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Neonatal Feeding Behavior as a Complex

Dynamical System
Eugene C. Goldfield, Ph.D.,1 Jennifer Perez, M.S., CCC-SLP,2 and
Katherine Engstler, M.A., CCC-SLP2

ABSTRACT

The requirements of evidence-based practice in 2017 are

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motivating new theoretical foundations and methodological tools for
characterizing neonatal feeding behavior. Toward that end, this article
offers a complex dynamical systems perspective. A set of critical concepts
from this perspective frames challenges faced by speech-language
pathologists and allied professionals: when to initiate oral feeds, how
to determine the robustness of neonatal breathing during feeding and
appropriate levels of respiratory support, what instrumental assessments
of swallow function to use with preterm neonates, and whether or not to
introduce thickened liquids. In the near future, we can expect vast
amounts of new data to guide evidence-based practice. But unless
practitioners are able to frame these issues in a systems context larger
than the individual child, the availability of “big data” will not be
effectively translated to clinical practice.

KEYWORDS: Dynamical systems, sucking, synergy, emergence

Learning Outcomes: As a result of this activity, the reader will be able to (1) describe how a dynamical
systems perspective may be used to assess when to initiate oral feeding in preterm neonates; (2) define a
synergy, and describe how it informs sucking and respiration behavior; and (3) describe the role of the
caregiver as part of a complex system.

T he interactions between multiple physi- intuitively identify when feeding is “going


ological systems, behavioral dynamics, and so- well” and when it is not, quantifying this gestalt
cial interactions make newborn feeding a characterization of the complexity of feeding is
complex, dynamical system. Although experi- quite challenging. The requirements of evi-
enced caregivers and clinicians are able to dence-based practice in 2017 are motivating

1
Department of Psychiatry, Harvard Medical School, Bos- Pediatric Dysphagia; Guest Editor, Gilson J. Capilouto,
ton, Massachusetts; 2Feeding and Swallowing Program, Ph.D., CCC-SLP, ASHA Fellow.
Boston Children’s Hospital, Boston, Massachusetts. Semin Speech Lang 2017;38:77–86. Copyright # 2017
Address for correspondence: Eugene C. Goldfield, Ph. by Thieme Medical Publishers, Inc., 333 Seventh Avenue,
D., Boston Children’s Hospital, 300 Longwood Avenue, New York, NY 10001, USA. Tel: +1(212) 584-4662.
Pavilion 159, Boston, MA 02115 DOI: http://dx.doi.org/10.1055/s-0037-1599105.
(e-mail: eugene.goldfield@childrens.harvard.edu). ISSN 0734-0478.
77
78 SEMINARS IN SPEECH AND LANGUAGE/VOLUME 38, NUMBER 2 2017

new theoretical foundations and methodologi- bestiary of underlying “attractors,” each with
cal tools for characterizing not only the anatomy a unique signature dynamics revealed in
and physiology of oropharyngeal structures, but measurements of neonatal behavior during
also how they are organized for the swallowing sucking, breathing, and swallowing.
function.1 The elegant architecture of the hun- 2. The nervous system controls the oropharyn-
dreds of muscles of the hydrostatic tongue and geal and respiratory anatomy not simply by
the muscles of the pharynx, lungs, and inter- activating individual muscles, but rather by
costals constitute hundreds of controllable de- collecting muscles and elastic tissue into
grees of freedom. Moreover, the ability of the functional groupings, or synergies, so that
pharyngeal anatomy to change its shape for adjustments in one part of the system are
different functions presents the newborn with automatically compensated in other parts.
the remarkable challenge of using the same The same parts of the system may be used in
anatomy in different ways for breathing, swal- different ways for different functions and so
lowing, and vocalizing. To do so requires rapid must rapidly assemble for one function (say,
transitions in the organization of these muscles vegetative breathing), dissolve that organi-

