Athetosis

Abstract

Energy requirements of children and adolescents with cerebral palsy appear to be disease-specific and different from the current recommendations for healthy children, varying depending upon functional capacity, degree of mobility, severity of disease, and level of altered metabolism. Feeding problems are prevalent m many of these children, and can result in inadequate energy intake. Wasting of voluntary muscles, a common symptom of cerebral palsy, contributes to reduced resting energy needs; nevertheless, the location of the central nervous system lesion may also influence energy requirements. To guarantee individualized, accurate, and optimal energy recommendations for this population, resting energy expenditure should preferentially be measured by indirect calorimetry. Equations and formulae to predict healthy people's resting energy expenditure are available, but tend to overestimate these children's energy needs. Future studies should address the role of the central nervous system in regulating energy metabolism in this population. When adequately nourished, children and adolescents with cerebral palsy appear more tranquil and require decreased feeding time, which gives caregivers time to develop the child's functional independence and character. Understanding energy requirements of this population will provide caregivers and health professionals with guidelines for providing optimal nutritional status.

(Can J Diet Prac Res 2004; 65:124-130)

Résumé

Les besoins en énergie des enfants et des adolescents souffrant d'infirmité motrice cérébrale semblent liés à la maladie, diffèrent des recommandations pour les enfants en bonne santé et varient selon la capacité fonctionnelle, le degré de mobilité, la gravité de la maladie et le degré d'altération du métabolisme. Les problèmes d'alimentation sont fréquents chez nombre de ces enfants et peuvent entraîner une insuffisance de l'apport énergétique. L'atrophie des muscles striés, symptôme courant de l'infirmité motrice cérébrale, contribue à réduire les besoins énergétiques au repos; néanmoins, l'emplacement de la lésion au système nerveux central peut également influencer ces besoins. Pour garantir à cette population des recommandations en énergie personnalisées, précises et optimales, la dépense énergétique au repos doit être mesurée de préférence par calorimétrie indirecte. On dispose d'équations et de formules pour prédire la dépense énergétique au repos des personnes en bonne santé, mais elles tendent à surestimer les besoins énergétiques de ces enfants. Des études ultérieures devraient porter sur le rôle du système nerveux central dans la régulation du métabolisme énergétique chez cette population. Lorsqu'ils sont nourris adéquatement, les enfants et adolescents atteints d'infirmité motrice cérébrale semblent plus calmes et leur alimentation demande moins de temps, ce qui libère le personnel soignant pour développer leur autonomie fonctionnelle et leur personnalité. La compréhension des besoins énergétiques de cette population fournira au personnel soignant et aux professionnels de la santé des lignes directrices pour assurer un état nutritionnel optimal.

(Rev can prat rech diétét 2004; 65:124-130)

INTRODUCTION

Cerebral palsy (CP) is a persistent, non-progressive brain disorder of infants and children. It is characterized by inadequate muscle tone, abnormal body posture, and disordered body movements (1). The most likely risk factors for CP are low birth weight or birth asphyxia (2). Four main types of CP exist.

The first is spastic CP, characterized by increased muscle tone, and further classified, depending upon the extremities involved, into 1. monoplegia, involving one limb; 2. hemiplegia, involving an arm or a leg on the same side of the body; 3. diplegia, involving the legs predominantly although there may be minor compromised motor function of the arms; 4. quadnplegia, involving all limbs; 5. a combination of all four classifications (1). The second type, athetoid CP, is characterized by decreased muscle tone, with uncontrolled, continuous, involuntary, worm-like movements of the face, neck, and trunk. Usually all four extremities are involved (1). Ataxia is the third type, and involves a disturbed sense of balance and depth perception. The fourth type, mixed CP, exhibits a combination of spastic and athetoid characteristics (1). The prevalence of CP is two per 1,000 live births (2).

