Research in Developmental Disabilities 38 (2015) 192201

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Research in Developmental Disabilities

Clinical signs suggestive of pharyngeal dysphagia in preschool

children with cerebral palsy
Katherine A. Benfer a,*, Kelly A. Weir b,c, Kristie L. Bell a,d, Robert S. Ware c,e,
Peter S.W. Davies d, Roslyn N. Boyd a
a
Queensland Cerebral Palsy and Rehabilitation Research Centre, The University of Queensland, Level 7 Block 6, Herston 4029, Queensland,
Australia
b
Speech Pathology Department, Royal Childrens Hospital, Herston 4029, Queensland, Australia
c
Queensland Childrens Medical Research Institute, The University of Queensland, Herston 4029, Queensland, Australia
d
Childrens Nutrition Research Centre, QCMRI, The University of Queensland, Herston 4029, Queensland, Australia
e
School of Population Health, The University of Queensland, Herston 4029, Queensland, Australia

A R T I C L E I N F O

A B S T R A C T

Article history:
Received 14 October 2014
Received in revised form 10 December 2014
Accepted 11 December 2014
Available online 3 January 2015

This study aimed to determine the discriminative validity, reproducibility, and prevalence
of clinical signs suggestive of pharyngeal dysphagia according to gross motor function in
children with cerebral palsy (CP). It was a cross-sectional population-based study of
130 children diagnosed with CP at 1836 months (mean = 27.4, 81 males) and 40 children
with typical development (TD, mean = 26.2, 18 males). Sixteen signs suggestive of
pharyngeal phase impairment were directly observed in a videoed mealtime by a speech
pathologist, and reported by parents on a questionnaire. Gross motor function was
classied using the Gross Motor Function Classication System. The study found that
67.7% of children had clinical signs, and this increased with poorer gross motor function
(OR = 1.7, p < 0.01). Parents reported clinical signs in 46.2% of children, with 60%
agreement with direct clinical mealtime assessment (kappa = 0.2, p < 0.01). The most
common signs on direct assessment were coughing (44.7%), multiple swallows (25.2%),
gurgly voice (20.3%), wet breathing (18.7%) and gagging (11.4%). 37.5% of children with TD
had clinical signs, mostly observed on uids. Dysphagia cut-points were modied to
exclude a single cough on uids, with a modied prevalence estimate proposed as 50.8%.
Clinical signs suggestive of pharyngeal dysphagia are common in children with CP, even
those with ambulatory CP. Parent-report on 16 specic signs remains a feasible screening
method. While coughing was consistently identied by clinicians, it may not reect
childrens regular performance, and was not sufciently discriminative in children aged
1836 months.
Crown Copyright 2014 Published by Elsevier Ltd. All rights reserved.

Keywords:
Orpharyngeal dysphagia
Deglutition disorders
Pharyngeal phase impairment
Oropharyngeal aspiration
Cerebral palsy
Children

ANZTR Trial Registration Number: ACTRN12611000616976.

Abbreviations: CP, cerebral palsy; CPFQ, Queensland Cerebral Palsy Feeding Questionnaire; GMFCS, gross motor function classication system; GNPA,
Growth, Nutrition, and Physical Activity (study); NHMRC, National Health and Medical Research Council (Australia); OPD, oropharyngeal dysphagia; SD,
standard deviation; TD, typical development; VFSS, Videouoroscopic Swallow Study.
* Corresponding author at: Queensland Cerebral Palsy and Rehabilitation Research Centre, The University of Queensland, Level 7 Block 6, Royal Brisbane
and Womens Hospital, Herston 4029, Queensland, Australia. Tel.: +61 7 3646 5372; fax: +61 7 3365 5192.
E-mail address: katherine.benfer@uqconnect.edu.au (K.A. Benfer).
http://dx.doi.org/10.1016/j.ridd.2014.12.021
0891-4222/Crown Copyright 2014 Published by Elsevier Ltd. All rights reserved.

