Interventions to Improve Oral Feeding Performance of ... · Interventions to Improve Oral Feeding Performance of Preterm Infants ... seal of the lips around the breast or bottle nipple,

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Interventions to Improve Oral Feeding Performanceof Preterm InfantsChantal Lau

Department of Pediatrics-Neonatology, Baylor College of MedicineHouston, TXOptima Feeding Systems LLCSanta Fe, NMFinancial Disclosure: Chantal Lau is an Associate Professor of Pediatrics-Neonatology at BaylorCollege of Medicine and Founder of Optima Feeding Systems LLC.Nonfinancial Disclosure: Chantal Lau has previously published in the subject area.

Abstract

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This review presents a summary of our current understanding of the development ofpreterm infant oral feeding skills, the feeding issues they are facing, and evidence-basedapproaches that facilitate their transition from tube to oral feeding.

The field of infant oral feeding research is understudied as the recognition of its importancetruly came about with the increased preterm population and the realization that a largenumber of these infants are not safe and competent oral feeders. It is understandable thatthis research has taken a “back seat” to the more immediate concerns of saving thesebabies’ lives. However, the time has now come when these infants make up a largeproportion of patients referred to feeding specialists for unresolved oral feeding problemsduring 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, availabletherapies are limited and lack evidence-based support. Fortunately, this growing medicalconcern is stimulating deeper research interests and funding.

It is hoped that the information provided will assist the development of systematicdifferential diagnostic approaches to address infant oral feeding issues.

This review is a summary of our understanding of the development of oral feeding skills ininfant, the feeding issues they face, the evidence-based interventions that can facilitate theirtransition from tube to oral feeding, and the translational impact that these approaches mayhave for current practices. The information is also relevant to term neonates exhibiting similardifficulties as together preterm and term infants reveal the developmental continuum of thehuman neonate.

As the survival of preterm infants is increasing due to medical advances, concerns ofhealth 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 attainmentof 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 feedingperformance in this population of newborns.

The field of infant oral feeding research is understudied as the recognition of itsimportance truly came about with the increased preterm population and the realization that alarge number of these infants are not safe and competent oral feeders. It is understandable thatthis 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

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referred to feeding specialists for unresolved oral feeding problems during their stay in neonatalintensive care units (NICUs) as well as post-discharge. Unfortunately, due to the limited researchso 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 adequateunderstanding 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 potentialpathophysiologies implicated (i.e., an attempt to narrow down the most probable candidates atthe root(s) of an illness). With such approach, caregivers, by process of elimination, developroadmaps/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 theirphysiologic 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 modelfollowed by medical teams. To do so, one must first gain an understanding of the extra-uterinematurational processes of the physiologic functions implicated in oral feeding so that, at any timein the course of these infants’ development, tasks asked of them can be tailored around theirfunctional maturity levels. Identification of the functions most likely at the origin of the observedsymptoms would direct interventions toward protecting, correcting, or enhancing theirfunctionality (e.g., sucking, swallowing).

Such understanding can best be attained by following the growth and development offeeders and growers who have no specific medical issues besides their prematurity. What welearn from these infants will help us devise efficacious therapies that take into account theircontinuously maturing skills. Once this milestone is attained, we will be better prepared toaddress more complicated cases with infants who, in addition to their prematurity, present withadditional 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 stomachsafely and efficiently requires the proper development of sucking, swallowing, respiration,esophageal function, and, most importantly, the coordination of all these activities.

Nutritive SuckingNutritive 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 todrinking from a straw). This is achieved by closure of the nasal passages by the soft palate, the tightseal 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 palateby compression or stripping to eject milk (Lau, Sheena, Shulman, & Schanler, 1997; Waterland,Berkowitz, Stunkard, & Stallings, 1998). A descriptive scale of the emergence and maturation ofthese 2 components has been published (Lau, Alagugurusamy, Schanler, Smith, & Shulman, 2000).It is characterized by 5 sequential steps: (1) appearance of expression; (2) expression acquiresrhythm; (3) appearance of suction; (4) suction acquires rhythm, suction/expression alternationappears; and (5) establishment of a rhythmic alternation of suction/expression with increasingsuction amplitude (see Figure 1).

