Oropharyngealdysphagia inpreschool childrenwithcerebral palsy:Oralphaseimpairments § Ka therine A. Be nf er a, *,Kelly A. Weir b,c , Kristie L. Bell a,d , Robert S. Ware c,e , Pe ter S.W. Davies d , Roslyn N. Boyd a a QueenslandCerebralPalsyandRehabilitationResearchCentre,TheUniversityofQueensland,Level7,Block6,Herston4029, Queensland,Australia b SpeechPathologyDepartment,RoyalChildren’sHospital,Herston4029, Queensland,Australia c QueenslandChildren’sMedicalResearchInstitute,TheUniversityofQueensland,Herston4029, Queensland,Australia d Children’sNutritionResearchCentre,QCMRI,TheUniversityofQueensland,Herston4029, Queensland,Australia e SchoolofPopulationHealth,TheUniversityofQueensland,Herston4029,Queensland,Australia ResearchinDevelopmentalDisabilities35(2014)3469–3481 ARTICLEINFO Article history: Received24July2014 Accepted20August2014 Ava ila ble onl ine 14 Sep tember 2014 Keywords: Orpharyngealdysphagia Deglutitiondisorders Oralphaseimpairment Cerebralpalsy Children ABSTRACT Purpose:This studyaimed to documentthe prevalence and patternsof oral phase or opharyng eal dyspha gi a (OPD) in pr eschool children wi th cerebral pa ls y (C P) , an d its ass oci ati on wit h mealti me dur ati on, freq uen cy and efficiency . Methods: Cross-sectional pop ulation-based cohort study of 130 chi ldre n diagnosed wit h CP at 18–36 month s ca (mean= 27.4 months, 81 males) an d 40 children with typical de ve lo pme nt (me an = 2 6. 2, 1 8 m a les ). F un ct i on al ab il it ie s of ch il dr en wi th CP wer e repr esen tati ve of a po pul at ion s ampl e (GMF CS I = 57, II= 15, III = 2 3, IV= 12, V = 23). Or al phase impairment was rat ed fr om vi deousi ng the Dys pah gia Dis orders Sur vey, Schedu le for Ora l Mot or Impair men t, and Pre-Spe ech Assessment Scale. Par ent -rep ort wascollec ted on a feedin g questi onn air e. Mealti me fre quen cy, dur ati on and efficiency wer e cal cul ated fr om a three day weighed fo od record comp leted by parents. Gross mo to r fu nc ti on was class ified using the Gross Motor Func tio n Classi ficat ion Syst em (GMFCS). Results: Ove ral l, 93. 8%of chil dren had di rectl y asses sed oral phase impairment s duri ng eating or drinking, or in controlling sa liva (78. 5% with modi fied cu t- points ). Direct ly assessed oral phas e impair ments wer e associated with decl ining gross motor functi on, wit h chi ldr en fro m GMF CS I hav ing a 2-f old increased lik eli hoo d of oral phase impairmen t co mp ared to the children wi th TD (OR = 2. 0, p = 0. 18), and al l ch ildren from GMFCS II –V havi ng oral phase impairments. Di f ficult y bi ti ng (70%), cl ean ing behavi ours (70%)and che wing (65%) were the mos t common imp airments on solids , and dif ficultysippin g from a cup (60%) for fluids. OPD severi ty and GMFC S were not rel ate d to mealtime frequenc y, durat ion or ef fic iency, al though chil dren on parti al tube feeds had si gni ficantl y reduced mealtime effici ency. Conclusions: Or al phase impairments were common in preschool chil dren wi th CP, wi th severity in cr easing stepwise with declinin g gr os s mo tor func ti on. Th e prevalence an d severity of oral phase impairments wer esignifican tl y gr ea ter for most tas kswhen compar ed to chi ldr en wit h typical dev elopment,even forthose wit h mil d CP.Child renwho wer e partial ly tube fed had si gni ficantl y lower feedi ng ef ficien cy, so this coul d be a us ef ul § ANZTRTrialRegistrationNumber:ACTRN12611000616976. *Correspondingauthorat:QueenslandCerebralPalsyandRehabilitationResearchCentre,TheUniversityofQueensland,Level7,Block6,RoyalBrisbane andWomen’sHospital,Herston,Queensland4029,Australia.Tel.:+610736465372;fax:+610733655192. E-mailaddresses:[email protected], [email protected](K.A.Benfer). ContentslistsavailableatScienceDirect Research in Developmental Disabilities http://dx.doi.org/10.1016/j.ridd.2014.08.029 0891-4222/2014ElsevierLtd.Allrightsreserved.
