Download - Oral motor performance in spastic cerebral palsy individuals: are hydration and nutritional status associated?

Oral motor performance in spastic cerebral palsyindividuals: are hydration and nutritional status associated?

Maria Teresa Santos1, Renato Batista

1, Elisangela Previtali

1, Adriana Ortega

1, Oliver Nascimento

2,

Jose Jardim2

1Universidade Cruzeiro do Sul, Persons with Disabilities Division; 2Universidade Federal de Sao Paulo, Respiratory Diseases

BACKGROUND: Previous studies reported alterations in

salivary parameters in cerebral palsy (CP) individuals;

however, none of these considered oral motor perfor-

mance as possibly responsible for these conditions. The

aim of this study was to investigate the influence of oral

motor performance on the nutritional status and salivary

parameters in individuals with CP.

METHODS: Forty-three individuals aged 11–19 years-

old, with spastic CP were included in this study. Oral

motor performance was evaluated using the Oral

Motor Assessment Scale, which classified the individuals

into two groups: subfunctional or functional. Unstimu-

lated saliva was collected and the flow rate was

calculated (ml ⁄ min). Salivary osmolality was measured

using a freezing point depression osmometer. Blood

samples were collected to evaluate complete blood

count, total protein, albumin ⁄ globulin ratio and trans-

ferrin levels.

RESULTS: The subfunctional (n = 21) and the functional

group (n = 22) did not differ regarding sex (P = 0.193),

however the functional group was older (P = 0.023) and

had a higher mean BMI (P < 0.001). The subfunctional CP

group presented a reduction in salivary flow rate (36.4%)

(P < 0.01) and an increase in salivary osmolality (35.5%)

(P < 0.001) compared to the functional group. Slightly

lower values for red blood cells (millions ⁄ mm3)

(P < 0.001), hemoglobin (g ⁄ dl) (P < 0.009), hematocrit (%)

(P = 0.001), number of platelets (N ⁄ mm3), total protein

(g ⁄ dl) and albumin ⁄ globulin ratio (P = 0.003 and P = 0.036,

respectively) were determined for the subfunctional

group, but within the normal range of normality.

CONCLUSION: Cerebral palsy individuals appear to

present impaired adequate hydration due to compro-

mised oral motor performance.

J Oral Pathol Med (2012) 41: 153–157

Keywords: cerebral palsy; saliva; salivary parameters; osmolality;

hydration; oral motor performance; nutritional status

Introduction

Individuals with functional neurological damage, par-ticularly those with cerebral palsy (CP), often presentseveral disorders that are accompanied by disharmonicmovements, including oral motor performance ofspeech, mastication and swallowing (1).

The limited motor performance of mastication andswallowing in children with CP, a neurodevelopmentaldisability (2), results in feeding dysfunctions thatinclude several interacting variables, including dys-functional oral motor control (weak sucking, persis-tent tongue thrusting and poor lip closure), abnormalneurological maturation (presence of oral pathologicalreflexes), and poor seating posture during feeding.These abnormalities may result in reduced dietaryintake, prolonged feeding times and poor nutri-tional status with their attendant physical compromise(3–7).

It has been reported that children with CP can presentlow salivary flow rate, pH and buffer capacity (8).Increased salivary osmolality and total protein concen-tration (9), as well as increased salivary, urine andplasma osmolalities were also verified in these individ-uals, characterizing impaired adequate hydration status(10). These findings lead us to believe that the dailyamount of liquid intake is usually reduced in theseindividuals. These conditions could be due either to alow amount of liquid offered to these individuals, or tocompromised oral motor performance that may hamperthe liquid diet intake. If it were the case that thehypohydration status was due to the insufficient offer bytheir caregivers, then subnutritional status should alsobe observed.

Considering the points raised above, the aim of thisstudy was to investigate the influence of oral motorperformance on the nutritional status and salivaryparameters in individuals with spastic cerebral palsy. It

Correspondence: Maria Teresa B. Santos DDS, PhDAssociate Professor, Individuals with Special Needs, UniversidadeCruzeiro do Sul, Rua Constantino de Souza, 454, apto 141 Zip code:04605-001 Sao Paulo, Brazil. Tel: +551199722301, Fax: +551150930865, E-mail:[email protected] for publication August 4, 2011

doi: 10.1111/j.1600-0714.2011.01074.x

J Oral Pathol Med (2012) 41: 153–157

ª 2011 John Wiley & Sons A/S Æ All rights reserved

wileyonlinelibrary.com/journal/jop

was hypothesized that compromised oral motorperformance interferes in liquid and solid dietintake, resulting in diminished health status for theseindividuals.