K.A. Benfer et al. / Research in Developmental Disabilities 38 (2015) 192201

193

1. Introduction
Oropharyngeal aspiration (food or uid entering the trachea below the vocal folds) (Brockett, 2006) is a commonly cited
risk factor for recurrent pneumonia (Vaughan & Katkin, 2002) occurring frequently in children with non-ambulatory
cerebral palsy (CP) and oropharyngeal dysphagia (OPD) (Mirrett, Riski, Glascott, & Johnson, 1994). In addition to causing
pneumonia, chronic aspiration may lead to interstitial lung disease, pulmonary brosis and bronchiectasis (Lefton-Greif &
McGrath-Morrow, 2007; Vaughan & Katkin, 2002). The nature of the aspirate, amount and frequency of aspiration all
inuence the consequent health outcomes, although the progression of respiratory sequelae and prognosis in children with
CP are poorly understood (Cass, Wallis, Ryan, Reilly, & McHugh, 2005; Lefton-Greif & McGrath-Morrow, 2007). Factors
related to respiratory status are of utmost importance, as respiratory-related factors are a leading cause of premature
mortality in individuals with CP (Blair, Watson, Badawi, & Stanley, 2001). CP is a motor disability arising from a nonprogressive neurological lesion, impacting on the strength and coordination of motor control (Smithers-Sheedy et al., 2013).
As such, neurologically mediated mechanisms can compromise the sensorimotor tasks of eating and drinking; with
impairments (OPD) occurring at any of the four phases of swallowing, including the oral-preparatory, oral-propulsive,
pharyngeal and oesophageal phases (Matsuo & Palmer, 2008).
The pharyngeal phase involves a complex set of sensory and motor responses as food or uid pass through the pharynx
(Matsuo & Palmer, 2008). The pharynx is a shared anatomical juncture, involved in the functions of swallowing and
respiration; hence, airway protection to prevent aspiration before, during and after bolus passage through the pharynx is
critical for respiratory health. Airway protection is achieved by closure of the true and false vocal folds, the epiglottis
inverting in response to the hyo-laryngeal excursion during the swallow, and nally deglutitive expiratory airow (glottal
release) (Lefton-Greif & McGrath-Morrow, 2007). Pharyngeal phase impairments in children with neurological conditions
include inadequate airway protection during the swallow, incomplete laryngeal clearance following the initial swallow
efforts, and/or decreased strength of pharyngeal contraction resulting in persistent residue in the hypopharynx postswallow (Morton, Minford, Ellis, & Pinnington, 2002). Problems with the volitional oral motor movements of the oralpreparatory and propulsive phases may also affect bolus transit and thus compromise airway protection.
In addition to the specic neurophysiological limitations to the oropharyngeal mechanism, OPD in children with CP is also
associated with their gross motor function (Benfer et al., 2013; Calis et al., 2008; Fung et al., 2002; Parkes, Hill, Plat, &
Donnelly, 2010; Reilly, Skuse, & Poblete, 1996; Sullivan et al., 2000; Waterman, Koltai, Downey, & Cacace, 1992). An unstable
pelvis and trunk can result in poor head and neck positioning, reducing the ability for controlled oropharyngeal movements
(Bosma, 1992; Langley & Thomas, 1991). Children with CP may use disordered patterns of movement to create a base of
stability, such as scapular retraction, which can inuence the position of the oropharyngeal structures and restrict their
mobility (Arvedson, Brodsky, & Reigstad, 2002). Poor head position has also been related to compromised airway protection
by opening the airway, and the inuence of gravity on ow rate of foods/uids swallowed (Arvedson et al., 2002; Ekberg,
1986; Lanert & Ekberg, 1995).
The safety of the swallow is initially screened for clinically, including a comprehensive evaluation of the mealtime, and
observation of clinical signs suggestive of pharyngeal phase impairment. A number of clinical signs have been used to
indicate aspiration, with varying levels of sensitivity/specicity when compared to instrumental assessment, depending on
the texture being assessed (Arvedson, Rogers, Buck, Smart, & Msall, 1994; DeMatteo, Matovich, & Hjartarson, 2005; Rogers,
Arvedson, Buck, Smart, & Msall, 1994; Warms & Richards, 2000; Weir, McMahon, Barry, Masters, & Chang, 2009). When food
or uid reaches the vocal folds, a protective cough may be triggered, although children with CP are at high risk of silent
aspiration (no coughing when foods/uids are aspirated), reported in between 82% (Weir, McMahon, Taylor, & Chang, 2011)
and 94% (Arvedson et al., 1994) of cases of aspiration. It is therefore important in this population to observe other signs of
aspiration such as wet/gurgly respiration or phonation, and fremitus (rattly chest). A child with clinical indications of
aspiration may have this conrmed through evaluation with videouoroscopic swallow study (VFSS). While widely
considered the gold standard for detecting aspiration, VFSS tends to be restricted to tertiary hospitals (requiring trained
personnel) and children are exposed to radiation during the procedure. Thus referral rates have remained relatively low,
depending on the geographical region (Clancy & Hustad, 2011; DeMatteo et al., 2005; Waterman et al., 1992).
A number of studies have explored the patterns of pharyngeal phase impairments in CP, using clinical (Arvedson et al.,
1994; Calis et al., 2008; Dahl, Thommessen, Rasmussen, & Selberg, 1996; Del Giudice et al., 1999; Erkin, Culha, Ozel, &
Kirbiyik, 2010; Fung et al., 2002; Gerek & Ciyiltepe, 2005; Reilly & Skuse, 1992; Reilly et al., 1996; Rogers et al., 1994; Santoro
et al., 2012; Sullivan et al., 2000; Wilson & Hustad, 2009; Yilmaz, Basar, & Gisel, 2004) and instrumental assessments
(Arvedson et al., 1994; Field, Garland, & Williams, 2003; Gisel, Applegate-Ferrante, Bensen, & Bosma, 1995; Griggs, Jones, &
Lee, 1989; Helfrich-Miller, Rector, & Straka, 1986; Morton et al., 2002; Rogers et al., 1994; Waterman et al., 1992; Weir et al.,
2007, 2011; Wright, Wright, & Carson, 1996), but estimates of specic clinical signs of pharyngeal phase impairment have
varied signicantly. Many of the studies identied clinical signs through parent-report and only recruited children with
moderate-severe CP or those with OPD. Further, children were either school-aged or recruitment spanned a broad age range
(from infancy to adolescence). Coughing and/or choking (17100%) (Del Giudice et al., 1999; Gerek & Ciyiltepe, 2005),
gagging (1469%) (Rogers et al., 1994) (Wilson & Hustad, 2009), and regurgitation (2.545%) (Erkin et al., 2010) (Reilly et al.,
1996) were most frequently reported. There is generally consensus from instrumental assessment that thin uids are the
most likely food/uid consistency to be aspirated in children with CP (Arvedson et al., 1994; Gisel et al., 1995; Morton et al.,
2002; Rogers et al., 1994; Weir et al., 2007, 2011).

