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Introduction
Oral feeding issues in preterm infants are a growing concern for neonatologists because
attainment of independent oral feeding is one of the prerequisites for hospital discharge.
With the increase in survival of infants born continuously more preterm, understanding
such issues has a certain urgency. Concerns do not pertain only to difficulties encountered
by neonatologists during the birthstay hospitalization, but also by pediatricians and
pediatric gastroenterologists who attend to long-term feeding difficulties/disorders, such
as oral feeding aversion. Indeed, greater than 40% of patients followed in feeding disorder
clinics are former preterm infants. Research over the last decade has begun to shed light on
the development of oral feeding skills in these infants as they mature, which has increased
understanding of their limited skills at varying postmenstrual ages. Such knowledge is
crucial in clinical practice insofar as expectations of these infants’ oral feeding performance
must take into account the ever-changing level of maturity of their skills.
This article focuses on the development of sucking, swallowing, and respiration (as it
pertains to oral feeding) and the coordination of these three functions. Additional factors,
separate from infant feeding skills, also are discussed because they can affect oral feeding
performance. This review examines information gathered from bottle feeding because
more extensive research has been conducted on bottle feeding than on breastfeeding.
However, in no way should bottle feeding be interpreted as favored over breastfeeding.
Respiration
Preterm infants often have respira-
tory issues, ranging from severe re-
spiratory distress syndrome, includ-
ing bronchopulmonary dysplasia,
to varying degrees of oxygen sup-
plementation early in life. How-
ever, as they mature, “healthy” pre-
term infants normally experience
decreasing episodes of oxygen de-
saturation or apnea during oral
feeding. Baseline respiratory rates
in these infants range from 40 to 60
breaths/min or 1.0 to 1.5 seconds
per respiratory cycle (inspiration/
expiration). The duration of the
swallowing event when airflow is
interrupted can range between
Figure 4. Schematic representation of: a. the independent relationship between sucking 0.35 and 0.7 seconds, as measured
and respiration during nonnutritive sucking and b. the dependency between sucking, by intrapharyngeal pressure in term
swallowing, and respiration during nutritive sucking. and preterm infants. With such re-
spiratory rates and swallow dura-
tion, little time may be left for res-
timely closure of the epiglottitis, but also of the aryepi- piration. In addition, during oral feeding, a number of
glottics and vocal folds. However, penetration and aspi- studies noted decreased minute ventilation, prolonged
ration may occur prior to swallowing because of poor expiration, and shortened inspiration, albeit no signifi-
bolus formation, during swallowing due to improper cant change in tidal volume. Thus, with all the respiratory
laryngeal closure, or after swallowing when residual alterations taking place, it is not surprising that some
pools around the valleculae and pyriform sinuses as a “healthy” preterm infants incur episodes of desaturation,
result of poor pharyngeal clearance. apnea, or bradycardia when feeding by mouth.
Infants*
Preterm Preterm
(1 to 2 oral (6 to 8 oral Term Term
feedings feedings Ad lib Ad lib Preterm Term
per day) per day) (First Week) (>2 Weeks) (Combined) (Combined)
Gestational age (wk) 26.8ⴞ2.7 — 39.1ⴞ1.1 — — —
Postnatal days (PMA) 44.6ⴞ9.8 63.6ⴞ12.5 6.5ⴞ3.3 20.6ⴞ6.5
(34.0ⴞ1.2) (36.7ⴞ1.8)
Mean bolus size (mL) 0.12ⴞ0.06 0.15ⴞ0.07 0.20ⴞ0.07 0.24ⴞ0.08 0.14ⴞ0.06a 0.22ⴞ0.07a
Sucking rate (#/min) 45ⴞ10 51ⴞ18 62ⴞ12 57ⴞ13 48ⴞ14b 59ⴞ12b
Suction Amplitude (mm Hg) ⴚ28.0ⴞ23.8 ⴚ69.2ⴞ61.0
c c,a
ⴚ130.0ⴞ34.1 ⴚ107.3ⴞ47.3 ⴚ53ⴞ54
a a
ⴚ118ⴞ42a
Swallowing rate (#/min) 41ⴞ11 49ⴞ16 56ⴞ18 55ⴞ13 45ⴞ14b 55ⴞ1b
d b,d b a
Rate of milk transfer (mL/min) 2ⴞ1 4ⴞ2 7ⴞ1 7ⴞ4 3ⴞ2 7ⴞ3a
*Mean⫾SD
PMA⫽postmenstrual age (wk)
Independent t-test, P values between symbols: aP⬍0.001; bP⬍0.01
Paired t-test, P values between symbols: cP⬍0.05; dP⬍0.01
From Lau C, Smith EO, Schanler RJ. Coordination of suck-swallow and swallow-respiration in preterm infants. Acta Paediatr. 2003;92:721–727.