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into functional groupings, under the guidance zational pattern, and become reassembled for
of exquisitely refined receptive fields. And yet, another function (say, feeding) while re-
most newborns are able to organize their maining stable despite these perturbations
breathing and vocalizing to cry robustly as a (i.e., remaining robust).
signal that they are hungry, then reorganize 3. Newborns use the mouth to spontaneously
their breathing to couple with swallowing as explore the properties of the breast and
they begin orally feeding, coo contentedly when milk—their taste, texture, temperature, elas-
sated, and change their breathing pattern when ticity—as sensory input for generating at-
they fall asleep. Why do some newborns have tractor dynamics that promote the functional
such great difficulty in feeding and in making activity of suckling. Through such active
these transitions between quiet breathing and exploratory behavior during suckling, infor-
swallowing during feeding? mation for regulating milk flow becomes
Despite the well-characterized anatomy coupled with the attractor dynamics govern-
and physiology underlying newborn feeding, ing action, forming a suckling system.
as well as the availability of sophisticated imag- 4. Growth, a biomarker of robust health, is an
ing and computer-aided measurement of the emergent property of all of the interacting
timing of swallowing events, practitioners still components that contribute to it and not
do not have adequate foundational theoretical predictable from any of the individual com-
and mathematical tools for revealing the “hid- ponents alone. As one illustration, obesity
den” information in “big data” for objectively may be an emergent property of body
identifying the empirical basis of their clinical growth, relative to the timing of introduc-
judgments. The result is that controversies in tion of formula, and of solid foods.
practice remain. For prematurely born neo- 5. The neonate is part of a larger complex
nates, when should full oral feedings begin? system, a consortium, which includes the
Should thickened fluids be used for treatment mother, as well as the newborn-host gut
of dysphagia? How do different levels of respi- microbiome. The gut microbiome is the
ratory support influence feeding behavior? This combined genetic material and metabolic
article offers the view that current approaches to activity of all micro-organisms found in
diagnosis and treatment of feeding problems in the gut, including 100 trillion archaea, bac-
newborns may be overlooking five critical char- teria, microscopic fungi, parasites, and
acteristics of feeding as a complex dynamical viruses.2
system:
Addressing these five characteristics of
1. The “primitive” parts involved in feeding neonatal feeding behavior as a complex dynam-
behavior, traditionally called reflexes or ical system—attractor dynamics, functional or-
rhythms, are governed instead by a small ganization into synergies, exploratory behavior,
NEONATAL FEEDING BEHAVIOR/GOLDFIELD ET AL 79

emergence, and consortia membership—may form coordinated patterns, resist perturbation,


require a conceptual framework not yet em- and are capable of switching from one stable state
braced by speech-language pathologists treat- to another are all evidence for underlying attrac-
ing dysphagia. This conceptual framework, a tors, elementary building blocks, sometimes
dynamical systems approach to development,1,3 called primitives for action.9,10
has already had a major impact on other clinical How is it possible to reveal attractors in
scientific fields, including physical and occupa- neonatal feeding behavior? One characteristic of
tional therapy and neurology.4,5 In this article, particular relevance to neonatal feeding is the
we consider how a dynamical systems approach coordination between sucking and respiration.
based upon the preceding five characteristics of Goldfield et al found, for example, that the
feeding behavior may help to address some of frequency of respiration changes dramatically
the controversies faced by speech-language between quiet breathing compared with breath-
pathologists in their daily practice of diagnosis ing during nutritive sucking.11,12 During a quiet
and intervention of neonatal feeding problems. and alert behavioral state, breathing occurs at a
The other articles in this special issue will frequency of 1 Hz, with little variability.13

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address each of these issues in greater detail. However, when newborns begin sucking and
Here, we frame these issues in a systems swallowing at the breast or from a bottle, the
context. frequency of breathing increases, and falls into a
stable integer ratio pattern of two sucks for each
breath, or three sucks for every two breaths.
A DYNAMICAL SYSTEMS Here, then, the two rhythms become coupled,
APPROACH TO NEWBORN and form a coordinated pattern. Coordination
FEEDING BEHAVIOR: dynamics are also evident in other aspects of
ATTRACTORS, EXPLORATORY neonatal behavior, including coordination of the
BEHAVIOR, SYNERGIES, two legs during kicking.14,15 This suggests that
EMERGENT FUNCTIONS, AND these behaviors may be revealing the underlying
CONSORTIA neural and biomechanical primitives contribut-
ing to pattern generating and switching.16
Attractors A second characteristic of neonatal sucking
Clinical practitioners are quite familiar with the patterns revealing an underlying signature of
concept of reflexes,6 a term used to characterize attractor dynamics is the rapid switching be-
certain newborn behaviors—sucking, turning tween two characteristic patterns seen in nutri-
the head toward the breast, and flexing the tive and nonnutritive sucking. To investigate this
arms to bring the hands to the mouth—and question, Goldfield et al conducted experiments
are taught how to elicit and evaluate these in which the milk supply was abruptly switched
behaviors. At the same time, however, careful off during nutritive sucking or switched on
observers of hungry newborns may readily notice during nonnutritive sucking.11,12 With milk
rhythmic mouthing behaviors that are not eli- off, newborns used a highly stable 2-Hz pattern
cited in any way and may continue spontaneous- of nonnutritive sucking. However, when milk
ly, even in sleep. So, is newborn sucking behavior was switched on, the pattern abruptly switched to
reflexive or spontaneous? Sucking has both the a slower, more variable 1-Hz pattern of suckling.
organizational integrity of a reflex, and the In terms of attractor dynamics, the rapid transi-
tendency to switch from a nonnutritive to nutri- tion between these two stable states indicates that
tive pattern relative to milk supply, and at the sucking is generated by a bi-stable attractor.
same time, is a spontaneous rhythmic pattern.
With advances in recording and in the mathe-
matical techniques for uncovering hidden pat- Exploratory Behavior
terns in data,7,8 it has become possible to reveal A dynamical systems approach to neonatal
the two-sided nature of this complex behavior. feeding considers behavior at the breast or
From a dynamical systems perspective, sucking bottle in terms of the joint physiological, be-
and other rhythmic behaviors that couple to havioral, and informational regulation of the
80 SEMINARS IN SPEECH AND LANGUAGE/VOLUME 38, NUMBER 2 2017