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Oropharyngeal dysphagia in preschool children with cerebral
palsy:
Oral
phase
impairments§
Katherine A. Benf er a,*,
Kelly A. Weir b,c, Kristie L. Bell a,d, Robert S. Ware c,e,Peter S.W. Daviesd, Roslyn N. Boyd a
aQueensland Cerebral Palsy and Rehabilitation Research Centre, The University of Queensland, Level 7, Block 6, Herston 4029,
Queensland, Australiab Speech Pathology Department, Royal Children’s Hospital, Herston 4029, Queensland, AustraliacQueensland Children’s Medical Research Institute, The University of Queensland, Herston 4029, Queensland, AustraliadChildren’s Nutrition Research Centre, QCMRI, The University of Queensland, Herston 4029, Queensland, Australiae School of Population Health, The University of Queensland, Herston 4029, Queensland, Australia
Research in Developmental Disabilities 35 (2014) 3469–3481
A R T I C L E I N F O
Article history:
Received 24 July 2014
Accepted 20 August 2014
Available online 14 September 2014
Keywords:
Orpharyngeal dysphagia
Deglutition disorders
Oral
phase
impairmentCerebral palsy
Children
A B S T R A C T
Purpose: This study aimed to document the prevalence and patterns of oral phase
oropharyngeal dysphagia (OPD) in preschool children with cerebral palsy (CP), and its
association with mealtime duration, frequency and efficiency.
Methods: Cross-sectional population-based cohort study of 130 children diagnosed with
CP at 18–36 months ca (mean = 27.4 months, 81 males) and 40 children with typical
development (mean = 26.2, 18 males). Functional abilities of children with CP were
representative of a population sample (GMFCS I = 57, II= 15, III = 23, IV= 12, V = 23). Oral
phase impairment was rated from video
using the Dyspahgia Disorders Survey, ScheduleforOral Motor Impairment, andPre-SpeechAssessment Scale. Parent-reportwascollected
on a feeding questionnaire. Mealtime frequency, duration and efficiencywere calculated
from a three day weighed food record completed by parents. Gross motor function was
classified using the Gross Motor Function Classification System (GMFCS).
Results: Overall, 93.8% of children had directly assessed oral phase impairments during
eating or drinking, or in controlling saliva (78.5% with modified cut-points). Directly
assessed oral phase impairments were associated with declining gross motor function,
with children from GMFCS I havinga 2-fold increased likelihood of oral phase impairment
compared to the children with TD (OR = 2.0, p = 0.18), and all children from GMFCS II–V
having oral phase impairments. Difficulty biting (70%), cleaning behaviours (70%) and
chewing (65%)were themost common impairments on solids, anddifficulty sipping from
a cup (60%)
for fluids. OPD severity and GMFCS were not related to mealtime frequency,
duration or efficiency, although children on partial tube feeds had significantly reduced
mealtime efficiency.
