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AORXXX10.1177/0003489420965636Annals of Otology, Rhinology & LaryngologyMills et al

Original Article
Annals of Otology, Rhinology & Laryngology

Flexible Endoscopic Evaluation of


1­–13
© The Author(s) 2020
Article reuse guidelines:
Swallowing in Breastfeeding Infants sagepub.com/journals-permissions
DOI: 10.1177/0003489420965636
https://doi.org/10.1177/0003489420965636

With Laryngomalacia: Observed Clinical journals.sagepub.com/home/aor

and Endoscopic Changes With Alteration


of Infant Positioning at the Breast

Nikki Mills, MBChB, FRACS, PhD1,2 , Melissa Keesing, BSLT3,


Donna Geddes, DMU, PhD4, and Seyed Ali Mirjalili, MD, PhD2

Abstract
Objectives: This retrospective cohort study uses endoscopic assessment of the pharyngeal phase of swallowing in
infants with laryngomalacia, to ascertain the impact of infant positioning on airway compromise and fluid dynamics during
breastfeeding. The study aims to identify whether modification of infant positioning at the breast may improve the possibility
of safe, successful breastfeeding in infants with laryngomalacia and concurrent breastfeeding difficulty.
Methods: Twenty-three infants referred for noisy breathing and difficulty feeding were assessed with flexible endoscopic
evaluation of swallowing (FEES) during breastfeeding. All had endoscopically confirmed laryngomalacia. During FEES,
observations were made of clinical signs of airway compromise as well as endoscopically observable anatomical features
and swallowing dynamics during breastfeeding, including tongue base position, view of laryngeal inlet and vocal folds,
dynamic supraglottic soft tissue collapse, timing of milk flow into pyriform fossae/hypopharynx relative to sucking, and
presence of penetration and/or aspiration. If airway and/or swallowing compromise was present, the infant’s initial position
at the breast was altered from supine or semi lateral decubitus position to semi-prone, with a description of the clinical
and endoscopically observable changes that subsequently occurred.
Results: Signs of dynamic airway obstruction and/or compromised airway protection with swallowing were present in 20
of the 23 infants (87%) in their initial supine or semi lateral decubitus position. These 20 infants were repositioned to semi-
prone, with improvement and/or resolution of stridor and an improved ability to maintain latch in all infants. Continued
endoscopic evaluation following positional change was possible in 16 infants, identifying anterior positioning of the tongue
base, reduced dynamic supraglottic tissue collapse, reduced volume of milk flow into pyriform fossae during pauses in
sucking and resolution of penetration and aspiration.
Conclusion: This study has shown how alteration of breastfeeding position to semi-prone may improve dynamic airway
obstruction and reduce aspiration risk in infants with laryngomalacia.

Keywords
breastfeeding, swallowing, laryngomalacia, flexible endoscopic evaluation of swallowing, positioning

Introduction 1
Paediatric Otolaryngology Department, Starship Children’s Hospital,
Auckland, New Zealand
Infants with noisy breathing are commonly referred to an 2
Department of Anatomy and Medical Imaging, Faculty of Medical and
otolaryngologist for diagnostic assessment. It is important Health Sciences, University of Auckland, Auckland, New Zealand
to recognize that infants with airway compromise may also 3
Paediatric Speech-Language Therapy Department, Starship Children’s
have difficulties feeding,1,2 with breastfeeding being par- Hospital, Auckland, New Zealand
4
School of Molecular Sciences, Faculty of Science, University of Western
ticularly challenging for infants with any form of airway
Australia, Crawley, Western Australia, Australia
compromise.3 Early breastfeeding difficulties may jeopar-
dize effective milk removal at the breast and impact on Corresponding Author:
Nikki Mills, BHB, MBChB, FRACS, Dip Paeds, IBCLC, PhD, Paediatric
establishment of milk supply, which may precipitate an
Otolaryngology Department, Starship Children’s Hospital, Park Road,
early transition to bottle feeding. In order to improve the Grafton, Auckland 1023, Private Bag 92024, Auckland 1142, New
possibility of safe, successful breastfeeding in this cohort, it Zealand.
is critical to understand how airway compromise impacts Email: nikki@webrage.co.nz
2 Annals of Otology, Rhinology & Laryngology 00(0)