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Figure 1. 5 Stages of Nutritive Sucking

Descriptive scale of the 5 stages of nutritive sucking as characterized by the presence/absence ofthe suction and expression components of sucking and the sequential appearance of theirrespective rhythmicity. Note. From Lau, C. (2006). Oral feeding in the preterm infant. NeoReviews,7, e19–e27. Used with permission.

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An “immature” suck consisting of expression alone is sufficient for completing a bottlefeeding, albeit not as efficiently as with the mature alternating suction/expression characteristicof 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 needsuction 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).

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Figure 2. Types and Functions of Maternal Nipples

Reprinted from Lau, C., & Hurst, N. (1999). Oral feeding in infants. Curr Probl Pediatr, 29, 105–124.Used with permission.

Table 1. Types and Functions of Nipple-Aareolar Complex

Appearance at Rest Functions (during a feeding)

a. Normal/Prominent– At rest, nippleprotrudes outward from areola

Protracts – extends further outward with Suctionfacilitating adequate latch-on and “milking” of thelactiferous sinuses

b. Flat – Nipple is flat with breast contour Protracts or Retracts, i.e., moving inward

c. Inverted – All or parts of the nipple isdrawn inward within areolar folds

Simple inversion – moves outward with SuctionComplete inversion - does not respond to manual pressuredue to adhesions binding nipple inward

d. Pedunculated - nipple sits on a stalkaway from areola

Nipple may be too big for infant’s mouthStalk may protract or retract

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It is interesting to note that nonnutritive sucking with a pacifier matures earlier thannutritive sucking as shown in the tracings of two preterm infants monitored for 2–3 minutes ona pacifier at the beginning of a feeding and immediately switched to bottle feeding thereafter (seeFigure 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 (seeFigure 3a). This contrasts with the infant taking four oral feedings per day who used a mature

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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 minimalswallowing (i.e., only saliva) in contrast to nutritive sucking. In the latter case, the sustained milkinflow into the mouth must be rapidly and safely transported to the stomach. This can only beachieved if sucking, swallowing, respiration, and esophageal function work hand-in-hand (Lau,2006). As swallowing is minimal during nonnutritive sucking, it becomes debatable whetherassessment of nonnutritive sucking alone is a sufficient marker for readiness to oral feed, althoughit 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 ofOral Feeding Advancement

Infants were monitored for 2–3 min on a pacifier at the beginning of a feeding and immediatelyswitched to bottle feeding thereafter: (a) The first infant fed ad libitum demonstrated both maturenonnutritive and nutritive sucking patterns (Stage 5); and (b) the second infant used a maturenonnutritive pattern with the pacifier (Stage 5) and immature nutritive pattern when bottle fed(Stage 2). Stages were assessed using the descriptive scale shown in Figure 1. Note. From Lau, C.,& Kusnierczyk, I. (2001). Quantitative evaluation of infant’s nonnutritive and nutritive sucking.Dysphagia, 16, 58–67. Used with permission.

Swallowing FunctionThe swallowing process consists of an oral, pharyngeal, and esophageal phase with each

phase of the reflex requiring complex sensorimotor interactions and executive motor outputs thatdevelopmentally 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 influxfrom the next suck takes place. Any delay(s) in bolus formation, pharyngeal, and esophagealtransport 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

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the swallow reflex may be affected by the proper coordination of the lingual musculature and thatof 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 properclosures 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 ofthese anatomical structures and their coordinated interactions with the sensory-neural control ofthe 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 oraspiration into the larynx/lungs and bolus disintegration (Jadcherla, Hogan, & Shaker, 2010). Todelay disintegration of a liquid bolus, increasing milk viscosity is often considered whetherthickeners such as rice cereal, special formula, or human milk thickeners are used. The necessityof thickening milk remains debatable and deserves revisiting.

