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This study was conducted at sector of Speech-Language, Pathology and Audiology, Associação de Assistência à Criança Deficiente – AACD – São Paulo (SP), Brazil. (1) Sector of Speech-Language, Pathology and Audiology (Perfectioning), Associação de Assistência à Criança Deficiente – AACD – São Paulo (SP), Brazil. (2) Associação de Assistência à Criança Deficiente – AACD – São Paulo (SP), Brazil.

Conflict of interests: No

Author’s contribution: NSL and TRBF contributed to all steps of the methodology of this research; CCS supervised the research, did part of the evaluation and contributed to the establishment of the necessary methodology.

Correspondence address: Carolina Castelli Silvério. Av. Professor Ascendino Reis, 724, Ibirapuera, São Paulo (SP), Brazil, CEP: 04027-000. E-mail: carol_silverio@hotmail.com

Received: 6/3/2013; Accepted: 8/14/2013

Temporal measurements of oral transit time in children

with cerebral palsy of different levels motors and the

relationship with the severity of dysphagia

Medidas de tempo de trânsito oral em crianças com paralisia

cerebral de diferentes níveis motores e sua relação com o grau de

severidade para disfagia

Natali da Silva Lustre1, Talita Regina Bezerra Freire1, Carolina Castelli Silvério2

ABSTRACT

Purpose: To verify the oral transit time in children with cerebral palsy, and relating it to the degree of dysphagia severity and motor level. Me-thods: The sample was 50 children with cerebal palsy, 23 males and 27 females, mean age of 3 years 7 months. The clinical assessment consis-ted in to provide food in liquid and pasty consistency. It measured the time of oral transit, and performed the diagnosis of swallowing function classifying it into normal, mild, moderate or severe dysphagia. Results: The mean of oral transit time was found to be 1.33 seconds to liquid and 3.33 seconds for pasty consistency. As higher the level of the motor group of children, higher the time for swallowing liquid consistency, which was statistically significant. Statistically significant difference was found between groups for both consistencies, with a progressive increase of the time in accordance with the increase in impairment of swallowing. Conclusion: The oral transit time in children with cerebral palsy was found increased and may represent the severity of dysphagia presented, because this time was longer as worse the impairment in swallowing function. The higher the overall motor impairment presented, the longer oral transit time.

Keywords: Cerebral palsy; Deglutition disorders; Time; Deglutition; Child

RESUMO

Objetivo: Verificar o tempo de preparo e de trânsito oral da deglutição de crianças com paralisia cerebral e relacioná-lo ao grau de severidade da disfagia e ao nível motor, de acordo com o Gross Motor Function Classification System. Métodos: Participaram desta pesquisa 50 crianças com paralisia cerebral, média de idade de 3,6 anos, sendo dez crianças de cada nível motor. A avaliação fonoaudiológica clínica da deglutição consistiu na oferta de alimentos nas consistências “líquido fino” (água) e “pastoso homogêneo” (iogurte tipo petit suisse). Foi mensurado o tempo de preparo e de trânsito oral e realizado o diagnóstico da função de de-glutição, classificando-a em normal, disfagia leve, moderada, ou grave. Resultados: A média do tempo de deglutição foi de 1,33 segundos para a consistência líquida e de 3,33 segundos para a consistência pastosa. Quanto maior o nível motor do grupo de crianças, maior o tempo de deglutição para a consistência líquida. Encontrada diferença significativa entre os grupos para as duas consistências, com aumento progressivo do tempo de deglutição quanto maior o comprometimento da função de deglutição. Conclusão: O tempo de trânsito oral em crianças com paralisia cerebral mostrou-se aumentado e pôde representar a gravidade da disfagia apresentada, já que esse aumento ocorreu conforme maior o comprometimento da função de deglutição. Quanto maior o compro-metimento motor global apresentado, maior o tempo de trânsito oral.

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INTRODUCTION

Cerebral palsy (CP) is a group of permanent disorders of the development of movement and posture, causing activity limitations that are attributed to nonprogressive disturbances that occur in the brain in childhood development(1).

Children with neuromotor disorders, as in the CP, frequent-ly present problens in swallowing function, leading to clinical disorders, including recurrent pneumonia and malnutrition. The CP is associated to the complex orofacial sensorimotor dysfunction, including dysphagia, dysarthria, alterations in chewing and drooling(2). Study(3) conducted with 1357 children with CP of several global motor impairment, found that 21% of these children had alterations in the functions of swallowing and / or chewing, and 22% excessive escape of saliva.

