Article | February 2014
Interventions to Improve Oral Feeding
Performance of Preterm Infants
Chantal Lau
Author Affiliations & Notes
SIG 13 Perspectives on Swallowing and Swallowing Disorders (Dysphagia), February 2014,
Vol. 23, 23-45. doi:10.1044/sasd23.1.23
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This review presents a summary of our current understanding of the development of
preterm infant oral feeding skills, the feeding issues they are facing, and evidence-based
approaches that facilitate their transition from tube to oral feeding.
The field of infant oral feeding research is understudied as the recognition of its importance
truly came about with the increased preterm population and the realization that a large
number of these infants are not safe and competent oral feeders. It is understandable that
this research has taken a “back seat” to the more immediate concerns of saving these
babies’ lives. However, the time has now come when these infants make up a large
proportion of patients referred to feeding specialists for unresolved oral feeding problems
during their stay in neonatal intensive care units (NICUs) as well as post-discharge.
Unfortunately, due to the limited research so far conducted in this domain, available
therapies are limited and lack evidence-based support. Fortunately, this growing medical
concern is stimulating deeper research interests and funding.
It is hoped that the information provided will assist the development of systematic
differential diagnostic approaches to address infant oral feeding issues.
This review is a summary of our understanding of the development of oral feeding skills in
infant, the feeding issues they face, the evidence-based interventions that can facilitate their
transition from tube to oral feeding, and the translational impact that these approaches may
have for current practices. The information is also relevant to term neonates exhibiting
similar difficulties as together preterm and term infants reveal the developmental continuum
of the human neonate.
As the survival of preterm infants is increasing due to medical advances, concerns of health
professionals and families are shifting towards resolving pragmatic issues such as infants’
ability to feed by mouth. The American Academy of Pediatrics (AAP) recommends that
attainment of independent oral feeding be a major criterion for hospital discharge
(AAP Policy Statement, 2008). Consequently, infants’ inability to reach this milestone often
extends their hospitalization, increases financial burden, and very importantly, delays
mother-infant reunion. Potential long-term feeding aversion further adds to the overall
concern of how to optimize oral feeding performance in this population of newborns.
The field of infant oral feeding research is understudied as the recognition of its importance
truly came about with the increased preterm population and the realization that a large
number of these infants are not safe and competent oral feeders. It is understandable that
this research has taken a backseat to the more immediate concerns of saving these babies’
lives. However, the time has now come when these infants make up a large proportion of
patients referred to feeding specialists for unresolved oral feeding problems during their
stay in neonatal intensive care units (NICUs) as well as post-discharge. Unfortunately, due
to the limited research so far conducted in this domain, available therapies are limited and
lack evidence-based support. Fortunately, this growing medical concern is stimulating
deeper research interests and funding.
In general, for any illness, medical managements only proceed following an adequate
understanding of the symptoms and cause(s) leading to them. Thus, prior to any treatment,
a differential diagnosis is first advanced based on a systematic review of potential
pathophysiologies implicated (i.e., an attempt to narrow down the most probable candidates
at the root(s) of an illness). With such approach, caregivers, by process of elimination,
develop roadmaps/algorhythms for how to best proceed with the care of individual patients.
Infants’ inability to feed by mouth is not an illness, but rather a drawback as their physiologic
functions are not yet mature to confront their extra-uterine environment. As such,
management of infant oral feeding issues would benefit from the differential diagnostic
model followed by medical teams. To do so, one must first gain an understanding of the
extra-uterine maturational processes of the physiologic functions implicated in oral feeding
so that, at any time in the course of these infants’ development, tasks asked of them can be
tailored around their functional maturity levels. Identification of the functions most likely at
the origin of the observed symptoms would direct interventions toward protecting,
correcting, or enhancing their functionality (e.g., sucking, swallowing).
Such understanding can best be attained by following the growth and development of
feeders and growers who have no specific medical issues besides their prematurity. What
we learn from these infants will help us devise efficacious therapies that take into account
their continuously maturing skills. Once this milestone is attained, we will be better prepared
to address more complicated cases with infants who, in addition to their prematurity,
present with additional pathologies (e.g., poor lung function, cardiac anomalies,
intraventricular hemorrhages, or genetic anomalies).
Development of Infant Oral Feeding Skills
The ability of infants to suck and transport a bolus from the oral cavity to the stomach safely
and efficiently requires the proper development of sucking, swallowing, respiration,
esophageal function, and, most importantly, the coordination of all these activities.
Nutritive Sucking
Nutritive sucking comprises two components: suction and expression. Suction corresponds
to the generation of an intraoral negative pressure to draw liquid into the mouth (i.e., similar
to drinking from a straw). This is achieved by closure of the nasal passages by the soft
palate, the tight seal of the lips around the breast or bottle nipple, and lowering of the lower
mandible (Wolf & Glass, 1992, p.18). Expression relates to the positive pressure exerted by
the tongue against the hard palate by compression or stripping to eject milk (Lau, Sheena,
Shulman, & Schanler, 1997; Waterland, Berkowitz, Stunkard, & Stallings, 1998). A
descriptive scale of the emergence and maturation of these 2 components has been
published (Lau, Alagugurusamy, Schanler, Smith, & Shulman, 2000). It is characterized by
5 sequential steps: (1) appearance of expression; (2) expression acquires rhythm; (3)
appearance of suction; (4) suction acquires rhythm, suction/expression alternation appears;
and (5) establishment of a rhythmic alternation of suction/expression with increasing suction
amplitude (see Figure 1).
