assessment of laryngopharyngeal sensation in children with dysphagia

The LaryngoscopeVC 2013 The American Laryngological,Rhinological and Otological Society, Inc.

Assessment of Laryngopharyngeal Sensation in Children

With Dysphagia

Seckin Ulualp, MD; Ashley Brown, CCC-SLP; Rina Sanghavi, MD; Yadira Rivera-Sanchez, MD

Objectives/Hypothesis: To assess laryngopharyngeal sensation, prevalence of laryngopharyngeal sensory deficit andabnormal swallowing function parameters in children with dysphagia.

Study Design: Retrospective chart review.Methods: The medical records of children who underwent flexible endoscopic evaluation of swallowing with sensory

testing (FEESST) were reviewed. Laryngopharyngeal sensory threshold (LPST) was assessed based on the threshold intensityof air pulse stimulation eliciting laryngeal adductor reflex. Swallowing function parameters including pharyngeal residue,hypopharyngeal pooling of secretions, premature spillage, laryngeal penetration, and aspiration were evaluated. Prevalence ofabnormal swallowing function parameters in children with normal and impaired LPST was compared.

Results: Forty children with dysphagia (28 male, 12 female; age range, 3 months to 17 years) underwent FEESST. LPSTwas normal in six patients, moderately impaired in 20 patients, and severely impaired in 10 patients. LPST could not bemeasured in four patients. Children showed one or more abnormal swallowing function parameters. The prevalence of abnor-mal swallowing parameters in patients with normal LPST was lower than that of patients with moderately or severelyimpaired LPST (P<.05). The prevalence of pharyngeal residue, hypopharyngeal pooling of secretions, and spillage in patientswith severely impaired LPST was higher than that of patients with moderately impaired LPST (P<.05).

Conclusions: The majority of children with dysphagia have impaired LPST. The prevalence of abnormal swallowing func-tion parameters in children with normal LPST is lower than that in children with moderately or severely impaired LPST. Prev-alence of aspiration tends to increase when the abnormal swallowing function parameters are associated with severelyimpaired LPST.

Key Words: Dysphagia, laryngeal sensation, premature spillage, laryngeal penetration, aspiration, pediatric.Level of Evidence: 4

Laryngoscope, 123:2291–2295, 2013

INTRODUCTIONNormal swallowing function is critical for survival

and development of children. Feeding and swallowingdisorders in children are associated with reduced qualityof life and increased morbidity and mortality.1 Dyspha-gia in children may occur in conjunction with multipleand complex medical and developmental conditions.Children with dysphagia present with feeding difficultiesor respiratory problems. Early diagnosis of children withdysphagia and identification of the specific level ofimpairment are critical for instituting appropriate inter-vention and counseling.

Intact neurosensory and motor function of the aero-digestive tract is critical for achieving normal swallowing.Flexible endoscopic evaluation of swallowing with sensorytesting (FEESST) enables evaluation of laryngopharyng-eal sensory motor function while visualizing the anatomyand physiology of the swallowing mechanism.2–6 Sincethe feasibility of FEESST in children was reported in2000, laryngopharyngeal sensory deficit has been docu-mented in children with apnea, gastroesophageal reflux(GER) disease, and laryngomalacia.7–10 To date, laryngo-pharyngeal sensation and its association with deficits inswallowing function parameters have not been systemati-cally studied in children with dysphagia. The aims of thisstudy were to assess laryngopharyngeal sensation in chil-dren with dysphagia and to evaluate the prevalence oflaryngopharyngeal sensory deficits and swallowing func-tion parameters including pharyngeal residue, hypophar-yngeal pooling, premature spillage, laryngeal penetration,and aspiration.

MATERIALS AND METHODSThe charts of children with dysphagia who had FEESST

between September 2009 and November 2011 were reviewedretrospectively. Children with dysphagia were outpatientsreferred by their physicians for FEESST. The study wasapproved by the local Institutional Human Research ReviewBoard. The study was designed to include all patients under the

From the Departments of Otolaryngology–Head and Neck Surgery(S.U.), Physical Medicine and Rehabilitation (A.B.), Gastroenterology andHepatology (R.S.), Pulmonology (Y.R.-S.), and Pediatric Airway and Swal-lowing Disorders Program (S.U., A.B., R.S., Y.R.-S.), University of TexasSouthwestern Medical Center and Children’s Medical Center, Dallas,Texas, U.S.A.