Respiratory FunctionPreterm 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 breathesat 1 cycle/sec and his/her swallow lasts 0.7 sec, only 0.3 sec is left for safe breathing. Undersuch conditions, few infants could tolerate oral feeding for a prolonged period of time.

Esophageal FunctionThe study of esophageal function in preterm infants has been restricted by the

technologies available. Fortunately over the last decade, novel devices designed for their smallsize and fragility have emerged such as endoscopic manometry, multichannel intraluminalimpedance (MII), and pH- MII.

The Upper Esophageal Sphincter (UES)

The upper esophageal sphincter (UES) plays an important role in bolus transport from thepharynx to the esophageal body. Studies have highlighted how readily oral feeding issues mayarise when pharyngeal-UES and UES-esophageal interactions are dys-coordinated. A recent studyconducted on preterm infants (28 ± 1.9 weeks gestation [GA] and monitored for 4 weeks between31 to 36 weeks postmenstrual age [PMA]0 observed that most preterm infants demonstrated poorPMA-related pharyngeal pressures that lead to poor coordination of pharyngeal bolus propulsionand timing of UES relaxation. However, increased pharyngeal pressure with well-developed UESand 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 resultof 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. Theperistaltic group distinguishes between the antero- and retro-grade waves. The anterograde wavetravels from the UES down to the lower esophageal sphincter (LES) and is responsible for thebolus transport to the stomach. The retrograde wave travels in the opposite direction towardsthe UES and, at times, is blamed for occurrences of regurgitation. The non-peristaltic groupincludes synchronous and incomplete wave patterns. With maturity, a decrease in incompletenon-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 acrossthe esophageal-gastric junction. Two types of LES relaxation (LESR) can be distinguished. Theswallow-related LESR (SLESR) is associated with the anterograde transport of nutrients into the

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stomach. The transient LES relaxation (TLESR), in turn, is independent of swallowing andassociated with belching or gastro-esophageal reflux (GER). TLESR may occur under differentconditions that are not necessarily related with nutrient intake (Omari, 2006). It remains unclearwhether TLESR occurs more frequently in preterm vs. term infants.

Gastric Emptying

Little is known about the development of gastric emptying in preterm infants. Gastricresidual is routinely measured prior to enteral/oral feeding. Depending upon individual NICUpractices, feeding may be halted depending upon the measured residual. It is of interest tomention that Omari et al. (2004) observed that lateral positioning of an infant following a feedingmay facilitate gastric emptying (Omari et al., 2004; van Wijk et al., 2007).

Suck-Swallow-Respiration-Esophageal CoordinationOral feeding problems would be minimized with the proper maturation of the above

physiologic functions. However, it is their “coordinated” interactions that will ensure safety andefficiency. But it is yet unclear what such coordination consists of. In practice, caregivers oftenpresume that sucking, swallowing, and respiration are coordinated if an infant feeds with noadverse events, such as oxygen desaturation, bradycardia, apnea, coughing, and choking. Butsuch presumption is not always correct as observed with aspiration/pneumonia potentiallycaused 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 between120 –160 beats/min. As such, one may speculate that coordination would be optimized if thesefunctions were to work in phase vs. out of phase from each other (see Figure 4). Indeed, when inphase, an additive/synergistic net effect would be expected, whereas when out-of- phase, theexpected net effect would be reduced.