Conclusions: Oral phase impairments were common in preschool children with CP, with
severity increasing stepwise with declining gross motor function. The prevalence and
severity of oral phase impairments were significantly greater for most tasks when
* Corresponding author at: Queensland Cerebral Palsy and Rehabilitation Research Centre, The University of Queensland, Level 7, Block 6, Royal Brisbane
13.1 (7.2–19.0) 28.6 (20.3–36.8) NA NA DDS: 76.5%, kappa = 0.30, p < 0.01
Difficulty biting/chewingd
% (CI)
26.9 (19.2–34.7) 62.1 (53.1–71.0) 47.7
(38.2–57.2)
63.1 (54.4–71.8) DDS: 54.3%, kappa = 0.19, p < 0.01
SOMA: 59.6%, kappa = 0.17, p = 0.02
PSAS: 50.8%, kappa = 0.12, p = 0.04
a Agreement
to
1
point
either
side
of
perfect
agreement
for
continuous
variable.b Proportion based on DDS impairment to fluid subtest, SOMA impairment to trainer cup or cup oral motor challenge category, PSAS impairment to
‘sucking from cup’.c Proportion based on DDS item 11 oral transit for non-chewable.d Proportion bsed on DDS impairment to chewable reception, SOMA impairment to ‘bite’ items, PSAS impairment to biting/chewing subteste Eating problem: sum of non-chewable and chewable subtests (out of 15), n = 125, drinking problem: fluid subtest (out of 7).f Eating problem: puree + semi-solid + cracker raw score (out of 39), n = 65, drinking problem: fluid raw score converted to 0–10 scale using sum of items
on most commonly used fluid utensil, n = 118.g Mean months delayed on combined food subtests (out of 125), n = 115/fluid subtests (out of 50), n = 107 (excluding swallow items); CI, confidence
interval;
CPFQ,
Queensland
Cerebral
Palsy
Child
Feeding
Questionnaire;
DDS,
Dysphagia
Disorders
Survey;
PSAS,
Pre-Speech
Assessment
Scale;
SOMA,Schedule for Oral Motor Assessment; t-cup, trainer-cup.
Fig. 1. Oropharyngeal dysphagia severity (Dysphagia Disorders Survey part 2) according to gross motor functional level (GMFCS). Key: linear regression
showed significantly higher scores for all GMFCS levels when compared to the children with TD (GMFCS I b = 1.6, p = 0.02; II b = 3.1, p < 0.01; III b = 6.0,
p<
0.01;
IV
b
=
11.3,
p
<
0.01;
V
b
=
18.4,
p
<
0.01).
DDS,
Dysphagia
Disorders
Survey;
GMFCS,
Gross
Motor
Function
Classification
System;
TD,
typicallydeveloping.
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5.
Discussion
Almost all children with CP (over 90%) had directly assessed impairments to the oral phase of feeding, with the only
children not classified as OPD belonging to GMFCS I. This finding was similar to that reported in children with CP aged
2–16
years by Kim
and
colleagues,
although
their sample
was
small
(n =
29) (Kim
et
al., 2013).
Generally,
children didnot have impaired saliva control in isolationof oral phase impairments in eating/drinking, although the reverse was true
in half of the children. About 20% of these ‘impairments’ may be associated with typical development, as was found
when the prevalence was calculated using the modified cut-points based on the typically developing reference group.
This modified prevalence was equivalent to the proportion of children with difficulty eating or drinking reported by
parents (about 80%), although the VAS was not restricted to oral phase impairments alone. There were more children
with oral phase OPD with poorer GMFCS function, whichwas consistent with oral phase findings by Kim and colleagues
(Kim et al., 2013). This was also consistent with our previous work (Benfer et al., 2013), and that by others (Calis et al.,
2008; Erkin, Culha, Ozel, & Kirbiyik, 2010; Fung et al., 2002; Parkes, Hill, Platt, & Donnelly, 2010; Reilly et al., 1996;
Santoro et al., 2012; Sullivan et al., 2000; Waterman, Koltai, Downey, & Cacace, 1992) looking more broadly at OPD.
The OPD severity of children with CP as a group was on average 3 out of 10 for solids and between 1 and 3 out of 10 for
fluids. The DDS, PSAS and parent-reported average severity scores for solids were all equivalent, which suggests that they are
all measuring a similar construct. The SOMA raw scores indicated the mildest OPD for both solids and fluids, which is likely
because
this
measure
is
only
detecting
more
clinically
significant
OPD,
and
missing
milder
cases.