In CP, dysphagia is often characterized by changes in the oral phase, voluntary motor activities, and pharyngeal with active order reflexive swallowing(4). Among the disorders in swallowing function, one of the most frequently refers to the increase in oral transit time, leading to greater energy expenditure during oral intake, worsening the maintenance and weight gain in children. Authors found in their study(5) that the stages of oral phase, both in the clinical assessment, as in videofluoroscopy of swallowing, are altered in children with CP spastic quadriplegia. In children with CP, the pres-ence of dysphagia is associated with delayed development, malnutrition and short stature(6).

Due to the nutritional impact resulting from increased oral transit time, it is necessary to know about the time that children with cerebral palsy exhibit, and correlated it with the severity of dysphagia. As the oral transit time is relevant information in relation to pathophysiology of swallowing, since it can show the wear to the task and, moreover, relates the disorders in oral preparation, knowing it results in an important data for the evaluation of children with neuropathy, attempting to demonstrate in a more quantitative manner, the significance of swallowing deficit in this population.

The more elements will be able to be measured in a clinical and quantitative evaluation, greater facility the speech thera-pist will have to classify the deglutition disorders presented in children with neuropathy, including set targets and defining better the goals and prognosis for each patient.

Among the methods of measuring time in swallowing function, there are those using videofluoroscopy of swal-low(7,8), which makes this process more effective, since objective images are used, making it possible to determine, with greater precision, the time at which the reaction of swal-low happens. However, in many services the availability of

videofluoroscopy is still small, indicating the need to measure the time of preparation and conducting oral in a clinical form.

Thus, this study aimed to verify clinically the time of the transit oral in children with CP, and relating it to the degree of dysphagia severity and motor level according to the Gross Motor Function Classification System (GMFCS )(9).

METHODS

This study was approved by the Research and Ethics Committee for Associação de Assistência à Criança Deficiente (AACD), protocol number 12/2011. All responsible for chil-dren signed the term of free and informed consent authorizing the participation in this study.

The sample was 50 children with CP who attend the Rehabilitation Center of AACD, 23 males and 27 females, aged from 1 year and 7 months to 4 years and 11 months (mean age of 3 years and 7 months).

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Exclusion criteria of this study: presenting pathologies associated with CP; make use exclusive or partial feeding tu-bes; present restrictions to intake of any of the components or consistency of foods offered, presenting cleft lip and/or palate.

Clinical evaluation of swallowing consisted in offering food in consistencies of “thin liquid” (water) and “pasty homogeneous” (yogurt petit suisse) by the child’s caregiver, if they could not feed herself, in the usual posture and with the usual eating utensils (spoons and cups).

The volume of each offering was up to the caregiver/sub-ject, according to the child’s eating routine. The volume to be provided influences the physiology of swallowing displayed, but the authors preferred to keep offering the routine of each patient, avoiding alterations in dynamics. Also, select a spe-cific volume for the evaluation would cause, in many cases, changing the usual eating utensil, which in children with neu-ropathy significantly alters the function of swallowing. Were performed at least two offers for each consistency, starting with the liquid since the pasty consistency is more likely to occur stasis of the bolus in the pharyngeal region.

During the intake, were measured the time for preparation and oral transit, which includes the period of time when the food is placed in the oral cavity until its first swallowing(10). The time was measured using the digital stopwatch Herweg® 8905-34 and was considered the result of the mean time of the two swallows presented for each food consistency offered.

At the same moment, the child received the diagnosis of swallowing function, according to the clinical evaluation of swallowing, classifying it as normal, mild, moderate or severe dysphagia. This classification was done at the AACD in São Paulo, and due the lack of severity ratings of dysphagia in children with neuropathy that cover the data of preparation, organization and oral transit time, as clinical signs of laryn-geal penetration and tracheal aspiration, the authors opted to maintain this rating, describing what they considered in each item. Also, keep the routine classification of the exper-tise in pediatric dysphagia, provided greater reliability of the results of this study. The classification, then, followed these criteria:

- Normal: efficient capture in removing the food from the utensil; absence escape extraoral; efficiency in preparing the bolus at the expected time; absence of residues in the mouth after swallowing, or small volume, spontaneously removed next swallowing; clean cervical auscultation; no clinical signs suggestive of laryngeal penetration and/or tracheal aspiration.

- Mild dysphagia: capture not effective for removing the food from the utensil; presence of escape extraoral to half volume given; inefficiency in preparing the bolus at the

expected time; residues in the mouth after swallowing, at any volume, with no clearance or partial clearance in the next spontaneous swallowing; clean cervical auscultation; absence of clinical signs suggestive of laryngeal penetra-tion and/or tracheal aspirapenetra-tion.