Figure 4. Net Effects of Phasic Systems Working In and Out of Phase

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We conducted a study to characterize the coordination of sucking, swallowing, andrespiration (Lau, Smith, & Schanler, 2003). We investigated separately the suck-swallow andswallow-respiration interactions. Infants born between 26.8 ± 2.7 weeks GA demonstrated aconsistent 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 thatits proper coordination was more relevant to safety (i.e., minimizing liquid penetration into thelarynx). We reasoned that the riskier times to swallow would be during inhalation as air rushesinto the lungs and deglutition apnea as increased risks of aspiration and oxygen desaturationwould occur, respectively (see Figure 5). As such, the percent frequency of when swallowsoccurred during the different phases of respiration was monitored. Table 2 shows that preterminfants 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 andend of inhalation when no air flow occurs. It is of interest to note that adults primarily swallowduring exhalation (McFarland, Lund, & Ganger, 1994; Nishino & Honda, 1982). McFarland et al.(1994) observed that, in adults, swallowing occurred at different phases of respiration dependingupon the feeding/eating posture and speculated that such alteration resulted from themechanical properties of the upper body (McFarland et al., 1994). If correct, infant feedingpositions may affect the swallowing safety with respect to respiration. An intriguing thought thatwould require future studies for evidence-based confirmation.

Figure 5. Respiratory Phases When Swallowing May Occur

(i) during inhalation; (start i) at start of inhalation; (end i) at end of inhalation; (e) during exhalation;(5i) during inhalation with incomplete inhalation; (5e) during exhalation with incomplete exhalation;DA during respiratory pauses ≥ 2 sec (Lau et al., 2003).

Table 2. Percent Occurrence of Swallow-Respiratory Interfacing with Maturation

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Concerns over the dys-coordination of sucking, swallowing, and esophageal functionprimarily reside in the adverse occurrences of regurgitation, choking, aspiration, GER, and/orpotential gastro-esophageal reflux disorder and esophagitis. This topic is not addressed here as itfalls 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-oralfeeding origins, namely infants’ clinical status, the NICU environment, and/or infants’ ownbehavioral states and organization.

Infant Clinical StatusIn 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/orbradycardia 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 EnvironmentAwareness that infants have been abruptly transitioned from an in- to extra-uterine

environment is important. Light, sound, touch, temperature, and mobility inside and outside thewomb are strikingly different (see Table 3). As such, the smoother the transition, the lessstressful infants’ adaptation will be.

Table 3. NICU Environment Inside vs. Outside the Womb

Factors Inside the womb. . . Outside the womb. . .

Light Dark Bright

Sound Muffled (voices) Loud (alarms)

Touch Consistent containment, smooth, calming Inconsistent containment, impersonal,aversive

Thermal Constant, warm Fluctuating

Mobility Day/night maternal input, fluid environment,Supported flexed posture

Limited maternal inputdry environment,Unsupported extended posture

Infant Behavioral StatesThe 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 areat 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 rapidlywould 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 OrganizationBehavioral 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 well-beingof the infant. For instance, an infant will be deemed organized if calm, relaxed, with regularbreathing, arms folded in midline, eyes closed or open. Disorganization will be characterized by

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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 evaluatethe severity level(s) of their symptoms, identify the most probable functional weakness(es), andconsider the available evidence- based interventions to resolve the problem.

Commonality of SymptomsA 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 associatefatigue with one or more of the following: poor tone, changes in behavioral state (e.g., sleep), “shutdown,” increase duration of sucking pauses, increased milk leakage or drooling. To the author’sknowledge, 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 non-specific symptom that results from manycauses. If there is no specific measure of “medical fatigue” in adults, it would be even moredifficult to define one in infants due to their developmental immaturity. This comment perfectlyrelates to the subjectivity/bias that we, as caregivers, may have when caring for our patients. Iffeeding 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 tosuck-swallow-respiration incoordination, coughing, choking, aspiration, poor self-pacing, oxygendesaturation, 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 paidto the appearance order of these symptoms, by the time they are observed, identification of theoriginal culprit(s) is difficult due to the commonality of the symptoms (see Table 4). However, ifinfants were closely watched from the start of a feeding, their sequential appearance, be itthrough their behavior or the alarm monitor, can provide early clues as to the origin of theproblem. For instance, by regularly watching the alarm monitors, one can catch whether oxygendesaturation, cardiac or respiratory activity pattern is first to change. Often times, this wouldappear before any observable behavior takes place.