newborn’s behavior. At the breast, nature pro- bation.19 This kind of experiment reveals the
vides newborns with an exquisitely tuned organ signature characteristic of a synergy: it is a
for feeding. Newborns actively look, touch, and cooperative organization of weakly coupled
taste breast milk during breast-feeding. The parts. What does the nervous system contribute
context of breast-feeding makes information to the formation and dissolution of synergies?
available for the guided discovery of how to A dramatic demonstration that muscle
regulate sucking and swallowing milk while synergies are encoded in the nervous system
maintaining vegetative breathing. Indeed, dur- comes from a series of studies by Overduin et
ing bottle-feeding, the challenge for a caregiver al,20,21 who applied long-duration electrical
is to try to emulate nature by observing the intracortical microstimulation (ICMS) to mo-
neonate to make some of the same kinds of tor areas in two awake monkeys and simulta-
postural and timing adjustments apparent dur- neously recorded muscle electromyography
ing breast-feeding. Clinicians and engineers (EMG) and finger movements. Overduin et
have sought to use computer-controlled devices al found that ICMS drives the hand and digits
to emulate the breast, but the realization of such toward particular postures at each stimulation

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a device still remains in the future. In current site.20 Moreover, the evoked EMG patterns
practice, information provided to the caregiver resembled muscle coactivations seen in tempo-
or clinician is referred to as cues, but a more rally complex behaviors, such as reach and
theoretically guided approach to how neonates grasp.22,23 As further evidence for cortical en-
explore available information to regulate their coding of synergies, Overduin et al examined
behavior may be found in the work of James and whether the muscle synergies evoked during
Eleanor Gibson (and see accounts of this ap- ICMS were similarly encoded during purely
proach in numerous reviews, such as Adolph voluntary behaviors.21 At each microstimula-
and Kretch17). In the Gibsonian view, infor- tion site, they determined that the synergy most
mation in a structured environment is revealed strongly evoked among those extracted from
through looking, listening, feeling, and tast- muscle patterns matched the synergy most
ing—all active processes of information pickup. strongly encoded during voluntary behavior
more often than expected by chance. At the
same time, however, our nervous systems are
Synergies and Multifunctionality embodied: our brain and spinal cord have
From a dynamical systems perspective, nature evolved to leverage the biomechanical proper-
may build the complex behaviors of feeding and ties of the body, such as the shapes possible by
speaking by coupling together self-sustaining our hydrostatic tongue, the elastic properties of
primitives to form a synergy, a functional unit in our lips, and the power of our jaw muscles, to
which multiple degrees of freedom behave as a perform the distinctive functions of eating and
single functional unit, so that perturbations to speaking. Are there synergies in neonatal feed-
some components are responded to by the ing behavior? An illustration of how the ner-
entire unit.18 An illustration of the adaptation vous system rapidly assembles functionally
of an entire ensemble of articulators to a specific synergies for feeding is in the transfor-
perturbation of just a part comes from a classic mation of the oral anatomy into a macroscopic
study by Kelso and colleagues.19 They applied functional device, a pumper.1
brief perturbations to the jaw of a speaker
repeating a single-syllable utterance. In the
case of the syllable /bab/, the jaw perturbation Emergent Functions: Pumping
was applied as it moved upward to close the Biological pumps, such as the heart, are a type of
vocal tract for producing the final phoneme /b/. positive displacement pump. Such pumps (1)
Kelso et al found that within 15 to 30 milli- move and accumulate successive boluses of fluid
seconds, there was also an adjustment of the into a confined space, (2) reduce the space
upper and lower lips, indicating that a collection enclosing the fluid to force it to leave by a
of articulators forming a synergy with the jaw, specific outlet, and (3) create a pressure differ-
and not the jaw alone, responded to the pertur- ence that moves a volume.24 The cooperative
NEONATAL FEEDING BEHAVIOR/GOLDFIELD ET AL 81

organization of the tongue and pharynx may pharynx on its journey to the upper esophageal
also serve the function of a positive displace- sphincter. Deglutition proper involves muscles
ment pump. However, unlike the heart, a pump controlling retrusion and protrusion of the
dedicated to circulating blood, a pump for tongue, contraction of palatal muscles, vocal
ingesting liquid and solid nutrients must be cord adduction, and contraction of the pharyn-
rapidly assembled and dissolved to allow the geal constrictors.27 Neonatal feeding, then, may
pharynx to switch between the multiple func- be made possible by the weak coupling of
tions of deglutition, vegetative breathing, and respiratory and suck-swallowing attractors,
speaking. How do the tongue and pharynx act and dysphagia may be a disorder of synergy
together to become a pumper during neonatal formation and dissolution.
feeding? The familiar pattern of neonatal suck-
ling may be thought of as the formation and
dissolution of a pumper for deglutition: the Consortia
coordination between oral, labial, mandibular, A dynamical systems approach places particular
and lingual-pharyngeal muscles draws milk into emphasis on the newborn as part of a consor-