- Moderate dysphagia: capture not effective for removing food from the utensil; escape extraoral presence of more than half the volume given; inefficiency in preparing the bolus in the time expected; residues in the mouth after swallowing, at any volume, with no clearance in swallowing spontaneously; noisy cervical auscultation, with noise clearance after next swallowing; clinical signs suggestive of laryngeal penetration and/or tracheal aspira-tion such as coughing and throat clearing, with apparent clearance of the airways.

- Severe dysphagia: capture not effective for removing food from the utensil; escape extraoral presence of more than half the volume given; inefficiency in preparing the bolus at the expected time; residues in the mouth after swallowing, at any volume, with no clearance in swallo-wing spontaneously; cervical auscultation noisy without clearance the noise; presence of clinical signs suggestive of laryngeal penetration and/or tracheal aspiration without apparent clearance airway.

Statistical analysis

The Jonckheere-Terpstra test(11) was applied to detect dif-ferences between the five motors levels and the diagnoses of dysphagia, when compared simultaneously, to the variables of time in both food consistencies offered. The data obtained were compared with the literature. Fixed at 0.05 or 5% the significance level

RESULTS

The mean time for swallowing to the 50 children of this study was 1.33 seconds for the liquid consistency and 3.33 seconds for the pasty. The higher the motor level, that is, the more severe motor impairment, longer the time for swallowing in liquid consistency, with a significant difference (p<0.001) between groups. To paste consistency, the difference found between the groups was statistically similar (Table 1).

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Table 1. Oral transit time, in seconds, of children with cerebral palsy, in the liquid and pasty consistencies, according to motor level by the GMFCS

Consistency Motor level n Mean SD Minimum Maximum p-value

Liquid

I 10 0.62 0.25 0.26 1.03

<0.001

II 10 0.98 0.50 0.32 2.26

III 10 1.09 0.58 0.25 1.79

IV 10 1.42 0.72 0.63 2.73

V 10 2.55 1.56 0.91 6.18

Total 50 1.33 1.05 0.25 6.18

Pasty

I 10 3.06 1.06 1.44 4.54

0.070

II 10 2.19 1.18 0.70 4.80

III 10 2.88 2.25 0.80 7.09

IV 10 2.93 1.34 1.01 5.19

V 10 5.59 3.19 1.05 10.91

Total 50 3.33 2.23 0.70 10.91

Note: The mean shown in the table is the sum of the oral transit times of all patients that level motor divided by the total number of patients in the same level. Jonckheere-Terpstra test (p<0.001for liquid and p=0.070 for pasty)

Note: SD = standar desviation; GMFCS = Gross Motor Function Classification System

Table 2. Oral transit time, in seconds, of children with cerebral palsy, in the liquid consistencies, according to impairment of swallowing

Time

Swallow n Mean SD Minimum Maximum p-value

Normal 31 0.87 0.47 0.25 2.26

<0.001

Mild dysphagia 6 1.40 0.62 0.82 2.47

Moderate dysphagia 7 2.14 0.89 0.91 3.30

Severe dysphagia 6 2.69 1.92 1.06 6.18

Total 50 1.33 1.05 0.25 6.18

Jonckheere-Terpstra test (p<0.001)

Note: SD = standard desviation

Table 3. Oral transit time, in seconds, of children with cerebral palsy, in the pasty consistencies, according to impairment of swallowing

Time

Swallow n Mean SD Minimum Maximum p-value

Normal 31 2.32 1.09 0.70 4.80

<0.001

Mild dysphagia 9 3.41 1.75 1.05 7.09

Moderate dysphagia 10 6.39 2.55 3.40 10.91

Severe dysphagia 50 3.33 2.23 0.70 10.91

Jonckheere-Terpstra test (p<0.001)

Note: SD= standard desviation

groups, with a gradual increase time as increasing severity of swallowing impairment (Tables 2 and 3)

DISCUSSION

Children with neurodevelopmental disorders, such as the CP, spina bifida, or inborn errors of metabolism, often have associated gastrointestinal disorders, such as oromotor dys-functions that lead to feeding difficulties, risk of aspiration and prolonged meal time and malnutrition(12).

The oral transit time is an important indicator of the severity of impaired swallowing function in children with neuromotor disorders, as it can represent one of the major aspects which lead to malnutrition. In children with moderate and severe impairment CP feeding disorders are common problems associated with poor nutritional status and health. Even children with mild eating disorders, which require ma-shed food, may be at risk of malnutrition(13).