Energy recommendations for children and adolescents with CP differ from recommendations for their normal peers, and depend upon the specific medical condition or degree of functional impairment (3-5), marked aberrations in body composition (1,6-10), altered growth patterns (11-12), and decreased mobility (3,5,11). Non-nutritional factors influencing energy requirements include level of physical activity (7,10,12), unit of body cell mass (6,9), decreased blood flow to muscles resulting m diminished muscle use (13), or type of paralysis (7,9,13). Caretakers and health professionals must be aware of this population's disease-specific energy requirements because children with CP are often unable to communicate their hunger and satiety; overfeeding may occur because the caregiver perceives that the child is malnourished (4).

People with CP are often short statured (1,3). To date, whether the short stature is due to genetics, chronic undernutrition, immobility, or a combination of many factors is unclear. Lack of physical activity and limited ability to ambulate also may contribute to the short stature because weight bearing leads to bone and muscle growth (6,14). Level of mobility, degree of ambulation, and muscle tone may affect energy expenditure, bone mineralization, and bone growth (3,14). Drug-nutrient interactions further compromise nutritional status and contribute to growth failure (15-17). Seizures occur in 35-65% of children with CP, and chronic anticonvulsant therapy such as phenobarbital results in accelerated metabolism of vitamins D and K and decreased serum levels of calcium, magnesium, vitamin C, vitamin B6, and folate, all of which further compromise bone growth (15-17).

This population's characteristic short stature led to earlier studies in which energy recommendations were based on height rather than weight (3), because reduced body size should necessitate reduced energy/metabolic needs (6). When compared with normal, healthy peers, children and adolescents with CP usually have been found to have decreased body cell mass, increased extracellular water (6,7,9), and varying levels of body fat (5-7,11). Azcue et al. (9) reported that although resting energy expenditure (REE) was reduced per unit of body cell mass in most subjects with spastic quadriplegia, a few of these children exhibited normal REE per unit of body cell mass. These authors and Pencharz (9,18) concluded that because of the diverse pathophysiology of specific CP types, height, weight, body composition measurements, or even body cell mass could not fully explain the variability in resting energy expenditure. They proposed that the influence of paralysis type and disease on energy regulation needs further study (9,18).

In this paper, we review what is currently known about energy requirements of children and adolescents with CP. We also profile energy assessment methodologies and the factors that alter energy requirements.

Feeding problems and altered energy consumption

Energy requirements are associated with functional capacity and decrease proportionally with disease seventy (3,4,6,10-12,19-23). Feeding problems are common in children and adolescents with CP (24-27); 36% are at risk for malnutrition because of severe oral motor dysfunction (27). The feeding process is prolonged, stressful for both the patient and the caretaker, and slow (25,27), often resulting in weight loss that further increases individual energy requirements (21-31). A multidisciplinary approach to managing and evaluating feeding problems is recommended (1,27). When children or adolescents receive partial or total nutrition through tube feeding, the challenge for caregivers and health professionals is to ensure adequate nutrient intake to meet energy requirements (10,28). Individualized assessment of energy needs is recommended (10-12,26,28-31).

Differing energy requirements

Energy requirements differ with specific CP types. Few authors have investigated energy expenditure in children with athetoid CP. Because of increased physical activity through involuntary movements, non-ambulatory children with athetosis are hyperactive and may have increased energy expenditure (1,23). These children tend to be underweight and emaciated, with decreased muscle tone (1,23). Because of the increased activity, energy requirements of ambulatory children with athetoid CP are expected to be comparable to those of healthy children (16 kcal or 67 kJ/cm height) (1,29). However, more study is needed to establish energy requirements in children with athetosis.

Immobile children with spastic CP, on the contrary, often have lower energy intakes but weigh more than healthy controls (1,6,9,23,32). These children have decreased energy requirements and often become obese despite reduced caloric intake normally appropriate for weight reduction (6,23,30,32). Some authors have reported energy needs of these children as approximately 80% of the recommended dietary allowance (RDA) (10,29).