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the mouth, seals the lips around the breast tium, which includes the mother and the new-
nipple and areola, and forces accumulated born-host gut microbiome. Within this
milk boluses into the pharyngeal space, increas- consortium, there are maternal offspring ex-
ing the potential energy of the elastic forces of changes of microbiota and nutrients provided
the soft tissue until the muscular event of the during breast-feeding. There is stepwise colo-
pharyngeal swallow.1 Like a physical pump, this nization of the neonatal gut at birth (delivery),
biological pump is most effective at particular during breast-feeding, and in contact with the
combinations of pressure and volume.24 This environment.28 Breast milk is a source of pro-
lawful relation between pressure and volume teins, maternal bacteria, and nutrients that
may be a clinically significant index of swallows contribute to establishment of the gut micro-
but is not conventionally measured in clinical biome and the immune system.29 A critical
practice. implication of considering the newborn as a
The newborn’s feeding behavior is also member of a host-microbiome consortium is
dependent on the lungs, as well as on a large that the individual nutritional and physical
group of muscles of the chest and abdomen, to health of the neonate emerges during a long
act synergistically as a respiratory pump. Suc- period of development of host-microbiome and
cessful feeding requires that the shaping of the caregiving environment. Foodstuffs and other
tongue relative to the functional anatomy of the ingested substances shape the proportional re-
pharynx creates particular patterns of constric- presentation of micro-organisms present in the
tion that act functionally as a set of valves for neonatal gut microbiome and perturbations of
regulating the flow of fluid, relative to the flow the microbiome may influence neonatal nutri-
of air for vegetative breathing. Against the tion and health.30
continual backdrop of the cyclical pattern of
the respiratory pump, muscle groups constrict
the entry to the nasopharyngeal passage and HOW COMPLEX DYNAMICAL
epiglottis and through changes in pressure force SYSTEMS INFORM NEONATAL
air from the lungs through openings that define FEEDING BEHAVIOR
the airway.25 This is accomplished through the The following sections consider how a dynam-
cooperative activations of the genioglossus and ical systems perspective may reframe four ques-
palatal elevator and by the palatoglossus and tions about neonatal feeding faced by
palatopharyngeus muscles and the posterior practitioners at each bedside visit: when to
cricoarytenoid.26 In preparation for a swallow, initiate oral feeds, how to determine the ro-
and for deglutition proper, a different set of bustness of neonatal breathing during feeding
anatomical constrictions and openings define a and appropriate levels of respiratory support,
pathway for fluid that excludes the bolus from instrumental assessments of swallow function in
the airway as it is forcefully pumped through the preterm newborns, and whether or not to
82 SEMINARS IN SPEECH AND LANGUAGE/VOLUME 38, NUMBER 2 2017

introduce thickened liquids. In each case, the process that mature convergently, but not nec-
concepts from a dynamical systems perspective essarily synchronously.40 Sucking and swallow-
place individual behaviors in a broader context. ing are a highly linked and softly assembled
synergy. Modifications to the kinematics of
sucking enable greater stability within the
When to Initiate Oral Feeds physiology of the pharyngeal swallow, facilitat-
In the decades since the 1997 articles on ing safe bolus passage.41 Providing small
neonatal feeding that appeared in this journal, amounts of breast milk or formula on a pacifier
the controversy over when to initiate oral feeds or finger promotes exploration of milk or
has been informed by a greater appreciation for formula taste, a means for establishing infor-
feeding complexity (i.e., an expanding of the mational coupling to guide sucking.42
range of variables that may be used to make Consistent with a dynamical systems
diagnostic judgments). Rather than simply fo- view, there are now subjective diagnostic
cusing on gestational age or on the expected age assessment tools that describe physiological
at which coordination between sucking and and behavioral parameters of “infant-driven,”