Table 4. Commonality of Oral Feeding Symptoms if Oral Feeding is Maintained

Physiological Behavioral

- Oxygen desaturation - Poor tone

- Apnea/bradycardia - Fall asleep

- Tachypnea - Agitated

- Choking/coughing - Pushing away

- Aspiration - Turning head away

- Emesis - State change -“shut down”

- Milk leakage - aversive to feeding

Evaluation ModalitiesThe development of instruments to evaluate infant oral feeding skills comprises qualitative

and quantitative approaches. Qualitative approaches, primarily conducted through observationaltechniques, document the presence/absence of specific behaviors and/or cues (Palmer, Crawley,& Blanco, 1993; Thoyre, Shaker, & Pridham, 2005). However, care must be taken in dataanalyses not to incorporate individual biases. Intra- and inter-reliability testing is essential. Using

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full term infants’ behavioral repertoire for instance as control standards would be inappropriateinsofar as preterm infants have not yet attained the same level of behavioral maturity due to theimmaturity of their motor and/or sensory development. A good example is illustrated again bythe occurrence of silent aspiration detected only after aspiration/pneumonia presents (Arvedsonet al., 1994; Weir et al., 2011).

Quantitative approaches require special equipment that can offer accurate measures ofspecific outcomes (e.g., sucking amplitude (mmHg), sucking frequency, temporal profiles ofsuck-swallow-respiration or esophageal motility). Some are offered through specialty services(e.g., pediatric gastroenterology for endoscopic manometry, MII, pH –MII; speech languagepathology 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 thepercent 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 OFSlevels 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 byPRO ≥ 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, aresultant of infants’ overall skills when fatigue came into play, was used as an index of overallendurance (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, albeitsmaller percentile of infants demonstrated OFS levels 1 with greater GA. Such broad variance inOFS 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/volumeprescribed 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 theirfeeding performance rather than their GA. It is of interest to note that infants using OFS levels 2and 3 perform equally well (i.e., taking between 70 to 80% of their prescribed feeding). This wouldsuggest 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

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Figure 7. Percent OFS Levels by Gestational Age at First Oral Feeding

Figure 8. Percent Overall Transfer (% volume taken/volume prescribed) by OFS Levels

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Potential Interventional ModalitiesInsofar 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 interventionssuch as tactile/kinesthetic, vestibular, and auditory stimulation have been demonstrated to benefitinfant 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-oralfeeding issues that may interfere with an infant’s feeding performance.

Studies have identified well-tolerated evidence-based modalities to assist oral feedingissues originating at the levels of sucking, swallowing, swallowing-respiratory interfacing, and/oresophageal functions.

SuckingNonnutritive oral stimulation, using different approaches, has been shown to improve the

oral feeding performance of preterm infants. An association between improved stability in thenonnutritive sucking pattern following therapy with the NTrainer, a nonnutritive suckingassessment device (Innara Health, Olathe KS) and the percent of the total daily intake taken bymouth vs. tube was observed (Poore, Zimmerman, Barlow, Wang, & Gu, 2008). These investigatorsused a particular therapy protocol providing 3-min epochs stimulations up to 4 times/dayduring scheduled gavage feeds until infants were able to take 90% of their feeds by mouth for

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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, and6–8 oral feedings/day. Compared to control counterparts, infants’ OT and RT were enhanced andindependent 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, subjectssimilarly attained independent oral feeding more rapidly, demonstrated more mature OFS levelprofile, greater suction and expression amplitude, and decreased episodes of deglutition apneawere observed (see Figure 9; Fucile, Gisel, McFarland, & Lau, 2011; Fucile, McFarland, Gisel, &Lau, 2012; Lau, Fucile, & Gisel, 2012).