FIGURE 1
5 Stages of Nutritive Sucking
Full Size | Slide (.ppt)
An “immature” suck consisting of expression alone is sufficient for completing a bottle
feeding, albeit not as efficiently as with the mature alternating suction/expression
characteristic of term infants (Lau et al., 1997). The absence of suction early on may explain
preterm infants’ inability to breastfeed. As the human nipple is not as rigid as that of a bottle,
infants would need suction to latch on to the nipple-areolar complex when feeding (Lau &
Hurst, 1999; see Figure 2). This may be further complicated by the varied shapes, sizes,
and functions of the maternal nipple (Table 1).
FIGURE 2
Types and Functions of Maternal Nipples
Full Size | Slide (.ppt)
TABLE 1Types
and Functions of Nipple-Aareolar Complex
Appearance at Rest
a. Normal/Prominent– At rest, nipple protrudes outward from areola
Protracts – extends further outward with S
b. Flat – Nipple is flat with breast contour
Protracts or Retracts, i.e., moving inward
c. Inverted – All or parts of the nipple is drawn inward within areolar folds
Simple inversion – moves outward with S
Appearance at Rest
d. Pedunculated - nipple sits on a stalk away from areola
Nipple may be too big for infant’s mouthS
View Large
It is interesting to note that nonnutritive sucking with a pacifier matures earlier than nutritive
sucking as shown in the tracings of two preterm infants monitored for 2–3 minutes on a
pacifier at the beginning of a feeding and immediately switched to bottle feeding thereafter
(see Figure 3a, Figure 3b; Lau & Kusnierczyk, 2001). The infant taking all his feeding by
mouth (ad libitum) used a mature sucking pattern on the pacifier, as well as during bottle
feeding (see Figure 3a). This contrasts with the infant taking four oral feedings per day who
used a mature nonnutritive pattern with the pacifier, but an immature nutritive pattern when
given a bottle (see Figure 3b). This may be explained by the fact that nonnutritive sucking
involves minimal swallowing (i.e., only saliva) in contrast to nutritive sucking. In the latter
case, the sustained milk inflow into the mouth must be rapidly and safely transported to the
stomach. This can only be achieved if sucking, swallowing, respiration, and esophageal
function work hand-in-hand (Lau, 2006). As swallowing is minimal during nonnutritive
sucking, it becomes debatable whether assessment of nonnutritive sucking alone is a
sufficient marker for readiness to oral feed, although it is a good indicator of sucking per se
(Lau & Kusnierczyk, 2001) as seen.
FIGURE 3
Nonnutritive and Nutritive Sucking Pattern of Two Preterm Infants at
Different Stages of Oral Feeding Advancement
Full Size | Slide (.ppt)
Swallowing Function
The swallowing process consists of an oral, pharyngeal, and esophageal phase with each
phase of the reflex requiring complex sensorimotor interactions and executive motor outputs
that developmentally immature infants may not readily accomplish (Leopold & Daniels,
2010; Wolf & Glass, 1992). As the frequency of nutritive sucking is around 1 suck per
second (Wolff, 1968), transport of the bolus from the oral cavity to the stomach must occur
swiftly before milk influx from the next suck takes place. Any delay(s) in bolus formation,
pharyngeal, and esophageal transport will impact on safety and competency (Lau,
2006; Lau, 2012; Lau & Hurst, 1999;Wolf & Glass, 1992). Bolus formation in the oral cavity
and propulsion into the pharynx to initiate the swallow reflex may be affected by the proper
coordination of the lingual musculature and that of the tongue with the soft palate (Bosma,
Hepburn, Josell, & Baker, 1990;Bu’Lock, Woolridge, & Baum, 1990; Goldfield et al.,
2010; Leopold & Daniels, 2010; Miller & Kang, 2007; Omari et al., 1999). Appropriate
pharyngeal transport of the bolus toward the esophagus requires proper closures of the
nasal, laryngeal, and oral openings to prevent milk leakage (Dantas, Dodds, Massey,
Shaker, & Cook, 1990; Wolf & Glass, 1992). This implies appropriate motor control of these
anatomical structures and their coordinated interactions with the sensory-neural control of
the pharyngeal musculature responsible for bolus transport to the upper esophageal
sphincter (Donner, Bosma, & Robertson, 1985; Humbert, Lokhander, Christopherson,
German, & Stone, 2012). Any delay(s) during this phase of swallowing increases risks of
liquid penetration or aspiration into the larynx/lungs and bolus disintegration (Jadcherla,
Hogan, & Shaker, 2010). To delay disintegration of a liquid bolus, increasing milk viscosity
is often considered whether thickeners such as rice cereal, special formula, or human milk
thickeners are used. The necessity of thickening milk remains debatable and deserves
revisiting.
Respiratory Function
Preterm infant’s respiratory rates range between 40 –60 breaths/min or 1.5 –1 cycle/sec
Swallows may last between 0.35–0.7 sec (Koenig, Daviers, & Thach, 1990). If an infant
breathes at 1 cycle/sec and his/her swallow lasts 0.7 sec, only 0.3 sec is left for safe
breathing. Under such conditions, few infants could tolerate oral feeding for a prolonged
period of time.
