (19.

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