Culley and Middleton (3) analyzed ten-day food records to study the caloric consumption of moderately to profoundly retarded children with athetoid or spastic CP. These children were well nourished and of normal weight for height. Energy requirements per centimeter of height were reported and found to be similar in all ambulatory CP children with mild to moderate motor dysfunction (3) (Table 1). On the other hand, non-ambulatory children with severe motor dysfunction required about 75% of the energy RDA (29) for healthy ambulatory children of the same height (3) (Table 1). Energy requirements were altered by functional capacity. Most studies have shown that energy needs of children with CP are influenced by severity of disease, altered body composition, level of physical activity, state of malnutrition, or type of paralysis (1,3,6,7,9,10).

Altered body growth and body composition

Because of the altered growth patterns in CP, anthropometric assessment of body height for age, weight for age, and triceps skin folds must be interpreted with caution (1,33). Although height for age is an important index of energy requirements, obtaining reliable measures of height from children with CP is difficult, particularly if they have contractures and cannot stand, have scohosis, and/or have involuntary movements (3,28). To assess linear growth in children with severe developmental disabilities, measuring upper arm length (34), lower leg length (34), or knee height (35) has been recommended.

In obese children, triceps skin-fold measurements are difficult to estimate because tissue may be firm and not easily deformed, or flabby and lacking compressibility. All these characteristics affect the accuracy and reliability of measurements (33,35). In addition, children with CP exhibit erratic movements and have difficulty relaxing during measurement. This further compromises the accuracy of results (26). Finally, skin-fold thickness may lead to an overestimation of body fatness. This is because fat thickness increases over paralyzed limbs (33).

Triceps skinfolds, height for age, and weight for age may be most appropriate for assessing body composition changes in these children (31), as well as outcomes resulting from nutrition intervention (8,31,33,36).

A study on body composition in 142 subjects, who were between two and 18 years old and had spastic quadriplegia CP (SQCP), showed that mean body weight and triceps skin-fold fat stores were 65% of median, subscapular skin-fold fat stores were 81% of median, and muscle stores were 88%) of median (11). Significant reductions in growth and nutritional status indicators, except muscle area, were seen in this population. Energy and nutritional status explained 10-15% of the remaining variation in linear growth (11).

Studies also have shown that children with SQCP who require tube feeding become overweight, consuming energy intake per unit of body weight that is less than the predicted REE (6,38). In subjects with SQCP, weight, stature assessed by alternative methods (34,35), triceps and subscapular skin folds, and upper arm circumference should be monitored to prevent under- and over-nutrition (5,12,36-39).

Indirect calorimetry

Recently, indirect calorimetry has been used to assess the REE or resting metabolic rate (RMR) of both healthy people and those with a wide range of CP types and severity (5,7,9,19,38); total daily energy expenditure (TDEE) has been assessed using the doubly labelled water method (5,7). These techniques provide a more accurate method of assessing energy expenditure patterns. In these studies, TDEE includes energy required for metabolism at rest (REE), the thermic effect of food, and physical activity (5,7,18). Energy for growth can be detected only in rapidly growing infants (18). In most healthy children, REE, determined by body composition and size, accounts for about 65-70% of total energy expenditure (18,40). The ratio of TDEE to REE/RMR is used to assess non-basal energy, or energy required for activity, and the thermic effect of food (7). Fat-free mass comprises extracellular mass plus body cell mass, the latter consisting of skeletal muscle and organ mass (40).