Esophageal Function
The study of esophageal function in preterm infants has been restricted by the technologies
available. Fortunately over the last decade, novel devices designed for their small size and
fragility have emerged such as endoscopic manometry, multichannel intraluminal
impedance (MII), and pH- MII.
The Upper Esophageal Sphincter (UES)
The upper esophageal sphincter (UES) plays an important role in bolus transport from the
pharynx to the esophageal body. Studies have highlighted how readily oral feeding issues
may arise when pharyngeal-UES and UES-esophageal interactions are dys-coordinated. A
recent study conducted on preterm infants (28 ± 1.9 weeks gestation [GA] and monitored
for 4 weeks between 31 to 36 weeks postmenstrual age [PMA]0 observed that most
preterm infants demonstrated poor PMA-related pharyngeal pressures that lead to poor
coordination of pharyngeal bolus propulsion and timing of UES relaxation. However,
increased pharyngeal pressure with well-developed UES and esophageal motility appear by
33 to 34 weeks PMA (Jadcherla, Duong, Hofmann, Hoffmann, & Shaker, 2005; Rommel et
al., 2011).
Esophageal Motility
It is recognized that esophageal motility in preterm infants is immature, a likely the result of
the immaturity of the central and peripheral neuro-motor properties of the esophageal body
(Gupta et al., 2009). Two categories of waves are identified: peristaltic and non-peristaltic.
The peristaltic group distinguishes between the antero- and retro-grade waves. The
anterograde wave travels from the UES down to the lower esophageal sphincter (LES) and
is responsible for the bolus transport to the stomach. The retrograde wave travels in the
opposite direction towards the UES and, at times, is blamed for occurrences of
regurgitation. The non-peristaltic group includes synchronous and incomplete wave
patterns. With maturity, a decrease in incomplete non-peristaltic and increase in
anterograde peristaltic waves are observed (Jadcherla, Duong, Hoffmann, & Shaker,
2003; Omari et al., 1995).
Lower Esophageal Sphincter (LES)
The primary role of the LES is to control the antero- and retro-grade nutrient flow across the
esophageal-gastric junction. Two types of LES relaxation (LESR) can be distinguished. The
swallow-related LESR (SLESR) is associated with the anterograde transport of nutrients
into the stomach. The transient LES relaxation (TLESR), in turn, is independent of
swallowing and associated with belching or gastro-esophageal reflux (GER). TLESR may
occur under different conditions that are not necessarily related with nutrient intake (Omari,
2006). It remains unclear whether TLESR occurs more frequently in preterm vs. term
infants.
Gastric Emptying
Little is known about the development of gastric emptying in preterm infants. Gastric
residual is routinely measured prior to enteral/oral feeding. Depending upon individual NICU
practices, feeding may be halted depending upon the measured residual. It is of interest to
mention that Omari et al. (2004) observed that lateral positioning of an infant following a
feeding may facilitate gastric emptying (Omari et al., 2004; van Wijk et al., 2007).
Suck-Swallow-Respiration-Esophageal Coordination
Oral feeding problems would be minimized with the proper maturation of the above
physiologic functions. However, it is their “coordinated” interactions that will ensure safety
and efficiency. But it is yet unclear what such coordination consists of. In practice,
caregivers often presume that sucking, swallowing, and respiration are coordinated if an
infant feeds with no adverse events, such as oxygen desaturation, bradycardia, apnea,
coughing, and choking. But such presumption is not always correct as observed with
aspiration/pneumonia potentially caused by silent aspiration (Arvedson et al., 1994; Kelly,
Huckabee, Jones, & Frampton, 2007; Weir, McMahon, Taylor, & Chang, 2011).
The physiologic functions implicated with oral feeding are rhythmic/phasic by nature.
Indeed, nutritive sucking occurs around 1 cycle/sec, nonnutritive sucking around 2 cycle/sec
(Wolff, 1968), infant respiratory rates vary between 30 – 60 breaths/min, and heart rate
between 120 –160 beats/min. As such, one may speculate that coordination would be
optimized if these functions were to work in phase vs. out of phase from each other (see
Figure 4). Indeed, when in phase, an additive/synergistic net effect would be expected,
whereas when out-of- phase, the expected net effect would be reduced.
FIGURE 4
Net Effects of Phasic Systems Working In and Out of Phase
Full Size | Slide (.ppt)
We conducted a study to characterize the coordination of sucking, swallowing, and
respiration (Lau, Smith, & Schanler, 2003). We investigated separately the suck-swallow
and swallow-respiration interactions. Infants born between 26.8 ± 2.7 weeks GA
demonstrated a consistent suck: swallow ratio of 1:1 when introduced to oral feeding at 34 ±
1.2 weeks PMA, suggesting that the sucking and swallowing functions were coordinated.
On the other hand, rather than defining coordination of swallow-respiration as a consistent
ratio, we speculated that its proper coordination was more relevant to safety (i.e.,
minimizing liquid penetration into the larynx). We reasoned that the riskier times to swallow
would be during inhalation as air rushes into the lungs and deglutition apnea as increased
risks of aspiration and oxygen desaturation would occur, respectively (see Figure 5). As
such, the percent frequency of when swallows occurred during the different phases of
respiration was monitored. Table 2 shows that preterm infants swallowed most frequently
during these two riskier phases of respiration. Fortunately, with maturation as observed with
term subjects, the occurrence of swallows shifted to start and end of inhalation when no air
flow occurs. It is of interest to note that adults primarily swallow during exhalation
(McFarland, Lund, & Ganger, 1994; Nishino & Honda, 1982). McFarland et al.
