Journal of Perinatology (2008) 28, 247–257

r 2008 Nature Publishing Group All rights reserved. 0743-8346/08 $30

www.nature.com/jp

STATE-OF-THE-ART
Sucking and swallowing in infants and diagnostic tools
SP da Costa1, L van den Engel–Hoek2 and AF Bos3
1
Department of Speech, School of Health, Hanze University Groningen, Groningen, The Netherlands; 2Department of Paediatric
Neurology, University Medical Centre St. Radboud, Nijmegen, The Netherlands and 3Department of Paediatrics, Neonatology, Beatrix
Children’s Hospital, University Medical Centre, Groningen, The Netherlands

could be the first indication that the infant has neurological

Preterm infants often have difficulties in learning how to suckle from the problems.2 Dysphagia is common in infants suffering from cerebral
breast or how to drink from a bottle. As yet, it is unclear whether this is part palsy or other developmental deficits.
of their prematurity or whether it is caused by neurological problems. Is it Preterm infants frequently have feeding problems during their
possible to decide on the basis of how an infant learns to suckle or drink first year of life. It is unclear whether these problems are related to
whether it needs help and if so, what kind of help? In addition, can any the neurological problems these infants often exhibit later on.3
predictions be made regarding the relationship between these difficulties Preterms in need of artificial respiration have more difficulty in
and later neurodevelopmental outcome? We searched the literature for stabilizing their physiological parameters. It is unclear whether their
recent insights into the development of sucking and the factors that play a sucking and swallowing problems stem from their reaction to the
role in acquiring this skill. Our aim was to find a diagnostic tool that tubes, from their breathing difficulties or from a combination of both.
focuses on the readiness for feeding or that provides guidelines for There is an urgent need for a user-friendly, reliable and
interventions. At the same time, we searched for studies on the relationship noninvasive tool that objectively measures sucking and swallowing
between early sucking behavior and developmental outcome. It appeared movements and the coordination between sucking, swallowing and
that there is a great need for a reliable, user-friendly and noninvasive breathing. On the one hand, such a tool would be useful to
diagnostic tool to study sucking in preterm and full-term infants. determine what kinds of interventions are required to facilitate
Journal of Perinatology (2008) 28, 247–257; doi:10.1038/sj.jp.7211924; sucking and swallowing. On the other hand, some predictions
published online 17 January 2008 could be made regarding the further development of the infant. In
addition, infants could be followed up to determine if and to what
extent sucking behavior has predictive value for the infant’s
Introduction outcome at a later age.
The aim of this review is threefold. Our first aim is to find out
Oral feeding in infants should be efficient to preserve energy for
what is known about the normal developmental course of sucking
growing. Moreover, it should be safe so as to avoid aspiration, and
and swallowing during early age. Our second aim is to evaluate a
it should not jeopardize respiratory status. This can only be
number of currently available diagnostic methods that measure the
achieved provided sucking, swallowing and breathing are properly
coordination of sucking and swallowing with breathing. Finally,
coordinated. This means that the infant can suck efficiently and
our aim is to establish the prognostic value of an abnormal
that it can swallow rapidly as the boluses are formed, thus
developmental course of sucking, swallowing and breathing for the
minimizing the duration of airflow interruption. Put differently, an
infant’s later neurodevelopmental outcome.
infant’s oral feeding skills are reflected by its skill to organize and
To achieve these aims, we searched the literature on Medline
coordinate oral-motor functions efficiently so that it takes in
and CINAHL using Silver Platter and WinSPIRS. The restrictions we
enough calories to grow.1
used were AGE (All Infants). TG: Human, PT: Journal-Article,
There are several circumstances that could compromise normal
publication date: 1995–2006. This search strategy consisted of all
coordination of sucking and swallowing. Congenital or acquired
combinations of (1) Sucking Ability [Mesh] OR Sucking Behaviour
damage to the central nervous system during the neonatal period
[Mesh] AND (2) Deglutition [Mesh] AND Respiration [Mesh].
may lead to feeding difficulties, such as slow or weak sucking. It
Fifty-two articles were found in this way. On the basis of the
Correspondence: SP da Costa, School of Health, Hanze University Groningen, Merodelaan 13, titles and abstracts, we selected 25 articles for further reading. The
Groningen 9721 XB, The Netherlands. main selection criterion was the patient group. We excluded articles
E-mail: [email protected]
Received 28 June 2007; revised 29 November 2007; accepted 13 December 2007; published
on infants with cleft palate, Pierre Robin sequence and cerebral
online 17 January 2008 palsy. We included articles on preterm and full-term infants
 Sucking and swallowing
SP da Costa et al
248