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 thenonnutritive therapy described above. We reasoned that, if this were achieved, it would be anintervention that parents could provide to their infants. The sucking-pacifier exercise was offered15-min per day, 5 days a week, beginning 48 hours post nCPAP and continued until infants attainedindependent oral feeding (8 oral feedings/day). The exercise consisted of gently moving the pacifier ina rhythmic up/down and posterior/anterior motion and reliably initiated sucking. Unfortunately, itdid not offer the benefit observed with our original nonnutritive oral motor stimulation programprovided by a therapist (Lau et al., 2012). Days from start to independent oral feeding and OFSlevel profile were not significantly different from those of control counterparts (Figure 10).

Figure 9. OFS Profiles of Infants Receiving Nonnutritive Oral Motor (NNMOT), Massage Therapy (MT),Combined NNOMT+MT, and Sham (Control) Interventions

Days from introduction of oral feeding to 3–5 and 6–8 oral feedings/day. SOF: Start of oralfeeding * p<0.001 vs control (Lau et al., 2012).

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Figure 10. OFS Profiles of Infants Receiving a Nonnutritive Exercise (Pacifier), a Swallow Exercise,and No Intervention (Sham Control)

Days from introduction of oral feeding to 3–5 and 6–8 oral feedings/day. SOF: Start of oralfeeding.* p<0.019 vs. control (Lau & Smith, 2012).

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SwallowingAs 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 receivingat the time (e.g., mother’s milk, formula) via a 1-ml syringe directly on the medial-posterior parton the tongue, approximately at the level of the hard and soft palate junction, close to the sitewhere the bolus rests prior to entering the pharynx (Arvedson & Lefton-Greif, 1998). The infantsstarted with 0.05 ml and the volume was increased by 0.05 ml increment to a maximum of 0.2 mluntil a swallowing reflex was observed or as tolerated (i.e., the intervention was halted at any signof adverse events such as unstable vitals, choking, fatigue, and/or disorganization). A maximumvolume of 0.2 ml was based on the knowledge that the bolus size of preterm infants averaged0.14 ± 0.06 ml. This compares to an average of 0.22 ± 0.07 ml in term infants during their firstmonth of life (Lau et al., 2003). Once the minimal volume necessary to initiate the swallow reflexwas visually identified, it was used for the duration of the exercise. This program shortened thenumber of days from start to independent oral feeding by six days and OFS profile were significantlymore mature as infants progressed vs. to control counterparts (see Figure 10).

Swallow-Respiration Interfacing — Feeding PositionsWith the knowledge that preterm infants swallowed at riskier respiratory phases than

term infants and that swallowing-respiration interfacings are affected by feeding/swallowing

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positions (McFarland et al., 1994), we speculated that oral feeding performance of infants may beinfluenced by their feeding position. Additionally, we were aware that caregivers advocated fordifferent 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 positionin the early 2000, over the last few years, the side-lying position was preferred. Two studiesconducted on feeders and growers born ≤ 34 weeks GA, when fed in the side-lying position, didnot 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 oforal feeding, such feeding position complemented with the CoReg feeding approach improvedinfant behavioral and physiologic responses vs. counterparts fed by the Usual Care. CoRegconsists of the transmission of infant respiratory and swallowing sounds during feeding tocaregivers 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, todetermine whether these different positions benefit oral feeding performance, VLBW infants wererandomized to being fed in the semi-reclined (control), upright, or side-lying position. Whenmonitored at 1–2, 3–5, and 6–8 oral feedings/day, no differences were observed in days toindependent oral feeding and OFS profiles (see Figure 11). Based on the average number of days toindependent oral feeding, one may conclude that feeding in the upright and side-lying positions donot 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 sizeof subjects. Knowing that infants within gestational and postmenstrual ages can demonstrate awide range of OFS levels (Lau & Smith, 2011), large variances in any outcome measure will readilylead to statistical non significance. Although such analytical procedures is essential in order toidentify the overall impact that an intervention can have on a particular subject population, itcannot identify individual subjects who may or may not have benefited from a treatment. Aspractitioners’ primary concern is to care for individual patients, we propose that routinemonitoring of infant’s OFS levels can help identify those who benefited from a particularintervention from those who did not. In the case of feeding positions, such practice would identifyinfants who benefit from the semi-reclined, upright, or side-lying. If used appropriately, the OFSscale can become a useful “tool” to individualized therapy/care.