(1994) observed that, in adults, swallowing occurred at different phases of respiration
depending upon the feeding/eating posture and speculated that such alteration resulted
from the mechanical properties of the upper body (McFarland et al., 1994). If correct, infant
feeding positions may affect the swallowing safety with respect to respiration. An intriguing
thought that would require future studies for evidence-based confirmation.
FIGURE 5
Respiratory Phases When Swallowing May Occur
Full Size | Slide (.ppt)
TABLE 2Percent
Occurrence of Swallow-Respiratory Interfacing with
Maturation
Full Size | Slide (.ppt)
Concerns over the dys-coordination of sucking, swallowing, and esophageal function
primarily reside in the adverse occurrences of regurgitation, choking, aspiration, GER,
and/or potential gastro-esophageal reflux disorder and esophagitis. This topic is not
addressed here as it falls under a distinct medical issue of its own.
Deterrent Factors That Can Affect Oral Feeding
Aside from immature physiologic functions, oral feeding problems can also be of non-oral
feeding origins, namely infants’ clinical status, the NICU environment, and/or infants’ own
behavioral states and organization.
Infant Clinical Status
In addition to their overall clinical status, appropriateness of oral feeding naturally depends
on their condition during the feeding. Any change in color from “pink” to “dusky” or “blue”
would be indicative of progressive oxygen desaturation which would lead to apnea and/or
bradycardia if unattended to. Although infant heart rates average between 120 –160
beats/min, it is important to be cognizant that there will be outliers with baseline rates below
100 beats/min. As such, verifying that alarms are set accordingly would be prudent.
NICU Environment
Awareness that infants have been abruptly transitioned from an in- to extra-uterine
environment is important. Light, sound, touch, temperature, and mobility inside and outside
the womb are strikingly different (see Table 3). As such, the smoother the transition, the
less stressful infants’ adaptation will be.
TABLE 3NICU
Environment Inside vs. Outside the Womb
Factors
Inside the womb…
Light
Dark
Sound
Muffled (voices)
Touch
Consistent containment, smooth, calming
Thermal
Constant, warm
Mobility
Day/night maternal input, fluid environment,Supported flexed posture
Outside
B
Loud
Inconsistent containm
Flu
Limited maternal inputdry enviro
View Large
Infant Behavioral States
The Newborn Individualized Developmental Care and Assessment Program (NIDCAP)
distinguishes 6 behavioral states (Als, 1986): (1) deep sleep, seldom seen in the preterm
infant; (2) light sleep; (3) drowsy/alert inactive; (4) quiet awake and/or alert; (5) actively
awake and aroused; and (6) highly aroused, agitated, upset, and/or crying. Oral feeding is
best recommended when infants are at states 3, 4, and 5 (Gill, Behnke, Colon, & Anderson,
1992; White-Traut, Berbaum, Lessen, McFarlin, & Cardenas, 2005). Awareness that
preterm infants’ behavioral states can fluctuate rapidly would assist caregivers understand
why an infant’s feeding can also fluctuate during a feeding. Halting a feeding may be
appropriate if an infant cannot regain a proper feeding state.
Infant Organization
Behavioral organization/disorganization is a term frequently used by therapists that
encompass a number of observational indicators so as to obtain a sense of the overall wellbeing of the infant. For instance, an infant will be deemed organized if calm, relaxed, with
regular breathing, arms folded in midline, eyes closed or open. Disorganization will be
characterized by splayed hands, protruding tongue, nasal flaring, gaze aversion, grimacing,
arms extended, and/or increased head/limb agitation (Wolf & Glass, 1992, p.160).
Modalities to Enhance Infant Oral Feeding Performance
To enhance infant oral feeding performance, it is essential to first identify and evaluate the
severity level(s) of their symptoms, identify the most probable functional weakness(es), and
consider the available evidence- based interventions to resolve the problem.
Commonality of Symptoms
A number of symptoms during oral feeding are observed regardless of the origins of the
causes if feeding is maintained. From their practice, healthcare providers customarily
associate fatigue with one or more of the following: poor tone, changes in behavioral state
(e.g., sleep), “shut down,” increase duration of sucking pauses, increased milk leakage or
drooling. To the author’s knowledge, no study has specifically demonstrated that these
events are correlated to fatigue. This is likely due to the fact that fatigue per se is a nonspecific symptom that results from many causes. If there is no specific measure of “medical
fatigue” in adults, it would be even more difficult to define one in infants due to their
developmental immaturity. This comment perfectly relates to the subjectivity/bias that we,
as caregivers, may have when caring for our patients. If feeding is maintained in the
presence of any of the above symptoms, increased respiratory rate, and eventually oxygen
desaturation, apnea and/or bradycardia will occur. If the cause is due to suck-swallowrespiration incoordination, coughing, choking, aspiration, poor self-pacing, oxygen
desaturation, apnea and/or bradycardia may be observed. Signs of reflux may include
choking, coughing, aspiration, arching, esophagitis, and/or oral feeding aversion. If little
attention is paid to the appearance order of these symptoms, by the time they are observed,
identification of the original culprit(s) is difficult due to the commonality of the symptoms
(see Table 4). However, if infants were closely watched from the start of a feeding, their
sequential appearance, be it through their behavior or the alarm monitor, can provide early
clues as to the origin of the problem. For instance, by regularly watching the alarm monitors,
one can catch whether oxygen desaturation, cardiac or respiratory activity pattern is first to
change. Often times, this would appear before any observable behavior takes place.