Prediction equations such as the Harris-Benedict equation (HBE) (41), the World Health Organization (WHO) equation (42), and others (43-47) previously have been used to assess healthy people's energy needs. Table 2 shows a comparison between RMR or REE calculated using indirect calorimetry in the CP population, and REE calculated using prediction equations (41,42). Descriptions of the study populations are presented. The REE was in the range of 500 to 1,000 kcal (2,091 to 4,182 kJ) per day versus 756 to 1,200 kcal (3,162 to 5,018 kJ) calculated using prediction equations (5,7,9,19,38), although requirements were disease specific. The authors reported that standardized prediction equations such as the HBE (41), the WHO equation (42), and the Mayo Clinic nomogram (43) overestimate energy needs for individuals with severe central nervous system (CNS) disabilities (38,41-43). The HBE and the WHO equation were reported to give root mean-squared prediction errors of 16-31% and 26-45% in REE, respectively, when applied to tube-fed, non-ambulatory individuals with CP (19); these errors led to an overestimation of energy needs by 121 to 241 kcal per day for the HBE and 137 to 249 kcal per day for the WHO equation. A general formula of REE X 1.1 is suggested for an appropriate estimation of caloric requirement in non-ambulatory, bedridden children with CP (7,9). The REE per unit of body cell mass is reduced in most subjects with CP (9,17,32).

Research has shown that children with SQCP have decreased body cell mass and increased body cell water (6,9,32). The decreased body cell mass may be related to inactivity or malnutrition (6,9,32). In a study of 61 children and adolescents with CP and 37 matched controls, growth failure and abnormal body composition were reported m those with CP (5) (Table 2). Subjects were subdivided into adequately and poorly nourished groups. Basal energy requirements for physical activity and spastic movements were evaluated. Energy and nutrient intake, assessed by three-day records, were over-reported and inaccurate, a finding that demonstrates the difficulty of assessing energy consumption in this population. The REE was assessed by indirect calorimetry, while TDEE was assessed by the doubly labelled water technique (5). Overall, REE, TDEE, and energy for physical activity were lower in children with SQCP than in controls, despite the "volitional" movements of this population (5). Energy for activity was assessed by the ratio of TDEE to REE. The REE adjusted for lean body mass, TDEE, triceps skinfolds or fat stores, as well as energy required for physical activity, were lower in the poorly nourished than in the adequately nourished SQCP group; this result suggests a metabolic response to poor nutritional status (5).

In a group of adolescents with CP, Bandini et al. (7) assessed RMR or REE by indirect calorimetry, and TDEE via the doubly labelled water method. Assessment of fat-free body mass was also reported. In most healthy adolescents, REE or RMR was found to be 61-87% (mean 73%) of TDEE (7). Both RMR and TDEE were significantly lower in subjects with CP than in healthy adolescent controls. The ratio of TDEE to RMR (=1.8) was similar in ambulatory subjects with CP and controls, while the ratio of TDEE to RMR was lower (=1.2) in non-ambulatory adolescents than in normal controls. The authors reported that energy requirements were reduced in CP because of inactivity and reduced fat-free mass; they suggested that the type of paralysis or brain defect may affect energy metabolism in people with more severe disabilities (7). In this study, one non-ambulatory boy with athetosis required 10.6 kcal/cm height and one ambulatory girl with athetosis required 16.1 kcal/cm height (7), findings that demonstrate the effect of ambulation on energy needs.

Limitations of previous research

Data from earlier studies on energy recommendations for people with CP have been problematic (3,32) because more accurate techniques of assessing energy expenditure, such as indirect calorimetry or the double labelled water method, were unavailable. Because of feeding problems and often multiple caregivers, useful dietary assessment data may be difficult to obtain in this population (5,27). Subjects over-reported food intake (5) and/or under-reported feeding time (27).

Generalizing the results of many studies has been hampered by small numbers of subjects and heterogeneous rather than homogeneous populations of children with CP (7,9,19,26,38). Because of the involuntary movements characteristic of this population, achieving the steady rest state required to perform REE with an indirect calorimeter is difficult.

SUMMARY AND RECOMMENDATIONS

Energy requirements vary with functional capacity, mobility level, disease severity (3-9,47), and, perhaps, type of paralysis or CNS impairment (7,9). More recently, REE has been used to determine energy expenditure accurately. Because access to calorimeters is limited in most health care settings, prediction equations and formulae also have been established for estimating energy needs in this population; however, these equations and formulae do have some degree of error.