on swallowing in breastfeeding infants, then to determine laryngeal anatomy that can be helpful in the diagnosis of
whether there are any potential modifications that may both airway and swallowing pathology.19-22 However, as
improve their airway and swallowing dysfunction. FEES lacks objective measures that are readily available
When infant airway and feeding difficulties are present, with VFSS, the understanding of the pharyngeal phase of
a thorough multidisciplinary assessment is essential, with a the infant swallow remains predominantly based on research
range of investigations used to diagnose or exclude a broad using VFSS viewing bottle feeding.
range of potential anatomical and neurological anomalies When aspiration is identified during VFSS, a trial of
that could impact on feeding.4 Awake flexible trans-nasal modifications is usually undertaken as part of the assess-
endoscopy is a valuable investigation for identifying the ment, to determine if any are effective at improving airway
location of upper airway obstruction when an infant has protection with swallowing. These modifications may
noisy breathing,5 with laryngomalacia being the most com- include thickening fluid to slow the speed of bolus transit,
mon endoscopically diagnosed cause of noisy breathing in using a slower flow teat, using frequent pauses to “pace”
infants.6,7 Infants with laryngomalacia classically have feeds, reducing bolus volume, or altering temperature to
worsening of stridor associated with increased effort of increase the thermal sensory stimulus.23 Unfortunately, all
breathing during feeding, as well as often being reported to these options for modification preclude the possibility of
have frequent interruption of feeding caused by coughing continued breastfeeding, with no research to date evaluating
and choking episodes.8 These symptoms raise concern any modifications that would support continued feeding
regarding aspiration possibly occurring in some of these at the breast when aspiration has been diagnosed. For
infants, with acknowledgment that silent aspiration could infants with laryngomalacia severe enough to warrant
be occurring even in the absence of these clinical signs. In surgical intervention, an improvement in feeding difficul-
one study of infants with laryngomalacia, 85% had dyspha- ties and aspiration has been reported in many patients
gia, 50% poor weight gain, and 57% penetration and/or post-operatively.24-26 However, as only the most severely
aspiration on videofluoroscopic swallow study (VFSS).9 affected infants usually proceed to surgery, for the large
VFSS is the most commonly utilized instrumental cohort of infants with mild to moderate laryngomalacia,
assessment of infant swallowing when aspiration during there are limited strategies for addressing feeding difficul-
feeding is suspected.10 However, using a bottle in a VFSS to ties that would support continued breastfeeding.
assess an exclusively breastfeeding infant’s swallow is of There is little research assessing the impact of specific
questionable validity, given increasing evidence of differ- infant body positioning on infant swallowing. Bottle feed-
ences between the biomechanics of sucking when compar- ing research has not led to a consensus regarding an “ideal”
ing breastfeeding and bottle feeding.11-13 Because of feeding position, with research predominantly limited to
practical challenges in imaging or viewing the breastfeed- premature infants and using physiologic outcome measures
ing swallow, there is still very little known regarding the such as oxygen saturation, respiratory rate, heart rate, and
differences in the pharyngeal phase of swallowing between heart rate variability.27-30 Willette et al’s20 study on FEES in
breastfeeding and bottle feeding. There are only 2 published breastfeeding infants in 2015 suggested positional modifi-
cine radiographic studies (VFSS or historic equivalent) of cation in 15% of the infants as a strategy to improve feed-
breastfeeding that describe suck-swallow dynamics.11,14 ing, but they did not include any details on how or when this
Both are limited by poor image resolution, unnatural posi- strategy might be utilized and did not provide evidence for
tioning of the mother, and the inability to visualize breast its use. The positioning of an infant for breastfeeding is well
milk under cine radiography/fluoroscopy. These factors, recognized as being important for achieving maternal com-
together with radiation exposure to the mother and infant, fort and efficient milk transfer at the breast, with a variety
make VFSS an unsuitable clinical modality for assessment of positions existing that accommodate the variability in
of the breastfeeding swallow. Magnetic Resonance Imaging both maternal and infant anatomy.31-33 A semi-reclined
(MRI) is a non-radiating imaging modality that has been maternal position, with the infant semi-prone and their
recently used for the first time to capture the breastfeeding chest and abdomen flat against the mother’s body, has been
swallow, however, practical issues currently prevent this shown to effectively utilize gravity to provide positional
from being useful in clinic practice.15 stability for the infant and ensure optimal intra-oral breast
Fibreoptic or Flexible Endoscopic Evaluation of tissue volume.34 This semi-reclined maternal positioning
Swallowing (FEES) requires specialized equipment and has also been shown to trigger a wide range of innate
significant expertise and training in both procedural tech- reflexes in the infant that assist with successful rooting,
nique and interpretation of findings, but has been validated latching, and sucking33-36 but no studies have described how
as a safe an appropriate alternative to VFSS.16-19 FEES has this specific positioning impacts the infant’s breathing and
also proven to be an appropriate and safe modality for swallowing.
assessing the breastfeeding swallow and is able to provide The influence of an infant’s positioning on dynamic air-
a dynamic three-dimensional view of pharyngeal and way compromise is widely recognized, with the supraglottic
Mills et al 3