TABLE 4Commonality
of Oral Feeding Symptoms if Oral Feeding is Maintained
Physiological
Behavioral
-
Oxygen desaturation
-
Poor tone
-
Apnea/bradycardia
-
Fall asleep
-
Tachypnea
-
Agitated
Physiological
Behavioral
-
Choking/coughing
-
Pushing away
-
Aspiration
-
Turning head away
-
Emesis
-
State change -“shut down”
-
Milk leakage
-
aversive to feeding
View Large
Evaluation Modalities
The development of instruments to evaluate infant oral feeding skills comprises qualitative
and quantitative approaches. Qualitative approaches, primarily conducted through
observational techniques, document the presence/absence of specific behaviors and/or
cues (Palmer, Crawley, & Blanco, 1993; Thoyre, Shaker, & Pridham, 2005). However, care
must be taken in data analyses not to incorporate individual biases. Intra- and interreliability testing is essential. Using full term infants’ behavioral repertoire for instance as
control standards would be inappropriate insofar as preterm infants have not yet attained
the same level of behavioral maturity due to the immaturity of their motor and/or sensory
development. A good example is illustrated again by the occurrence of silent aspiration
detected only after aspiration/pneumonia presents (Arvedson et al., 1994; Weir et al., 2011).
Quantitative approaches require special equipment that can offer accurate measures of
specific outcomes (e.g., sucking amplitude (mmHg), sucking frequency, temporal profiles of
suck-swallow-respiration or esophageal motility). Some are offered through specialty
services (e.g., pediatric gastroenterology for endoscopic manometry, MII, pH –MII; speech
language pathology for modified barium swallow study). Others are commercially available
(e.g., NTrainer, Innara Health, Olathe KS; Finan & Barlow, 1996) or remain in the research
domain (Lau & Schanler, 1996; Medoff-Cooper, Weininger, & Zukowksy, 1989; White-Traut
et al., 2013). Unfortunately, they are not readily available for the daily use of feeding
therapists in NICUs.
We recently developed a simple quantitative scale for preterm infants (26 –36 weeks GA),
that does not require any special equipment to measure infant oral feeding skills (OFS; Lau
& Smith, 2011). OFS levels were delineated by infants’ respective proficiency (PRO)
defined as the percent volume taken during the first 5 min of a feeding/total volume
prescribed and rate of transfer (RT) defined as the total volume taken over the duration of
an entire feeding (ml/min). Four OFS levels were delineated by PRO ≥ or < 30% and RT≥ or
< 1.5 ml/min. OFS 1, the most immature, was defined by PRO < 30% and RT < 1.5 ml/min;
OFS 2 by PRO < 30% and RT≥1.5 ml/min; OFS 3 by PRO ≥ 30% and RT< 1.5 ml/min, and
OFS 4, the most mature, by PRO ≥ 30% and RT RT≥1.5 ml/min. PRO was used as an
index of infants’ “true” skills as fatigue was deemed minimal and RT, a resultant of infants’
overall skills when fatigue came into play, was used as an index of overall endurance (see
Figure 6). Two observations of note were made. First, within each GA stratification (26–29
weeks, 30–33 weeks, 34–36 weeks), infants exhibited all 4 OFS levels at similar PMA,
albeit smaller percentile of infants demonstrated OFS levels 1 with greater GA. Such broad
variance in OFS supports the notion that preterm infants born at similar GAs do not mature
at the same rate (see Figure 7). Second, the overall feeding performance or transfer (OT; %
volume taken/volume prescribed for a feeding) of infants was significantly correlated with
OFS levels, but not with GA, suggesting that the maturity level of infants’ oral feeding skills
were the determinant of their feeding performance rather than their GA. It is of interest to
note that infants using OFS levels 2 and 3 perform equally well (i.e., taking between 70 to
80% of their prescribed feeding). This would suggest that good skills and good endurance
are equally efficient (see Figure 8).
FIGURE 6
Interpretation of OFS Levels as a Function of Feeding Skills and Endurance
Full Size | Slide (.ppt)
FIGURE 7
Percent OFS Levels by Gestational Age at First Oral Feeding
Full Size | Slide (.ppt)
FIGURE 8
Percent Overall Transfer (% volume taken/volume prescribed) by OFS
Levels
Full Size | Slide (.ppt)
Potential Interventional Modalities
Insofar as oral feeding issues may be of oral- and/or non-oral origin, availability of
interventions addressing both possibilities must be taken into account. Sensorimotor
interventions such as tactile/kinesthetic, vestibular, and auditory stimulation have been
demonstrated to benefit infant growth and development (Dieter & Emory, 1997; Korner,
1990; White-Traut et al., 2002). Additionally, common sense judgment when caring for
infants often helps in identifying non-oral feeding issues that may interfere with an infant’s
feeding performance.
Studies have identified well-tolerated evidence-based modalities to assist oral feeding
issues originating at the levels of sucking, swallowing, swallowing-respiratory interfacing,
and/or esophageal functions.