In the mid-1980s, Schofield (44) conducted a meta-analysis of 114 studies on determining basal metabolic rate, and developed a set of prediction equations that can be used for clinical populations; the equations use weight alone or both weight and height. These equations are known as the SCHO-HTWT and the SCHO-WT equations. The Schofield formulae have the lowest energy prediction error of available formulae (18,44).

Kaplan et al. (46) found that the SCHO-HTWT equation provided a better prediction of measured energy requirements. Although the SCHO-WT equations have been used, the SCHO-HTWT equations more closely predicted REE in young children (101% ± 23%) and children with failure to thrive (101% ± 20%) or obesity (95% ± 17%). Nonetheless, these equations predicted true REE in only 40% of the clinical subjects (46). Prediction of energy requirements is not recommended in most clinical situations/disease states because indirect calorimetry provides the most accurate REE assessment (46).

Table 1 lists formulae and equations available to assess energy requirements in this population when calorimetry is not available. Ambulatory children with mild to moderate motor dysfunction require about 13.9 kcal/cm height, and non-ambulatory children with severe motor dysfunction require 11.1 kcal/cm height (3). Krick et al. (47) reported a method of calculating energy needs of children with CP, which takes into consideration several different factors and presents a mean energy requirement of 79.4 ± 20.9 kcal/kg body weight (Table 1).

In non-ambulatory children and adolescents, both RMR and TDEE are lower than in healthy children (7,11,38). Individual energy expenditure should be assessed (9) and frequently evaluated (9,11,12,37). Further study is needed to assess whether the type of paralysis in children with CP affects metabolic rate (7,9). Because of the characteristic short stature, increased extracellular water, and reduced muscle mass of this population, prediction equations such as the WHO equation (42), the HBE (41), or the Mayo clinic nomogram (43) are not recommended for quantifying energy requirements (7,9,19). Remembering that body cell mass explains about 82% of the variance in resting energy metabolism is important (42). The TDEE:REE ratio, an index of activity and non-basal energy, may be similar in some ambulatory patients but lower for non-ambulatory people with CP (7,9). Research with accurate techniques to assess energy requirements and nutritional status is needed to establish energy requirements of children with athetoid and other types of CP; extremely low energy recommendations and intakes often make health professionals hesitant to accept the adequacy of these diets.

RELEVANCE TO PRACTICE

Because of severe feeding problems, children and adolescents with CP are at risk for inadequate energy/nutrient intake (4,20-24,27). Individualized energy and dietary prescriptions have improved these children's nutritional status (24,26,29), and reduced hospitalizations and morbidity (24). The challenge for caregivers and health professionals is ensuring that enteral nutrition provides adequate nutrient intake congruent with reduced energy requirements (10). Chronic undernutrition has been associated with decreased immunological factors (1,4), respiratory muscle strength (11-12), attention span and learning, mobility, and energy available for play and rehabilitation (1,12). Preventing energy malnutrition will improve growth as well as functional capacity (11,12,26). When adequately nourished, children and adolescents with CP appear calmer and require decreased feeding time, which gives parents and caregivers time to develop the children's functional independence and character (27,37). If nutritional care is to be adequate, all children and adolescents with CP must be assessed regularly for body growth and composition, feeding skills, and dietary intake (5,8,11,37).

As dietitian-nutritionists, we must encourage the prevention of nutrition-related problems in children with CP. Guidelines for assessing energy requirements are provided in Tables 1 and 2. Indirect calorimetry is the recommended method for assessing energy; nonetheless, Table 1 provides health professionals and dietitians with formulae and equations that have been scientifically assessed and shown to indicate energy requirements when indirect calorimetry is unavailable (3,39,44,47). The REE x 1.1 is probably the most supported formula (9,38). Caregivers and health professionals must understand energy requirements to ensure optimal growth and nutritional status for all children and adolescents with CP (5,11,12,37). Finally, health professionals should provide an interdisciplinary, family-centred approach to treatment (9,27,48).

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S. EILEEN HOGAN, PhD, PDt, School of Nutrition and Dietetics, Acadia University, Wolfville, NS

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