Editor’s Note: This Manuscript was accepted for publicationJanuary 8, 2013.

Presented at the Annual Meeting of American Society of PediatricOtolaryngology, San Diego, California, U.S.A., April 20–22, 2012.

The authors have no funding, financial relationships, or conflictsof interest to disclose.

Send correspondence to Seckin O. Ulualp, MD, Department of Oto-laryngology–Head and Neck Surgery, University of Texas SouthwesternMedical Center, 5323 Harry Hines Blvd Dallas, TX 75390-9035. E-mail:[email protected]

DOI: 10.1002/lary.24024

Laryngoscope 123: September 2013 Ulualp et al.: FEESST in Children With Dysphagia

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age of 21 years. Children were not excluded because of neuro-logic impairment, congenital heart disease, craniofacial anoma-lies, and developmental delay.

The laryngopharyngeal sensory discrimination test wasperformed before introduction of varying textures of food for en-doscopic evaluation of swallowing. Laryngopharyngeal sensorythreshold (LPST) was determined by endoscopically deliveredair pulse stimuli to the aryepiglottic mucosa and observation oflaryngeal adductor reflex (LAR). For stimulation of aryepiglotticfold, a calibrated air stimulator unit (AP-4000 Air Pulse Sen-sory Stimulator; Pentax, Montvale, NJ) connected to a flexiblelaryngoscope (2.4 mm, ENT-1000; Vision Sciences, SouthOrangeburg, NY) with an accessory channel (Slide-on SensorySheath 1.2 mm; Medtronics, Minneapolis, MN) was used todeliver air pulse for 50 milliseconds in all patients. LAR wasinduced by delivering air pulse stimuli with intensities rangingfrom 2 to 9.9 mm Hg. The procedure was performed while thepatient was seated in an upright position in the lap of a care-giver. After applying 2% viscous lidocaine to the intranasal cav-ity using medical cotton-tipped applicator in all patients, theflexible laryngoscope was introduced through the nasal cavity,and the tip of the laryngoscope was advanced to a positionwithin 2 to 3 mm of the aryepiglottic fold. To prevent intersub-ject differences in the distance between the tip of the laryngo-scope and the aryepiglottic fold, the laryngoscope was advanceduntil the view of the targeted region was blurred, and then thelaryngoscope was withdrawn until the mucosa of targetedregion became clearly visible. At this point, an air pulse wasdelivered; successful delivery of air stimulation was confirmedby the development of a mucosal deflection by air pulse. Thefirst air-pulse stimulus was delivered at an intensity of 6 mmHg pressure. If the LAR was triggered, the pressure wasreduced by 0.5-mm Hg decrements, down to minimum pressureof 2 mm Hg or until the LAR was no longer seen. Once the LARwas no longer triggered, the pressure was raised by 0.5 mm Hg,and if the LAR could again be triggered, the same pressure wastested one more time and was considered sensory threshold ifthe LAR was triggered on two occasions. If no LAR was trig-gered with 6 mm Hg pressure, the pressure was increased in 2-mm Hg stepwise increments to a maximum of 10 mm Hg. Oncethe LAR was triggered, the pressure was reduced by 0.5 mmHg until the LAR was no longer triggered, and the lowest pres-sure that triggered the LAR was considered to be the sensorythreshold. If no LAR was triggered with the maximal air-pulsepressure of 10 mm Hg, the testing was completed. The LPSTwas considered to be normal if the LAR was stimulated by pres-sure of less than 4 mm Hg, moderately impaired if LAR wasstimulated by pressure of 4 to 6 mm Hg, and severely impairedif LAR was stimulated by pressure of more than 6 mm Hg.3

