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Purpose: The purpose of this study is to examine (a) the mealtime duration and DDS Part 1, rs = .514 [.045–.797],
reliability of newly developed measures of mealtime duration p = .035; Part 2, rs = .528 [.064–.804], p = .029; and total
and (b) their relationship to clinical feeding/swallowing scores, rs = .665 [.271–.868], p = .004, and between total
performance in children with spastic cerebral palsy (SCP). solid/bite duration and DDS Part 1, rs = .579 [.137–.828],
Method: Seventeen self-feeding children (9 boys, 8 girls) with p = .015; Part 2, rs = .620 [.199–.847], p = .007; and total
SCP (age range = 5;1 [years;months] to 17;6, Gross Motor scores, rs = .762 [.444–.909], p < .001. Children with unilateral
Function Classification System range = I–IV) were assessed brain involvement exhibited significantly lower DDS total
during mealtimes using the Dysphagia Disorder Survey (DDS; ( p = .049) and Part 2 scores ( p = .026), indicating better
Sheppard, Hochman, & Baer, 2014). Children were divided into feeding/swallowing performance/skills. They also had
2 groups, children with primarily unilateral or bilateral brain shorter mealtime duration ( p = .019) and solid/bite duration
involvement. Duration measures included mealtime duration ( p = .025) compared with children with bilateral involvement.
and total sip/bite duration for each bolus type (liquid and solid). Conclusions: Our new mealtime duration measures are
Results: Excellent intra- and inter-rater reliability for all reliable and correlate with feeding/swallowing performance
duration measures was observed (intraclass correlation in a sample of self-feeding children with SCP. Therefore,
coefficient [ICC] = 1.00 and 0.955, respectively, for mealtime they may be useful supplements to feeding/swallowing
duration; ICC = 1.00 and 0.963, respectively, for solid/bite assessments for this population.
duration; ICC = 1.00 and 0.957, respectively, for liquid/sip Supplemental Material: https://doi.org/10.23641/
duration). Positive correlations were found between total asha.5715076
C
erebral palsy (CP) is the most common neuro- somatosensation, communication, and musculoskeletal
motor disability of childhood with a prevalence of function (Rosenbaum et al., 2007).
2–3/1,000 births (Kirby et al., 2011). CP has been Feeding and swallowing disorders (dysphagia) are
described as a nonprogressive encephalopathy affecting also reported in 19% to up to 99% of children with CP
movement and postural development and has been asso- (Calis et al., 2008; Fung et al., 2002; Parkes, Hill, Platt,
ciated with several comorbidities involving cognition, & Donnelly, 2010). In pediatrics, feeding and swallowing
are often viewed as a continuum, because they are inti-
mately related (Malas, Trudeau, Chagnon, & McFarland,
a
Department of Biobehavioral Sciences, Teachers College, Columbia 2015), and comprise four coordinated phases: preoral, oral,
University, New York, NY pharyngeal, and esophageal. Dysphagia in CP can affect
b
Department of Speech, Language, & Hearing Sciences, College of all phases of swallowing and may include difficulty in plac-
Health and Human Sciences, Purdue University, West Lafayette, IN ing and containing the food in the mouth, oral motor dis-
Correspondence to Georgia A. Malandraki: malandraki@purdue.edu coordination, reduced oropharyngeal strength, abnormal
Avinash Mishra is now at the Speech-Language Pathology and Audiology, tone, pathological oral reflexes, and poor texture advance-
Hunter College, City University of New York, New York, NY. ment, and may result in coughing, choking, and nutritional
Editor: Krista Wilkinson
Associate Editor: Julie Barkmeier-Kraemer
Received November 14, 2016
Disclosure: Justine J. Sheppard discloses that she developed the Dysphagia Disorder
Revision received May 10, 2017 Survey (one of the instruments used in this study) and is a member of the Nutritional
Accepted August 3, 2017 Management Associates, LLC. The other coauthors have declared that no competing
https://doi.org/10.1044/2017_AJSLP-16-0224 interests existed at the time of publication.
American Journal of Speech-Language Pathology • Vol. 27 • 99–107 • February 2018 • Copyright © 2018 American Speech-Language-Hearing Association 99
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failure (Calis et al., 2008; Rogers, Arvedson, Buck, Smart, foods, but not liquids). Duration was measured from place-
& Msall, 1994). Without proper treatment, dysphagia in ment of the bolus into the oral cavity until the swallow
CP can significantly increase the risk for recurrent aspiration was visually noted. Prolonged duration among solid, puree,
leading to respiratory infections, lung disease, failure and viscous food types was observed as compared to norma-
to thrive, and death (Calis et al., 2008; Lefton-Greif & tive data obtained by the same researchers in a prior study
McGrath-Morrow, 2007; Rogers et al., 1994). (Gisel, 1988).