Figure 1. Cradle-hold: infant in supine or semi lateral decubitus position. Mother upright or slightly leaning over infant; infant supine,
with slight lateral tilt into semi lateral decubitus position. Weight of the infant supported by Mother’s hand, arm, and/or pillow.

soft tissue prolapse occurring with laryngomalacia known to nasogastric tube. All had been referred for feeding difficul-
be exacerbated when the infant is supine.9,37 This has been ties and/or airway compromise (n = 23 infants). All FEES
confirmed radiologically, with posterior displacement of the took place at a tertiary referral pediatric hospital with
tongue base, retroflexion of the epiglottis and narrowing of approval for this retrospective audit given by the National
the 3-dimensional space of the pharyngeal airway when Ethics Committee. Patient demographics and medical infor-
imaging is captured in the supine position.38 The impact of mation were retrieved from electronic patient records,
gravity on an infant’s airway is commonly utilized in clinical including referral source, primary presenting symptoms, the
practice in infants with Pierre Robin Sequence, with prone presence of a nasogastric tube, oxygen requirement, and
positioning improving the pharyngeal airway by displacing any prior VFSS assessments.
the tongue base anteriorly.39,40 Takagi et al has reported suc- The multidisciplinary FEES team included a pediatric
cessful feeding of infants with Pierre Robin Sequence and otolaryngologist with lactation consultant training (N.M.),
airway compromise using prone positioning, which was at least one pediatric speech-language pathologist (SLP), a
enabled in the study using a specially modified bottle.41 pediatric nurse specialist, and when possible, a lactation
In spite of the body of knowledge on the importance of consultant was also present. The FEES were performed in
positioning for infants with dynamic airway compromise, the outpatient clinic or at bed-side for inpatients. When
we have not identified any publications specifically compromised breathing and/or swallowing was present dur-
assessing the impact of infant positioning during feeding ing breastfeeding, the endoscope was kept in situ to observe
in infants with laryngomalacia. Aiming to further under- swallowing following modification of latching position, to
standing in this area, this retrospective study uses FEES to determine if altered positioning improved the dynamic air-
describe the clinical and endoscopically observed changes way collapse and/or aspiration.
occurring with alteration of breastfeeding positioning in a
cohort of infants presenting with laryngomalacia and feed-
ing difficulties. FEES Protocol for Breastfeeding Infants
The infant was positioned on the mother’s lap, with prepa-
Methods and Participants ration for the mother to transition as easily as possible to
breastfeed in their usual feeding position without readjust-
Study Design and Participants ment of clothing or position. All mothers chose which breast
This is a descriptive study of infants with laryngomalacia, to feed from and started by latching their infant in their
involving a retrospective audit of our clinical practice using usual breastfeeding position. For all, the initial position of
FEES to assess swallowing whilst feeding at the breast and choice was a cradle hold, with the infant supine or semi-
trialing repositioning of the infant as a modification if signs lateral decubitus and the mother using their arm or a pillow
of compromised airway and/or swallowing were present. to support the weight of the infant (Figure 1).
We reviewed all FEES that assessed breastfeeding of infants Video and audio recordings were captured of the endo-
with endoscopically diagnosed laryngomalacia, performed scopic procedure using a Storz Telepack with a 1.9 mm flex-
or directly supervised by the lead author (N.M.) between 1st ible fiberoptic endoscope. The endoscope was lubricated
September 2016 and 31st October 2019. All infants were with a small amount of viscous 2% lidocaine and passed
breastfed, with some receiving supplementary calories via a through the side of the infant’s nasal airway closest to the
4 Annals of Otology, Rhinology & Laryngology 00(0)

Figure 2. Use of rubber band to help secure endoscope position at infant nares.