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breathing emerges,31 evidence-based practice or responsive feeding in determining readiness
is now turning to considerations of the new- to initiate oral feeding. Among these tools are
born’s signs of readiness to initiate oral feeding the Early Feeding Skills Assessment, a check-
such as level of alertness, state regulation, list for assessing not only newborn readiness
demonstration of hunger “cues,” and the extent for and tolerance of oral feedings, but also for
to which the newborn requires respiratory sup- assessing specific feeding skills, such as re-
port (see Shaker, this issue).32–34 maining engaged in feeding, coordinating
Earlier diagnostic assessments focused on swallowing and breathing, and maintaining
sucking and oral motor function, such as the physiologic stability.43 Another is the Support
Neonatal Oral Motor Assessment Scale,35 to of Oral Feeding for Fragile Infants, an assess-
characterize neonatal feeding. When consid- ment that examines feeding behavior rather
ering feeding in a dynamical systems ap- than the amount of food ingested.44 These
proach, oral motor function is only a small two approaches to determining feeding readi-
component of the larger decision-making ness are part of the current trend toward
process in initiating oral feeding. Healthy establishing in the neonatal intensive care
preterm newborns may be able to successfully unit (NICU) a “culture of feeding” (see
initiate oral feedings earlier and achieve full Shaker, Part II, this issue).32,45
oral feeding faster,36 and a “term sucking
pattern” is not necessarily required for suc-
cessful oral feeding.37 Conversely, preterm Oral Feeds and Level of Respiratory
newborns with more complicated courses Support: The Role of Robustness
and higher neonatal morbidity may require Another major outcome of the current appre-
additional time before they are appropriate to ciation for the synergy between sucking, swal-
consider for initiation of oral feeding.38 lowing, and breathing during oral feedings is an
When sucking alone is assessed in deter- attempt to address questions that clinicians may
mining feeding readiness, the synergistic nature have regarding appropriate feedings at different
of oral feeding and the intricate requirements of levels of neonatal respiratory support while in
coordination between sucking, swallowing, and the NICU (see Gross and Trapani-Hanase-
breathing are not taken into account. When wych, this issue).46 These questions include
viewed through a dynamical systems model, on whether oral feeds should be initiated during
the other hand, the neonate’s ability to feed the period of respiratory support with continu-
successfully is assessed based on his or her ous positive airway pressure (CPAP) or high-
physiologic stability, state regulation, respira- flow nasal cannula (HFNC). Here, we offer a
tory patterns, and attention/interaction, in ad- concept from dynamics, called robustness to
dition to his or her ability to suck.39 There are perturbation, as a potential way of helping
multiple subsystems involved in the feeding clinicians to decide whether or when to initiate
NEONATAL FEEDING BEHAVIOR/GOLDFIELD ET AL 83

oral feedings while newborns are being sup- line respiratory disease, considering that flow
ported by CPAP or HFNC. rate required may serve as a proxy for severity of
The robustness of a complex system is an illness. Second is the manner by which in-
indication of its ability to maintain functionality creased pressure force from nCPAP or
despite internal and external perturbations. As HFO2-NC may impact (1) swallow function,
one illustration, neural circuits are robust be- (2) airway protection from above, and (3) risk of
cause they maintain target performance despite bolus misdirection resulting in aspiration.51
ongoing neuron channel and receptor turn- Because the majority of newborns who aspirate
over.47 In the context of attractor dynamics, during the swallow do so silently,52 to reliably
robustness refers to the way that a system may assess the impact of HFO2-NC or nCPAP on
either return to its current attractor or move to a swallow function, instrumental assessment
new one that maintains a system’s functions. would be indicated. Conversely, it is also worth
Consider the respiratory pattern of a newborn considering if the neonate’s lung capacity may
during quiet sleep, apparently governed by a be improved on HFO2-NC or nCPAP, may
limit-cycle attractor with a characteristic signa- make the newborn better able to tolerate respi-

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ture of 1 Hz. Internal perturbations of the ratory suppression during the swallow, and, if
respiratory cycle during quiet sleep include his or her work of breathing is improved,
natural fluctuations in neural excitation, includ- whether sucking-swallowing-breathing coordi-
ing muscle “twitches.”48 External perturbations nation may also be improved.
of breathing include swallowing in response to
accumulations of saliva, loud sounds, or care-
giver postural adjustments. Preterm newborns Use of Instrumental Swallowing
who experience apneic breathing may be more Assessments
susceptible to both internal and external per- Given the increased risk of silent aspiration in
turbations and have particular difficulty in newborns who aspirate,52 instrumental swal-
adapting their breathing to deglutition. In other lowing assessments, such as the videofluoro-
words, compared with term newborns, the scopic swallow study (VFSS) or fiberoptic
breathing patterns of many premature neonates endoscopic evaluation of swallowing (FEES),
are less robust. allow for further definition of physiological
Clinical interventions to support respira- swallow function (see Arvedson and Lefton-
tion of neonates in intensive care may also Greif, this issue).53 The VFSS examines swal-
influence the robustness to deglutition pertur- low function in all phases of neonatal swallow-
bations during introduction of oral feedings. ing, providing rich information for an
These interventions include nasal CPAP, or assessment of feeding as a complex, dynamical
nCPAP, and high-flow oxygen via nasal can- system. However, the use of ionizing radiation
nula (HFO2-NC). HFO2-NC is defined as and thickening agents for assessment make the
small, thin tapered nasal tubes that deliver use of VFSS in newborns controversial. Issues
oxygen or blended oxygen/air at gas flows of include: (1) liquids tested (i.e., barium) during
more than 1 L/min.49 Oxygen delivered by VFSS may not match the prescribed liquids in
HFNC is often heated and humidified. The terms of viscosity,54,55 and (2) the amount of
goal of HFNC is to wash out nasopharyngeal radiation exposure during VFSS to a preterm or
dead space and increase pharyngeal pressure to term newborn is not insignificant. Benefits of
reduce work of breathing.50 using FEES versus VFSS include the ability to
When considering if it is appropriate to assess breast-feeding in a more natural setting/
initiate oral feeding with newborns in the position and no exposure to radiation during
NICU who require nCPAP or HFO2-NC FEES assessment. However, FEES provides a
for respiratory support, there are several factors limited view of the swallow with whiteout
that must be taken into consideration. The first during airway closure, which may make it
question to be asked is why the neonate may difficult to capture aspiration during the swal-
require this level of respiratory support, includ- low, in particular with consecutive sucking and
ing the newborn’s respiratory status and base- swallowing bursts.56
84 SEMINARS IN SPEECH AND LANGUAGE/VOLUME 38, NUMBER 2 2017