MethodsSubjectsThis project was approved by the Cruzeiro do SuIUniversity Institutional Review Board (IRB) underprotocol number 045 ⁄ 2010. After being informed ofthe aim of the investigation, written informed consentfor participation and publication was obtained from theadult responsible for each individual.Forty-three male and female individuals, aged

11–19 years old, diagnosed with spastic cerebral palsy,who attended the Fraternidade Irma Clara Institution,in Sao Paulo, Brazil, were included in this study. Theinclusion criteria were: individuals with a clinical med-ical diagnosis of spastic cerebral palsy; and the exclusioncriteria were use of any drug that could interfere withsaliva secretion (anticholinergic and neuroleptic drugs,benzodiazepines) for at least 72 h prior to examination,a history of head and neck radiation and surgicalprocedures to reduce drooling.The patient’s medical records were reviewed for

demographic and clinical data and body mass index(BMI).

Oral motor performancePatient oral motor performance was evaluated duringthe feeding process using the Oral Motor AssessmentScale (11). The following topics were evaluated: mouthclosure, lip closure onto the utensils, lip closure duringdeglutition, control of food during swallowing(solid ⁄ semisolid), mastication, straw suction and controlof liquids during deglutition.A score was given for each topic of the oral motor

skill assessed. A final classification of the oral motorskill was obtained based on the most frequent score.The individuals were classified as: passive (severelycompromised oral motor performance), subfunctional(moderately compromised oral motor performance),semi-functional (slightly compromised oral motor per-formance) and functional (very slightly compromisedoral motor performance) (11).

Saliva collectionUnstimulated whole saliva was collected using slightsuction through a soft plastic catheter. The salivaproduced in the first 10 s was discarded and allsubsequent saliva was collected for exactly 5 min in agraduated cylinder in order to calculate the flow rate(ml ⁄min). During the collection period, all the childrenremained comfortably seated in a ventilated and illumi-nated room. When it was not possible to collect salivafrom a child due to crying, they were excluded. Soonafter collection, the saliva sample was frozen in dry ice,transported to the laboratory and stored at )80�C untilanalysis. Salivary osmolality was measured using afreezing point depression osmometer (Model Wide-

Range Osmometer 3W2; Advanced Instruments, Need-ham, MA, USA).

Body mass index calculationSince individuals with CP present difficulties instanding straight, height was measured by the tibiasegment length in centimeters and the estimatedstature was determined from segmental measures usingthe equation: Stature = (3.26 x tibia segment) +30.8 cm (12). For individuals seated in a wheelchair,weight was measured with the patient sitting in theirwheelchair in a digital balance, and later the weightof the chair was subtracted from the total. Finally,body mass index was calculated as weight ⁄ stature2(kg ⁄m2).

Blood collectionBlood samples were collected to evaluate completeblood count, total protein, albumin ⁄ globulin ratio andtransferrin levels using venostasis from an antecubitalvein into separate Vacuteiner tubes containing ethylen-ediaminetetraacetic acid (EDTA) (Becton Dickson, Juizde Fora, Brazil).

Statistical analysisTo evaluate proportional differences between the groupsstudied, the chi-square test was used. The Student’st-test was used to verify the hypothesis of equalitybetween the two groups. Spearman’s correlation coeffi-cient was used to associate the behavior of fourvariables. The significance level was set at P < 0.05.

Results

Individuals determined as having a final predominancetype of passive and subfunctional (severely and moder-ately compromised oral motor performance) were clas-sified into a single group that was denominated thesubfunctional group (n = 21), while the semi-functionaland functional individuals (slightly and very slightlycompromised oral motor performance) were denomi-nated the functional group (n = 22).

The individuals from both groups did not differregarding sex (P = 0.193), but the functional group was

Table 1 Descriptive characteristics of individuals with cerebral palsywith subfunctional and functional oral motor performance groups

Individual variables

Subfunctionalcerebral palsy(n = 21)

Functionalcerebral palsy(n = 22) P value*

Sex, n (%) 0.193a

Female 15 (71.4) 17 (77.3)Male 6 (28.6)) 5 (22.7)Age, mean [±SD] years 14.2 ± 2.8 16.2 ± 2.9 0.023*b

BMI (kg ⁄m2) 14.2 ± 2.1 16.9 ± 0.83 <0.001*b

aThe data were compared by chi-square test.b The data were compared by Student’s t-test.*P < 0.05.