endoscopist or on the same side as the nasogastric tube if present, the infant was repositioned at the breast to be
present, to leave the other nostril unimpeded for breathing. semi-prone, with the mother in a “laid-back” position.
As the endoscope was advanced, observation was made This transition was done by bringing the infant into a side
of the nasal airway, soft palate, pharyngeal, and laryngeal lying position with their abdomen in close contact with the
anatomy. The endoscope was secured in position at the mother, then gently reclining the mother to bring the infant
nares utilizing a rubber band, which was slid down the into a semi-prone position (Figure 3). Exact positioning
endoscope and taped to the dorsum of the infant’s nose was modified as needed to adapt to the individual mother
(Figure 2). This is a low-cost technique developed to give and infants’ anatomy and optimal comfort. The majority of
some security to endoscope positioning without the endos- infants had the axis of their body orientated horizontally,
copist’s hand impeding the mother’s visual and physical with a few improving further if positioned more diago-
access to her infant for latching. Once the endoscope was nally across their mother’s abdomen (with the infant’s feet
positioned in the pharynx, observations were made of the lower than their head), maintaining a semi-prone but more
infant’s vocal fold movement, dynamic supraglottic tissue upright position (Figure 4). Repositioning was facilitated
prolapse, pharyngeal constrictor function, and management by using a chair that accommodated the mother being
of saliva and secretions. reclined, however, these positional adaptations were still
The infant was then allowed or assisted by their mother possible in a standard chair with an upright back (Figure
to latch, with our nurse specialist aiding in minimizing 3). Clinical observation documented any change in the
endoscope displacement during this maneuver. Once the noise or work of breathing and endoscopic observation
infant was latched and sucking established, the breastfeed noted any changes to airway dynamics and/or the pharyn-
was observed endoscopically, noting tongue base position, geal phase of the swallow.
dynamic supraglottic soft tissue collapse (and correlation Following completion of the procedure, the video (with
with audible stridor), dynamics of milk flow into the hypo- combined audio) recording was reviewed and assessed by
pharynx, the presence of penetration and or aspiration, and the otolaryngologist and SLP, with the images transferred to
any observable cough response if/when this occurred. a computer to allow slow motion and frame-by-frame
Penetration was defined as milk being seen to enter the review. The captured images and videos are also used to
laryngeal inlet prior to swallow initiation and aspiration explain findings to the parents.
diagnosed when milk was visualized passing below the
vocal folds, either before or after swallowing.
Detailed Analysis of Captured Imaging
For the purposes of this audit, a detailed descriptive analy-
Alteration of Infant Positioning sis of the endoscopically observed dynamic pharyngeal
After an initial period of observation of active sucking, if anatomy and swallowing was then undertaken (as part of
airway compromise and/or penetration or aspiration were the primary author’s PhD research). This review focused on
Mills et al 5

Figure 3. Semi-prone positioning. Mother is slightly reclined, infant horizontal (right side lower) but positioned semi prone and held
closely (“tummy-to-tummy”) to mother.

Figure 4. Variations of semi-prone positioning. In all variations, the infant is semi prone and held closely (“tummy to tummy”) with
their mother. Images (A and F) show the infant in horizontal positioning, (B and C) show diagonal positioning, (D) more upright infant
position, (E) infant almost fully prone with the mother lying almost flat (image taken from above infant).

describing general features observable during FEES of the supraglottic soft tissues), dynamic supraglottic soft tissue
breastfeeding infant. This included evaluation of tongue collapse and the timing, and flow of milk visible in the
base and epiglottic position, a visual perception of volume hypopharynx as temporally related to the infant’s active
capacity of the pyriform fossae, the view of the glottic inlet sucking, with these observations being presented as a
and vocal cords (and relative obscuring of this view by descriptive summary.
6 Annals of Otology, Rhinology & Laryngology 00(0)

Table 1. Patient Demographics and Clinical Variables.

Demographics and Clinical Number of Infants, Percentage


Variables Variables n = 23 (%)
Gender Male 11 48
Female 12 52
Ethnicity European 13 56
Maori 3 13
Pacific Island 5 22
Asian 2 9
Age, wk Range 1-37
Average 11
Referred by Neonatologist/pediatrician 15 65
Speech-language pathologist 2 9
General practitioner (family doctor) 3 13
Otolaryngologist 2 9
Lactation consultant 1 4
Indication for referral (may Difficulty feeding 23 100
have multiple ~) Noisy breathing (worsened with feeding) 21 91
Coughing/choking/not able to maintain latch 19 83
Concerns regarding aspiration 16 70
Current mode of feeding Exclusive breastfeeding 19 83
Breastfeeding (with nasogastric top-ups) 4 19
Previous VFSS No 22 96
Yes (showing aspiration) 1 4
Supraglottoplasty Prior to FEES 3 13
After FEES 1 4