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presents itself increased, can facilitate directing the conduct, particularly with respect to changes in food consistency and indication of feeding tubes. Early identification of clinical signs of dysphagia can facilitate their treatment, and referrals and instrumental evaluations when necessary(14). The indica-tion feeding tubes in children with neuropathy and dysphagia becomes necessary in front of clinical changes. A significant reduction in parental concern in relation to nutritional status of their children after gastrostomy, is followed by the per-ception of improvement in clinical conditions and significant reduction in the time spent to feeding(15).

Study in the literature(10) analyzed the time to swallow the liquid consistency in 15 normal children, divided into three groups according to age. Among other aspects, the authors called time measures of oral phase, regarding to filling oral and oral transit time. Taking in consideration the Group III of the study of literature, formed by four children 2-4 years old, were found the mean time of 0.58 ± 0.13 to 1.63 ± 1.56 seconds for filling oral and 0.66 ± 0.24 to 1.79 ± 1.96 seconds for oral transit time.

Comparing the data of the liquid consistency of this rese-arch to the study cited(10), there was considerable increase in time of swallowing of children with CP, compared with normal children. When we selected the preparation and transit time in children with motor level V, according to the GMFCS, those with higher global motor impairment and oropharyngeal, the difference was even higher, with a mean of 2.55 ± 1.56 seconds to liquid consistency and 5.59 ± 3.19 for pasty con-sistency. No studies were found to compare the data recorded for swallowing paste consistency with normality.

In a study(16), 45 children with spastic cerebral palsy, there was the mean of total time spent feeding during a day of < 1 hour in 24%, and > 4 hours in 7% of children. However, the feed most frequently took 2-4 hours in 42% and approximately 2 hours in 27% of the children.

In comparing the time for swallowing the liquid consis-tency between the groups of children, divided according to the GMFCS motor level, a significant difference was observed, with higher values for higher levels of motor impairment, IV and V. This finding reinforces the clinical observation of more severe oral motor impairment in children with higher motor levels, that is, with a more severe global motor. Thus, it is expected to occur most severe cases of dysphagia, with a more severe clinical impairment in a nutritional viewpoint, in children for the IV and V motor level, due to the increased time taken during swallowing. Research conducted(17), finds the correlation between the severity of swallowing disorders and type of CP.

As noted, the disorders that affect the oropharyngeal

phase occurs mainly in children with severe motor disorders – quadriplegia. Literature study also verifies that dysphagia is strongly related to global motor functions in children with CP and the impairments in swallowing function are often found in more severe motor disorders(18).

Research of the literature(19) noted that there was a gra-dual relationship between dysphagia and GMFCS levels, increasing the probability of occurrence children in level V, compared with children of level I.

Children with severe CP with severe oromotor impair-ments, showed significant and generalized alterations in feeding, which demonstrate some fluctuations over time, but usually shows stability. Children with CP without oral motor impairment and those who have mild to moderate impairment, also show little or no change over time and less problems when compared to children with severe impairment(20). The oral motor difficulties and the alterations in feeding are related to the gross motor function(21,22).

The same statistical significance was not found for the pasty consistency, which does not reflect what was observed clinically. Analyzing the data, it was found that the signi-ficance has not occurred due to swallowing time found in the group of children motor level I, which showed close to group IV motor level. In the other groups (II to V) observed a progressive increase as higher motor level. According to the data, the ten children with motor level I, nine had nor-mal swallowing and one mild oropharyngeal dysphagia. It is believed that the increased in time swallowing of these children does not come from oral motor deficits, but rather due to the reduction of attention during the offer and longer duration of oral manipulation performed, seeking more time to taste the food, since during evaluation revealed that the children remained with the food in the oral cavity without manipulating it voluntarily.

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Comparing the values of oral transit time for liquid and paste of children with normal swallowing according to the clinical evaluation of this research, with the data of normal children of age group around the study cited above(10), there are similarity to the time data for swallowing the liquid. Thus, it is found that children with CP and lower levels motors, ac-cording to the GMFCS may present normal swallowing. The same result was not observed for the pasty consistency, due to voluntary behavior to keep the food in the oral cavity without manipulating it, seen among the children of the motor level I, as already explained. However, despite the similarity of the results with normality, it is recommended conducting clinical evaluation in children of lower levels of GMFCS motors, sin-ce two children, one motor level I and one level II had mild dysphagia. Dysphagia is present at all levels of the GMFCS, demonstrating the need to undertake early assessments and screenings in children with CP, promoting nutritional gains and respiratory stability(19).

CONCLUSION

The oral transit time in children with cerebral palsy was found increased to the food consistency offered, and may represent the severity of dysphagia presented, since that time was was longer as worse the impairment in swallowing function, and patients who took the longest were classified as having severe dysphagia. As the higher global motor impair-ment presented, that is, the higher the classification level of the GMFCS, the longer oral transit time presented.

