Athetosis

Effect of Upper Extremity Posturing on Measured Resting Energy Expenditure of Nonambulatory Tube-Fed Adult Patients With Severe Neurodevelopmental Disabilities*

ABSTRACT. Purpose: To ascertain the effect of upper extremity posturing on measured resting energy expenditure (MEE) for patients with severe neurodevelopmental disabilities. Methods: Twenty-four nonambulatory adult patients with severe neurodevelopmental disabilities referred for evaluation of enteral tube feeding and who had a steadystate MEE performed were studied. Steady-state indirect calorimetry measurements were done through a canopy system. Patients were stratified according to the topography of their neuromotor impairment and motor function as having either fixed upper extremity contractures (Fixed UE) or with preservation of limited functional and nonfunctional upper extremity movement (Preserved UE). Results: Despite a similar age, weight, height, and gender distribution between groups, those patients with Fixed UE (n = 13) had a signif

icantly lower MEE than those with Preserved UE (n = 11): 893 +/- 91 versus 1144 +/- 262 kcal/d (p

*Presented in part at the 26th A.S.P.E.N. Clinical Congress, February 26, 2002, San Diego, California.

Patients with severe neurodevelopmental disabilities are at risk for malnutrition because of inadequate intake and numerous medical problems including gastroesophageal reflux disease, swallowing disorders, chronic infections, and severe neuromotor impairment.1-12 Many adult patients with severe neurodevelopmental disabilities have severe growth stunting and abnormalities in both skeletal and muscular development. As a result, defining the appropriate amount of calories to give the adult patient with severe neurodevelopmental disabilities is particularly problematic, because estimates of energy expenditure from equations such as the Harris-Benedict and World Health Organization (WHO) equations were developed in normal healthy subjects. There is very limited information regarding energy requirements of adult patients with cerebral palsy,13-15 despite that most children with cerebral palsy are expected to survive until adulthood.16 There is even less information regarding energy needs of the most severely affected adults who have severe neuromotor involvement resulting in dysphasia, delayed gastric emptying, and severe reflux disease requiring tube feeding by a permanent enterostomy.13

In a previous study, we found that the measured energy expenditure (MEE) of nonambulatory, tube-fed patients with severe neurodevelopmental disabilities was significantly lower than the Harris-Benedict and WHO equations.13 However, not all patients with cerebral palsy are similar in energy requirements, because differences in ambulation, differences in muscle atrophy, and presence of athetosis influence energy expenditure.14,15,17 Some patients have more extensive disease, resulting in fixed upper extremity contractures, whereas others may have preservation of limited functional and nonfunctional upper extremity movement. About two-thirds of our population of patients with severe neurodevelopmental disabilities who need enteral feeding by permanent ostomy have fixed upper extremity contractures. The intent of this study was to ascertain whether the absence of functional and non-- functional upper extremity movement significantly alters resting energy for nonambulatory, tube-fed adult patients with severe neurodevelopmental disabilities.

CLINICAL RELEVANCY

This paper evaluates the MEE of nonambulatory, tube-fed patients with cerebral palsy with preservation of limited functional and nonfunctional upper extremity movement compared with those with fixed upper extremity contractures. These data indicate significant differences in energy expenditure between the groups of patients, evaluates energy expenditure relative to fat-free mass (FFM), and provides some practical guidelines for estimating energy requirements in these populations.

MATERIALS AND METHODS

Adult patients, greater than or equal to 18 years of age, referred to the Nutrition Support Consultative Services for evaluation of enteral tube feeding through a permanent ostomy at a 380-bed, regional state-- funded, residential center for persons with developmental disabilities (Arlington Developmental Center, Arlington, TN) were reviewed for potential inclusion into the study. Resting energy expenditure and a patient assessment were conducted as part of the routine clinical care of these patients. Patients excluded from study entry were those with malignancy, infection requiring systemic antibiotic therapy, admission to the infirmary (a nursing ward for intensive patient observation) within 5 days before the measurement, fever (otic temperature > 38 deg C), hypothermia (otic temperature