performance, we observed that “healthy” preterm infants alert. However, due to their immaturity, one of the
(⬍30 weeks’ gestation) can alter their sucking pattern characteristics of preterm infants is their inability to reg-
depending on the flow rate of the bottle nipples used. ulate their states. Because they spend most of their time
From these results, we speculated that infants can modify transitioning from one state to another, some infants
their sucking skills to maintain a rate of milk transfer that cannot feed by mouth for extended periods of time.
they can handle safely or that is compatible with the level Neurobehavioral studies have proposed that an orga-
of suck-swallow-breathe coordination they have at- nized pattern of state regulation is a good indicator of an
tained. Because the studied infants were “healthy” and infant’s ability to cope with his or her environment,
medically stable, we hypothesize that their ability to particularly that of a neonatal intensive care unit. As a
modify specific sucking variables to maintain appropriate result, improvement in state regulation is interpreted as
flow rates requires the integrity of afferent sensory feed- evidence of central nervous system maturation and can
back to the sucking, swallowing, and respiratory centers be key to an infant’s ability to orally feed successfully for
in the brainstem. This concept is supported by the work an extended period of time.
of Finan and Barlow, who speculated that the sucking Behavioral organization is identified by the calmness,
motor pattern of infants is under the control of a central relaxation, and regular breathing that an infant exhibits
pattern generator that adapts to changing environmental at a particular time. Not necessarily linked to a particular
conditions via afferent sensory feedback. Craig and Lee behavioral state, this condition needs to be taken into
have proposed a similar theory, with the existence of an account when feeding infants. Feeding therapists com-
intrinsic tau-guide acting as a common process linking monly identify infants as organized when their bodies are
various forms of timing events within the motor function gently flexed, their arms are folded toward midline,
(eg, the control of sucking pressure in infants). Under hands are placed under the chin, and there are no facial
such conditions, oral feeding can be successful if the adverse expressions (eg, grimace). It is under these cir-
infants are allowed to regulate their own milk flow. cumstances that oral feeding is best achieved, likely be-
cause infants, in the absence of any additional stimula-
tion, can focus on the task at hand. Thus, behavioral state
Infant’s Condition(s)
and organization can affect significantly the ability of a
Medical Condition(s)
preterm infant to feed by mouth.
Oral feeding safety and success is not solely dependent on
an infant’s oral feeding skills. Indeed, it may be disrupted
Developmental Care Program
by fluid penetration or aspiration into the larynx caused
Given the type of stimulations that preterm infants expe-
by unrelated factors, such as gastrointestinal immaturity
rience in nurseries, debate has arisen regarding the ap-
or the infant’s behavioral state and organization at the
propriate stimulations that such infants should receive.
time of the feedings. Fluid backflow into the larynx may
Caretakers have long recognized different types of sen-
occur not only as a result of pooling at the level of the
sory stimulations. Some provided during routine nursing
valleculae and pyriform sinuses resulting from poor pha-
care are aversive (eg, venipuncture, heelsticks, suction-
ryngeal clearance, but also as a result of improper timing
ing) and “impersonal” (eg, regular diaper changes, tem-
of the relaxation or constriction of the upper or lower
perature monitoring, positioning). Others, often pro-
esophageal sphincters, gastroesophageal reflux, im-
vided by parents, are calming and soothing (eg, holding,
proper esophageal motility, or delayed gastric emptying.
stroking, or rubbing). To address these issues, two dif-
Because these different aspects of gastrointestinal imma-
ferent approaches are taken. The first reduces or limits
turity are addressed in other articles in this issue, only the
the aversive stimulations occurring in nurseries and the
infant’s behavioral state and organization and environ-
second provides additional stimulations that benefit the
mental factors are discussed here.
infants.