Oral Feedings and Consortia dynamical system. In the near future, we can
If a newborn exhibits oropharyngeal dysphagia expect vast amounts of new data on interactions
on videofluoroscopy that does not improve with between developing neonate, microbiome,
the use of therapeutic feeding interventions such caregiver, and environment to guide evidence-
as slow flow nipples, side-lying position, and based practice. But unless practitioners are able
pacing, then thickened liquids may be consid- to integrate these “big data” into their daily
ered a treatment option. The use of thickened decision making, progress in therapeutic inter-
liquids in pediatrics to treat dysphagia, and ventions will not be effectively translated to the
particularly with neonates, remains controver- clinic.
sial. A new direction for evaluating the potential
negative effects of thickening agents is to iden-
DISCLOSURES
tify their effects on the community structure of
Eugene C. Goldfield receives salary from
the neonatal gut microbiome.57 In this approach,
Boston Children’s Hospital and from the
deviations from normal microbiota development
Wyss Institute.
may be used as a measure of risk assessment for

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Jennifer Perez receives a salary from Boston
disease, such as necrotizing enterocolitis (NEC).
Children’s Hospital.
In the first postnatal week, the full-term neona-
Katherine Engstler receives a salary from
tal gut microbiome is primarily colonized by
Boston Children’s Hospital.
members of the Actinobacteria, Proteobacteria,
Bacteroidetes, and to a lesser extent Firmi-
cutes.58 By contrast, the gut microbiome of ACKNOWLEDGMENT
newborns weighing less than 1,200 g is domi- The writing of this manuscript was supported in
nated by Firmicutes and Tenericutes. Postnatal part by the Wyss Institute, and BCH IDDRC,
nutrition plays a fundamental role in the succes- 1U54HD090255.
sion of bacterial colonization: healthy breast-fed
newborns receive a mix of nutrients, bacteria,
and oligosaccharides that are believed to prevent REFERENCES
the attack of enteropathogens.59 In addition to
this altered microbial diversity in the gut micro- 1. Goldfield EC. A dynamical systems approach to
biome, premature newborns are immunode- infant oral feeding and dysphagia: from model
ficient, predisposing them to invasion by system to therapeutic medical device. Ecol Psychol
pathogens that may lead to disease processes 2007;19:21–48
2. Spanogiannopoulos P, Bess EN, Carmody RN,
such as NEC.60 It is this context within which
Turnbaugh PJ. The microbial pharmacists within
future research may fruitfully determine the us: a metagenomic view of xenobiotic metabolism.
association between thickening agents and Nat Rev Microbiol 2016;14(5):273–287
NEC. 3. Goldfield EC. Emergent Forms: Origins and Early
Development of Human Action and Perception.
New York, NY: Oxford University Press; 1995
CONCLUSIONS 4. Kubo M, Wagenaar RC, Saltzman E, Holt KG.
Biomechanical mechanism for transitions in phase
A fundamental and daunting task of speech-
and frequency of arm and leg swing during walking.
language pathologists and other members of the Biol Cybern 2004;91(2):91–98
feeding team is to diagnose why a newborn is 5. Boonstra TW, Daffertshofer A, van As E, van der
not eating and gaining weight, and to imple- Vlugt S, Beek PJ. Bilateral motor unit synchroni-
ment therapies that promote improved health. zation is functionally organized. Exp Brain Res
Our hope is that the systems approach pre- 2007;178(1):79–88
sented here may (1) stimulate an appreciation of 6. Miller AJ. Oral and pharyngeal reflexes in the
mammalian nervous system: their diverse range in
a perspective that includes the rich context of
complexity and the pivotal role of the tongue. Crit
the newborn and caregiver, and (2) modify Rev Oral Biol Med 2002;13(5):409–425
practice in a way that reflects advances in 7. Goldfield EC, Richardson MJ, Lee KG, Margetts
what we now know about the multiple compo- S. Coordination of sucking, swallowing, and
nents of the newborn as part of a complex breathing and oxygen saturation during early infant
NEONATAL FEEDING BEHAVIOR/GOLDFIELD ET AL 85

breast-feeding and bottle-feeding. Pediatr Res cortex of monkeys. J Neurophysiol 2005;94(6):