without congenital anomalies. We selected a further 25 articles by feedback and suprabulbar parts of the brain. The central pattern
reviewing the references of all the articles identified. generator for sucking seems to consist of two distinct parts: (a) the
brain stem (in the nucleus tractus solitarius and the dorsal
medullar reticular formation) for motor control, and (b) parts of
The normal developmental course of the coordination of the surrounding reticular formation for sensory control.
sucking, swallowing and breathing from fetal life up to During pharyngeal swallowing, respiration is inhibited
10 weeks’ post-term centrally.7 The three parts of the cerebral cortex that are involved
Sucking and swallowing, and the brain structures involved in chewing and swallowing are the primary motor cortex, the
The sucking pattern of full-term infants is composed of the premotor cortex anterior to it and the anterior insula.8 These areas
rhythmic alternation of suction and expression. Two forms of process incoming and outgoing signals to and from the swallowing
sucking are distinguished: nutritive sucking (NS) and non- center in the brain stem. This is the case for both the reflexive and
nutritive sucking (NNS). NS is an infant’s primary means of voluntary stages of swallowing.
receiving nutrition while NNS can have a calming effect on the
infant. Moreover, NNS is regarded as an initial method for The development of sucking and swallowing from fetal age to
exploring the environment. The rate of NNS is approximately twice term age
as fast as that of NS.4–6 Both NNS and NS provide insight into an At approximately 26 days’ fetal age, the developmental trajectories
infant’s oral-motor skills. In NS however, the ability to integrate of the respiratory and swallowing systems diverge and start to
breathing with sucking and swallowing is a prerequisite for develop independently. Swallowing in fetuses has been described as
coordinated feeding. early as 12 to 14 weeks’ gestational age. A sucking response can be
During NS, fluid moves primarily due to change in pressure. provoked at 13 weeks’ postconceptional age by touching the lips.9 Real
With the oral cavity sealed, as the jaw and tongue drop down, the sucking, defined by a posterior–anterior movement of the tongue, in
cavity is enlarged. This enlargement creates negative intraoral which the posterior movement is dominant, begins at 18 to 24 weeks’
pressure, suction, which draws fluid into the mouth and propels postconceptional age.10 Between 26 and 29 weeks’ gestational age,
the expressed fluid backwards toward the pharynx for the swallow. there is probably no significant further maturation of sucking.6,11
Jaw and tongue movements are also involved in the propulsion of By week 34, most healthy fetuses can suck and swallow well
the fluid. As the tongue compresses the nipple, sufficient positive enough to sustain nutritional needs via the oral route, if born at
pressure, compression, is created by the jaw and the front part of this early age. Sucking movements increase in frequency during
the tongue pressing the nipple against the hard palate to draw the the final weeks of fetal life. This is accompanied by an increase in
fluid from the nipple. The tongue plays a key role in all aspects of amniotic fluid swallowed by a fetus during pregnancy from initially
sucking by helping to seal the oral cavity. It does so, anterior, in 2 to 7 ml a day to 450 ml a day. This is approximately half of the
conjunction with the lower lip, and posterior, by sealing against the total volume of amniotic fluid at term.8,12,13
soft palate during swallowing. In addition, the tongue stabilizes the
lower jaw and transports the bolus to the pharynx. The jaw The development of sucking and swallowing from birth at term
provides a stable base for movements of the tongue, lips and up to the first months of life
cheeks. The normal maturation of sucking and swallowing during the first
The next phase is pharyngeal. Swallowing is elicited involuntary months of life after full-term birth can be summarized by
by afferent feedback from the oral cavity and has a duration of increased sucking and swallowing rates, longer sucking bursts and
approximately 530 ms. It depends on a critical volume of fluid, larger volumes per suck.6,14–17 The skill of safe and efficient oral
gathered in the valleculae. To initiate and modify the swallow, the feeding is based on oral-motor competence, neurobehavioral
pharynx and larynx are richly supplied with chemoreceptors, slow- organization and gastro-intestinal maturity.18 It is important that
adapting stretch and pressure receptors and temperature receptors. the behavioral states are well controlled, that the airway is patent
Effective sucking requires coordination of both the swallowing and that the overall cardiorespiratory activity is stable.19 Internal
and breathing processes in which many brain structures are factors that influence the normal development of sucking and
involved, including cranial nerves, brain stem areas and cortical swallowing patterns are the infant’s state of health, his oral feeding
areas. The rhythmic processes involved in NS are under maturing experience, the ability to regulate oxygen, development of alertness
bulbar control, especially in the regions of the nuclei ambiguus, and sucking strength and the organization of the sucking pattern.
solitarius and hypoglossus in the lower medulla. Efferent and External factors are size and speed of milk flow, the impact of
afferent cranial nerves (N V, VII, IX, X and XII) are involved in nasogastric tubes in place during feeding and the type of feeding
deglutition (which includes mastication, respiration and support provided by the caregiver.1
swallowing). These movements are considered to be under the Normal infants are able to adapt to varying environments. They
control of central pattern generators and are controlled by sensory are able to distinguish differences in fluctuations of milk flow,

Journal of Perinatology
 Sucking and swallowing
SP da Costa et al
249

nipple hole, taste and temperature, and they can adapt their interruption.22 In full-term infants, the coordination between
sucking behavior to these variations.17 breathing and swallowing develops and matures during the first
month of life.16
Rhythmicity. The underlying rhythms of sucking and swallowing In general, swallowing rhythm is maintained at the expense of
follow quantifiable, predictable maturational patterns that correlate functional and rhythmic respiration, even in full-term infants.25
with postmenstrual age (PMA). From this point of view, it is likely Deviations from these patterns can be predictive of feeding,
that these behavioral patterns are congenital rather than respiratory and neurodevelopment disorders.25 Various studies
acquired.20 However, the rhythmicity of the suck–swallow–breath demonstrated that sucking and swallowing influence the normal
relationship depends also on nonmaturational factors, such as pattern of breathing: it decreased inspiratory time, decreased
satiety, behavioral state and milk flow. Milk flow depends on the respiratory frequency, decreased minute ventilation and decreased
hole size of the nipple (bottle feeding), the milk ejection reflex (in tidal volume.25,26 This is important in pathological circumstances
breastfeeding), but it also depends on the infant. Within certain when breathing is compromised.
ranges the infant can autoregulate milk flow by changing the Studies of the coordination between sucking, swallowing and
suction pressure and frequency.17,21 breathing show the following possibilities: a swallow could be
Rhythmic stability can be expressed in a measure used by preceded by inspiration, expiration or apnea and could be followed
Gewolb et al.,20,22 the coefficient of variation. The coefficient of by inspiration, expiration or apnea, yielding nine possible
variation is the standard deviation of the intervals between two relationships.21 Sixty percentage of full-term neonates have an
processes (such as swallow–swallow, suck–suck, suck–swallow) inspiration–swallow–expiration (I–S–E) or an expiration–
divided by the mean interval between these processes. It is swallow–inspiration (E–S–I) relationship. Swallows followed by
independent of the number of sucking movements per swallow. expiration would be safer because any milk remaining in the
A low coefficient of variation indicates that the rhythm is normal. pharynx would be cleared before the next inspiration. Besides, it is
The higher the coefficient of variation, the more variable the most efficient to swallow after inspiration because then pharyngeal
rhythm. The rhythmic stability of sucking and swallowing changes pressure is at its highest.15 The optimal pattern in nutritive feeding
during the first month of life, both individually and interactively. thus seems to be I–S–E.
The biorhythms of sucking and swallowing follow a predictable Whether breast-fed or bottle-fed with expressed breast milk,
maturational pattern (stabilization of sucking rhythmicity, more infants show a significantly higher breathing rate than when
sucking movements and swallows in bursts and quicker and longer receiving other liquids. Coordination between swallowing and
sucking bursts). This stabilization correlates more with PMA than breathing could improve with breast milk.27
with postnatal age.20 The studies by Gewolb et al.20 show that
rhythm is an integrated part of maturation. Quereshi et al.16 expand Special considerations on the development of sucking and
on this theme by explaining that the changes observed at 1 month of swallowing in preterm infants
age may be an adaptation of the drinking pattern to include volition, When describing the normal development of the preterm infant,
with longer sequences and a larger number of sucking movements. one is in fact describing an abnormal situation: a preterm infant
It would seem, therefore, that these rhythms follow a reasonably develops in an extrauterine environment while intrauterine
predictable maturational pattern and that disturbance of this development would be normal. This complicates the matter of
maturation could be an important diagnostic clue. distinguishing between normal and abnormal development of
sucking and swallowing. Which aspects of the development of
Interaction with breathing. Feeding activity appears to override sucking and swallowing in the preterm infant are deviant and what
normal ventilatory chemoreceptor control mechanisms23 and the is part of normal maturation? With this in mind, we would like to
act of swallowing has a significant impact on breathing during make the following comments.
feeding. As infants commonly swallow as often as 60 times a The moment an infant gains sufficient control over his
minute, and there is an airway closure averaging 530 ms associated physiological parameters determines the time he is ready to
with swallows, this means that during the initial period of successfully process oral feeding. From the literature, it would
continuous sucking, the airway closure lasts up to 30 s a minute.24 appear that it is taken for granted that on reaching term age, the
This makes it important for respiration to be exquisitely infant has developed a sucking pattern (or that the infant is able to
coordinated with swallowing. coordinate sucking, swallowing and breathing) that is comparable
During feeding, swallowing is segregated from breathing. to that of a full-term infant. If the infant is unable to do this, his
Sucking and breathing patterns create ‘windows of opportunity’ for development is considered to be deviant or premature.4
swallows and the central nervous system may look for opportunities Gewolb et al.20 indicated that the number of sucking
within ongoing sucking and breathing patterns in which to fit movements in preterm infants increases from 55 per minute at 32
swallows, allowing an infant to continue feeding without weeks’ PMA to 65 per minute at 40 weeks. This is comparable to