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The aforementioned studies provide a greater understanding of pharyngeal phase impairments in older children with
moderate-severe CP, but there are no studies to our knowledge exploring this in a population-based sample of preschool-aged
children with CP. The current study aimed to determine the discriminative validity, reproducibility and prevalence of clinical
signs suggestive of pharyngeal dysphagia according to gross motor function in children with CP. In order to improve earlier
screening of potential pharyngeal dysphagia in children with CP aged 1836, we need to consider which signs are associated
with typical development at this age, and therefore may not be robust indicators of impairment. Furthermore, signs which can
not be reliably observed between clinicians or on multiple ratings by the same clinician may not be suitable to use in screening.
It was hypothesised that clinical signs would be prevalent in more than half of the children with CP, across all gross motor levels
(GMFCS IV), and the proportion with signs increase with poorer gross motor function (GMFCS IV and V).
2. Materials and methods
This is a cross-sectional population-based study of preschool-aged children with CP, conducted in Queensland, Australia
between April 2009 and March 2013. It is part of two concurrent longitudinal studies, the Queensland CP Child: Motor
Function and Brain Development study (National Health and Medical Research Council, NHMRC 465128) (Boyd et al., 2013)
and the Queensland CP Child: Growth, Nutrition and Physical Activity study (GNPA, NHMRC 569605) (Bell et al., 2010; Benfer
et al., 2012). Ethics approvals have been reported in study protocol papers (Bell et al., 2010; Benfer et al., 2012; Boyd et al.,
2013). All families gave written informed consent to participate.
2.1. Participants
Three samples were recruited for this study, as shown conceptually in Fig. 1. All children with a conrmed diagnosis of CP,
aged 1836 months corrected age, and born in Queensland between 2006 and 2009 were invited to participate in the GNPA
sample (Bell et al., 2010). Children with neurodegenerative conditions were excluded.
Forty children with typical development (TD) were recruited through convenience sampling. Children were term births
(>37 weeks), did not have a diagnosis requiring neonatal admission or ongoing medical/allied health treatment, and were
not on regular medication. Recruitment was stratied by age (1824 and 3036 months).
Forty children (eight/GMFCS level) were selected randomly by an independent researcher for analysis of intra-rater and
inter-rater reproducibility of clinical signs. Thirty of these children were from the GNPA sample, with an additional ten
children recruited (included for pragmatic reasons, forming part of another study). These children also had a conrmed
diagnosis of CP, aged 1836 months corrected age, and those who were non-oral due to tube feeding were excluded.
2.2. Procedures
Children attended the hospital or were seen at home for direct mealtime assessment, according to the snack protocol
(Benfer et al., 2012). Four signs (gurgly voice, wet breathing, fremitus, cough) were rated live pre- and post-mealtime by a

Fig. 1. Participant numbers for oropharyngeal dysphagia study: Growth Nutrition and Physical Activity, Reproducibility and Typically Developing Samples.
Key: CPFQ Queensland Cerebral Palsy Child Feeding Questionnaire; GNPA, Growth, Nutrition and Physical Activity; OPD, oropharyngeal dysphagia; TD,
typically developing.