A patient assessment was conducted for all individuals referred to the nutrition support service. This assessment included estimation of total body fat from skinfold thickness measurements because they correlate strongly with percentage of body fat for patients with cerebral palsy.4,17,18 The multiple skinfold technique of Slaughter et al19 was used to estimate percentage of body fat.4,13 FFM was calculated by subtracting body fat weight (derived from percentage of body fat) from current body weight. Laboratory data, body weight, height, physical evidence of hydration status, and abdominal activity (presence of distension, bowel sounds, bowel movements) were also evaluated. Measurement of body weight was determined while the patients were in light clothing with the use of a body sling. The patients' height or length was estimated using a flexible tape measure in short straight segments along the bony prominences of the body while the patient was supine. This method has been shown to be more reproducible than other methods such as calculating length with a measuring board.10

All patients in this study were classified as having severe cerebral palsy because they were nonambulatory and their self-care skills were inadequate, requiring that they be institutionalized. Patients were furthered grouped according to the topography of their neuromotor impairment and motor function. Patients were either considered as having cerebral palsy with fixed upper extremity contractures or as having cerebral palsy with severe neuromotor impairment with preservation of limited functional and nonfunctional upper extremity movement. The latter group included those persons with dyskinetic quadriplegia, mixed dyskinetic spastic quadriplegia, and spastic diplegia. Patients in the latter group could include those with dystonia, chorea, or athetosis. Patients with ballismus were excluded because of the extreme difficulty in measuring energy expenditure with a canopy system in these individuals. Management of contractures and spasticity included therapeutic positioning, splinting, physical therapy, and medications including baclofen, dantrolene, and diazepam.

A steady-state indirect calorimetry measurement using a computer-interfaced, ventilated canopy system to determine oxygen consumption, carbon dioxide production, respiratory quotient, and resting energy expenditure was conducted for each patient. The patient's blood oxygen saturation was constantly monitored by a pulse oximeter during the indirect calorimetry measurement. The MetaScope Metabolic Cart II (Sensormedics, Yorba Linda, CA) was used for the indirect calorimetry measurements. The MetaScope Metabolic Cart II has a differential paramagnetic oxygen analyzer accurate to 0.01% on a scale of 1% to 100% for measured inspired and expired oxygen concentrations, infrared carbon dioxide analyzer, Fleish pneumotachometer, and a baffled 3-L mixing chamber. The indirect calorimetry measurements were performed in 20-minute intervals up to a maximum of 3 intervals per patient until steady-state measurements were achieved. Inspired oxygen and carbon dioxide fractions were performed during the initial and final 2 minutes of the interval. Expired oxygen and carbon dioxide fractions were measured during the middle 16 minutes of the interval. Initial and terminal inspiratory gas fraction values were averaged and used as the mean Fio^sub 2^ and Fico^sub 2^ values for the interval. This process provides adjustments for the effects of small variations in Fio^sub 2^ and Fico^sub 2^, barometric pressure, and minor analyzer drifts.20 Gas analyzers were calibrated immediately before each measurement using 95% oxygen/5% carbon dioxide and 100% nitrogen reference gases. Daily pneumotachometer calibration was conducted using a 3-L syringe; 3 consecutive determinations with

During the indirect calorimetry measurement, the patient was verbally comforted by the presence of their familiar caretaker (developmental disabilities technician) in an effort to reduce any anxiety from being within the canopy. Some minor voluntary or involuntary movement by the patient was allowed and no attempt was made to restrain the patient. Patients were provided with a continuous infusion of enteral nutrition support with minimal (