Results Observations of Swallowing During


Breastfeeding
Participant Demographics, Comorbidities, and
Endoscopic Diagnoses FEES was completed with the mother’s breastfeeding in
their usual latching position, which for all was a cradle or
Analysis was made of data from 23 infants with laryngo- cross-cradle position with the infant in a supine or semi-
malacia who had undergone FEES whilst breastfeeding. lateral decubitus position, with their weight supported by a
Patient demographics, referrer, indication for referral, and pillow or their mother’s arms. A summary of endoscopic
current feeding mode are outlined in Table 1. Twelve observations of the breastfeeding infant’s swallow are
patients had no known co-morbidities. The other 11 patients detailed in Table 2 and an example of imaging captured
had one or more comorbidities, which included 5 infants shown in Supplemental Video 1. We include a description
with neurologic diagnoses and/or conditions associated of features of pharyngeal anatomy and the pharyngeal phase
with low muscle tone, 2 infants with Down Syndrome, of swallowing that were well visualized endoscopically and
4 with primary congenital cardiac anomalies, 4 who had outline aspects that were not easy to view or assess.
been born prematurely (30-35 weeks gestation), and 2 who
had repaired tracheo-esophageal fistulas. Three of the Observed Changes Associated With Modified
infants had undergone supraglottoplasty prior to the FEES
but were referred for persistent feeding difficulties. One Latching Position
infant had significant nocturnal airway compromise associ- In 3 infants, there was no clinically or endoscopically
ated with their laryngomalacia and proceeded subsequently observable compromise of breathing or swallowing during
to supraglottoplasty. Five infants were on low flow nasal the assessment and therefore no indication for positional
prong oxygen with the remainder breathing spontaneously modification. Twenty infants had compromised breathing
in room air. All of the infants were exclusively breastfeed- and/or swallowing during breastfeeding with 16 (80%) of
ing, with 4 receiving supplementary calories via a nasogas- these infants having stridor induced during the feeding with
tric tube. No complications occurred during any of the observable prolapse of supraglottic soft tissues on inspira-
FEES procedures. tion, 11 (55%) being unable to maintain their latching
Mills et al 7

Table 2. Endoscopic Observations of the Breastfeeding Swallow During FEES.

Assessment during the


Breastfeeding Swallow Endoscopic Visualization
General observations •• Sucking movement was visible with an antero-posterior movement of the tongue base and
associated “rocking” movement of the epiglottis
•• The soft palate remained in apposition with the tongue base during sucking
•• The free edge of the soft palate was usually near the vallecula and the tip of the epiglottis gliding
up into the nasopharynx
•• Milk flows into the gravity dependent (lower) pyriform fossa if side lying
•• Milk continued to flow (into the pyriform fossa) during pauses in sucking
•• The volume of milk visible in the pyriform fossa prior to the swallow being initiated varied
throughout the feed in every infant. A larger volume of milk was likely to accumulate in the
pyriform fossa when the infant paused for sequential breaths without sucking or swallowing
•• The milk volume and flow rate were variable during a feed (fastest during milk ejection reflex/es)
and varied significantly between mother and infant dyads
•• Sucking and swallowing patterns varied throughout the feed and appeared very responsive to
visible changes in milk flow
Diagnosis of penetration •• Pre-swallow penetration was usually easily visualized and was the most common timing for
and aspiration penetration/aspiration events seen in our study
•• Penetration (milk passing into the laryngeal inlet) occurring before the swallow was usually well
visualized, but was dependent on endoscope positioning and supraglottic anatomy
•• Aspiration (milk passing through the vocal folds) was more difficult to directly visualize, as
a direct view of the vocal folds was usually intermittent whilst the infant was feeding. With
laryngomalacia, the supraglottic soft tissues often obscured the view of the vocal folds,
particularly when the infant was supine
•• More subtle events required diagnosis on slow motion video review
•• Events (including aspiration) that occur during the swallow are poorly visualized, as a “white-
out” (a brief loss of view) occurs during swallow secondary to pharyngeal constriction
momentarily closing soft tissues over the endoscope lens as the peristaltic movement propels
the liquid bolus through the pharynx
•• Aspirated milk could occasionally be seen expelled from below the vocal folds into the laryngeal
inlet on expiration immediately post swallow
•• Post swallow pharyngeal residue (+/− aspiration of residue) is usually well visualized