Feeding and swallowing assessments in CP involve While these studies provide objective data, they have
multiple components, including medical and developmental used variable measurements for mealtime duration on the
history, clinical feeding observations, cranial nerve exami- basis of caregiver reports or responses for mealtime conclu-
nations and, when necessary, instrumental evaluations sion (Erkin et al., 2010; Gisel & Alphonce, 1995; Reilly
(Arvedson, 2008). In addition, mealtime duration is often & Skuse, 1992; Wilson & Hustad, 2009). Also, mealtime
assessed. Clinically, mealtime duration in excess of 20–30 min subcomponents have been investigated only by one prior
has been considered as a possible sign of dysphagia, as well study, which used visual detection of the swallow (Gisel &
as inefficient and insufficient nutritional intake (Arvedson, Alphonce, 1995). In children with CP and known aberrant
2008). However, the empirical evidence/literature supporting motor control and oropharyngeal discoordination, visual
this statement for children with CP is contradictory. detection of the swallow (typically conducted by observing
Studies of mealtime duration that have relied on the thyroid notch movement during the swallow) is extremely
parent reports have reported mixed results. In a study by challenging. It has been suggested that obtaining a valid
Erkin, Culha, Ozel, and Kirbiyik (2010), a representative measure of mealtime duration can provide insight into not
sample of 120 children with CP and parent-reported feeding only observed deficiencies but also potential for growth
dysfunction, aged 2–12 years, had significantly longer (Rogers, 2004). Therefore, it is important to develop direct
mealtime durations compared with their counterparts with- mealtime duration and subcomponent measurements that
out feeding difficulties (114 min/day vs. 84 min/day, respec- are clearly defined, highly reliable (replicable), and easy
tively). Likewise, Wilson and Hustad (2009) descriptively to use. To address this gap, we aimed (a) to examine the
reported that five out of 37 children with CP and oral intra- and inter-rater reliabilities of direct measures of meal-
motor involvement (11–58 months old), as determined by time duration and its subcomponents that were developed
parental responses to a 12-item feeding and swallowing ques- for this study and, (b) as a measure of preliminary validity,
tionnaire developed by the authors, required 30–60 min to to determine the relationship of these objective measures
consume a meal. In contrast, Benfer et al. (2014) analyzed to clinical feeding and swallowing performance in children
parental responses in 3-day food logs and did not find with spastic CP who presented with bilateral or unilateral
significant relationships between mealtime duration and brain involvement. It is well known that feeding and
severity of dysphagia in a sample of 130 preschool children swallowing require the highly complex sensorimotor
aged 18–36 months with CP. These mixed findings may be coordination of multiple structures, muscles, brainstem
due to the fact that these studies relied solely on caregiver centers, and areas in the cortex and subcortex bilaterally
reports (Benfer et al., 2014; Erkin et al., 2010; Wilson & (Hamdy, Rothwell, Aziz, & Thompson, 2000; Humbert
Hustad, 2009). & Joel, 2012; Lowell, Reynolds, Chen, Horwitz, & Ludlow,
Reilly and Skuse (1992) performed direct mealtime 2012; Malandraki, Sutton, Perlman, & Karampinos, 2010).
observations in 12 children with CP aged 15–39 months In children with unilateral early brain injuries manifesting
and 12 age-matched controls. Mealtime duration was defined as CP, we recently showed that adaptive contralesional
as the interval between the presentation of the first bolus and neuroplastic compensations/communications for func-
the mother’s signal of meal conclusion. All mothers in this tional swallowing are seen when sensorimotor areas of
study were instructed to feed their children, and no signifi- one hemisphere are affected (Mourao et al., 2017). It
cant differences were found between groups. The same is only logical to assume that these neuroplastic effects
research group used parent questionnaires and a direct would be less pronounced in children with bilateral
video-recorded assessment in another study of 49 children lesions, although data are still emerging. Therefore, from
with CP between 1 year and 6 years of age (Reilly, Skuse, a neurophysiological and neuropathological standpoint,
& Poblete, 1996). They observed that children with severe it is important to investigate differences between these two
oral motor dysfunction demonstrated shorter mealtime groups.