All
children
with
CP
hadsignificantly higher scores on the DDS compared to children with TD, even children from GMFCS I. There was a stepwise
Fig. 2. Agreement between parent-reported and directly assessed oropharyngeal dysphagia severity in preschool children with cerebral palsy. Key: mean of
differences for parent-reported OPD on solids and (i) DDS = 0.0 (SD = 2.9), (ii) SOMA = 2.4 (SD = 4.0), (iii) PSAS = 0.3 (SD = 3.6); mean of differences for parent-
a Unable to separate drooling from food loss in DDS item therefore included only in food containment.b Most children who are unable to bite cracker were not assessed on this texture.c Totals include Thomas-Stonell and Greenberg Saliva Scale, proportion = 41.4%.d Indicates delay to subtest greater than 1 month of age; SOMA items exclude those pertaining to the swallow (pharyngeal phase) including lip closure
during swallow (ss) and gagging (ck).e Item is framed as ability rather than impairment, therefore the proportion with impairment is reported.
* Significantly greater proportion impairment on logistic regression ( p < 0.05) in GMFCS level relative to TD sample.
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Table 4
Prevalence of specific oral phase impairments in young children with cerebral palsy, overall and according to gross motor function: fluids.
DDS, n (%) SOMA, n (%) PSAS, n (%) Total
impaired % (CI)
Sub-group:
TD/GMFCS
Orienting to the
bolus
Orientation
(fluid):
17 (15.2)
bAnticipatory mouth opening
(bottle r2): 5 (23.8)
NA 16.1 (9.2–23.0) TD: 0.0
No liquid enters the mouth (bottle
r4): 1 (4.8)
I: 0.0
bAccepts within 2 s (bottle, cup a2):
7 (9.9)
II: 14.3*
Panic reactions when liquid
presented (t-cup, cup sq2): 4 (4.2)
III: 5.6*
IV: 36.4*
V: 78.6*
Stripping teat (bottle),
n = 21
NA Upper lip seals firmly around teat
(l3): 6 (28.6)
Bottle ‘dysfunction’ score:
8 (38.1)
47.6 (24.3–70.9) TD: 0.0
Intermittent/incomplete upper lip
contact/seal (l5): 5 (23.5)
I: NA
Intermittent/incomplete lower lip
contact/seal
(l6):
6
(28.6)
II: 16.7*
III: NA
IV: 83.3*
V:
100.0*
Sipping from cup,
n = 66
Reception
(fluid)a:
42 (37.5)
NA bSucking pattern: 29 (22.3) 60.3 (51.5–69.2) TD: 17.5
(bt), jaw alignment swallow (sw1), panic reaction after swallow (sw4), no swallow (sw5), choking (sq3), gagging (sw9).b Item is framed as ability rather than impairment, therefore the proportion with impairment is reported.
* Significantly greater proportion impairment on logistic regression ( p < 0.05) in GMFCS level relative to TD sample.
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be inflated by limitations to oral tasks associated with typical development. Ability to do a sustained bite requires the child to
have developed graded jaw movement, as well as adequate muscle strength to be able to break through the food without
overflow movements (Morris, 2003). Impairments to these skills have been noted in the literature (Erkin et al., 2010). Other
literature
has
suggested
that
tasks
performed
on
the
midline
(such
as
biting
and
spoon
feeding)
were
better
than
thoserequiring multiple planes of movement (such as chewing and cup drinking) (Gisel et al., 2000; Yilmaz et al., 2004). Oral
transport of purees and orienting were least frequently impaired, consistent with the clinical picture that these skills are
likely to be associated with more severe OPD.
Difficulty actively sipping from a cup (with a stable jaw) was the most frequently observed impairment with fluids
(in 60% of children), followed by difficulty in oral transport of fluids (in half) and stripping a bottle teat (in half of those
assessed on a bottle). Liquid loss was quite common even in the children with TD (20%), but was less common in GMFCS
IV–V than other impairments, perhaps due to parents positioning their child (reclined or with head back) and/or
limiting bolus delivery (smaller and single sips only, and modified utensils) in this group. Generally there were more
children with CP who had specific oral phase impairments compared to children with TD, with the exception of oral
transport of solids (only significant for GMFCS III–V) and liquid loss (significant for GMFCS IV–V). Looking at the raw
data, it appears that fewer children from GMFCS III have liquid loss; however, it is important to note that the DDS does
not account for children’s use of different fluid utensils. When we look at the utensil use of children, we see that most
children in
level
III are using a
trainer
cup or
bottle, which
limits the flow rate,
thus making the
fluids easier
to manageorally with less liquid loss. The number of children not using a cup was significantly higher for children with CP
compared to the children with TD, which may obscure some of the differences in skills between these groups.