position due to airway compromise or choking, and 15 decubitus position, the infant’s tongue base was displaced
(75%) having endoscopically observed aspiration and/or posteriorly and the epiglottis was generally retroflexed.
penetration (with 10 of these infants having silent events, This was associated with increased signs of airflow
with no overt cough response). obstruction (clinically and endoscopically) in 20 of the 23
Accordingly, 20 infants proceeded to a trial of modified infants during feeding. In these 20 infants, modification to
positioning. In 4 (20%) procedures, the endoscope was dis- semi-prone position led to a reduction or resolution of
placed during the change in infant positioning, so subse- audible stridor, with all infants able to maintain their latch
quent assessment was made using only clinical observation. with no coughing or choking. In the 16 infants where con-
Continued endoscopic assessment following positional tinued endoscopic observation was possible following
modification was possible in 16 (80%) infants. A summary positional change, all had reduced dynamic prolapse of
of endoscopically observed changes following altered posi- supraglottic tissues. This, together with more anterior
tioning are described in Table 3, with focus on the perceived positioning of the tongue base and reduced retroflexion of
impact on the infant’s airway and on the dynamics of milk the epiglottis, created an improved view of the laryngeal
flow as observed in transit through the pharynx. inlet and vocal folds. Figure 5 and Supplemental Video 2
show imaging captured before and after positional change
Impact of Positional Change on Dynamic Airway to illustrate these changes in 1 infant. The findings of
reduced endoscopically visible signs of dynamic airway
Compromise obstruction correlated with the clinically observed reduc-
When the infants were positioned for feeding in a traditional tion in audible stridor and signs of reduced work of breath-
cradle hold, with a predominantly supine or semi-lateral ing in all patients.
8 Annals of Otology, Rhinology & Laryngology 00(0)

Table 3. Endoscopic Observations: Relative Changes With Infant Positioning During FEES.

Infant Positioning Endoscopic Observations


Supine •• Tongue base displaced posteriorly
•• Reduced volume capacity of pyriform fossae
•• Epiglottis retroflexed (resting position)
•• Compromised view of laryngeal inlet/vocal folds
•• Increased dynamic supraglottic airway collapse (+/− stridor and increased work of breathing)
•• Milk flow visible into pyriform fossae/pharynx when sucking paused (associated with increase in
pre-swallow penetration/aspiration events)
Changes observed: moving •• Tongue base positioned more anteriorly
from supine to semi-prone •• Increased volume capacity in pyriform fossae
•• Epiglottis more upright at rest
•• Improved view of laryngeal inlet/vocal folds
•• Reduced dynamic supraglottic airway collapse (reduced stridor and work of breathing)
•• Less milk visible flowing into pyriform fossae during pauses in sucking (with associated
resolution of pre-swallow penetration/aspiration events)
•• Earlier initiation of swallow (before or as milk enters pyriform fossae)
•• Maintenance of latch (reduced milk flow +/− airway related disruption)
Side lying •• Milk always flows into pharynx via the gravity dependent (lower) pyriform fossa

Figure 5. Endoscopic view of pharynx with infant positioned supine (left image) then semi-prone (right image). Both images captured
during a pause in sucking.
Abbreviations: E, epiglottis; TB, tongue base; PF, pyriform fossae.

Impact of Positional Change on Visible Milk Flow during the feed, milk would continue to visibly flow and
Into Pharynx accumulate in the space of the pyriform fossa during these
pauses in active sucking. During these pauses, the pyriform
With FEES allowing observation of a full breastfeed, we fossa would act briefly as a fluid reservoir, with its volume
were able to identify significant variability in milk flow rates, capacity dependent on its specific dimensions. A swallow
infant sucking patterns and the timing of swallowing and would usually be triggered before the milk filled the capacity
breathing. The flow and volume of milk entering the pyri- of the pyriform fossa and flowed over the free edge of the
form fossa prior to swallow initiation varied both during a aryepiglottic fold into the laryngeal inlet (Figure 6). Infants
feed as well as varying between individuals. Our observation with increased respiratory rate and/or effort of breathing
was that all infants had active sucking bursts, interspersed required more frequent and longer pauses in active sucking.
with pauses of variable duration. In all infants, at times In this cohort, during these pauses, milk was more likely to
Mills et al 9

Figure 6. Sequential FEES images: milk filling right pyriform fossa during pause in active sucking. Infant positioned side-lying, with
right side dependent. Images (A-H) show sequential images when sucking was paused during a “breathing break”; showing milk
continuing to flow into the right (gravity dependent) pyriform fossa. Images (D-H) show milk filling right pyriform fossae up to “rim”
of aryepiglotti.
Abbreviations: L, left; R, right; P, posterior (pharyngeal wall).
Black arrow: vocal folds.
Dotted line: epiglottis (anterior).