durations than children with milder oral motor deficits. We hypothesized that longer mealtime durations
They also reported that directly measured durations were would be associated with increased clinical signs of feeding
approximately 10 min shorter than parent-reported dura- and swallowing difficulties. In addition, given what we
tions. The only prior study, to our knowledge, that looked know about the neural control of swallowing (Hamdy
into mealtime subcomponents (i.e., bolus consistencies, et al., 2000; Humbert & Joel, 2012; Lowell et al., 2012;
such as liquids, solids, and semisolids) in children with CP was Malandraki et al., 2010; Mourao et al., 2017), we hypothe-
a study by Gisel and Alphonce (1995). These investigators sized that children with primarily bilateral brain involvement
aimed to classify feeding impairments in a representative manifesting as bilateral spastic CP (BSCP) would demon-
sample of 100 children across CP types on the basis of dura- strate more signs of feeding and swallowing dysfunctions
tion of mealtime subcomponents (solid, puree, and viscous and significantly longer mealtime durations than children
Note. Age is reported in years;months. GMFCS = Gross Motor Function Classification System; MACS = Manual Ability
Classification System; DDS1 = DDS Part 1; DDS2 = DDS Part 2; DDST = DDS total; F = female; M = male.
Figure 1. Correlations between total mealtime duration and DDS scores. DDS = Dysphagia Disorder Survey. *p < .05.
that these measures are reliable and show preliminary associ- by the caregiver and only investigated total mealtime dura-
ations with clinical dysphagia signs for this population. tion (and not mealtime subcomponents; Reilly & Skuse,
Specifically, reliability testing revealed excellent 1992; Reilly et al., 1996). Reilly and Skuse (1992) found
intra- and inter-rater agreement for total mealtime duration no differences between mealtime duration in preschool chil-
(ICCs = 1.00 and 0.955, respectively), total solid/bite dura- dren with CP and age-matched controls, whereas Reilly
tion (ICCs = 1.00 and 0.963, respectively), and total liquid/ et al. (1996) reported shorter mealtime durations in children
sip duration (ICCs = 1.00 and 0.957, respectively), sug- with CP and severe oral motor dysfunction compared with
gesting that these measures are highly reliable within and children with milder oral motor deficits. Differences in
between raters. We developed these measurements to be methods used to measure mealtime duration, as well as in
practical in a clinical setting, while also being accurate dur- participants’ age ranges (1–6 years) may explain these
ing live evaluations and/or video recordings. Direct meal- contradictory findings. Younger children with CP do not
time duration has been assessed in prior research with typically feed themselves and rely more heavily on liquids
variable results. Gisel and Alphonce (1995) examined dura- (that are generally cleared more quickly from the orophar-
tion of mealtime subcomponents by visually detecting the ynx) to meet nutritional demands. Although Gangil, Patwari,
swallow through video-recorded analysis and did not report Aneja, Ahuja, and Anand (2001) identified liquids and
reliability of their data; visual detection of the pharyngeal semisolids as the primary diet in 100 children aged 1–9 years
swallow in children without the use of instrumental evalua- with CP, in our sample, even children who were the most
tion is extremely challenging and prone to inaccurate severely impaired (GMFCS Level IV) self-fed and ate a
judgment (DeMatteo, Matovich, & Hjartarson, 2005). variety of solids. Our measures were novel in that we used
In particular, in children with CP, movement of the hyo- child-controlled events that were easily and visually identifi-
laryngeal mechanism may not always indicate a swallow able to signify the beginning and end of total mealtime
given postural instability and oropharyngeal discoordina- duration, as well as bite and sip durations. This was deemed
tion (Carlberg & Hadders-Algra, 2005; Krigger, 2006). more appropriate as our sample included older children who
Two other studies determined total mealtime duration from were self-feeding.
presentation of first bolus to the signaled meal conclusion Furthermore, we identified positive correlations
between total mealtime duration and DDS scores, as well
as between total solid duration and DDS scores, suggesting
Table 3. Unilateral versus bilateral group comparisons—demographic that mealtime duration and duration of solid consumption
variables. are longer for children with more clinical signs of dysphagia.
These findings are in agreement with some prior studies that
Variable z Value p Value
have shown increased mealtime duration for children with
Age −0.293 .769 CP and more severe oromotor involvement (Erkin et al.,
Sex −0.282 .778 2010; Gisel & Alphonce, 1995; Wilson & Hustad, 2009).
GMFCS −3.662 .000* Our findings relating to the longer duration of solid con-
MACS −1.298 .194 sumption with increasing clinical signs of dysphagia in CP
Note. GMFCS = Gross Motor Function Classification System; are also in agreement with previous research. In particular,
MACS = Manual Ability Classification System. prolonged oral transit times across all bolus types have been
*p < .05. reported in children with CP, and significantly longer times
have been reported with solid boluses (Casas, McPherson,
Note. USCP = unilateral spastic cerebral palsy; BSCP = bilateral spastic cerebral palsy.