Hydration status in cerebral palsy

Maria Teresa Santos et al.

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significantly older (P = 0.023) and had a significantlyhigher BMI (P < 0.001) (Table 1).

Data of salivary flow rate (ml ⁄min) and salivaryosmolality (mOsm ⁄ kgH2O) from the subfunctional andfunctional CP groups are presented in Table 2. Thesubfunctional CP group presented a 36.4% reduction insalivary flow rate (P < 0.01) and an increase of 35.5%in salivary osmolality (P < 0.001) compared to thefunctional group.

The subfunctional group presented lower values forred blood cells (millions ⁄mm3) (P < 0.001), hemoglo-bin (g ⁄ dl) (P < 0.009), hematocrit (%) (P = 0.001)and number of platelets (N ⁄mm3) (Table 3). Addition-ally, this group presented significantly lower values fortotal protein (g ⁄ dl) and the albumin ⁄ globulin ratio(P = 0.003 and P = 0.036, respectively) (Table 4).

Table 5 shows the values of the Spearman’s correla-tion coefficient for salivary flow rate, salivary osmolal-ity, BMI, total protein and albumin ⁄ globulin ratio ofthe two groups studied. Salivary osmolality was nega-tively correlated with salivary flow rate (R = )0.82,P < 0.01), BMI (R = )0.66, P < 0.01), total protein(R = )0.54, P < 0.01) and albumin ⁄ globulin ratio(R = )0.52, P < 0.01). Salivary flow rate correlatedpositively with BMI (R = 0.74, P < 0.01) and totalprotein (R = 0.57, P < 0.01).

Discussion

Understanding the impact of oral motor dysfunctionmay be helpful in identifying individuals at high risk ofdeveloping oral diseases. The results of this studysuggest that individuals with CP presenting greater oralmotor performance impairment also present reducedsalivary flow rate and increased salivary osmolality,which is indicative of hypohydration status compared tothose with better oral motor performance. However, inboth groups, nutritional status was within the normalrange, according to the parameters evaluated. Analysisof these results does not support the hypothesis raised inthis study, since compromised oral motor performancein individuals with CP only interferes in liquid dietingestion, confirming the hypohydration status previ-ously reported (8–10).

The tool used in this study to assess oral motorperformance is an accurate and valid method forevaluating feeding dysfunction in this population (11)and made possible to divide the individuals studied intotwo distinct groups.

Even though CP results from a permanent staticlesion to the central motor cortex (2), the lesion itselfdoes not change, but the clinical manifestations of thelesion may change as the child grows up (13). Althoughthe functional and subfunctional oral motor perfor-mance groups differ regarding age, it is important totake into account the fact that oral motricity is directlyrelated to the brain damage caused by CP, rather thanassociated with developmental changes that are modi-fied by hormones and puberty.

Table 2 Salivary flow rate (ml ⁄min) and salivary osmolality(mOsm ⁄ kg H2O) of individuals with cerebral palsy with subfunctionaland functional oral motor performance groups

ParametersSubfunctionalcerebral palsy

Functionalcerebral palsy P value*

Salivary flow rate 0.32 ± 0.15 0.88 ± 0.21 <0.001*Saliva osmolality 107.3 ± 14.1 69.2 ± 13.3 <0.001*

The data were compared by the Student’s t-test.*P < 0.05.

Table 3 Complete blood count of individuals with cerebral palsy withsubfunctional and functional oral motor performance groups



Red blood cells(millions ⁄mm3)

4.2 ± 0.47 4.7 ± 0.41 <0.001*

Hemoglobin(g ⁄ dl)

13.5 ± 0.70 14.1 ± 0.75 0.009*

Hematocrit (%) 38.2 ± 2.5 40.6 ± 2.1 0.001*Mean corpuscularvolume (fl)

83.8 ± 6.7 86.8 ± 5.4 0.115

Mean corpuscularhemoglobin (pg)

27.6 ± 2.7 29.7 ± 2.1 0.139

Leukocytes(N ⁄mm3)

6999.5 ± 1822.1 6913.6 ± 1638 0.872

Platelet(N ⁄mm3)

231.4762 ± 58195.9 274.500 ± 68985.7 0.033*


Table 4 Total protein, albumin globulin, albumin ⁄ globulin ratio, andtransferrin of individuals with cerebral palsy with subfunctional andfunctional oral motor performance groups