Journal of Perinatology
 Sucking and swallowing
SP da Costa et al
250

Table 1 The five primary stages of non-nutritive sucking (NNS) and nutritive of swallowing stabilizes before suck rhythmicity does. A stable
sucking (NS) swallow rhythm already exists at the age of 32 weeks’ PMA and
Stage 1a The sucking pattern consists primarily of arrhythmic expression without does not change from 32 weeks’ PMA to term age. Concerning
suction. sucking rhythm, stability is established later.
Stage 1b Sucking with attempts to generate suction and expression. Mizuno and Ueda15 found significantly increased sucking
Stage 2a Although suction may be still absent, the expression component becomes efficiency, (sucking pressure and frequency) between 34 and 36
rhythmic. weeks’ gestational age. They found a 30 s continuous phase
Stage 2b The alternation of suction/expression begins to appear. Rhythmicity not (during the continuous phase, the sucking pattern is stable and is
yet established. only influenced by oral reflex activity) and an intermittent phase
Stage 3a Sucking still consists of rhythmic expression without suction. (the sucking pattern changes and becomes less stable as a result of
Stage 3b The appearance of more rhythmic alternation of suction/expression with
fatigue, gastro-intestinal and respiratory influences) during
longer sucking bursts and stronger suction amplitude.
sucking. Although only bottle-fed infants were observed in most
Stage 4 Only rhythmic alternation of suction and expression is observed.
Stage 5 Greater suction amplitude and longer duration of sucking bursts than
studies, it is supposed that the basic rhythmic pattern is similar in
seen in stage 4 breastfeeding, even though breastfeeding often involves more
sucking movements.
Adapted in 2005 by Rogers and Arvedson19 from Lau and Schanler.11

the level reached by full-term infants at 1 month of age. On the Interaction with breathing. The coordination of breathing and
one hand, this implies that during the first days after birth, the swallowing undergoes significant developmental maturation from
sucking rate does not follow the maturation curve. On the other 34 to 42 weeks’ PMA. Generally speaking, minute ventilation
hand, age expressed in terms of PMA correlates better with the increases during sucking and swallowing with increasing PMA.16
development of sucking and swallowing than chronological age, This might influence sucking and swallowing patterns in infants
which presumes that oral feeding is a congenital behavioral pattern whose minute ventilation is at risk under normal circumstances,
rather than acquired behavior.28 for example, in infants suffering from bronchopulmonary dysplasia
Lau and Kusnierczyk6 divided the normal maturational process (BPD). Gewolb et al.20,31 described the development of sucking and
into five primary stages based on the presence or absence of suction swallowing in preterm infants suffering from severe BPD. Up to 35
and rhythmicity for the two components of sucking: suction and weeks’ PMA, sucking and swallowing develop as in healthy preterm
expression/compression (Table 1). Lau and Kusnierczyk6 used this infants. Subsequently, difficulties in coordinating breathing and
scale to indicate the relation between the development of sucking sucking arise to an increasing extent, but the rate of swallowing,
and the preterm infant’s oral feeding skill. The scale can be applied length of the swallowing sequence and the swallow–swallow
to both NS and NNS. interval are not influenced by BPD. The main problem arises in the
coordination between breathing and sucking and swallowing.
Non-nutritive sucking. In the past, several studies on NNS were Because of BPD, swallowing is relatively long to meet the infant’s
performed in preterm infants because this behavioral pattern is ventilatory demands, whereas sucking patterns are not adapted to
more readily observed in preterm infants than is NS. Usually, NNS this situation. If the infant continues to suck, desaturation occurs
is at the same stage of development as NS or one level ahead.6,11 due to the necessity to swallow, with insufficient time to breathe,
The stage of NNS is an indication of the infant’s oral-motor skills. leading to deglutition apnea. Only after a number of weeks after
If an infant shows stage 5 NNS and its NS skill is stage 2, then the term age does coordination recover and does the infant develop a
coordination of swallowing or breathing is ineffective. Oral feeding normal sucking pattern once again. This may possibly be caused
performance improves as the infant’s sucking skills mature.6,9 A by discongruent maturation of the breathing and swallowing
significant correlation was found between the level of maturation centers in the brainstem. The coordination of swallow–respiration
of an infant’s sucking skill and gestational age and the infant’s and suck–swallow rhythms may be predictive of feeding,
skill to ingest oral food. respiratory and neurodevelopmental abnormalities.23 Infants with
Several studies have shown the advantages of NNS. These BPD, however, do not follow predicted maturational patterns of
include a quicker change from tube feeding to oral feeding and sucking–swallowing rhythmic integration. A follow-up study of
better saturation during NS when the infant received NNS prior to Gewolb and Vice32 suggests that ventilatory needs may modulate
NS. NNS at the empty breast promotes infant-state control, weight sucking rhythm and organization.
gain, breast-feeding skill and milk production in the mother.6,29,30 Hanlon et al.33 investigated the maturation of deglutition apnea
times in full-term and preterm infants (28 to 37 weeks’ gestational
Rhythmicity. In preterm infants of 26 to 33 weeks’ gestational age). They found that deglutition apnea times decrease as
age at birth, Gewolb et al.20 found that the basic rhythmic nature infants mature, as does the number and length of episodes of