K.A. Benfer et al. / Research in Developmental Disabilities 38 (2015) 192201

195

researcher, and mealtimes were videoed for rating by a speech pathologist. Three standardised presentations of four textures
(puree, semi-solid, chewable and uid) were presented by the caregiver using the childs regular utensils before allowing
completion of the snack. Children with CP also had gross motor assessment conducted by two physiotherapists.
2.3. Measures
2.3.1. Clinical signs suggestive of pharyngeal phase impairment
A determination of pharyngeal phase OPD was noted if children demonstrated any one of 16 signs, selected from the
literature (DeMatteo et al., 2005; Lefton-Greif & McGrath-Morrow, 2007) and research conducted by our co-author (Weir
et al., 2009). These signs included gagging, coughing, choking, vomiting, throat clearing, multiple swallows, wheezing,
stridor, rapid or laboured breathing, wet breathing, gurgly voice, rattly chest, snufy nose, eye tearing, or circumoral
cyanosis/duskiness, noted for each food/uid texture. Wet voice (sensitivity 0.67, specicity 0.92), wet breathing (sensitivity
0.33, specicity 0.83) and cough (sensitivity 0.67, specicity 0.53) were considered good clinical markers of oropharyngeal
aspiration (compared to VFSS) on thin uids, but not for pureed textures (Weir et al., 2009).
2.3.2. Parent-reported clinical signs suggestive of pharyngeal phase impairment
The same clinical signs were documented by parents on the Queensland Cerebral Palsy Child Feeding Questionnaire
(CPFQ) according to written descriptions of terms (Appendix A, adapted from the Childrens Feeding Skills Questionnaire,
Royal Childrens Hospital, Brisbane). Presence or absence of specic signs was prospectively recorded for each texture across
a number of mealtimes.
2.3.3. Gross motor function
Childrens gross motor function was classied according to the ve levels of the GMFCS (Palisano et al., 1997) on the <2
year and 24 year age bands. Motor type (spastic, dyskinetic and hypotonic) and distribution (unilateral, bilateral, and
number of limbs) were also classied according to the Surveillance of CP in Europe (Cans, 2000; Sanger, Delgado, GaeblerSpira, Hallett, & Mink, 2003).
3. Calculations
All data analyses were performed using Stata 10.0 (Statcorp 2007), with signicance set at p < 0.05. Demographic data
were presented with descriptive statistics. Discriminative validity was determined through logistic regression for each sign
compared to the TD sample. In order to account for clinical signs associated with typical development, signs observed in
more than 25% of children with TD were excluded from the modied prevalence estimate. Inter- and intra-rater
reproducibility were assessed using Cohens Kappa and percentage agreement (overall and by specic sign). The prevalence
of clinical signs suggestive of pharyngeal phase impairment (overall and of specic signs; based on direct-assessment and
parent-report) were presented according to GMFCS. The agreement between direct-assessment and parent-report for each
sign was reported with percentage agreement.
4. Results
There were 178 eligible children referred, of which 132 families consented to participate in the GNPA study, with 130 children
completing the mealtime assessment (Fig. 1). Seven children defaulted to impaired for overall elds in the direct-assessment
(pharyngeal phase overall, and each texture overall) as they were unsafe to have all foods orally (indicated prior to research
participation, by their primary medical team). There were 21 males (52.5%) in the sample of children with typical development,
with a mean age of 27.4 months (SD = 6.0). The sample characteristics of the GNPA sample are shown in Table 1. The GNPA
sample has been shown previously to be representative of the population of children with CP (Benfer et al., 2013).
4.1. Validation of clinical signs suggestive of pharyngeal phase impairment
The prevalence of clinical signs in children with TD was 37.5%, with 14/15 children with signs observed during ingestion
of thin uids. Ten of the children with clinical signs were aged 1824 months and ve were 3036 months. Two different
signs were observed in the children with TD; coughing (n = 15, 37.5%) and wet breathing (n = 3, 7.5%). Three children with TD
had signs across multiple textures, (one on thin uid and pureed food; and two on thin uid, pureed and chewable foods) and
a further two children had multiple coughs on a single texture. There were signicantly more signs observed in children from
GMFCS IV and V compared to the TD sample (b = 0.9, p = 0.03, b = 3.6, p < 0.01, respectively).
4.2. Reproducibility of clinical signs suggestive of pharyngeal phase impairment
Results of the reproducibility study are presented in Table 2. The inter- and intra-rater reproducibility of clinical signs
were strong overall with >90% agreement between raters, and >95% for a single rater. Agreement was marginally better for
intra-rater compared to inter-rater for each of the signs. The signs with the strongest agreement between raters were gag,

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K.A. Benfer et al. / Research in Developmental Disabilities 38 (2015) 192201

Table 1
Characteristics of participants of the Growth, Nutrition and Physical Activity
Study.
GNPA participants (n = 130)
Gender, males (n, %)
Age (mean, SD)
GMFCS level (n, %)
I
II
III
IV
V
Primary motor type (n, %)
Unilateral spasticity
Bilateral spasticity
Dystonia
Ataxia
Hypotonia
Athetoid
Motor distribution (n, %)
One limb
Two limbs
Three limbs
Four limbs
Tube fed (n, %)
Partial
Complete
VFSS (any)
Within study period (1836 months)

81 (62.3)
27.2 (5.4)
57
15
23
12
23

(44.2)
(11.6)
(17.8)
(9.3)
(17.7)