*p < .05.
& Kenny, 1995). Recent research has also shown that these Furthermore, when comparing children with bilateral
children exhibit difficulty in oral containment and formation brain involvement manifesting as BSCP and children with
of the bolus, at times resulting in aspiration of solids and unilateral brain involvement manifesting as USCP, we
induction of fatigue (Kim, Han, Song, Oh, & Chung, 2013). saw that children in the first group exhibited significantly
Therefore, children with CP are often introduced to solid higher DDS Part 2 and DDS total scores than children
boluses at later periods than typically developing children, in the second group, but no group differences were ob-
which may also place them at a disadvantage in fully acquir- served for DDS Part 1. DDS Part 1 examines diet, indepen-
ing the skills to manage these foods (Salghetti & Martinuzzi, dence, adaptive utensils used, positioning, postural control,
2012). Regarding liquid consumption, many of the children and feeding techniques. Children in both groups were on
were observed to complete sequential swallows, and there- unrestricted oral diets and did not have comorbidities that
fore, higher total liquid/sip duration may not necessarily could influence DDS Part 1 scores. DDS Part 2 contains
reflect abnormal swallowing patterns for liquids; on the items specific to oropharyngeal swallowing skills. Our results
contrary, it may even reflect greater swallowing/drinking suggest that children with bilateral brain involvement have
skills for some children. It is possible that, because for more clinical signs of dysphagia and longer mealtime dura-
some children this measure reflected higher swallowing tions than children with unilateral brain involvement. How-
skills and, in some, poorer skills, overall, no significant ever, because signs of dysphagia were present in all children
correlations were observed between DDS scores and total (DDS scores ≥ 3) of both groups, the results further show
liquid/sip duration. Perhaps, additional criteria are required that clinical swallowing difficulties and mealtime duration
when measuring liquid durations to ensure that this measure elements can be affected even in the milder forms of motor
can provide consistent evaluative information. Such criteria involvement in CP (Benfer et al., 2014, 2015; Malandraki,
should be explored in future studies. Mishra, Gordon, & Sheppard, 2014).
To further examine the potential impact of other USCP is the manifestation of unilateral brain lesions,
factors influencing self-feeding, such as functional gross including periventricular lesions and cortical dysplasia, which
motor and manual ability classification levels (GMFCS result in primarily unilateral motoric deficits (Krägeloh-Mann
and MACS), on mealtime durations, we also examined & Cans, 2009). BSCP may result from more systemic brain
additional correlations between GMFCS levels and meal- lesions affecting both hemispheres and resulting in bilateral
time durations and MACS levels and mealtime durations. motoric compromise (Himmelmann, Beckung, Hagberg,
Similar to DDS scores, GMFCS level also significantly & Uvebrant, 2007; Krägeloh-Mann & Cans, 2009). Oro-
correlated with total mealtime duration and total solid/bite pharyngeal swallowing is a complex sensorimotor function
duration, but not with total liquid/sip duration. This finding controlled by a network of peripheral and central neural
is not surprising if we consider that a positive relationship mechanisms that involve both hemispheres and bilateral
between oropharyngeal dysphagia and gross motor function control of the head and neck (Malandraki, Sutton, Perlman,
has been well documented in children with CP (Benfer et al., Karampinos, & Conway, 2009). We recently showed pre-
2013; Calis et al., 2008; Fung et al., 2002; Kim et al., 2013). liminary evidence suggesting that children with unilateral
Given the relatively small sample size, multivariate analyses early brain lesions may be able to use recovery mechanisms
to determine the relative contributions of DDS scores versus of the contralesional hemisphere to develop their swallowing
GMFCS levels in duration measures were not possible at skills (Mourao et al., 2017). Studies focusing on motor
this time; however, this relationship should be further inves- hand control in children with USCP have also shown that
tigated with larger samples. MACS levels did not signifi- the contralesional hemisphere possesses substantial compen-
cantly correlate with any of the duration measures in this satory potential for motor function recovery (Staudt, 2007).
study. This may be because most children in our sample These recovery mechanisms may not be as widely available
(13 out of 17) had MACS levels of I or II; therefore, the in children with bilateral and more systemic brain lesions,
sample was relatively skewed to milder manual ability and further investigation of these differential neuroplastic
involvement. mechanisms is warranted.