Journal of Perinatology
 Sucking and swallowing
SP da Costa et al
251

multiple-swallow deglutition apnea. The maturation appears to be articles from our literature search, we selected six approaches
related to PMA rather than feeding experience (chronological age). that all stem from nursing practice. On the basis of the setup
Reliance on preterm infant behavioral cues for impaired of the study, whether or not it is standardized and the description
oxygenation during bottle feeding will be insufficient for the of the items to be observed, we selected two methods
detection of oxygen desaturation during oral feeding. Attention to (Table 2).
changes in breathing sounds and to the pattern of sucking are McGain and Gartside35 described the use of NNS to promote
potentially important intervention strategies to prevent the decline awake behavior for feeding, the use of behavioral assessment to
of oxygenation during feeding. Sucking pauses may be a moment identify readiness for feeding and systematic observation of and
when preterm infants aim to regulate their breathing pattern and response to infant behavioral cues to regulate frequency, length
thereby increase oxygenation.34 It remains unclear whether this and volume of oral feeding.
pattern changes on reaching term age. In preterm infants, the They used individualized semi-demand feeding. This means
predominant breathing patterns are E–S–I and E–S–E with that every 3 h the infant is offered NNS for 5 to 10 min, followed by
‘apnoeic swallows’ or ‘apnoeic-related’ swallows accounting for an assessment of the infant’s behavioral state. If asleep, the infant
approximately 30% of all swallows in infants p35 weeks’ PMA and is permitted to sleep for another half an hour and then again
approximately 15% in preterm infants of 35 to 40 weeks’ PMA. This offered NNS. If awake and restless, the infant is offered
is quite different from the situation in full-term infants, where the nipple feeding, if the infant is still sleeping, the feeding is given by
predominant pattern is I–S–E and where ‘apnoeic(-related)’ gavage.1
swallows are rare. Thoyre et al.1 developed the Early Feeding Skills Assessment.
This tool is a 36-item observational scale divided into three
Diagnostic methods to investigate an abnormal sections: early feeding readiness, oral feeding skills and oral feeding
developmental course of the coordination of sucking, recovery. In addition, the Early Feeding Skills Assessment must be
swallowing and breathing re-administered at each feeding to determine whether the infant is
able to feed orally, how it reacts to the feeding and how it recovers
The reasons to carefully study both the preconditions for sucking from the effort. The physiological parameters are monitored during
and how an infant sucks are to determine if an infant is ready to feeding. In the case of early feeding readiness, the infant has to
feed orally and to detect the nature of the feeding problems. In demonstrate ‘behavioural organization and energy for the work
addition, an abnormal sucking pattern may be an indication of the of feeding by attaining and maintaining an awake state, a flexed
neurological development of the infant that is not progressing body posture with sufficient muscle tone, and interest in sucking’
normally. (1, p. 10). Gestational age is less important. For oral feeding skill,
We performed a literature search for both types of assessments the coordination of sucking, swallowing and breathing, and the
and distinguished between the following elements: sucking and swallowing movements are observed. During 5 min
1. the reliability of the study following feeding, the caregiver observes the behavioral and
2. the reliability and validity of the tool physiological recovery from feeding to determine oral feeding
3. whether the tool can be used for preterm infants recovery. This information is of great importance when deciding
4. whether the tool is designed for breastfeeding, bottle feeding or whether or not to feed the infant orally the next time it needs
for both to be fed.
5. for which age is it suited?
6. how invasive is it/hands off or hands on? Methods for detecting feeding problems in young infants
7. what does it measure? To detect feeding problems, a diagnostic tool is needed to assess the
8. is the tool designed for NS or NNS or for both? oral-motor patterns underlying poor feeding.
9. how much does the tool cost and what costs are involved in its In general, one can distinguish between clinical feeding
use? assessment and swallowing assessment.7 Whether NNS or NS and
swallowing are observed as standard procedure depends on the
Determining whether an infant is ready to feed orally infant’s age and on the clinical situation.
Certain physiological parameters, behavioral aspects, NNS and the No standardized method is available to assess NNS. A common
infant’s behavioral state are important indicators, apart from the approach to assess NNS is to place one’s little finger into the
infant’s oral-motor functioning, to determine whether a preterm infant’s mouth halfway the tongue. The rate of NNS should be
infant is ready to feed orally.1,34 approximately two sucks per second. If the infant shows good NNS,
The vision on readiness is strongly determined by the fast- this does not automatically mean that it is ready for oral feeding.
increasing options of medical treatment of preterm infants in the During NNS, only sucking and breathing are coordinated, and not
NICU. Basing ourselves primarily on the date of publication of the sucking, swallowing and breathing as in NS.9