Sucking
Nonnutritive oral stimulation, using different approaches, has been shown to improve the
oral feeding performance of preterm infants. An association between improved stability in
the nonnutritive sucking pattern following therapy with the NTrainer, a nonnutritive sucking
assessment device (Innara Health, Olathe KS) and the percent of the total daily intake
taken by mouth vs. tube was observed (Poore, Zimmerman, Barlow, Wang, & Gu, 2008).
These investigators used a particular therapy protocol providing 3-min epochs stimulations
up to 4 times/day during scheduled gavage feeds until infants were able to take 90% of their
feeds by mouth for 2 consecutive days. The study of Fucile, Gisel, and Lau, 2002,
conducted on very low birth weight (VLBW) infants used a 15-min stimulation program
based on the Beckman’s principles (Beckman, 1986) beginning 48 hours after
discontinuation of nasal continuous positive airway pressure (nCPAP) and provided once a
day for 10 consecutive days, 15–30 mins prior to a gavage feeding. Subjects were
monitored at 3 time points, when taking 1–2 (start of oral feeding), 3–5, and 6–8 oral
feedings/day. Compared to control counterparts, infants’ OT and RT were enhanced and
independent oral feeding attained was 7 days sooner (Fucile et al., 2005). In a subsequent
study, in which VLBW infants received this therapy twice a day, 15-min per intervention,
subjects similarly attained independent oral feeding more rapidly, demonstrated more
mature OFS level profile, greater suction and expression amplitude, and decreased
episodes of deglutition apnea were observed (see Figure 9; Fucile, Gisel, McFarland, &
Lau, 2011;Fucile, McFarland, Gisel, & Lau, 2012; Lau, Fucile, & Gisel, 2012).
FIGURE 9
OFS Profiles of Infants Receiving Nonnutritive Oral Motor (NNMOT),
Massage Therapy (MT), Combined NNOMT+MT, and Sham (Control)
Interventions
Full Size | Slide (.ppt)
In a recent study on a similar population of infants, we investigated whether an “active”
nonnutritive sucking exercise using a pacifier could replicate the benefits observed with the
nonnutritive therapy described above. We reasoned that, if this were achieved, it would be
an intervention that parents could provide to their infants. The sucking-pacifier exercise was
offered 15-min per day, 5 days a week, beginning 48 hours post nCPAP and continued until
infants attained independent oral feeding (8 oral feedings/day). The exercise consisted of
gently moving the pacifier in a rhythmic up/down and posterior/anterior motion and reliably
initiated sucking. Unfortunately, it did not offer the benefit observed with our original
nonnutritive oral motor stimulation program provided by a therapist (Lau et al., 2012). Days
from start to independent oral feeding and OFS level profile were not significantly different
from those of control counterparts (Figure 10).
FIGURE 10
OFS Profiles of Infants Receiving a Nonnutritive Exercise (Pacifier), a
Swallow Exercise, and No Intervention (Sham Control)
Full Size | Slide (.ppt)
Swallowing
As oral feeding can be affected by swallowing difficulties, we investigated the efficacy of a
swallowing exercise to facilitate infant oral feeding. The study design followed that of the
sucking-pacifier exercise. It consisted of placing a bolus of 0.05–0.2 ml of the milk infants
were receiving at the time (e.g., mother’s milk, formula) via a 1-ml syringe directly on the
medial-posterior part on the tongue, approximately at the level of the hard and soft palate
junction, close to the site where the bolus rests prior to entering the pharynx (Arvedson &
Lefton-Greif, 1998). The infants started with 0.05 ml and the volume was increased by
0.05 ml increment to a maximum of 0.2 ml until a swallowing reflex was observed or as
tolerated (i.e., the intervention was halted at any sign of adverse events such as unstable
vitals, choking, fatigue, and/or disorganization). A maximum volume of 0.2 ml was based on
the knowledge that the bolus size of preterm infants averaged 0.14 ± 0.06 ml. This
compares to an average of 0.22 ± 0.07 ml in term infants during their first month of life (Lau
et al., 2003). Once the minimal volume necessary to initiate the swallow reflex was visually
identified, it was used for the duration of the exercise. This program shortened the number
of days from start to independent oral feeding by six days and OFS profile were significantly
more mature as infants progressed vs. to control counterparts (see Figure 10).
Swallow-Respiration Interfacing — Feeding Positions
With the knowledge that preterm infants swallowed at riskier respiratory phases than term
infants and that swallowing-respiration interfacings are affected by feeding/swallowing
positions (McFarland et al., 1994), we speculated that oral feeding performance of infants
may be influenced by their feeding position. Additionally, we were aware that caregivers
advocated for different feeding positions, albeit no evidence was available to support their
benefits. Indeed, whereas feeding in the upright position was favored over the conventional
semi-reclined position in the early 2000, over the last few years, the side-lying position was
preferred. Two studies conducted on feeders and growers born ≤ 34 weeks GA, when fed in
the side-lying position, did not demonstrate consistent benefits in infant physiological
stability (e.g., oxygen saturation, heart rate) while infant consumption were not significantly
different (Clark, Kennedy, Pring, & Hird, 2007;Dawson et al., 2013). In a sample of infants at
similar GA requiring oxygen at time of oral feeding, such feeding position complemented
with the CoReg feeding approach improved infant behavioral and physiologic responses vs.