Once the LPST was determined, a swallowing assessmentwas performed with liquids and with a variety of textures ifdevelopmentally appropriate. Data presented include a swallow-ing assessment performed with thin liquid. The swallowingfunction parameters evaluated were pharyngeal residue, hypo-pharyngeal pooling (pooling of secretions in pyriform sinus), la-ryngeal penetration, and aspiration.11 The pharyngeal residuewas defined as the food material remaining in the hypopharynxafter completion of the swallow. Premature spillage was definedas the progressing of the material over the tongue base intopyriform sinus in the absence of purposeful oral transfer beforethe initiation of swallowing. Laryngeal penetration was definedas passage of material into the larynx that did not pass belowthe vocal folds. Aspiration was defined as passage of materialbelow the level of the true vocal folds into the trachea.

Data pertaining to demographics, medical history, LPST,and findings of swallowing evaluation were recorded. Data anal-ysis was targeted at determining the presence of laryngophar-

yngeal sensory deficit and identifying the prevalence oflaryngopharyngeal sensory deficit and abnormal swallowingfunction parameters including pharyngeal residue, hypophar-yngeal pooling of secretions, premature spillage, laryngeal pene-tration, and aspiration. Statistical comparison between groupswas performed using parametric (one-factor analysis of variance[ANOVA]) and nonparametric (Kruskal-Wallis one-way ANOVAon ranks) tests as indicated. If the differences were significant,to isolate which group or groups differed from the others, a mul-tiple-comparison procedure (Student-Newman-Keuls method orDunn method) was used for data that were or were not nor-mally distributed, respectively, and for prevalence, v2 test asindicated. Values in the text are presented as mean 6 standarddeviation.

RESULTSForty children with dysphagia (28 male, 12 female;

age range, 3 months to 17 years) underwent FEEST.Symptoms suggestive of dysphagia included cough, gag-ging, choking, congestion, wet voice or cry, gurgly respi-ration, or wheeze during feeding. Comorbid conditionsincluded GER in 17 patients, asthma in eight, seizuredisorder in 15, cerebral palsy in five, Down syndrome inone, velocardiofacial syndrome in three, neonatal hypoto-nia in two, excision of posterior fossa ependymoma inone, spinal muscular dystrophy in one, and trisomy 9 inone. Three patients did not have comorbid conditions.Patients with GER received acid-suppressive medicationand did not have signs and symptoms of GER and lar-yngopharyngeal reflux at the time of FEESST.

All patients had normal bilateral vocal cord adduc-tion and abduction. Laryngopharyngeal sensation couldnot be measured in four patients (3 male, 1 female; agerange, 2–17 years) because LAR was not elicited withthe use of stimulus intensities reaching 9.9 mm Hg. Ofthe four patients with no inducible LAR, three patientsexperienced seizure and cerebral palsy, and one patienthad GER, asthma, and seizure. Two patients had pha-ryngeal residue, hypopharyngeal pooling, laryngeal pen-etration, and aspiration. One patient showed pharyngealresidue, hypopharyngeal pooling, and laryngeal penetra-tion. One patient had pharyngeal residue. LPST wasnormal in six patients (range, 2–3.5 mm Hg), moderatelyimpaired in 20 patients (range, 4–6 mm Hg), andseverely impaired in 10 patients (range, 6.5–9.5 mm Hg)(Fig. 1). Between-group comparisons showed no signifi-cant difference in the age of patients between thepatients with normal LPST (range, 9 months to 10years; median, 1.8 years) and patients with moderately(range, 3 months to 12 years; median, 1.3 years) orseverely (range, 6 months to 10 years; median, 2 years)impaired LPST.

In the group of patients with normal LPST, wedocumented hypopharyngeal pooling of secretions in onepatient, hypopharyngeal pooling and spillage in one, andlaryngeal penetration that was cleared in two. Pharyn-geal residue did not occur. No abnormal swallowingparameter was documented in two patients. In the groupof patients with moderately impaired LPST, we docu-mented pharyngeal residue in three, hypopharyngealpooling of secretions in 13, spillage in nine, laryngeal


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penetration in eight, and aspiration in six. Four of the12 patients with laryngeal penetration were able to clearlaryngeal penetration and had no aspiration. In thegroup of patients with severely impaired LPST, we docu-mented pharyngeal residue in three patients, hypophar-yngeal pooling of secretions in nine, spillage in seven,laryngeal penetration in four, and aspiration in four.None of the patients with severely impaired LPST wasable to clear laryngeal penetration.