Journal of Perinatology
Journal of Perinatology

252
Table 2 Standardized diagnostic tools for assessing an infant’s readiness for oral feeding

Assessment Description Reliability of the study Reliability and validity of Age Breast or NS or NNS What is measured? Degree of Cost
the tool suitability bottle invasiveness
feeding

1. An evidence-based The method combines the A semidemand method Different elements of this Preterm Both Both State, behavioral Noninvasive The method requires a
guideline for introducing use of non-nutritive based on a randomized approach are based on infants organization, suck– trained nurse and time
oral feeding to healthy sucking to promote experimental study of 41 evidence found in swallow–breathe pattern investment; no capital
preterm infants, McCain30 waking behavior for healthy preterm infants references and cardiorespiratory outlay required

Sucking and swallowing

feeding, the use of (32–34 weeks PMA). control
behavioral assessment to Making the transition from

SP da Costa et al
identify readiness for gavage to oral feeding 5
feeding and systematic days (P<0.001) faster
observation of and compared to a control
response to infant group (n ¼ 41)
behavioral cues to
regulate frequency, length
and volume of oral
feedings

2. Early Feeding Skills A checklist for assessing The authors based all the The authors state that Preterm Both Both EFS is a 36-item Noninvastive Does not require any
Assessment for Preterm infant readiness for and items of the tool on 69 ‘content validity has been infants observational measure, apparatus. Requires a
Infants (EFS), Thoyre tolerance of feeding and references. No information established with expert used to assess four 2-day workshop to
et al.1 for profiling the infant’s is provided about the neonatal nurses’ and domains: to remain train nursing staff in
developmental stage results of the EFS, about ‘intra- and inter-rater engaged in feeding; to using the tool
regarding specific feeding the study group, control reliability have been found organize oral-motor
skills group, and so on to be stable and functioning; to coordinate
acceptable’, but no data swallowing and breathing
are provided to support this and to retain
statement physiological stablility
 Sucking and swallowing
SP da Costa et al
253

Standardized assessments are available to assess NS or oral problems, but less so when it comes to sucking patterns in preterm
feeding. A literature search using the nine search elements infants.49
mentioned earlier resulted in our finding seven assessment tools
(Table 3). Four of these were suited exclusively for breastfeeding,
two for bottle feeding and only one for both breastfeeding and The prognostic value of an abnormal developmental
bottle feeding. The assessments designed exclusively for course of sucking, swallowing and breathing for later
breastfeeding also include maternal elements such as the mother’s neurodevelopmental and feeding outcome
feeding position, nipple pain and the mother’s health. The part It is known that early feeding problems may be the first symptom
aimed at the oral-motor patterns is limited: two out of five items in of disability. Infants with severe neurodevelopmental problems in
the case of latch, audible swallowing, type of nipple, comfort, hold later life did not generate sucking pressure or coordinate suction
(LATCH),37,38 nine of the 22 subitems in the Preterm Infant Breast- and expression during their neonatal period. Several studies found
feeding Behavior Scale,43 four out of eight items in the breast- that both feeding problems and nutritional problems are most
feeding evaluation for term infants.44 common in children with severe disability.2,50 Gisel and Patrick43
Seven out of eighteen items in the Systematic Assessment of the suggest that early quantitative assessment of feeding efficiency
Infant at the Breast (SAIB).36 The Preterm Infant Breast-feeding should be made to identify infants who cannot be nourished
Behavior Scale was the only tool subjected to tests of validity and adequately without ancillary feeding. The identification of risk
reliability. factors associated with malnutrition is important for its early
The noninvasive assessment tools for bottle feeding only focus detection and treatment and for the prevention of later behavioral,
on the intraoral movements of the infant. Both assessments are still health and growth consequences. However, only few studies have
in an experimental stage (N ¼ 1 and N ¼ 12). Nevertheless, they prospectively identified risk factors in cohorts of full-term and
seem to offer many possibilities for the future.41,42 preterm infants. Moreover, there are hardly any publications on the
Because the only assessment tool used for breastfeeding and relationship between the development of sucking and later
bottle feeding is the noninvasive Neonatal Oral-Motor Assessment neurodevelopmental outcome, even though there are several
Scale (NOMAS),4 we describe it here in more detail. The tool authors who suspect that the relationship does exist.
contains checklists for feeding behavior and provides an analysis Since the rhythmic processes involved in feeding are under
of, and diagnoses, sucking patterns by assessing the oral-motor bulbar control, quantitative analyses of rhythms and patterns of
components of the tongue and jaw during neonatal sucking. In feeding times can be meaningful. This is the case especially after
addition, it identifies the type of sucking pattern the infant uses. the 35th week of PMA, not only as an indication of feeding
Two abnormal patterns are defined: a disorganized sucking pattern problems but also as predictors of subsequent long-term
and a dysfunctional sucking pattern. A disorganized sucking neurological problems.26
pattern refers to a lack of rhythm in the total sucking activity. This The eating and drinking patterns of 34 former preterms
means that the infant is unable to coordinate sucking and (with an average gestational age of 34 weeks) and 21 healthy
swallowing with breathing. When an infant’s sucking pattern is infants born at term were studied from 6 to 12 months.50 At the age
disorganized, it is unable to feed well and may exhibit labored of 6 months, 12 former preterms were more likely to vomit and
breathing with color changes and/or spells of apnea and were slightly more inclined to cough when fed viscous food. At the
bradycardia. A dysfunctional sucking pattern is characterized by age of 12 months, the same 12 children had more problems with
abnormality in orofacial tone. In case of orofacial hypertonia, a small chunks in their food and they coughed much more often
restriction in the range of motion at the tempomandibular joint when eating chewable food. Only six of these children and their
may result, in turn resulting in minimal jaw excursions and/or parents enjoyed the meal.
tongue retraction. In case of orofacial hypotonia, one may note a Palmer48 followed 18 children whom she had assessed with
flaccid tongue and/or excessively wide excursions of the jaw when NOMAS shortly after birth. She saw the children again between the
sucking. Infants with dysfunctional sucking patterns are likely to ages of 24 and 36 months. For these assessments, she used the
benefit from therapeutic intervention providing compensatory Bayley Scales of Infant Development and the Vineland Social
strategies during oral feeding. Maturity Scale. All seven children who had a dysfunctional sucking
Palmer published data concerning the reliability of the NOMAS pattern in infancy showed developmental delay. The two children
in 1993. NOMAS is not a reliable tool as the intrarater agreement who had a normal sucking pattern in infancy developed normally.
with respect to the diagnosis is ‘moderate’ to ‘substantial’ (Cohen’s K Of the nine children who had shown a disorganized sucking
between 0.40 and 0.65).43 In recent years, a number of articles by pattern in infancy, four had developed abnormally at the age of
Palmer4,45 –47 and others48,49 have been published in which the 24 months. However, the numbers in this study are limited and
NOMAS was employed as a diagnostic tool. The NOMAS seems no specific details are provided about the extent of the
particularly useful for studying full-term infants with sucking developmental delay.