“overflow” into the laryngeal inlet before a swallow was Another incidental observation was that if the infant was
triggered, causing pre-swallow penetration or aspiration. tilted into a side-lying position, all milk was diverted into
With alteration of infant positioning to semi-prone, 2 the lower (gravity dependent) pyriform fossa.
changes occurred that appeared to reduce the risk of pre-
swallow aspiration (as summarized in Figure 7). The first Discussion: Summary of Findings and
observation was that tongue base position altered with infant
Clinical Implications
position which, as a consequence, appeared to alter the appar-
ent spatial volume or capacity of the pyriform fossa. With the FEES is a valuable clinical tool that has improved our
soft tissues of the aryepiglottic folds forming the medial wall understanding of swallowing dynamics when assessing
of the pyriform fossa, this space forms a natural conduit or infants with laryngomalacia who are experiencing difficulty
channel on either side of the laryngeal inlet. With alteration breastfeeding. Furthermore, FEES has provided endoscopic
from supine to semi-prone, the infant’s tongue base became evidence for the potential use of infant positioning as a
positioned more anteriorly, which in turn altered the position modifiable variable, by understanding the impact of infant
of the epiglottis and the aryepiglottic folds. This correlated position on dynamic airway compromise and on fluid
with apparent widening of the pyriform fossae, thereby dynamics in the pharyngeal phase of the swallow.
increasing the volume of milk able to be accommodated in Using FEES, we have identified a number of specific
this space without overflow into the laryngeal inlet. anatomical and physiological variables associated with a
The second observation was that the volume of milk higher risk of penetration and/or aspiration (Table 4).
flowing into the pyriform fossa prior to swallow initiation Penetration or aspiration occurring before the swallow is
was greatest during the milk ejection but was also influ- initiated is usually well visualized during FEES, being
enced by infant position. Milk was visible flowing into the the most common timing of airway compromise with swal-
piriform fossa prior to swallow initiation when the infant lowing identified in this study. As pre-swallow penetration
was supine, but this was reduced or absent when the infant and aspiration resolved in all participants following posi-
was repositioned to semi-prone, correlating with reduced tional modification, fluid dynamics during the pharyngeal
pre-swallow aspiration risk. phase of swallowing during breastfeeding appears to be
10 Annals of Otology, Rhinology & Laryngology 00(0)

Table 4. Variables Associated With Higher Incidence of Pre-swallow Penetration/Aspiration.

Anatomical •• Shallow (or asymmetric) pyriform fossae creating low milk volume capacity
•• Flimsy, short epiglottis (uncommon anatomical variant) with dynamic retroflexion of epiglottis into laryngeal
inlet (loss of epiglottic “barrier” to milk flowing from vallecula into laryngeal inlet)
Physiological •• Fast milk flow (usually associated with milk ejection reflex)
•• Supine positioning (variation of “cradle-hold”). Commonly associated with increased volume of milk visible
in hypopharynx prior to swallow initiation
•• Increased respiratory rate
•• Longer pauses in active sucking and swallowing (particularly when occurring at times of faster milk flow)
•• Absence of cough response to penetration (suggesting sensory impairment)
Dynamic •• Dynamic supraglottic soft tissue prolapse (poor coordination of timing of swallowing and breathing relative
to milk being present in hypopharynx)
•• Increased pharyngeal constrictor tone (when crying, the space of the pyriform fossae is often obliterated
and any milk present easily overflows into the laryngeal inlet)