The prevalence of abnormal swallowing parametersin patients with normal LPST and impaired LPST isshown in Figure 2. Aspiration and pharyngeal residuewere not observed in patients with normal LPST. In thegroup of patients with moderately impaired LPST, hypo-pharyngeal pooling of secretions occurred in the majorityof patients (65%). The majority of the patients withseverely impaired LPST had hypopharyngeal pooling ofsecretions (90%) and spillage (70%). Between-group com-parison showed that the prevalence of abnormal swal-lowing parameters in patients with normal LPST waslower than that of patients with moderately and severelyimpaired LPST (P<.05). Prevalence of pharyngeal resi-due, hypopharyngeal pooling of secretions, and spillagein patients with severely impaired LPST were higherthan in patients with moderately impaired LPST(P<.05). Prevalence of laryngeal penetration and aspira-tion in patients with severely impaired LPST was simi-lar to that in patients with moderately impaired LPST.

In between-group comparisons, LPSTs of patientswith pharyngeal residue, hypopharyngeal pooling ofsecretions, laryngeal penetration, or aspiration were notsignificantly different than those of patients withoutpharyngeal residue, hypopharyngeal pooling, laryngealpenetration, or aspiration (P>.05) (Fig. 3). LPST inpatients with spillage (6.3 6 2.0 mm Hg) was higherthan that of patients with no spillage (4.6 6 1.6 mm Hg)(P<.05).

In the group of patients with hypopharyngeal pool-ing of secretions, aspiration occurred in three (27%) ofthe 11 children with moderately impaired LPST. Three

(33%) of the nine children with severely impaired LPSTand hypopharyngeal pooling had aspiration. Among thepatients with premature spillage, aspiration occurred in

Fig. 1. Laryngopharyngeal sensory threshold in patients with nor-mal laryngopharyngeal sensation and impaired laryngopharyngealsensation is shown. Data for each patient group have been plot-ted. The mean value of each group is shown by horizontal line.

Fig. 2. Bar graphs display prevalence of swallowing abnormalitiesin relation to the groups of patients with normal and impairedlaryngopharyngeal sensory threshold (LPST). Prevalence of abnor-mal swallowing parameters in patients with normal LPST was lowerthan that of patients with moderately and severely impaired LPST(P<.05). Prevalence of pharyngeal residue, hypopharyngeal pool-ing, and spillage in patients with severely impaired LPST was higherthan that of patients with moderately impaired LPST (P<.05). How-ever, prevalence of laryngeal penetration and aspiration in patientswith severely impaired LPST was similar to that of patients withmoderately impaired LPST. A 5 aspiration; HP 5 hypopharyngealpooling; LP 5 laryngeal penetration; PR 5 pharyngeal residue;S 5 premature spillage.

Fig. 3. Bar graph displays the laryngopharyngeal sensory thresh-old (LPST) (mean 6 standard error [SE]) to induce laryngeal adduc-tor reflex in patients with abnormal swallowing functionparameters as well as in patients with normal swallowing functionparameters. Although there is trend for patient groups with pha-ryngeal residue, hypopharyngeal pooling, laryngeal penetration, oraspiration to have higher LPST, these observations did not reachstatistical significance compared with patients groups withoutpharyngeal residue, hypopharyngeal pooling, laryngeal penetra-tion, or aspiration. LPST in patients with spillage was higher thanthat of patients with no spillage (P<.05).


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two (22%) of the nine children with moderately impairedLPST and three (43%) of the seven patients withseverely impaired LPST.