counterparts fed by the Usual Care. CoReg consists of the transmission of infant respiratory
and swallowing sounds during feeding to caregivers via an earpiece so as to increase their
sensitivity and responsiveness to the infant (Thoyre, Holditch-Davis, Schwartz, Melendez
Roman, & Nix, 2012). From our own research, to determine whether these different
positions benefit oral feeding performance, VLBW infants were randomized to being fed in
the semi-reclined (control), upright, or side-lying position. When monitored at 1–2, 3–5, and
6–8 oral feedings/day, no differences were observed in days to independent oral feeding
and OFS profiles (see Figure 11). Based on the average number of days to independent
oral feeding, one may conclude that feeding in the upright and side-lying positions do not
have any significant effect when compared to the semi- reclined feeding position (Lau,
2013). However, with the information provided by OFS profiles, an important observation
was made. Statistical significance is based on the “averaging” of a particular measure for a
given sample size of subjects. Knowing that infants within gestational and postmenstrual
ages can demonstrate a wide range of OFS levels (Lau & Smith, 2011), large variances in
any outcome measure will readily lead to statistical non significance. Although such
analytical procedures is essential in order to identify the overall impact that an intervention
can have on a particular subject population, it cannot identify individual subjects who may or
may not have benefited from a treatment. As practitioners’ primary concern is to care for
individual patients, we propose that routine monitoring of infant’s OFS levels can help
identify those who benefited from a particular intervention from those who did not. In the
case of feeding positions, such practice would identify infants who benefit from the semireclined, upright, or side-lying. If used appropriately, the OFS scale can become a useful
“tool” to individualized therapy/care.
FIGURE 11
Infant OFS Profiles When Fed in Semi-Reclined (Control), Upright, and SideLying Position
Full Size | Slide (.ppt)
Swallow-Esophageal Interfacing
Inappropriate swallow-esophageal interfacing is well-known to lead to regurgitation, reflux,
esophagitis, and potential long-term feeding aversion if left untreated. As identification of the
potential esophageal cause(s) cannot yet be readily identified, no succinct evidence-based
support for a potential treatment has yet been described. However, in the meantime, other
approaches ought to be considered such as allowing infants to regulate their own feeding
with no “encouragement” from caregivers (see self-paced feeding below).
Massage/Tactile-Kinesthetic Therapy
Tactile/kinesthetic stimulation may focus on particular functions similar to a nonnutritive oral
stimulation program aimed at sucking or a swallow exercise aimed at the swallow reflex.
However, this type of stimulation can also be applied to the whole body as used in massage
therapy. The latter practice has been used on infants for centuries in Eastern societies and
its acceptance is growing in Western cultures (Fan, 2004; Fogaca et al., 2005; Leboyer,
1976). Massage therapy has demonstrated benefits for preterm infants (Diego et al.,
2007; Field, Deigo, & Hernandez-Rief, 2011; Livingston et al., 2007; Mathai, Fernandez,
Mondkar, & Kanbur, 2001). However, a recent Cochrane Review did not find sufficient
support to recommend its use on infants due to the quality in study design and differing
approaches used in the studies reviewed (Bennett, Underdown, & Barlow, 2013). In a
recent study, we examined its impact on preterm infant oral feeding using the method
developed by Field et al for this population (Field et al., 1986). With the same study design
as our study on nonnutritive oral stimulation, VLBW infants who received the massage
treatment attained independent oral feeding faster than control counterparts; their OFS
profiles and the coordination of swallow-respiration were more mature. However, combining
both nonnutritive oral stimulation and massage treatment was not of further benefit (see
Figure 9; Fucile et al., 2011; Fucile et al., 2012; Lau et al., 2012).
Self-Pace Feeding
The principle of self-paced feeding is based on the recognition that caregivers cannot
identify infants’ true feeding ability or limitation solely from visual observations. As such, we
reasoned that preterm infants with normally developing neurologic functions (i.e., “feeders
and growers”), can reflexively protect themselves, if given that opportunity. To test this
hypothesis, we developed a “self-paced” feeding system to give control of the feeding to the
infants. This was achieved by eliminating the positive hydrostatic pressure always present
when a bottle is tilted so that milk outflow only occurred when infants were sucking. This
would allow them to pause/rest and breathe whenever necessary without milk dripping into
their mouth. Additionally, this feeding system continuously prevented the natural vacuumbuild up that occurs as a container empties thereby eliminating the resistance against milk
outflow from the bottle that naturally occurs (Lau & Schanler, 2000). VLBW infants feeding
with the self-paced system demonstrated significantly greater OT, RT, and PRO than
counterparts feeding with a conventional bottle at 1–2, 3–5, and 6–8 oral feedings/day.
Additionally, they demonstrated more mature sucking stages than recognized by caregivers
(Fucile, Gisel, Schanler, & Lau, 2009). These data suggested that not only could
interventions facilitate infant oral feeding, but tools could be developed to assist as well.
Common Sense Modalities Affecting Non-Oral Feeding Issues
Although infants cannot speak, they do communicate. Thus it is important to watch them as
feeding progresses. Tables 5 and Table 6 list some of their communicative skills and
“common sense” approaches to consider while feeding an infant, respectively.