Journal of Perinatology
Journal of Perinatology

254
Table 3 Standardized diagnostic tools for assessing NS or oral feeding

Diagnostic tool Description Reliability of the study Reliability and validity Age suitability Breast or NS or NNS What is measured? Degree of Equipment, costs,
of the tool bottle feeding invasive-ness training

1. Systematic Assessment Observations related to No data are available for No information is Suitable for fullterm Breast NS Eighteen aspects are Not Training of nurse
of the Infant at the alignment (5 items), assessing this tool. The provided regarding infants, but probably observed, seven of and mother
Breast (SAIB), areolar grasp, (8 items) setup of the tool is reliability and validity also for preterm which refer to sucking/
Association of Women’s areolar compression based on 21 references. infants swallowing movements
Health, Obstetric and (2 items) and audible Not subjected to any test
Neonatal Nursing, 198936 swallow (3 items) of validity

Sucking and swallowing

2. The Neonatal Oral- Checklists of 26 items Thirty-six infants, term In a previous version, From birth up to 8 Both Both Coordination between Hands off, Video camera. A
Motor Assessment Scale in categories of normal, and preterm. No control interrater agreement was weeks’ corrected age. sucking, swallowing bedside 3-day certification
(NOMAS), Palmer et al.4 disorganized and

SP da Costa et al
group. Twenty references determined on the basis of Suitable for both and breathing. Jaw observation course
dysfunctional tongue and were used. For more than percentage agreement. groups, according to and tongue
jaw movements half of the items, there is After revision, the final the authors. In the movements are divided
no acknowledgement of scale was not tested for manual, hardly any into three categories
the source. The method reliability distinction is made for jaw movements
was not subjected to any regarding the assess- and three categories
test of validity ment of preterms for tongue movements

3. LATCH: a breast- A systematic method for Riordan et al.38 measured No distinction is Breastfeeding NS The tool assigns a Mainly hands Training in scoring
feeding charting system gathering information the validity of 133 dyads made in terms of numeral score to five off, except for and cervical
and documentation tool, about individual breast- and the relationship gestational age when key elements, two of cervical auscultation
Jensen et al.37 feeding sessions between the LATCH scores using this tool which refer to sucking auscultation
and duration of and swallowing
breastfeeding

4. Preterm Infant Breast- Diary kept by mother: Study of 35 infants: 12 Interrater agreement Suitable for both Breastfeeding NS Nine aspects are Hands off, No apparatus.
feeding Behaviour Scale rooting, amount of fullterms (control group) of the PIBBS was tested groups measured and direct Training required
(PIBBS), Nyqvist et al.39 breast in mouth, and 23 preterms. Thirty- on the basis of eight subdivided into 22 observation
latching, sucking, eight references. The infants and adjusted subitems. Nine of these
sucking bursts, source of all nine accordingly. Subsequently, refer to sucking
swallowing, state, elements is acknowledged. the interrater agreement
letdown and time The tool is subjected to of the tool was tested twice
tests of both reliability and and adjusted
discriminative validity
 Table 3 Continued
Diagnostic tool Description Reliability of the study Reliability and validity Age suitability Breast or NS or NNS What is measured? Degree of Equipment, costs,
of the tool bottle feeding invasive-ness training

5. Breast-feeding A take-home sheet No data are available No information is Suitable for full-term Breastfeeding NS Eight aspects are Hands off, Applying the tool is
evaluation and education gives parents’ ample for assessing this tool. provided regarding infants observed, four of direct typified as being
tool, Tobin40 criteria for determining The setup of the tool is reliability and validity which refer to observation ‘simple’ and
how based on six references, sucking movements. A ‘inexpensive’
well breastfeeding is four of which have not description of the test
progressing been published. Not has not been published
subjected to any test of
validity

6. Analysis of feeding By placing markers on Ten ‘normal’ infants According to their Not indicated. Bottle-feeding NS and NNS Suction and Hands off, Digital videocamera.
behavior with direct the lateral angle of the (control group) and two previously published data expression pressure direct Training in placing
linear transformation, eye, tip of the jaw and infants with neurological on infants with severe and the movements observation the markers and in
Mizuno et al.41 throat during sucking disorders were studied. neurological disorders, of jaw and throat are interpreting the
while the face of the Eleven references were who were unable to measured to detect analysis
infant is recorded in used. Not subjected to any generate intraoral abnormal movements,
profile, the jaw and substantial test of validity negative pressure, the for instance, in infants
throat movements are authors observed a with neurological

SP da Costa et al
Sucking and swallowing
calculated using the significant relationship disorders
direct linear between throat movement
transformation (DLT) and suction pressure
procedure

7. Ultrasound Examination of the N ¼ 1 as a pilot study The authors underscore Full-term and Bottle-feeding NS and NNS It is used to discern Hands on, B-mode ultrasound
observation of lingual lingual-hyoid to find out whether the importance of lingual preterm aspects of oral yet imaging system.
movement patterns, mechanics with a ultrasound can be used motor activity as a driver feeding candidacy, noninvasive, Training in using
Miller and Kang42 noninvasive ultrasound to determine abnormal of sucking mechanics. In which is the according to ultrasound and in
imaging technique lingual movements. addition, they describe the evaluation of the authors interpreting the
Thirty-two references were differences in lingual intraoral lingual images
used. Not subjected to any movements between NS movements during
test of validity and NNS sucking
Journal of Perinatology