REFERENCES

1. Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, Damiano D, et al. A report: the definition and classification of cerebral palsy April 2006. Dev Med Child Neurol Suppl. 2007;(109):8-14. 2. Avivi-Arber L, Martin R, Lee J-C, Sessle BJ. Face sensorimotor

cortex and its neuroplasticity related to orofacial sensorimotor functions. Arch Oral Biol. 2011;56(12):1440-65.

3. Parkes J, Hill N, Platt MJ, Donnelly C. Oromotor dysfunction and communication impairments in children with cerebral palsy: aregister study. Dev Med Child Neurol. 2010;52(12):1113-9. 4. Erasmus CE, van Hulst K, Rotteveel JJ, Willemsen MAAP, Jongerius

PH. Clinical practice: swallowing problems in cerebral palsy. Eur J Pediatr. 2012;171(3):409-14.

5. Furkim AM, Behlau MS, Weckx LLM. Avaliação clínica e videofluoroscópica da deglutição em crianças com paralisia cerebral tetraperética espástica. Arq Neuropsiquiatr. 2003;61(3-A):611-6. 6. Han TR, Bang MS, Chung SG, Shin HI, Jeon JY. The pattern of

malnutrition in cerebral palsy and relating factors. J Korean Acad

Rehabil Med. 2001;25(1):18-25.

7. Spadotto AA, Gatto AR, Cola PC, Montagnoli AN, Schelp AO, Silva RG, et al. Software para análise quantitativa da deglutição. Radiol Bras. 2008;41(1):25-8.

8. Molfenter SM, Steele CM. Temporal variability in the deglutition literature. Dysphagia. 2012;27(2):162-77.

9. Palisa R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to clarify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39(4):214-23.

10. Weckmueller J, Easterling C, Arvedson J. Preliminary temporal measurement analysis of normal oropharyngeal swallowing in infants and young children. Dysphagia. 2011;26(2):135-43.

11. Jonckheere AR. A distribution-free k-sample test again ordered alternatives. Biometrika.1954;41:133-45.

12. Sullivan PB. Gastrointestinal disorders in children with neurodevelopmental disabilities. Dev Disabil Res Rev. 2008;14(2):128-36.

13. Fung EB, Samson-Fang L, Stallings VA, Conoway M, Liptak G, Henderson RC, et al. Feeding dysfunction is associated with poor growth and health status in children with cerebral palsy. J Am Diet Assoc. 2002;102(3):361-73.

14. Calis EAC, Veugelers R, Sheppard JJ, Tibboel D, Evenhuis HM, Penning C. Dysphagia in children with severe generalized cerebral palsy and intellectual disability. Dev Med Child Neurol. 2008;50(8):625-30.

15. Sullivan PB, Juszczak E, Bachlet AME, Lambert B, Vemon-Roberts A, Grant HW, et al. Gastrostomy tube feeding in children with cerebral palsy: a prospective, longitudinal study. Dev Med Child Neurol. 2005;47(2):77-85.

16. Soylu OB, Unalp A, Uran N, Dizdarer G, Ozgonul FO, Conku A, et al. Effect of nutritional support in children with spastic quadriplegia. Pediatr Neurol. 2008;39(5):330-4.

17. Otapowicz D, Sobaniec W, Okurowska-Zawada B, Artemowicz B, Sendrowski K, Kulak W, et al. Dysphagia in children with infantile cerebral palsy. Adv Med Sci. 2010;55(2):222-7.

18. Kim JS, Han ZA, Song DH, Oh H-M, Chung ME. Characteristics of dysphagia in children with cerebral palsy, related to gross motor function. Am J Phys Med Rehabil. 2013;4(ahead of print).

19. Benfer KA, Weir KA, Bell KL, Ware RS, Davies OS, Boyd RN. Oropharyngeal dysphagia and gross motor skills in children with cerebral palsy. Pediatrics. 2013;131(5):1553-62.

20. Clancy KJ, Hustad KC. Longitudinal changes in feeding among children with cerebral palsy between the ages of 4 and 7 years. Dev Neurorehabil. 2011;14(4):191-8.

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22. Waterman ET, Koltai PJ, Downey JC, Cacace AT. Swallowing disorders in a population of children with cerebral palsy. Int J Pediatr Otorhinolaryngol. 1992;24(1):63-71.

Imagem

Table 2.  Oral transit time, in seconds, of children with cerebral palsy, in the liquid consistencies, according to impairment of swallowing

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