Total protein (g ⁄ dl) 6.7 ± 0.48 7.2 ± 0.47 0.003*Albumin 4.13 ± 0.43 4.23 ± 0.45 0.491Globulin (g ⁄ dl) 2.91 ± 0.54 2.99 ± 0.24 0.527Albumin ⁄ globulinratio (g ⁄ dl)

1.33 ± 0.19 1.45 ± 0.16 0.036*

Transferrin (mg ⁄ dl) 249.5 ± 60.1 257.5 ± 46.3 0.716


Table 5 Values for Spearman’s correlation coefficient between thevalues of salivary osmolality, flow rate and body mass index

ParametersSalivaryosmolality

Salivary flowrate

Salivary osmolality (m0sml) – )0.82*Body mass index (kg ⁄m2) )0.66* 0.74*Total protein (g ⁄ dl) )0.54* 0.57*Albumin ⁄ globulin ratio (g ⁄ dl) )0.52* 0.263

*Spearman’s correlation coefficient, P < 0.01*.



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The severe oral motor dysfunction observed in CPindividuals with subfunctional oral motor performancein this study was responsible for the significant reducedBMI observed, since the development of successfulfeeding skills requires the presence of normal anatomicalstructures involved in oral preparation, the swallowreflex, and the natural progression of learned behaviorto achieve the complex process of feeding (14). Inaddition, this condition may cause limited food andwater intake, poor growth and may indicate a risk foroverall health (15).Salivary osmolality has been described as a reliable

parameter of hydration status and reflects changes inplasma and urine osmolality in CP individuals (10).The higher salivary osmolality observed in the CPindividuals with subfunctional oral motor performanceis very similar to the osmolality presented by individ-uals submitted to conditions of dehydration (9), sug-gesting a reduced amount of liquid diet intake by thisgroup.The hemoglobin level has been widely accepted as an

important index of nutritional status (16). The CPindividuals with subfunctional oral performance in thisstudy showed a slight but significant reduction inhemoglobin levels in comparison to the functionalgroup, although the hemoglobin of both groups werewithin the normal range of normality (13.9 ± 0.52 formales and 13.4 ± 0.76 for females). Few studies havediscussed this issue in CP individuals (16, 17). Norm-ocytic normochromic anemia was described in 19 casesof a sample composed by 90 institutionalized, adult,Japanese, CP individuals with a mean age of 42.1(±10.7) years old. It should be highlighted that theindividuals evaluated in the study (16) were almostthree times the age of those evaluated in the presentstudy and that the cause of anemia could be due todiminished iron absorption, common in older individ-uals.No protein deficit was observed in either of the CP

groups in this study, demonstrating that the proposednutritional monitoring (behavior therapy, follow-upmonitoring, anthropometric measurements and nutri-tional education) provided for the individuals with CPby the institution was sufficient to maintain theirnutritional status, but not their hydration status.The issue of hydration status and liquid diet intake

in individuals with CP has rarely been described in theliterature (9, 10). Solid and semisolid food consistenciesprovide greater proprioceptive stimuli inside themouth, which facilitates the control of swallowing. Inindividuals with CP who cannot sustain lips closure,the liquid diet intake usually flows out of the mouth,resulting in the lack of negative pressure for swallow-ing, which may cause choking. In individuals with CP,water intake is generally below the required standards(18) and the management of solid alimentary bolus iseasier than liquid ingestion; small liquid boluses areeasier to ingest than large liquid boluses. Moreover,these individuals tend to consume small volume ofliquids (19). All of these facts could explain the

hypohydration status observed in the individuals ofthis study.

In conclusion, analysis of the data obtained suggeststhat cerebral palsy individuals present impaired ade-quate hydration due to compromised oral motorperformance.

References

1. Koolstra JH. Dynamics of the human masticatory system.Crit Rev Oral Biol Med 2002; 13: 366–76.

2. Rosenbaum P, Paneth N, Leviton A, et al. A report: thedefinition and classification of cerebral palsy April 2006.Dev Med Child Neurol Suppl 2007; 109: 8–14.

3. Calis EA, Veugelers R, Rieken R, Tibboel D, EvenhuisHM, Penning C. Energy intake does not correlate withnutritional state in children with severe generalized cere-bral palsy and intellectual disability. Clin Nutr 2010; 29:617–21.

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Acknowledgements

This study was supported by the Fundacao de Amparo a Pesquisa do

Estado de Sao Paulo (FAPESP) under protocol number 08 ⁄ 00960-6.



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