DISCUSSIONSynchronous functioning and intact sensorimotor

processing of upper aerodigestive tract structures arecritical for the ability to swallow normally. With theadvent of FEESST, laryngopharyngeal sensorimotorfunction is safely and quantitatively assessed.2,4 FEESSThas been used to evaluate laryngopharyngeal sensorimo-tor and swallowing function parameters in adults withdysphagia. Despite the extensive research in the applica-tion of FEESST to the assessment of dysphagia in adults,the role for laryngopharyngeal sensorimotor functiontesting in the evaluation of dysphagia in children has notbeen widely studied. Since Link et al. reported the feasi-bility of FEESST and correlation between swallowingfunction parameters and laryngopharyngeal sensation ina diverse cohort of children in 2000, laryngopharyngealsensory function has been evaluated in children withapnea of infancy, laryngomalacia, and GER disease.7–10

In the present study, we assessed laryngopharyngeal sen-sation in children with dysphagia and evaluated theprevalence of laryngopharyngeal sensory deficit andabnormal swallowing function parameters.

The prevalence of laryngopharyngeal sensory deficitand abnormal swallowing function parameters asdetected with FEESST has not been studied in childrenwith dysphagia. Link et al. reported the assessment ofLPST and swallowing function parameters in a cohort ofchildren evaluated for feeding difficulty, dysphagia,upper airway abnormality, or airway reconstructive sur-gery.7 Because the findings of this cornerstone FEESSTstudy in children were not stratified for each group ofpatients, prevalence of laryngopharyngeal sensory deficitand the association among laryngopharyngeal sensorydeficit and swallowing function parameters in eachgroup of patients could not be assessed. Our findingsshowed that the majority of children evaluated for dys-phagia had an impaired LPST, and the prevalence ofabnormal swallowing parameters in patients with nor-mal LPST was significantly lower compared with that ofpatients with moderately and severely impaired LPST.Study findings also showed that prevalence of pharyn-geal residue, hypopharyngeal pooling of secretions, andspillage in patients with severely impaired LPST washigher than that of patients with moderately impairedLPST. These findings support the notion that the pres-ence of laryngopharyngeal sensory deficit increases thelikelihood of abnormal swallowing parameters in chil-dren evaluated for dysphagia.

Pharyngeal residue is suggested as a sign of ineffi-cient swallow to clear material from the hypopharynx.11

The presence of pharyngeal residue is correlated withaspiration as detected with videofluoroscopic swallowstudy in adults.12 Possible association between pharyn-geal residue and laryngopharyngeal sensorimotor func-tion in children has not been studied. In the present study,children with normal LPST did not have pharyngeal resi-

due. Pharyngeal residue occurred in 15% of children withmoderately and 30% of children with severely impairedLPST. Aspiration was documented in 33% of children withpharyngeal residue and moderately or severely impairedLPST. These findings provide preliminary evidence forimpaired laryngopharyngeal sensation in a group of chil-dren with pharyngeal residue and dysphagia. In agree-ment with our findings, pharyngeal residue was alsodocumented in adults with impaired pharyngeal motorfunction and laryngopharyngeal sensation.13 The underly-ing mechanism of pharyngeal residue has not beendelineated; however, motor and sensory abnormalities ofthe hypopharynx may contribute to pharyngeal residue.Pharyngeal motor function in adults is assessed by pha-ryngeal squeeze maneuver, which consists of examiningpharyngeal muscle strength and noting the presence orabsence of pharyngeal muscular contraction during volun-tary forceful adduction of the vocal folds.14–16 In adultswith pharyngeal motor dysfunction, the prevalence ofaspiration increases in the presence of severely or moder-ately impaired laryngopharyngeal sensation or absent lar-yngopharyngeal sensation.14–16

Hypopharyngeal pooling of secretions is associatedwith impaired LPST in children.7 In children, theamount of pooled secretions increases as the LPSTincreases. Hypopharyngeal pooling of secretions is asso-ciated with laryngeal penetration, aspiration, recurrentpneumonia, and neurologic disorder. Present study find-ings documented that the majority of the children withdysphagia and impaired LPST had hypopharyngeal pool-ing of secretions, which was not quantified; however,children with dysphagia and hypopharyngeal pooling ofsecretions showed a tendency to have higher LPST thanthe children with dysphagia and no hypopharyngealpooling of secretions. Considering that aspirationoccurred in 27% of the children with hypopharyngealpooling of secretions and moderately impaired LPST and33% hypopharyngeal pooling of secretions and severelyimpaired LPST, clinicians should be cognizant that aspi-ration may occur in children with hypopharyngeal pool-ing of secretions when LPST is impaired.