41 (31.5)
72 (55.4)
2 (1.5)
2 (1.5)
9 (6.9)
4 (3.1)
2 (1.6)
67 (51.5)
13 (10.0)
48 (36.9)
11 (8.4)
5 (3.9)
19 (14.6)
9 (6.9)

Key: GMFCS, gross motor function classication system; SD, standard

deviation; TD, typical development; VFSS, videouoroscopic swallow study.

cough, choke, laboured breathing and colour change. The signs with the lowest agreement between raters (less than 85%)
were gurgly voice, snufy nose and multiple swallows.
4.3. Prevalence of clinical signs suggestive of pharyngeal phase impairments, and relationship to gross motor function
Overall, 67.7% of children with CP had clinical signs, rated by the clinician (live and/or from video) in a single mealtime.
There was a stepwise increase in the proportion of children with clinical signs for each increase in level of gross motor
function, as shown in Table 3. This was only signicant for those in GMFCS IV and V (overall) when compared to the TD
sample. This association with gross motor function was also noted for each individual clinical sign, except for cough, choke,
throat clear, respiratory rate and snufy nose. The most common signs on direct-assessment were coughing (44.7%),

Table 2
Reproducibility (inter-rater and intra-rater) of clinical signs suggestive of pharyngeal phase impairment in preschool children with cerebral palsy.
Inter-rater (n = 40)

Overall
Gag
Cough
Choke
Vomit
Throat clear
Multiple swallow
Wheeze
Stridor
Respiratory rate
Laboured breathing
Wet breath
Gurgly voice
Snufy nose
Eye tearing
Colour change

Intra-rater (n = 40)

Reliability (k)

Agreement (%)

Reliability (k)

Agreement (%)

0.7*
0.6*
0.9*
0.4*
NC
0.5*
0.3*
NC
NC
NC
0.7*
0.6*
0.3*
0.0
0.4*
0.4*

90.0
90.0
92.5
92.5
NC
95.0
80.0
NC
NC
NC
97.5
85.0
77.5
82.5
87.5
90.0

0.9*
0.9*
1.0*
0.7*
NC
0.3
0.5*
NC
NC
0.0
0.0
0.7*
0.5*
1.0*
0.0
0.8*

95.0
97.5
100.0
97.5
NC
92.5
85.0
NC
NC
97.5
95.0
90.0
82.5
100.0
90.0
97.5

* p value < 0.001. k < 0 poor, 0.010.20 slight, 0.210.40 fair, 0.410.60 moderate, 0.610.80 substantial, and 0.811.0 almost perfect; NC due to too few
rating categories.

K.A. Benfer et al. / Research in Developmental Disabilities 38 (2015) 192201

197

Table 3
Clinical signs suggestive of pharyngeal phase impairment in preschool children with cerebral palsy, by GMFCS and food/uid texture.

Overall
Coughb
Multiple swallow
Gurgly voice
Wet breath
Gag
Rattly chest
Respiratory effort
Choke
Throat clear
Respiratory rate
Snufy nose
Eye tearing
Colour change

TD: n (%)
N = 40

I: n (%)
N = 57

II: n (%)
N = 15

III: n (%)
N = 23

IV: n (%)
N = 12

15
15
0
0
3
0
0
0
0
0
0
0
0
0

32
26
1
5
8
3
2
0
0
2
1
0
1
0

9 (60.0)
4(26.7)
1 (6.7)*
1 (6.7)*
2 (13.3)
1 (6.7)*
1 (7.1)*
0 (0.0)
0 (0.0)
0 (0.0)
0 (0.0)
0 (0.0)
0 (0.0)
0 (0.0)

15
10
7
4
3
1
1
0
0
2
0
0
0
1

9
6
6
5
2
1
1
0
1
1
0
1
0
1

(37.5)
(37.5)
(0.0)
(0.0)
(7.5)
(0.0)
(0.0)
(0.0)
(0.0)
(0.0)
(0.0)
(0.0)
(0.0)
(0.0)

(56.1)
(45.6)
(1.8)*
(8.8)*
(14.0)
(5.3)*
(4.1)*
(0.0)
(0.0)
(3.5)*
(1.8)*
(0.0)
(1.8)*
(0.0)

(65.2)
(43.5)
(30.4)*
(17.4)*
(13.0)
(4.3)*
(5.0)*
(0.0)
(0.0)
(8.7)*
(0.0)
(0.0)
(0.0)
(4.3)*

V: n (%)
N = 23

(75.0)*
(50.0)
(50.0)*
(41.7)*
(16.7)
(8.3)*
(11.1)*
(0.0)
(8.3)
(8.3)
(0.0)
(8.3)
(0.0)
(8.3)*