Oral phase impairments are known to reduce the efficiency of bolus processing (Gisel, 1988), which may lead to
prolonged mealtimes (Dahl, Thommessen, Rasmussen, & Selberg, 1996; Sullivan et al., 2000; Waterman et al., 1992;
Wilson & Hustad, 2009), with mealtime duration suggested to be a reliable measure of OPD severity (Sullivan et al.,
2000). Our study findings showed no difference in the number of meals, average daily feeding duration or feeding
efficiency (kJ per minute or grams per minute) based on gross motor level or OPD severity. The exception was the
reduced feeding efficiency (kJ and grams) of childrenwith partial tube feedings, all of whom were from GMFCS IV and V.
There was a lot of variability of the duration/frequency/efficiency variables within GMFCS levels (and OPD scores),
suggesting that parents of a child with significant oral phase impairments may have hadmodifications to the texture or
energy density of their diet, and consequently be performing well for their level. As children’s mealtime efficiency
(different from the ‘feeding efficiency’ of an individual bolus, as reported by Gisel (1988)) also was not significantly
different
with
more
severe OPD,
we
can
propose
that
the modifications
made
to
the textures in
children’s diets(Benfer, 2014 [unpublished work]) on the whole may be adequate to maintain their efficiency of intake. Our previous
Table 5
Feeding frequency, duration and efficiency of preschool children with cerebral palsy, by gross motor function (GMFCS).
Mean DDS
score SD
Mean
feeding
frequency
per day
B
( p value)
Mean
feeding
duration
per day
B
( p value)
Feeding
efficiency
(kJ per
minute)
B
( p value)
Feeding
efficiency
(grams per
minute)
B
( p value)
GMFCS I, (n = 50)
Actual 2.6
3.0 7.1
1.5 Ref. 118.2
50.0 Ref. 38.8
18.2 Ref. 8.4
4.2 Ref.
Estimated NA NA – 143.8 72.1 Ref. 37.3 24.8 Ref. 9.0 5.4 Ref.
Estimated NA NA – 158.4 49.2 14.6 (0.58) 28.7 17.3 8.6 (0.34) 7.7 3.7 1.4 (0.61)
Partial tube, (n = 8)
Actual 16.7
6.3 6.1
2.3 1.0 (0.17) 105.0
NC 13.2 (0.80) 13.8
12.4 25.0 (<0.01) 3.4
4.2 5.0 (0.03)
Estimated NA 137.2
126.1 6.6 (0.84) 15.2
12.7 22.1 (0.02) 4.1
4.7 4.9 (0.08)
Key: n = 110 with completed food records, 4 were 100% tube fed, therefore excluded from this analysis (n = 106); actual time n = 37 (GMFCS I = 15, II = 5,
III = 9, IV = 2, V = 5, tube = 1).a Only completely orally fed children; b values show linear regression for mealtime outcomes and GMFCS; DDS, Dysphagia Disorders Survey; GMFCS,
Gross Motor Function Classification System; kJ, kilojoules; NA, not applicable, as only actual values available; NC, confidence interval not calculable as n = 1;
ref., reference group for analysis.
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work also found a reduced energy intake was associated with children with lower gross motor function (Benfer,
2014 [unpublished work]), so interventions to support overall energy intake in children with poorer gross motor
function may be indicated.