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Figure 11. Infant OFS Profiles When Fed in Semi-Reclined (Control), Upright, and Side-LyingPosition

Days from introduction of oral feeding to 3–5 and 6–8 oral feedings/day. SOF: Start of oralfeeding * p<0.001 vs control (Lau et al., 2012).

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Swallow-Esophageal InterfacingInappropriate swallow-esophageal interfacing is well-known to lead to regurgitation,

reflux, esophagitis, and potential long-term feeding aversion if left untreated. As identification ofthe potential esophageal cause(s) cannot yet be readily identified, no succinct evidence-basedsupport for a potential treatment has yet been described. However, in the meantime, otherapproaches ought to be considered such as allowing infants to regulate their own feeding withno “encouragement” from caregivers (see self-paced feeding below).

Massage/Tactile-Kinesthetic TherapyTactile/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 massagetherapy. The latter practice has been used on infants for centuries in Eastern societies and itsacceptance 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 oninfants 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 preterminfant 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 infantswho received the massage treatment attained independent oral feeding faster than controlcounterparts; their OFS profiles and the coordination of swallow-respiration were more mature.

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However, combining both nonnutritive oral stimulation and massage treatment was not of furtherbenefit (see Figure 9; Fucile et al., 2011; Fucile et al., 2012; Lau et al., 2012).

Self-Pace FeedingThe 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, wereasoned that preterm infants with normally developing neurologic functions (i.e., “feeders andgrowers”), can reflexively protect themselves, if given that opportunity. To test this hypothesis, wedeveloped a “self-paced” feeding system to give control of the feeding to the infants. This wasachieved by eliminating the positive hydrostatic pressure always present when a bottle is tilted sothat milk outflow only occurred when infants were sucking. This would allow them to pause/restand breathe whenever necessary without milk dripping into their mouth. Additionally, thisfeeding system continuously prevented the natural vacuum-build up that occurs as a containerempties thereby eliminating the resistance against milk outflow from the bottle that naturallyoccurs (Lau & Schanler, 2000). VLBW infants feeding with the self-paced system demonstratedsignificantly 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 thanrecognized by caregivers (Fucile, Gisel, Schanler, & Lau, 2009). These data suggested that not onlycould interventions facilitate infant oral feeding, but tools could be developed to assist as well.

Common Sense Modalities Affecting Non-Oral Feeding IssuesAlthough 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 “commonsense” approaches to consider while feeding an infant, respectively.

Table 5. Babies 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,

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

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Table 6. Common Sense Approaches to Consider

Approach Why How

Reduce noise/light levels - Minimize external over-stimulations, behavioraldisorganization

- Switch off overhead light- Moderate voice level

Adjust feeding position - To facilitate organization,respiration, swallowing,decrease potential reflux

- Slightly upright, cradled- Body/head in midline- Upper chest/head well supported,- No crouching

Let infant regulate milk flow - We do not know infants’physical and physiologiclimitations

- Allow infant to self-pace (e.g.,to rest, catch-up breathing)

- Do not “encourage” feeding

Vary number and/orduration of oral feeding experience

- To reduce adverse events(e.g., fatigue, aspiration)

- To develop good OFS- To offerpositive experience

- To avoid oral feeding aversion

- Decrease number of dailyoral feedings, or

- Decrease oral feedingdurations, or

- Maintain number of dailyoral feedings,but decrease duration of oralfeeding by tube feed remaining

→ offers positive oral feedingexperience when fatigue is minimal

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Modalities and Considerations for Practice

Preterm infants are challenged not only by developmental delays due to their imposedextra-uterine maturation, but also by the negative sensory inputs in the NICU necessitated bytheir fragile medical condition and the tasks asked of them such as oral feeding. Oral feedingconcerns, as mentioned earlier, is a relatively new recognition and thus lacks guidelines andevidence-based support for many of the current practices.