Continuous data were expressed as mean +/- SD. All statistical analyses were conducted using SPSS for Windows, version 6.1 (SPSS, Inc, Chicago, IL). Differences in pair-wise comparisons were conducted using the Mann-Whitney U test. All nominal data were tested for statistical significance with Fisher's exact test or chi^sup 2^ test of homogeneity. The Wilcoxon matched-- pairs signed-rank test was used for pair-wise comparisons between the MEE and predicted energy expenditure by the Harris-Benedict equations. Goodness of fit of the linear model between 2 variables was assessed from the coefficient of determination (r^sup 2^) that was derived from linear correlation using the Pearson product moment correlation coefficient. After construction of a correlation matrix to determine which factors significantly contribute to the variance in the MEE, analysis of covariance was employed to test for adjusted means for energy expenditure between groups using the most significant factors as the covariates. The parallelism of the regression lines between those with fixed upper extremity contractures and preserved upper extremity movement was compared by a test of homogeneity of the slopes. The rationale and technique for evaluating MEE by analysis of covariance and normalization of the data based on significant covariates has been described elsewhere.29-31 The significance testing and reported p values were 2-sided for all variables. A probability value

RESULTS

Thirty patients were initially evaluated for study inclusion. Six patients did not achieve steady state during the indirect calorimetry measurement after multiple attempts and were dropped from enrollment. Two of the 6 patients had fixed upper extremity contractures, whereas the remaining 4 patients had upper extremity movement. The latter 4 patients were physically active during the measurement or became agitated during the measurement, necessitating discontinuation of the indirect calorimetry measurement. The remaining 24 nonambulatory tube-fed patients with severe neurodevelopmental disabilities who achieved steady state were used for evaluation. Thirteen of the patients were noted to have fixed upper extremity contractures, and 11 had limited functional and nonfunctional upper extremity movement. All patients were nonambulatory. Patients received an enteral tube feeding infusion for 18 to 24 hid. Average caloric intake for both groups was 1465 +/- 339 kcal/d or 1.48 +/- 0.29 times the MEE. Protein intake averaged 61 +/- 14 g/d or 1.60 +/- 0.45 g/kg per day. Both groups were similar (p = N.S.) in age, height, weight, percentage of body fat, body surface area, body temperature, serum albumin concentration, FFM, caloric intake (percentage of MEE), and protein intake (grams per kilogram per day) as given in Table I. The distribution of male and female patients for each group was also similar with 4 female patients in each group (Table I; p = N.S.).

Indirect calorimetry measurements and normalized resting energy expenditure parameters are provided in Table II. A significant decrease in oxygen consumption and carbon dioxide production was evident for those with fixed upper extremity contractures compared with those with preserved upper extremity movement (p

The mean MEE (kilocalories per day) for those with fixed upper extremity contractures was 28% less than those with preserved limited functional and nonfunctional upper extremity movement (p 110% of predicted (Fig. 1).

To ascertain which variables might best explain the observed variation in MEE, a correlation matrix was constructed from the variables for the entire population and separately for each group (Table III). These data indicate that neither age, height, weight, body surface area, percentage of body fat, nor FFM had a significant correlative effect with MEE for patients with fixed upper extremity contractures. However, height, weight, body surface area, and FFM had significant correlative relationships with MEE for patients with preserved upper extremity movement. FFM had among the highest correlative relationship of all the variables with MEE (Table III and Fig. 2); however, the mean FFM in the preserved upper extremity movement group was slightly greater than the fixed upper extremity group (Table I). Figure 2 illustrates the relationship between MEE and FFM for both groups. Patients with preservation of upper extremity movement exhibited a significant linear relationship between MEE and FFM (r^sup 2^ = .655, p = .003; Fig. 2). However, patients with fixed upper extremity contractures had a poor relationship between MEE and FFM (r^sup 2^ = .062, p = N.S.), and MEE was highly variable for any given amount of FFM. Analysis of covariance with FFM as the covariate demonstrated the regressions to be significantly different from each other (p

The respiratory quotients (RQ) ranged from 0.76 to 0.94, suggesting none of the patients were overfed or experienced hyperventilation at the time of the measurement. This variability in RQ could be explained by timing of the measurements in relation to feeding as not all of the patients were being fed at the time of measurement (Table IV). Although no significant differences in any of the indirect calorimetry variables were observed for the fed versus un-fed groups, the mean RQs expectedly were slightly higher in the fed groups (Table IV). Energy expenditure was about 5% higher in the fed group for those patients with fixed upper extremities; however, energy expenditure was lower by about 20% in the fed group for those with preserved upper extremities. This conflicting observation was likely caused by the limited number of subjects in each group of this subanalysis, and further study is required.