influenced at least in part by gravity. In the absence of active a clear understanding of the impact of varying infant posi-
sucking, with the infant in a supine position, milk was tioning on swallow and airway dynamics which has not
observed continuing to flow from the oral cavity into the been possible with other imaging modalities to date.
pharynx, consistent with this occurring as a passive process, It is important to acknowledge that the majority of babies
similar to water flowing “downhill” in a river. In the semi- are able to feed efficiently and safely in a wide range of
prone position, the milk bolus appeared to be more effec- latching positions, with no requirement to make positional
tively maintained (with gravity) in the oral cavity during adjustments when the mother and infant are breastfeeding
these pauses in sucking, with base of tongue motion required without difficulties. However, if problems with breastfeed-
to actively propel the bolus from the oral cavity “uphill” to ing occur, this can be a significant source of stress for a
the pharynx. As the continued flow of milk into the pyri- family49 and the potential loss of breastfeeding can be dev-
form fossae during pauses in sucking appears to be a major astating for new parents, particularly when their motivation
factor associated with pre-swallow penetration/aspiration and expectation of breastfeeding their infant has been
events (when supine), understanding how this can be modi- high.50 When problems occur, an understanding of potential
fied with alteration of infant positioning (to semi-prone) is causes and actively supporting continued breastfeeding
a significant clinical breakthrough. whenever possible is critical. This FEES-based research
The majority (10/15, 67%) of aspiration and penetration confirms that airway compromise can create increased dif-
events observed in this study did not stimulate a cough ficulty for the infant in coordinating breathing and safe
response, indicating clinical assessment can be hampered swallowing during breastfeeding.3 The potential disruption
by the absence of this symptom. This is consistent with of feeding caused by airway compromise can be associated
other studies of infant aspiration42-47 and confirms consider- with frequent unlatching and re-latching, potentially con-
ably higher silent aspiration rates in infants than is reported tributing to maternal nipple discomfort and trauma and
in adults.48 The clinical implication is that the absence of causing infant distress. This research clarifies the impact of
overt clinical signs does not exclude the presence of aspira- positional modification on infant breathing and/or swallow-
tion in infants with laryngomalacia, thus reliance on clinical ing during breastfeeding, therefore in the absence of FEES
feeding evaluation alone is likely to under diagnose aspira- availability, it may still be possible to apply the principles of
tion in breastfeeding infants. this research to improve breastfeeding in many infants with
Although awake trans-nasal flexible endoscopy is avail- laryngomalacia.
able as a diagnostic procedure in many centers for assessing This is one of the largest studies on breastfeeding FEES
infants with noisy breathing, breastfeeding FEES is not as and is the first to specifically assess infants with laryngoma-
widely available. As a procedure, FEES presents many lacia, a patient cohort recognized to have difficulty breast-
practical challenges, requiring specialized equipment, a feeding. Although the severity of laryngomalacia in the
multidisciplinary team and a significant time commitment, participants was not quantified, the group represented a
as well as having a steep learning curve in both the technical broad range of symptom severity, with all infants having
aspects and interpretation of the captured imaging. symptoms sufficient to warrant referral to a tertiary referral
Procedural success is dependent on a well-informed, toler- pediatric hospital for assessment and management.
ant mother and a compliant infant and even then, acquisi- We acknowledge that this study is descriptive, based on
tion of adequate views for meaningful analysis is not always subjective interpretation of findings and is therefore lacking
possible. However, in spite of these challenges, detailed objective measures. However, the use of FEES in research
analysis of FEES imaging during breastfeeding has enabled on infant swallowing is hindered by the difficulties in
Mills et al 11

Figure 7. Summary of impact of gravity on airway and swallow dynamics during breastfeeding.

providing objective measurements from captured videos suggests that infant positioning at the breast is a modifiable
and images. In spite of this drawback, FEES is currently the variable that may improve the possibility of successful and
only instrumental tool available for assessing the pharyn- safe breastfeeding in infants with laryngomalacia.
geal phase of swallowing in breastfeeding infants. A
descriptive analysis of FEES imaging at present seems to be Declaration of Conflicting Interests
the most appropriate starting point for understanding breast- The author(s) declared no potential conflicts of interest with respect
feeding swallowing dynamics until more sophisticated to the research, authorship, and/or publication of this article.
technology is available to provide objective measures.
When an infant present with airway and feeding compro-
Funding
mise, we highlight the importance of an individualized
assessment of functional anatomy with consideration of The author(s) disclosed receipt of the following financial support
other factors, such as laryngeal sensation, fatigue and for the research, authorship, and/or publication of this article: D.G.
received funding from an unrestricted grant from Medela AG,
comorbidities that may impact on feeding and airway pro-
Baar, Switzerland.
tection. Further research is required to assess the impact of
positioning during breastfeeding on infants with other air-
way pathologies, as well the impact on bottle-feeding. ORCID iD
Nikki Mills https://orcid.org/0000-0003-4214-7521

Conclusion
Supplemental Material
FEES has provided an improved understanding of the breast- Supplemental material for this article is available online.
feeding swallow and the impact of infant positioning at the
breast on airway and swallowing dysfunction in infants with References
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