This study represents the first to our knowledge to document the patterns of oral phase impairments using
standardised OPD measures, according to GMFCS, across the full spectrum of gross motor function. While the use of
standardised OPD measures is a step forward in understanding the clinical presentation of children with CP, there were
a number of limitations surrounding these measures. While the measures were focused predominately on the oral
phase, a
couple of
the items in
the
DDS
and
SOMA pertained to the pharyngeal phase, which may influence the overalloral phase prevalence estimates. In addition, due to the lack of a gold standard measure, we reported a combined total
estimate based on a positive OPD classification on one or more of the DDS, SOMA or PSAS which may inflate the
estimate. Some measures had multiple items pertaining to a single oral task, which may inflate the prevalence of that
particular task relative to other oral tasks, so this needs to be considered when interpreting the findings. The use of raw
scores as measures of OPD severity have not been validated for this purpose, as a stepwise change in scores may not
represent a linear change in severity, particularly for the SOMA whose scoring was structured to be a discriminative
measure rather than evaluative. Finally, using the three day weighed food record, an already high-burden data
collection method, to collect mealtime duration, meant that there were moderate levels of missing data across the
records. To account for this, we reported on both actual and estimated mealtime durations, which did not differ
significantly.
There are implications for clinicians and researchers with regards to therapy planning, screening (particularly using
parent report) and nutritional management. The findings from this study will provide useful information to assist in
planning
therapy
interventions,
particularly
specific
oral
sensorimotor
approaches.
Children
with
better
gross
motorfunction tended to have isolated oral phase impairments, whereas those with poorer gross motor function had more
systematic impairments involving multiple oromotor subsystems. This data will also provide a foundation for future
research on feeding therapies, in targeting specific approaches to specific CP sub-groups. Certain ‘impairments’ were
present in a large number of children with TD, which should be considered in clinical management of children with CP,
particularly those with mild impairments. These ‘impairments’ need to be examined more closely to understand if
those observed in typical development can be differentiated from those representing delayed or disordered patterns,
with regards to quality of the movement or frequency.
Parent report has been used extensively in research on OPD to date, although there is a limited understanding of
the accuracy of this as a proxy for a direct objective assessment. This study suggested that parents were in agreement
with direct assessment only about half the time, although they were not systematically under-reporting. More
specifically worded questions and those asking about more overt OPD tended to have better agreement with direct
assessment.
We
found that
children who
were
partially tube fed had significantly lower
feeding
efficiency,
so this
could
be auseful early indicator of children needing supplementation to their nutrition (through increasing energy density of
foods/fluids, or tube feeds). Our findings suggested that the child’s OPD severity or gross motor level was not
significantly influencing the efficiency of their mealtime, although an association may be obscured by parents who are
already modifying textures or energy density of their child’s food to account for their OPD. Previous findings (Benfer,
2014 [unpublished work]) suggest a lower energy intake of children with lower gross motor function, thus parent
education around increasing energy density of easier to manage textures, and an increased frequency of meals for these
children may be important to improve their nutritional outcomes.
6.
Conclusions
Oral phase OPD was common in preschool children with CP, present in 93.8% of children when directly assessed
(78.5% with modified cut-points), and 79.2% based on parent report. The agreement between direct assessment and
parent
reported oral phase
OPD
was
only fair,
although parents
did not consistently under-report. More
specificallyworded questions and those asking about more overt OPD tended to have better agreement with direct assessment,
which should be considered when implementing parent-reported screening. OPD severity and GMFCS were not related
to mealtime frequency, duration or efficiency, although children on partial tube feeds had significantly reduced
mealtime efficiency. These findings highlight the importance of considering feeding efficiency as an early marker for
children needing nutritional supplementation or modifications to their diet.
Competing interests
The authors declare they have no competing interests.
Funding
This
project
was
supported
by
the
National
Health
and
Medical
Research
Council
Postgraduate
Medical
and
DentalScholarship (1018264 – KB), Career Development Fellowship (APP1037220 – RB) and Project Grants (569605 and 465128).
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Acknowledgements
We would like to thank Physiotherapists Rachel Jordan (BPT) and Chris Finn (BPT) for data collection and gross motor
ratings and Dietitians Stina Oftedal (B.Hlth.Sc (Hons) Nutr & Diet) and Camilla Davenport (B.Hlth.Sc (Hons) Nutr & Diet) for
data collection of feeding videos.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/
j.ridd.2014.08.029.
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