23
9
16
10
8
8
4
5
1
0
2
2
2
5

OR (CI); p

(100.0)*
(56.3)
(100.0)*
(62.5)*
(50.0)*
(50.0)*
(36.4)*
(31.3)*
(6.3)*
(0.0)
(12.5)*
(12.5)*
(12.5)*
(31.3)*

1.7
1.1
9.9
2.5
1.5
2.3
2.1
38.7
3.5
1.2
2.1
5.0
2.3
5.1

(1.3,
(0.9,
(3.9,
(1.8,
(1.1,
(1.5,
(1.3,
(3.6,
(0.7,
(0.7,
(0.9,
(1.0,
(1.0,
(1.8,

2.1); <0.01
1.3); 0.32
25.3); <0.01a
3.6); <0.01b
1.9); <0.01
3.4); <0.01
3.4); <0.01
inf); <0.01c
16.2); 0.12
2.1); 0.41
4.5); 0.07
25.9); 0.06
5.2); 0.05
14.3); <0.01

Vomit, stridor and wheeze not reported as not observed in the live ratings; seven children defaulted to impaired overall as nil by mouth; thin uids n = 119
(12 defaulted to impaired, but no uid rated), thick uids n = 11 (7 defaulted to impaired), puree n = 114 (10 defaulted to impaired), semi-solid n = 86
(7 defaulted to impaired), chewable n = 126 (18 defaulted to impaired); inf, innity; NA, not applicable, as no children on thickened uids from GMFCS level;
NC, not calculable; TD, typical development.
a
Gender signicantly related.
b
Age signicantly related.
c
Calculated using episheet for GMFCS V compared to TD only.
* Indicates signicantly greater proportion in GMFCS level compared to children with TD (p < 0.05).

multiple swallows (25.2%), gurgly voice (20.3%), wet breathing (18.7%) and gagging (11.4%) (Fig. 2). Many of the signs were
more commonly observed on uids, although multiple swallows and gag were more common on solid foods (Supplementary
1). Using the modied OPD cut-point (based on the validation with the TD sample), a more conservative prevalence estimate
of 50.8% was found (TD = 12.5%, GMFCS I = 35.1%, II = 13.3%, III = 56.5%, IV = 66.7%, V = 100.0%).
Supplementary 1 related to this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ridd.2014.12.
021.
Parents reported clinical signs suggestive of pharyngeal phase impairment during mealtimes in 46.2% of their children.
The proportion of children with signs increased with poorer gross motor function (GMFCS I: 36.8%, II: 40.0%, III: 43.5%, IV:
58.3%, V: 69.6%). The association was signicant for the overall model (OR = 1.4, p = 0.08), however only signicant for level V
compared to level I (OR = 3.9, p = 0.01). The most common signs based on parent-report were coughing (30.5%), gagging

50

Proporon of children with CP (%)

45

Clinician
rang
Parent report

61.0

40
68.3

35

72.4

30
25
20

78.1

76.4

15
10
5

86.4

91.9 85.4

85.9

83.6

86.7

83.6

93.8

88.3

89.1

Clinical Sign Suggesve of Pharyngeal Phase Impairment

Fig. 2. Percentage agreement for clinical signs suggestive of pharyngeal phase impairment, based on direct ratings and parent report.
Percentage agreement between clinician rating and parent report indicated above bars; aClinician rating completed live and conrmed from video; bWet
breathing was not included in the CP Child Feeding Questionnaire (parent-report); cClinician rating completed live only (detected through touch).