TABLE 5Babies
Can Communicate — Watch for cues …
I am Ready To Feed
I am NOT ready, STOP feeding
Eyes open or closed
Cannot wake up, eyes, closed
Responsive to light touch, relaxed
Frantic, arching,
I am Ready To Feed
I am NOT ready, STOP feeding
Looks at caregiver
Staring, gaze aversion,
Regular breathing
Increased respiratory rate, vital instability, color change
Hands towards mouth, folded in midline
arms extended, fingers splayed, protruding tongue, grimacing, nasal flaring
Rooting or sucking
Spitting up, gagging, gasping, excessive yawning
Smooth motor movements
Tremor, startling
Calm/quiet
Panic or worried look
View Large
TABLE 6Common
Sense Approaches to Consider
Approach
Why
Reduce noise/light levels
- Minimize external over- stimulations, behavioral disorganization
Adjust feeding position
- To facilitate organization, respiration, swallowing, decrease potential reflux
Let infant regulate milk flow
- We do not know infants’ physical and physiologic limitations
Vary number and/or duration of oral feeding
experience
- To reduce adverse events (e.g., fatigue, aspiration)- To develop good OFS- T
avoid oral feeding aversion
View Large
Modalities and Considerations for Practice
Preterm infants are challenged not only by developmental delays due to their imposed
extra-uterine maturation, but also by the negative sensory inputs in the NICU necessitated
by their fragile medical condition and the tasks asked of them such as oral feeding. Oral
feeding concerns, as mentioned earlier, is a relatively new recognition and thus lacks
guidelines and evidence-based support for many of the current practices.
Due to limited availability of quantitative evaluation and diagnostic devices, caregivers have
justifiably turned to qualitative methodologies. In this regard, the current popular cue-based
feeding approach (Garber, 2013; Kirk, Alder, & King, 2007; Ludwig & Waitzman,
2007; Puckett, Grover, Holt, & Sankaran, 2008), has raised concerns as to whether preterm
infants are sufficiently mature to demonstrate behaviors indicative of feeding readiness.
Indeed, “[they may] not have yet developed the level of brain maturation that coordinates
hunger/satiety with sleep/alertness [used for] cue-based feeding” (Nyqvist, 2012). As such,
cue-based feeding may need to be a more individualized approach by taking into
consideration the differing stages of behavioral development, clinical stability, motor skills,
and endurance that individual infants encounter. Therefore, the currently identified “feeding
cues” may not apply across the board to particular populations of infants (Barbosa,
2013; Garber, 2013;Nyqvist, 2012; Roca, 2013).
Practice of cue-based feeding in NICUs has grown over the last few years despite lack of
solid evidence-based support (Tosh & McGuire, 2006). The notion of whether preterm
infants have a “sense” of hunger/satiety is unknown. Hunger is defined as “a feeling of
discomfort or weakness caused by lack of food, coupled with the desire to eat” (“Hunger,”
n.d.) . As a sensory stimulus, it implicates a certain level of neuro-physiologic-endocrine
maturity that preterm infants may not have attained. Therefore, cues for hunger are difficult
to identify. This is well illustrated by the study of Hodges and colleagues (2008) suggesting
that qualitative assessment may differ between mothers “in the extent to which they
perceive and rely upon infant hunger and fullness cues to initiate and terminate feeding”.
Such variance in caregivers’ perception of what infant observational cues may project raises
concerns over whether their nutritional needs could be met on a consistent level. If only a
cue-based feeding approach were used, knowledge of the maturation level of individual
infants’ motor development at assessment times would be essential.
Little is known regarding when the sense of hunger/satiety develops. A hunger center in the
lateral hypothalamus has been long recognized (Wise, 1974) and particular stomach, body,
and antral muscular activity interacting with the lateral hypothalamic hunger site has been
shown to regulate degrees of hunger/satiety (Kromin & Zenina, 2013). Additionally,
hormonal involvement (e.g., insulin, ghrelin, growth hormone) are known to be implicated
(Pradhan, Samson, & Sun, 2013). How the physiologic bases of hunger are reflected in
preterm infants’ behavioral repertoire is unknown. It is primarily for these reasons that
concerns have been raised over the use of cue-based feeding alone.
The above discussions are presented as potential means to develop an organized and
more systematic differential diagnostic approach to address infant oral feeding issues.
In the presence of oral feeding symptoms, one may want to determine whether: (a) feeding
ought to be halted (see Table 5); (b) NICU environment (light and sound), swaddling,
feeding position are appropriate (see Table 6); or (c) the infant is feeding at his/her own
pace with no encouragement from caregiver. At the end of the feeding, assessing OFS
levels may help identify the quality of feeding skills and endurance (see Table 7). If feeding
skills need to be improved, appropriate evidence-based directed intervention may be
considered. If endurance is the issue, an “oral feeding training” may be beneficial (e.g.,
more frequent feeding sessions of shorter duration). Increasing training opportunities when
fatigue is minimal will favor the development of good skills.
TABLE 7Potential
Interventions to Consider
OFS Levels
Feeding skills (PRO)
Endurance (RT)
Potential Interventions
1
Poor
Poor
Appropriate evidence-based directed intervention(s)+“oral f
2
Poor
Good
Appropriate evidence-based directed interventio
3
Good
Poor
“oral feeding training”
4
Good
Good
none
View Large
Summary and Conclusions
In brief, this review presents the current understanding of the development of infant oral
feeding skills from which efficacious evidence-based interventions were developed. As the
goal of research is to advance medical practice, it underscores the translational value of
these interventions. Currently, there are no robust guidelines to follow and the lack of
evidence-based interventions used does not receive support from a number of disciplines.
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