255
 Sucking and swallowing
SP da Costa et al
256

Mizuno and Ueda15 studied the relationship between the feeding above and one that is applicable to both breastfeeding and bottle
behavior (measured in terms of expression and suction) of 65 feeding. With such a tool in hand, we would be able to determine
neonates (mean gestational age 37.8 weeks, s.d. 0.5) and which interventions to use to enhance sucking and swallowing in
neurological development (measured with the Bayley Scales of newborns. It is tempting to speculate that such a tool could also
Infant Development II) at 18 months of age. They found an predict later development or neurodevelopmental sequelae or later
association, namely, the weaker the suction and expression, the feeding problems. In that case, it would enable us to decide which
lower the score on the Bayley Scales of Infant Development II. interventions to use to enhance sucking and swallowing in infants,
Pridham et al.51 explored the level and variation in feeding skill and hopefully improve their outcomes.
performance in 45 preterm infants at 1, 4, 8 and 12 months’ post-
term age using the Child Feeding Skills Checklist. They found that
feeding skill performance varied widely among infants at all four References
assessments. A minority of infants had a delay and lack of 1 Thoyre SM, Shaker CS, Pridham KF. The early feeding skills assessment for preterm
opportunity to engage skills like eating new food, drinking from a infants. Neonatal Netw 2005; 24(3): 7–16.
cup and self-feeding skills at the age of 8 and 12 months. 2 Reilly S, Skuse D. Characteristics and management of feeding problems
of young children with cerebral palsy. Dev Med Child Neurol 1992; 34:
Medoff-Cooper44 did a study in 19 very low birth weight infants
379–388.
to identify early predictors of developmental outcome. They found 3 Wolf LS, Glass R. Feeding and Swallowing Disorders in Infancy 1992. Therapy Skill
that the mean pressure generated by each suck and the length of Builders: San Antonio, TX.
sucking bursts correlated positively with the Psychomotor Scale of 4 Palmer MM, Crawley K, Blanco I. The neonatal oral-motor assessment scale: a
the BSID at the age of 6 months. reliability study. J Perinatol 1993; 13(1): 28–35.
In summary, we can state that over the years, a relationship 5 Morren G, van Huffel S, Helon I, Daniels H, Devlieger H, Casaer P. Effects of
nonnutritive sucking on heart rate, respiration, and oxygenation: a model-based signal
between sucking patterns and later outcome has been suggested by processing approach. Comp Biochem Physiol 2002; 132: 97–106.
several authors, but exact data do not exist. There is an urgent 6 Lau C, Kusnierczyk I. Quantitative evaluation of infant’s nonnutritive and nutritive
need for prospective studies on feeding behavior and later sucking. Dysphagia 2001; 16(1): 58–67.
neurodevelopmental and motor outcome. To begin with, a reliable 7 Doty R, Bosma JF. An electromyography analysis of reflex deglutition. J Neurophysiol
and noninvasive research tool to assess sucking and its 1956; 19: 44–60.
8 Bosma JF. Development of feeding. Clin Nutr 1986; 5: 210–218.
development is required to achieve this aim.
9 Moore KL. The Developing Human: Clinically Oriented Embryology, 4th edn. WB
Saunders: Philadelphia, 1988.
10 Morris SE, Klein MD. Pre-Feeding Skills: A Comprehensive Resource For Feeding
Conclusion Development. Therapy Skill Builders: Tucsun, AZ, 1987.
Many studies on sucking and the development of sucking in 11 Lau C, Schanler RJ. Oral feeding in premature infants: advantage of a self-paced milk
preterm infants and infants born at term have been published over flow. Acta Paediatr 2000; 89(4): 453–459.
12 Milla PJ. Feeding, tasting, and sucking. In: Walker-Smith WA, Watkins JB (eds).
the past 7 years. A number of these publications assume that there Pediatric Gastrointestinal Disease. BC Decker: Philadelphia, 1991, pp 217–223.
is a relationship between the way an infant sucks and his later 13 Pritchard JA. Fetal swallowing and amniotic fluid volume. Obstet Gynecol 1966; 28:
neurodevelopmental and feeding outcome. In these studies, various 606–610.
aspects of learning how to suckle from the breast or how to drink 14 Mathew O. Science of bottle feeding. J Pediatr 1991; 119: 511–519.
from a bottle are mentioned and investigated. Internal and 15 Mizuno K, Ueda A. The maturation and coordination of sucking, swallowing, and
respiration in preterm infants. J Pediatr 2003; 142: 36–40.
external factors are distinguished. Internal factors are stable
16 Qureshi MA, Vice FL, Taciak VL, Bosma JF, Gewolb IH. Changes in rhythmic suckle
physiological parameters, rooting, suction pressure and suction feeding patterns in term infants in the first month of life. Dev Med Child Neurol 2002;
frequency, movements of jaw and tongue, the rhythmicity of the 44(1): 34–39.
suck–swallow–breathe relationship, length of sucking bursts and 17 Eishima K. The analysis of sucking behaviour in newborn infants. Early Hum Dev
alertness. External factors are milk flow, nipple size, nasogastric 1991; 27: 163.
tube in situ and the role of the caregiver. Several research tools 18 Lemons PK, Lemons JA. Transition to breast/bottle feedings: the premature infant.
J Am Coll Nutr 2001; 2: 126–135.
have been developed to assess sucking behavior. In these studies, 19 Rogers B, Arvedson J. Assessment of infant oral sensorimotor and swallowing function.
only a few aspects of the development of sucking are measured or Ment Retard Dev Disabil Res Rev 2005; 11(1): 74–82.
investigated; often they cannot be used for both breastfeeding and 20 Gewolb IH, Vice FL, Schwietzer-Kenney EL, Taciak VL, Bosma JF. Developmental
bottle feeding, are more or less invasive and require expensive or patterns of rhythmic suck and swallow in preterm infants. Dev Med Child Neurol
complicated measuring equipment. Most studies were done with a 2001; 43(1): 22–27.
21 Koenig JS, Davies AM, Thach BT. Coordination of breathing, sucking and swallowing
small experimental group and often without a control group. Only
during bottle feedings in human infants. J Appl Physiol 1990; 69: 1623–1629.
a few tools were tested for validity (specificity and sensitivity). 22 Gewolb IH, Vice FL. Abnormalities in the coordination of respiration and swallow in
Therefore, the need remains for a user-friendly, reliable and preterm infants with bronchopulmonary dysplasia. Dev Med Child Neurol 2006; 48:
noninvasive tool to measure objectively all the aspects mentioned 599–604.