2006;60(4):450–455 4209–4223
8. Goldfield EC, Buonomo C, Fletcher K, et al. 23. Graziano MS, Aflalo TN. Rethinking cortical
Premature infant swallowing: patterns of tongue- organization: moving away from discrete areas
soft palate coordination based upon videofluoro- arranged in hierarchies. Neuroscientist 2007;
scopy. Infant Behav Dev 2010;33(2):209–218 13(2):138–147
9. Flash T, Hochner B. Motor primitives in verte- 24. Vogel S. Comparative Biomechanics: Life’s Physi-
brates and invertebrates. Curr Opin Neurobiol cal World. 2nd ed. Princeton, NJ: Princeton Uni-
2005;15(6):660–666 versity Press; 2013
10. Hogan N, Sternad D. Dynamic primitives of motor 25. Miller MJ, Kiatchoosakun P. Relationship between
behavior. Biol Cybern 2012;106(11–12):727–739 respiratory control and feeding in the developing
11. Goldfield EC, Schmidt RC, Fitzpatrick P. Coor- infant. Semin Neonatol 2004;9(3):221–227
dination dynamics of abdomen and chest during 26. Miller AJ. The neurobiology of swallowing and
infant breathing: a comparison of full-term and dysphagia. Dev Disabil Res Rev 2008;14(2):77–86
preterm infants at 38 weeks postconceptional age. 27. Sawczuk A, Mosier KM. Neural control of tongue
Ecol Psychol 1999;11:209 movement with respect to respiration and swallow-
12. Goldfield EC, Wolff PH, Schmidt RC. Dynamics ing. Crit Rev Oral Biol Med 2001;12(1):18–37

Downloaded by: University of Texas at Dallas. Copyrighted material.


of oral-respiratory coordination in full-term and 28. Rautava S, Luoto R, Salminen S, Isolauri E.
preterm infants: I. Comparisons at 38–40 weeks Microbial contact during pregnancy, intestinal col-
postconceptional age. Dev Sci 1999;2:363 onization and human disease. Nat Rev Gastro-
13. Goldfield EC, Wolff PH. A dynamical systems enterol Hepatol 2012;9(10):565–576
perspective on infant action and it’s development. 29. Gensollen T, Iyer SS, Kasper DL, Blumberg RS.
In: Bremner G, Slater A, eds. Theories of Infant How colonization by microbiota in early life shapes the
Development. Oxford, UK: Wiley-Blackwell; immune system. Science 2016;352(6285):539–544
2004:400 30. Subramanian S, Blanton LV, Frese SA, Charbon-
14. Dominici N, Ivanenko YP, Cappellini G, et al. neau M, Mills DA, Gordon JI. Cultivating healthy
Locomotor primitives in newborn babies and their growth and nutrition through the gut microbiota.
development. Science 2011;334(6058):997–999 Cell 2015;161(1):36–48
15. Hsu WH, Miranda D, Young D, Cakert K, 31. Hack M, Estabrook MM, Robertson SS. Develop-
Qureshi M, Goldfield E. Developmental changes ment of sucking rhythm in preterm infants. Early
in coordination of infant arm and leg movements Hum Dev 1985;11(2):133–140
and the emergence of function. J Mot Learn Dev 32. Shaker C. Cue-based co-regulated feeding in the
2014;2:69–79 neonatal intensive care unit: Supporting parents in
16. Ijspeert AJ, Nakanishi J, Hoffmann H, Pastor P, learning to feed their preterm infant. Newborn
Schaal S. Dynamical movement primitives: learn- Infant Nurs Rev 2013;13:51–56
ing attractor models for motor behaviors. Neural 33. Wellington A, Perlman JM. Infant-driven feeding
Comput 2013;25(2):328–373 in premature infants: a quality improvement proj-
17. Adolph KE, Kretch KS. Gibson’s Theory of ect. Arch Dis Child Fetal Neonatal Ed 2015;
Perceptual Learning. International Encyclopedia 100(6):F495–F500
of the Social and Behavioral Sciences, 2nd edi- 34. Shaker C. Infant-guided, co-regulated feeding in
tion, Volume 10. New York: Elsevier; 2015: the neonatal intensive care unit (NICU) part I:
127–134 theoretical underpinnings for neuroprotection and
18. Turvey MT. Action and perception at the level of safety. Speech Lang 2017;38(2):96–105
synergies. Hum Mov Sci 2007;26(4):657–697 35. Palmer MM, Crawley K, Blanco IA. Neonatal
19. Kelso JA, Tuller B, Vatikiotis-Bateson E, Fowler Oral-Motor Assessment scale: a reliability study.
CA. Functionally specific articulatory cooperation J Perinatol 1993;13(1):28–35
following jaw perturbations during speech: evi- 36. Simpson C, Schanler RJ, Lau C. Early introduction
dence for coordinative structures. J Exp Psychol of oral feeding in preterm infants. Pediatrics 2002;
Hum Percept Perform 1984;10(6):812–832 110(3):517–522
20. Overduin SA, d’Avella A, Carmena JM, Bizzi E. 37. Lau C, Sheena HR, Shulman RJ, Schanler RJ. Oral
Microstimulation activates a handful of muscle feeding in low birth weight infants. J Pediatr 1997;
synergies. Neuron 2012;76(6):1071–1077 130(4):561–569
21. Overduin SA, d’Avella A, Carmena JM, Bizzi E. 38. Dodrill P, Donovan T, Cleghorn G, McMahon S,
Muscle synergies evoked by microstimulation are Davies PS. Attainment of early feeding milestones in
preferentially encoded during behavior. Front preterm neonates. J Perinatol 2008;28(8):549–555
Comput Neurosci 2014;8:20 39. Shaker C. Feed me only when I am cueing: moving
22. Graziano MS, Aflalo TN, Cooke DF. Arm move- away from a volume-driven culture in the NICU.
ments evoked by electrical stimulation in the motor Neonatal Intensive Care 2012;25:27–32
86 SEMINARS IN SPEECH AND LANGUAGE/VOLUME 38, NUMBER 2 2017