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(31.3%), choking (18.8%), and multiple swallows (25.2%) (Fig. 2). The parent-report agreed with direct-assessment in 60% of
cases (kappa = 0.2, p < 0.01, Fig. 2). The mean of differences between the average number of signs per texture was 0.3
(SD = 2.2) suggesting no bias in parents over/under-reporting.
5. Discussion
This study is the rst to our knowledge to report a representative population-based estimate of the prevalence of clinical
signs suggestive of pharyngeal dysphagia in young children with CP. In particular, the discriminative validation of these signs
in a sample of children with typical development, and testing of their reproducibility, gives greater condence in the
interpretation of the ndings.
Clinical signs suggestive of pharyngeal dysphagia were observed in over a third of children aged 1836 months with
typical development. Only two signs were observed as part of typical development; coughing and wet breathing. In most
cases, only a single cough on thin uids was noted, and as such, this met our a priori criteria for excluding this sign in our
denition of possible pharyngeal dysphagia. This study was focusing on the clinical observation of signs suggestive of
pharyngeal phase impairment, thus we are unable to differentiate the causation of the observed sign (developmental,
structural, physiological or neurological), and whether this varied between the TD and CP samples. In order to retain the
naturalistic component of the mealtime, the volume and means of intake were not standardised between children. Thus,
the increased coughing observed, particularly in the TD sample and in those with ambulatory CP, may also be associated
with the introduction of more challenging uid utensils (with less controlled ow rates and volumes, such as open cups
and straws) and childrens initiation of consecutive uid swallows. DeMatteo and colleagues explored the diagnostic
accuracy of clinical signs, proposing that predictive clusters of signs, such as a cough combined with voice changes and
gag, was most predictive of uid aspiration (DeMatteo et al., 2005). Thus a single cough, particularly on thin uids, may
not have sufcient discriminative validity to suggest pharyngeal dysphagia, particularly if only a single mealtime is
observed.
Overall, the reproducibility of the clinical signs was strong, both with repeated ratings by one clinician, and between
clinicians. As expected, signs which were more overt, such as coughing, choking and gagging, had the strongest
reproducibility. Signs which were detected through more subtle perceptual changes, such as wet breathing, gurgly voice, eye
tearing, snufy nose, had lower reproducibility, particularly between clinicians. The presence of a cough, being among the
most overtly observable signs, was the most reliably identied clinical sign by clinicians (almost perfect).
Clinical signs suggestive of pharyngeal phase impairment were common in 68% of preschool-aged children with CP. These
ndings were similar to those of Del Giudice, who studied clinical signs based on parent-report in children with CP (mean
5.2 years) (Del Giudice et al., 1999), although our estimate based on parent-report was lower. We found that there was a
stepwise increase in proportion of children with clinical signs with each increase in GMFCS level, consistent with the broader
literature on OPD (Benfer et al., 2013; Calis et al., 2008; Fung et al., 2002; Parkes et al., 2010; Reilly et al., 1996; Sullivan et al.,
2000; Waterman et al., 1992). A surprising nding was the notable proportion of children from GMFCS I and II with clinical
signs, even after applying the modied cut-points from the validation study (35.1 and 13.3%, respectively). Little has been
reported on children with ambulatory CP in the literature with regards to clinical signs, so further investigation of this subgroup is warranted. Children with non-ambulatory CP almost consistently demonstrated clinical signs (in 91% of GMFCS IV
and V). Previous studies have generally used indirect report of clinical signs or have not described their ndings according to
GMFCS, which reduces our ability to compare with our data. Only one study, by Calis and colleagues, used direct-assessment
of clinical signs on the Dysphagia Disorders Survey, nding an equivalent proportion of children from GMFCS IV and V (91%)
showed signs (Calis et al., 2008).
Coughing, multiple swallows, gurgly voice, wet breathing and gagging were the most commonly observed signs
(>10% of children), with few children showing evidence of the other signs in a single mealtime. There were similar
proportions of children demonstrating coughing during mealtimes in the current study compared to two other studies
of preschool children with CP, although the gross motor severity of these samples was not well dened (Clancy &
Hustad, 2011; Wilson & Hustad, 2009). In a third study of preschool children, by Reilly et al., the estimate was higher
(70%), but included coughing and choking combined (Reilly et al., 1996). As Clancy and Hustad described, children with
CP, even those assessed to have normal oromotor skills, may continue to demonstrate coughing during mealtimes until
six years of age, suggesting a later maturation compared to children with TD (Clancy & Hustad, 2011). Fewer children
from GMFCS V coughed on thin uids compared to other GMFCS levels, which may reect the ndings in previous
studies showing high rates of silent aspiration in children with more signicant neurological lesions (Arvedson et al.,
1994). This difference may also be attributable to children from GMFCS IV and V having more controlled uid intake
(due to modied utensils such as infant bottles and trainer cups, smaller volumes or single sips, or bolus pacing by the
feeder).
This study showed that when parents were asked to observe specic clinical signs which were described in written
form, their report agreed with direct-assessment in about 60% of the cases. This was not biased to consistently over- or
under-report the number of signs compared to direct-assessment. The discrepancy in agreement may arise from
differences in the number of mealtimes observed, the quantity and type of textures included (being a restricted range of
textures in the standardised assessment), and the mealtime context. Interestingly, agreement was lower for the signs
for which we would expect better accuracy by parents, such as coughing and gagging, being more overtly observable and

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199

everyday familiar terms. Conversely, parents reported a surprisingly high prevalence of signs such as wheezing, stridor,
respiratory rate and effort, vomiting and snufy nose, which were almost non-existent in the direct-assessments. This
may be related again to the duration and method of direct-assessment (video rating in a single mealtime), but may also
reect lack of clarity for parents surrounding some terms (Mellis, 2009). A cough was more commonly noted by
clinicians than parents. Of those children observed to cough clinically but whose parents indicated their child does not
cough, 81% had mild OPD. We hypothesise thus that the parent-report may be giving a more accurate reection of
children who cough regularly at mealtimes (which may be a better indicator of pharyngeal dysphagia), whereas the
observation in a single mealtime may detect cases of isolated coughing. Parents were able to report on signs over a
number of mealtimes, which meant their estimates may be more accurate in instances, as long as the term is clearly
understood.
5.1. Limitations
This study has provided valuable data to ll a signicant research gap, but had some key limitations. The study would
have been strengthened by including an instrumental assessment for all children displaying any clinical signs (beyond a
single cough on thin uids). We reviewed data from videouoroscopies performed as part of the childrens standard clinical
management, however only nine children had VFSS during the study period, which was insufcient for analysis. Without
instrumental data, we are only able to comment on the presence of signs rather than infer impairment.
The location of neurological lesion inuences the motor type which characterises an individuals CP. This may also
inuence the patterns of clinical signs observed during mealtimes. While this is an important interaction to be aware of in
the eld of OPD, the small numbers of the non-spastic motor types which are present in a representative population-based
sample (i.e. dyskinetic, ataxic and hypotonic) were insufcient for statistical analysis of this relationship.
This study was conducted longitudinally over a 4 year period, and as such live clinical assessment by a speech pathologist
was not feasible. Many of the clinical signs may be more accurately detected live, and better determined across a number of
mealtimes, which may result in under-reporting in the direct-assessment.