Journal of Perinatology
 Sucking and swallowing
SP da Costa et al
257

23 Bu’Lock F, Woolridge MW, Baum JD. Development of coordination of sucking, 36 Association of Women’s Health, Obstetric, and Neonatal Nurses. Systematic Assessment
swallowing, and breathing: ultrasound study of term and preterm infants. Dev Med of the Infant at the Breast (SAIB). AWHONN: Washington DC, 1989.
Child Neurol 1990; 32: 669–678. 37 Jensen D, Wallace S, Kelsay P. LATCH: a breastfeeding charting system and
24 Durand M, Leahy FN, Maccallum M, Cates DB, Rigato H, Chermick V. Effect of feeding documentation tool. J Obstet Gynecol Neonatal Nurs 1994; 23: 27–32.
on the chemical control of breathing in the newborn infant. Pediatr Res 1981; 5: 38 Riordan J, Bibb D, Miller M, Rawlins T. Predicting breastfeeding duration using the
509–512. LATCH breastfeeding assessment tool. J Hum Lact 2001; 17: 20–23.
25 Goldfield EC, Richardson MJ, Lee KG, Margetts S. Coordination of sucking, swallowing, 39 Nyqvist KH, Rubertsson C, Ewald U, Sjoden PO. Development of the Preterm Infant
and breathing and oxygen saturation during early infant breast-feeding and bottle- Breast-feeding Behavior Scale (PIBBS): a study of nurse-mother agreement. J Hum
feeding. Pediatr Res 2006; 60: 450–455. Lact 1996; 12: 206–219.
26 Gewolb IH, Bosma JF, Taciak VL, Vice FL. Abnormal developmental patterns of suck and 40 Tobin DL. A breast-feeding evaluation and education tool. J Hum Lact 1996; 12:
swallow rhythms during feeding in preterm infants with bronchopulmonary dysplasia. 47–49.
Dev Med Child Neurol 2002; 43: 454–459. 41 Mizuno K, Aizawa M, Saito S, Kani K, Tanaka S, Kawamura H et al. Analysis of feeding
27 Mathew OP, Clark ML, Pronske ML, Luna-Solazano HG, Peterson MD. Breathing behavior with direct linear transformation. Early Hum Dev 2006; 82: 199–202.
pattern and ventilation during oral feeding in term newborn infants: assessment and 42 Miller JL, Kang SM. Preliminary ultrasound observation of lingual movements patterns
facilitation of breastfeeding. Clin Perinatol 1987; 14: 109–130. during nutritive versus non-nutritive sucking in a premature infant. Dysphagia 2007;
28 Bamford O, Taciak V, Gewolb IH. The relationship between rhythmic swallowing 22: 150–160.
and breathing during suckle feeding in term neonates. Pediatr Res 1992; 31: 43 da Costa SP, van der Schans CP. The reliability of the neonatal oral-motor assessment
616–624. scale. Acta Paediatr (in press).
29 Mizuno K, Ueda A, Takeuchi T. Effects of different fluids on the relationship between 44 Medoff-Cooper B. Nutritive sucking research from clinical questions to research
swallowing and breathing during nutritive sucking in neonates. Biol Neonate 2002; answers. J Perinat Neonatal Nurs 2005; 19: 265–272.
81: 45–50. 45 Palmer MM. Recognizing and resolving infant suck difficulties. J Hum Lact 2002;
30 McCain GC. An evidence-based guideline for introducing oral feeding to healthy 18(2): 166–167.
preterm infants. Neonatal Netw 2003; 22(5): 45–50. 46 Palmer MM, VandenBerg KA. A closer look at neonatal sucking. Neonatal Netw 1998;
31 Gewolb IH, Vice FL. Maturational changes in the rhythms, patterning, and coordination 17: 77–79.
of respiration and swallow during feeding in preterm and term infants. Dev Med Child 47 Palmer MM, Heyman MB. Developmental outcome for neonates with dysfunctional and
Neurol 2006; 48: 589–594. disorganized sucking patterns: preliminary findings.. Infant-Toddler Intervention
32 Gewolb IH, Vice FL. Neonatal rhythmic feeding score correlates with short-term 1999; 3: 299–308.
neurodevelopmental outcome in premature infants >33 weeks gestation. PAS 2005; 48 Hawdon JM, Beauregard N, Slattery J, Kennedy G. Identification of neonates at risk of
57: 3290. developing feeding problems in infancy. Dev Med Child Neurol 2000; 42(4):
33 Hanlon MB, Tripp JH, Ellis RE, Flack FC, Selley WG, Shoesmith HJ. Deglutition apnoea 235–239.
as an indicator of maturation of suckle feeding in bottle-fed premature infants. Dev 49 Mizuno K. Neonatal feeding performance as a predictor of neurodevelopmental
Med Child Neurol 1991; 39: 534–542. outcome at 18 months. Dev Med Child Neurol 2005; 47: 299–304.
34 Thoyre SM, Carlson JR. Preterm infant’s behavioural indicators of oxygen decline 50 Gisel EG, Patrick J. Identification of children with cerebral palsy unable to maintain a
during bottle feeding. J Adv Nurs 2003; 43: 631–641. normal nutritional state. The Lancet 1988; 1: 283–286.
35 McGain GC, Gartside PS. Behavioral responses of preterm infants to a standard-care 51 Pridham K, Steward D, Thoyre S, Brown R, Brown L. Feeding skill performance in
and semi-demand feeding protocol. Newborn Infant Nurs Rev 2002; 2: 187–193. premature infants during the first year. Early Hum Dev 2007; 83: 293–305.

Journal of Perinatology