DISCUSSION

Assessing the energy needs of adult patients with severe neurodevelopmental disabilities is challenging. Unfortunately, there are extremely limited data regarding energy needs of adults with neurodevelopmental disabilities.l3-15 The severity of the disease and the extent of ambulation are important factors affecting the energy requirements of adult patients with neurodevelopmental disabilities.3,13-15,17 Our data indicate that nonambulatory, tube-fed adult patients with fixed upper extremity contractures have a lower caloric expenditure than those with preservation of limited functional and nonfunctional upper extremity movement. Despite similar predicted energy expenditures based on the Harris-Benedict equations, those with fixed upper extremity contractures had a 28% lower MEE than those with preservation of upper extremity movement (Table III). Most patients with fixed upper extremity contractures were

Although energy expenditure is conventionally expressed in terms of predicted energy expenditure, body weight, FFM, or other mathematical ratios such as those listed in Table II, the validity of these methods for normalization of resting energy expenditure has been questioned.30 It has been argued that the ratio method does not take into account the non-zero gamma intercept of the relationship between MEE and a given variable. Therefore, the ratio method does not fully remove the effect of the variable (eg, body weight and FFM) and may lead to erroneous results. As a result, it has been suggested that analysis of covariance be used to normalize MEE.

This observation of differing energy expenditures based on absence of upper extremity movement may be explained by the fact that patients with fixed upper extremity contractures are likely to have less upper body muscle mass,4 and possibly, a lower energy expenditure.3,32 Although weight and FFM tended to be greater in those with upper extremity movement, these differences were not statistically significant (Table II). Figure 2 depicts the relationship between MEE and FFM for both populations and provides further insight regarding differences in energy expenditure between groups. As FFM increases, resting energy expenditure increases linearly at a mean rate of about 24 kcal/kg FFM for those patients with limited functional and nonfunctional upper extremity movement. However, for those individuals with fixed upper extremity contractures, MEE was not significantly correlated with amount of FFM (Table III; Fig. 2). Differences in resting energy expenditure by normalization of the MEE to FFM with the use of the regression modeling techniques of Poehlman and Toth and Toth et al30,31 supports true differences of MEE between groups that is independent of FFM (Table II; Fig. 2). Our data also suggest that the Harris-Benedict equations may provide a reasonable estimate for determining resting energy expenditure in nonambulatory tube-- fed adult patients with preservation of limited functional and nonfunctional upper extremity movement. However, the Harris-Benedict equations should not be used in those patients with fixed upper extremity contractures.

Our data parallel the findings of Azcue et al,10 who examined energy expenditure and body composition of children with spastic quadriplegic cerebral palsy compared with normal healthy children of similar age. Children with spastic quadriplegia had a significantly lower MEE and FFM and lower MEE normalized to FFM when compared with healthy control children. In addition, height, weight, or any body compartments including FFM could not explain the variability in MEE of patients with spastic quadriplegia. Our findings regarding differences in MEE based on preservation of upper extremity movement are further supported by Johnson et al.14 Their data indicated that adult patients with cerebral palsy who had athetotic movements had a 14% higher energy expenditure (adjusted to FFM) when compared with normal control subjects.14 Application of their regression analysis formula regarding estimation of resting energy expenditure in our population resulted in a gross overestimation of our patients' actual MEE. This error may be explained by differences in our patient populations. Despite a similar age between our study population and Johnson's population,14,15 our population tended to be shorter, lighter, and have less FFM. Our entire population was institutionalized and nonambulatory. In addition, all patients in our population had to be fed by tube feedings through a permanent enterostomy because of severe oral-motor impairment, swallowing dysfunction, or decreased gastroesophageal motility with a history of repeated hospitalizations for aspiration pneumonia. As a result, our patients were fed either by gastrostomy with inclusion of prokinetic pharmacotherapy, gastrostomy with Nissan fundiplication, or by a jejunostomy. Therefore, it is evident that our patient population represents those adult patients with more severe or advanced disease and complements rather than conflicts with the data of Johnson et al.14,15

Gender is another consideration that needs to be taken into account in interpretation of MEE data. Gender could be potentially confounding because resting metabolic rate is lower in healthy women than in men and that these differences seem to be independent of differences in body composition and aerobic fitness.29 However, the distribution of women in both groups were similar for both populations (p = N.S.; Table I), and it is unlikely that gender confounded our data. Unfortunately, the number of subjects in this study prohibits meaningful subanalysis of these data based on gender.