The presence of premature spillage in children doesnot always indicate abnormal swallowing function, asnormal children may exhibit premature spillage. Thepathologic significance of premature spillage in childrenhas not been well established because of a tendency tooverestimate premature spillage in children becauseflexible endoscopic evaluation of swallowing allows directvisualization of premature spillage.11 In the presentstudy, premature spillage was documented in one of thesix children with normal LPST. Premature spillageoccurred in 45% of children with moderately impairedLPST and 70% of children with severely impaired LPST.Aspiration in the presence of premature spillageoccurred in two (22%) of the nine children with moder-ately impaired LPST and three (43%) of the sevenpatients with severely impaired LPST. These findingsprovide preliminary evidence to emphasize the role forpremature spillage in the assessment of dysphagia inchildren. Clinicians have to be aware that prematurespillage in children with dysphagia may occur in the


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presence of impaired laryngopharyngeal sensation, andchildren with premature spillage and impaired LPSTmay have aspiration. As normal children may exhibitpremature spillage, a meticulous synthesis of informa-tion obtained from a complete clinical history and exami-nation, FEESST, and clinical impression of swallowingsafety is essential for the thorough assessment of thesignificance of premature spillage in children withdysphagia.

The clinical significance of laryngeal penetration isclosely related to the volume of material entering intothe larynx because laryngeal penetration is seen in nor-mal adults with no history or suspicion for swallowingdysfunction.17,18 Laryngeal penetration reaching to theregion between arytenoids and vocal folds has been sug-gested as a predictor of aspiration. Children with laryn-geal penetration showed increased LPST compared tochildren with no laryngeal penetration.7 Similar to pre-vious studies in adults,15 in the present study, laryngealpenetration occurred in few children with normal LPST;however, these children cleared the material from thelarynx.

Topical anesthesia to the nasal mucosa for FEESSThas been widely used in adults and children. Topicalanesthesia can be applied to the nasal cavity duringLPST without altering laryngopharyngeal sensation.19

However, clinicians and researchers should be awarethat spillage of topical anesthesia material has potentialto anesthetize the laryngopharynx. The limitations ofthe present study include its retrospective nature andthe lack of a control group including age-matched, non-syndromic, neurologically and developmentally normalchildren with dysphagia. Nonetheless, we believe pres-ent study findings are an important contribution to eval-uation of laryngopharyngeal sensory function andidentification of the association between the laryngo-pharyngeal sensation and abnormal swallowing functionparameters in infants and children with dysphagia. Ourfindings of increased likelihood of abnormal swallowingparameters in the presence of laryngopharyngeal sen-sory deficit support the notion that the assessment oflaryngopharyngeal sensory function may be used toincrease the diagnostic sensitivity of flexible endoscopicevaluation of swallowing and to aid safer dietary recom-mendations for the management of children with dys-phagia. A plausible application of increased LPST is toaid dietary recommendations in children who cannot befully tested for different textures of food during flexibleendoscopic evaluation of swallowing.

CONCLUSIONThe majority of children evaluated for dysphagia had

impaired LPST. The prevalence of abnormal swallowingfunction parameters in patients with normal LPST was

lower than that of patients with moderately and severelyimpaired LPST. The presence of severely impaired LPSTwas associated with a significant increase in the preva-lence of pharyngeal residue, hypopharyngeal pooling, andspillage. Prevalence of aspiration showed a tendency toincrease when the abnormal swallowing function parame-ters were associated with severely impaired LPST. Thesefindings highlight the role for evaluation of laryngophar-yngeal sensation along with abnormal swallowing func-tion parameters in the assessment of children withdysphagia.

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assessment of laryngopharyngeal sensation in children with dysphagia

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