Due to limited availability of quantitative evaluation and diagnostic devices, caregivershave justifiably turned to qualitative methodologies. In this regard, the current popular cue-basedfeeding approach (Garber, 2013; Kirk, Alder, & King, 2007; Ludwig & Waitzman, 2007; Puckett,Grover, Holt, & Sankaran, 2008), has raised concerns as to whether preterm infants aresufficiently 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 bea more individualized approach by taking into consideration the differing stages of behavioraldevelopment, clinical stability, motor skills, and endurance that individual infants encounter.Therefore, the currently identified “feeding cues” may not apply across the board to particularpopulations 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 ofsolid evidence-based support (Tosh & McGuire, 2006). The notion of whether preterm infantshave a “sense” of hunger/satiety is unknown. Hunger is defined as “a feeling of discomfort orweakness caused by lack of food, coupled with the desire to eat” (“Hunger,” n.d.). As a sensorystimulus, it implicates a certain level of neuro-physiologic-endocrine maturity that preterminfants may not have attained. Therefore, cues for hunger are difficult to identify. This is wellillustrated by the study of Hodges and colleagues (2008) suggesting that qualitative assessmentmay differ between mothers “in the extent to which they perceive and rely upon infant hungerand fullness cues to initiate and terminate feeding”. Such variance in caregivers’ perception ofwhat infant observational cues may project raises concerns over whether their nutritional needs

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could be met on a consistent level. If only a cue-based feeding approach were used, knowledgeof the maturation level of individual infants’ motor development at assessment times would beessential.

Little is known regarding when the sense of hunger/satiety develops. A hunger center inthe lateral hypothalamus has been long recognized (Wise, 1974) and particular stomach, body,and antral muscular activity interacting with the lateral hypothalamic hunger site has beenshown to regulate degrees of hunger/satiety (Kromin & Zenina, 2013). Additionally, hormonalinvolvement (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’ behavioralrepertoire is unknown. It is primarily for these reasons that concerns have been raised over theuse of cue-based feeding alone.

The above discussions are presented as potential means to develop an organized andmore systematic differential diagnostic approach to address infant oral feeding issues.

In the presence of oral feeding symptoms, one may want to determine whether: (a) feedingought to be halted (see Table 5); (b) NICU environment (light and sound), swaddling, feedingposition are appropriate (see Table 6); or (c) the infant is feeding at his/her own pace with noencouragement from caregiver. At the end of the feeding, assessing OFS levels may help identifythe 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 shorterduration). Increasing training opportunities when fatigue is minimal will favor the development ofgood skills.

Table 7. Potential Interventions to Consider

OFS Levels Feeding skills (PRO) Endurance (RT) Potential Interventions

1 Poor Poor Appropriate evidence-based directed intervention(s)+

“oral feeding training”

2 Poor Good Appropriate evidence-based directed intervention(s)

3 Good Poor “oral feeding training”

4 Good Good none

Summary and Conclusions

In brief, this review presents the current understanding of the development of infant oralfeeding skills from which efficacious evidence-based interventions were developed. As the goal ofresearch 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 interventionsused does not receive support from a number of disciplines.

Acknowledgment

The author wishes to thank her many collaborators who have supported her work overthe years and for support from the National Institute of Health (R01-HD-28140; HD 044469;MO1RR000188). The contents of this publication are solely the responsibility of the author anddo not necessarily represent the official views of the National Institute of Child Health and HumanDevelopment or the National Institutes of Health.

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Interventions to Improve Oral Feeding Performance of ... · Interventions to Improve Oral Feeding Performance of Preterm Infants ... seal of the lips around the breast or bottle nipple,