The physiologic mechanisms for observed decrease in MEE for patients with fixed upper extremity contractures were not examined in this study and are unclear in the literature. Hypothyroidism was ruled out as a potential etiology by evaluation of serum thyroxin and thyroid stimulating hormone levels. Azcue et al10 has suggested that perhaps an alteration in the sympathetic nervous system or centrally mediated catecholamine regulation may be the etiology of this lower metabolic rate in patients with more severe neurodevelopmental disease. However, direct evidence for these hypotheses are lacking, and further research is necessary to elucidate the pathogenesis for this aberration in energy metabolism.

Because total energy expenditure is highly variable and greater than resting energy expenditure for patients with cerebral palsy,15,17 it is recommended that initial caloric goals modestly exceed estimated resting energy expenditure for weight maintenance or weight gain. Patients should be closely followed to insure nutritional outcome goals are achieved. Caloric intake should be more conservative for those nonambulatory tube-fed adult patients with fixed upper extremity contractures compared with those with preservation of limited functional and nonfunctional upper extremity movement.

CONCLUSION

Estimation of caloric expenditure of nonambulatory, tube-fed patients with severe neurodevelopmental disabilities should be differentiated according to extent of upper extremity movement. Patients with fixed upper extremity contractures had a significantly lower MEE than patients who had preservation of limited functional and nonfunctional upper extremity movement. The measured resting energy expenditure of nonambulatory tube-fed patients with severe neurodevelopmental disabilities and fixed upper extremity contractures was significantly lower than predicted by the Harris-- Benedict equations.

REFERENCES

1. Brown RO, Dickerson RN, Hak EB, et al: Impact of a pharmacist-- based consult service on nutritional rehabilitation of nonambulatory patients with severe developmental disabilities. Pharmacotherapy 17:796-800, 1997

2. Stallings VA, Charney EB, Davies JC, et al: Nutrition-related growth failure of children with quadriplegic cerebral palsy. Dev Med Child Neurol 35:126-138, 1993

3. Stallings VA, Zemel BS, Davies JC, et al: Energy expenditure of children and adolescents with severe disabilities: A cerebral palsy model. Am J Clin Nutr 64:627-634, 1996

4. Stallings VA, Cronk CE, Zemel BS, et al: Body composition in children with spastic quadriplegic cerebral palsy. J Pediatr 126: 833-839, 1995

5. Stallings VA, Charney EB, Davies JC, et al: Nutritional status and growth of children with diplegic or hemiplegic cerebral palsy. Dev Med Child Neurol 35:997-1006, 1993

6. Thommessen M, Kase BF, Riis G, et al: The impact of feeding problems on growth and energy intake in children with cerebral palsy. Eur J Clin Nutr 45:479-487, 1991

7. Rempel GR, Colwell SO, Nelson RP: Growth in children with cerebral palsy fed via gastrostomy. Pediatrics 82:857-862, 1988 8. Evers S, Munoz MA, Vanderkooy P, et al: Nutritional rehabili

tation of developmentally disabled residents in a long-term-care facility. J Am Diet Assoc 91:471-473, 1991

9. Rogers B, Stratton P, Msall M, et al: Long-term morbidity and management strategies of tracheal aspiration in adults with severe developmental disabilities. Am J Ment Retard 98:490498, 1994

10. Azcue MP, Zello GA, Levy LD, et al: Energy expenditure and body composition in children with spastic quadriplegic cerebral palsy. J Pediatr 129:870-876, 1996

11. Patrick J, Pencharz PB, Belmonte M, et al: Undernutrition in children with neurodevelopment disability. Can Med Assoc J 151:753-759, 1994