6. Conclusions
This study has contributed to our understanding of which signs are most valid and reliable when applied to
preschool children with CP. All 16 clinical signs used in this study had strong reproducibility by clinicians, suggesting
they may be useful in the clinical setting, although further testing may be required to strengthen use in research.
Exploring the test-retest reproducibility of these signs would assist in determining which are consistent between
mealtimes and which are subject to greater variation. Cough was consistently identied by clinicians, but may not
adequately reect the childs performance across a number of mealtimes. The single cough on thin uids was also
common in children with TD, suggesting an isolated cough on thin uids is not sufciently discriminative in children
aged 1836 months. Considering coughing over a number of mealtimes, on multiple textures, or clustered with other
signs may be a more appropriate marker in this age range. This study found clinical signs suggestive of pharyngeal
phase impairments to be common in approximately 68% of children with CP, and this was present across all levels of
gross motor function, including those with ambulatory CP. It is important for clinicians working in this eld to be
actively monitoring these signs, particularly as the available standardised OPD assessments focus on the oral phase
and are not designed to assess the pharyngeal phase in adequate detail. The use of parent-report in both clinical
screening and research studies remains a feasible method. Training parents to detect medical terms, such as stridor,
wheeze, and rattly chest, and development of online training resources such as video-clips, may make this modality of
screening more viable (Mellis, 2009). While studies analyzing the diagnostic accuracy of these signs related to
aspiration on instrumental evaluation are available for the paediatric population, more studies of this kind are needed,
particularly specic to CP.

Competing interests
The authors declare they have no competing interests.
Acknowledgements
We would like to thank Physiotherapists Rachel Jordan (BPT) and Chris Finn (BPT) for data collection and gross motor
ratings; and Dietitians Joanne McMah (M Nutr & Diet), Stina Oftedal (B.Hlth.Sc (Hons) Nutr & Diet) and Camilla Davenport
(B.Hlth.Sc (Hons) Nutr & Diet) for data collection of feeding videos. This project was supported by the National Health and
Medical Research Council Postgraduate Medical and Dental Scholarship (1018264KB), Career Development Fellowship
(APP1037220RB) and Project Grants (569605 and 465128). Funding was also received from the Speech Pathology Australia
Post Graduate Student Research Grant to conduct reliability ratings.

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Appendix A. Clinical signs with descriptions provided to parents on the Queensland Cerebral Palsy Child Feeding
Questionnaire
10. Summary of my childs signs and symptoms during eating or drinking. These are a list of signs and symptoms of swallowing
difculty that your child may demonstrate during eating or drinking.
Place a tick (U) in the box if you see your child doing this behaviour during eating or drinking for each consistency.
Signs or Symptoms

Does this
happen
at all?

My child. . .. . ..

I dont know

If you ticked Yes, indicate (U) the types of drinks or food

textures on which your child demonstrates these signs or
symptoms.
No

Yes

Thin
drink

Thick
drink

Smooth
puree

Lumpy
semi-solid

Finger
foods

Gags when eating or drinking.

Coughs when eating or drinking.
Child chokes when eating or drinking.
Vomits when eating or drinking.
Clears his/her throat often during or after meals.
Needs to swallow a number of times to clear
each mouthful of food or drink.
Wheezes during/after eating or drinking.
(Wheezing is a whistling sound from
the chest during breathing).
Has stridor when breathing in or out during
eating or drinking. (Stridor is a harsh,
high-pitched, vibratory noise in the
throat particularly when breathing in.)
Becomes breathless and breathes quickly
during eating or drinking.
Breathing becomes laboured or effortful
during eating or drinking.
Has a rattly chest after eating or drinking.
Gets a snufy nose after eating or drinking.
Has a gurgly voice after eating or drinking.
Has runny eyes or eye tearing after
swallows of certain food or drinks.
Seems to go blue around the lips/face or
turn dusky or pale after drinking or eating.
Regularly gets high temperatures.
Generally refuses to eat or drink some food or
uid textures.

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