The establishment of developmental care programs
Behavioral State and Organization primarily led by nursing staff focuses on the first ap-
The National Neonatal Individualized Developmental proach. For example, effort is made to cluster care or to
Care and Assessment Program (NIDCAP) distinguishes carry out painful procedures within a specific time of the
six levels of state organization: quiet sleep, active sleep, day rather than throughout the day. The light in nurser-
drowsiness, quiet alert, active alert, and crying/fussing. ies is dimmed, isolette covers are used to reduce back-
Based on this classification, the optimal states for oral ground light and noise, and containment methods (eg,
feeding appear to be drowsiness and quiet and active swaddling) are used as calming interventions. The sec-
ond approach focuses on providing supplemental stimu- ment. Under such a program, caretakers must become
lations to counterbalance the negative effect(s) of the cognizant of all aspects of their patient’s limitations and
immediate adversities and the developmental deficits as- “adjust” their feeding approach accordingly. Table 3
sociated with prematurity, such as skin-to-skin holding. shows some of the facts and recommendations we pro-
pose.
Caretaker’s Oral Feeding Approach
Currently, when infants are deemed ready to feed orally,
an important sign of success is completion of their feed- Summary
ings (ie, the ability to take the volume prescribed within From our studies on nutritive sucking, we observed that
an allotted period of time), which is key to advancement the mature sucking pattern is not necessary for safe and
of oral feeding and earlier attainment of independent oral successful oral feeding. Readiness to feed orally should
feeding. Under such pressure, caretakers often inappro- not be based only on sucking skills, but rather on the
priately “encourage” infants to finish their feeding no coordination of sucking, swallowing, and respiration.
matter what the consequences (eg, choking, fatigue, Because the various skills implicated in oral feeding ma-
emesis). We speculate that the high occurrence of oral ture at different times, it is speculated that neurologically
feeding aversion observed in nurseries and following intact “healthy” infants can coordinate these three func-
discharge may result from such technique. Conse- tions if allowed to regulate and control their own feed-
quently, we have proposed a developmental oral feeding ing. In addition, oral feeding performance does not
approach that, most importantly, takes into consider- depend only on oral motor skills but also on the infant
ation the limitations of these infants. In brief, infants are behavioral state and organization and his or her environ-
advanced in their daily oral feedings only if they do not ment. It is essential, therefore, that all these factors be
demonstrate any adverse events or aversive behavior. taken into consideration when weaning an infant from
Completion of feedings is not a requirement for advance- tube feeding.
Suggested Reading blood levels of gastrin, motilin, insulin and insulin-like growth
Als H. A synactive model of neonatal behavior organization: frame- factor 1 in premature infants receiving enteral feedings. Acta
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neonatal intensive care environment. Phys Occup Ther Pediatr. sucking, and swallowing during bottle feedings in human in-
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NeoReviews Quiz
5. For preterm infants, readiness to feed orally depends on the maturation of sucking, swallowing, and
respiration and the coordination of these activities. Of the following, the postmenstrual age at which
preterm infants who have stable cardiopulmonary status and no neurologic abnormalities are likely to be
introduced to oral feeding is closest to:
A. 28 weeks.
B. 30 weeks.
C. 32 weeks.
D. 34 weeks.
E. 36 weeks.
6. Sucking includes a nutritive component in which milk is ingested from the breast or the bottle and a non-
nutritive component in which no milk intake is involved. Of the following, the most accurate statement
regarding non-nutritive sucking in preterm infants is that it:
A. Enhances the infant’s behavioral state and organization.
B. Increases the circulating levels of gastrointestinal hormones.
C. Is a good index of the infant’s readiness to feed by mouth.
D. Retards gastrointestinal motility.
E. Slows the transition from gavage to oral feeding.