40. Thoyre S. Developmental transition from gavage to feeding. National Association of Neonatal
oral feeding in the preterm infant. In: Miles M, Therapists; 2014
Holditch-Davis D, eds. Annual Review of Nursing 51. Dodrill P, Gosa M, Thoyre S, et al. First do no
Research. New York, NY: Springer; 2003:61–92 harm: a response to “Oral alimentation in neona-
41. McGrattan KE, Sivalingam M, Hasenstab KA, tal and adult populations requiring high-flow
Wei L, Jadcherla SR. The physiologic coupling oxygen via nasal cannula.”. Dysphagia 2016;
of sucking and swallowing coordination provides a 31(6):781–782
unique process for neonatal survival. Acta Paediatr 52. Uhm KE, Yi SH, Chang HJ, Cheon HJ, Kwon JY.
2016;105(7):790–797 Videofluoroscopic swallowing study findings in
42. Ross ES, Browne JV. Developmental progression full-term and preterm infants with dysphagia.
of feeding skills: an approach to supporting feeding Ann Rehabil Med 2013;37(2):175–182
in preterm infants. Semin Neonatol 2002;7(6): 53. Arvedson J, Lefton-Greif M. Instrumental assess-
469–475 ment of pediatric dysphagia. Semin Speech Lang
43. Thoyre SM, Shaker CS, Pridham KF. The early 2017;38(2):135–146
feeding skills assessment for preterm infants. Neo- 54. Cichero J, Nicholson T, Dodrill P. Liquid barium
natal Netw 2005;24(3):7–16 is not representative of infant formula: characteri-
44. Ross ES, Philbin MK. Supporting oral feeding in sation of rheological and material properties. Dys-

Downloaded by: University of Texas at Dallas. Copyrighted material.


fragile infants: an evidence-based method for qual- phagia 2011;26(3):264–271
ity bottle-feedings of preterm, ill, and fragile in- 55. Stuart S, Motz JM. Viscosity in infant dysphagia
fants. J Perinat Neonatal Nurs 2011;25(4): management: comparison of viscosity of thick-
349–357, quiz 358–359 ened liquids used in assessment and thickened
45. Shaker C. Infant-guided, co-regulated feeding in liquids used in treatment. Dysphagia 2009;24(4):
the neonatal intensive care unit (NICU) part II: 412–422
interventions to promote neuroprotection and safe- 56. Willette S, Molinaro LH, Thompson DM,
ty. Semin Speech Lang 2017;38(2):106–115 Schroeder JW Jr. Fiberoptic examination of swal-
46. Gross R. Trapani-Hanasewych M. Breathing and lowing in the breastfeeding infant. Laryngoscope
swallowing - the next frontier. Semin Speech Lang 2016;126(7):1681–1686
2017;38(2):87–95 57. Blanton LV, Barratt MJ, Charbonneau MR,
47. Marder E, Taylor AL. Multiple models to capture Ahmed T, Gordon JI. Childhood undernutrition,
the variability in biological neurons and networks. the gut microbiota, and microbiota-directed thera-
Nat Neurosci 2011;14(2):133–138 peutics. Science 2016;352(6293):1533–1539
48. Blumberg MS, Marques HG, Iida F. Twitching in 58. Prince AL, Chu DM, Seferovic MD, Antony KM,
sensorimotor development from sleeping rats to Ma J, Aagaard KM. The perinatal microbiome and
robots. Curr Biol 2013;23(12):R532–R537 pregnancy: moving beyond the vaginal microbiome.
49. Wilkinson D, Andersen C, O’Donnell CP, De Cold Spring Harb Perspect Med 2015;5(6):5
Paoli AG, Manley BJ. High flow nasal cannula for 59. Putignani L. Human gut microbiota: onset and
respiratory support in preterm infants. Cochrane shaping through life stages and perturbations.
Database Syst Rev 2016;2:CD006405 Front Cell Infect Microbiol 2012;2:144
50. Glass R, Wolf L. Don’t go with the flow: 60. Gritz EC, Bhandari V. The human neonatal gut
understanding the relationship of HFNC and microbiome: a brief review. Front Pediatr 2015;3:17

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