12. Wilson DC, Pencharz PB: Nutritional care of the chronically ill. IN Nutrition During Infancy: Birth to 2 Years, Tsang R (ed). Digital Educational Publishing, Inc, Cincinnati, OH, 1997, pp 37-56

13. Dickerson RN, Brown RO, Gervasio JG, et al: Measured energy expenditure of tube-fed patients with severe neurodevelopmental disabilities. J Am Coll Nutr 18:61-68, 1999

14. Johnson RK, Goran MI, Ferrara MS, et al: Athetosis increases resting metabolic rate in adults with cerebral palsy. J Am Diet Assoc 96:145-148, 1996

15. Johnson RK, Hildreth HG, Contompasis SH, et al: Total energy expenditure in adults with cerebral palsy as assessed by doubly labeled water. J Am Diet Assoc 97:966-970, 1997

16. Evans PM, Evans SJ, Alberman E: Cerebral palsy: Why we must plan for survival. Arch Dis Child 65:1329-2333, 1990

17. Bandini LG, Schoeller DA, Fukagawa NK, et al: Body composition and energy expenditure in adolescents with cerebral palsy or myelodysplasia. Pediatr Res 29:70-77, 1990

18. Hildreth HG, Johnson RK, Goran MI, et al: Body composition in adults with cerebral palsy by dual-energy X-ray absorptiometry, bioelectrical impedance analysis, and skinfold anthropometry compared with the 180 isotope-dilution technique. Am J Clin Nutr 66:1436-1442, 1997

19. Slaughter MH, Lohman TG, Boileau RA, et al: Skinfold equations for estimation of body fatness in children and youth. Hum Biol 60:709-723, 1988

20. Thureen PJ, Phillips RE, DeMarie MP, et al: Technical and methodologic considerations for performance of indirect calorimetry in ventilated and nonventilated preterm infants. Crit Care Med 25:171-180, 1997

21. Feurer ID, Crosby LO, Mullen JL: Measured and predicted energy expenditure in clinically stable patients. Clin Nutr 3:27-34, 1984 22. Weir JDV: New methods for calculating metabolic rate with

special reference to protein metabolism. J Appl Physiol (Lond) 109:1-9, 1949

23. Dickerson RN, Rosato EF, Mullen JL: Net protein anabolism with hypocaloric parenteral nutrition in obese stressed patients. Am J Clin Nutr 44:747-755, 1986

24. Dickerson RN, Guenter PA, Gennarelli TA, et al: Increased contribution of protein oxidation to energy expenditure in head-- injured patients. J Am Coll Nutr 9:86 - 88, 1990

25. Dickerson RN, Vehe KL, Mullen JL, et al: Resting energy expenditure in patients with pancreatitis. Crit Care Med 19:484-490, 1991

26. Dickerson RN, White KG, Curcillo PG, et al: Resting energy expenditure of patients with gynecologic malignancies. J Am Coll Nutr 14:448-454, 1995

27. Dickerson RN, Gervasio JM, Riley ML, et al: Accuracy of predictive methods to estimate resting energy expenditure of thermally-injured patients. JPEN 26:17-29, 2002

28. Dempsey DT, Knox LS, Mullen JL, et al: Energy expenditure in malnourished patients with colorectal cancer. Arch Surg 121: 789-795, 1986

29. Arciero PJ, Goran MI, Poehlman ET: Resting metabolic rate is lower in women than in men. J Appl Physiol 75:25142520,1993

30. Poehlman ET, Toth MJ: Mathematical ratios lead to spurious conclusions regarding age- and sex-related differences in resting metabolic rate. Am J Clin Nutr 61:482-485, 1995

31. Toth MJ, Goran MI, Ades PA, et al: Examination of data normalization procedures for expressing peak V02 data. J Appl Physiol 75:2288-2292, 1993

32. Zurlo F, Larson K, Bogardus C, et al: Skeletal muscle metabolism is a major determinant of resting energy expenditure. J Clin Invest 86:1423-1427, 1990

Roland N. Dickerson, PharmD*; Rex O. Brown, PharmD*; Debra L. Hanna, MD^; and John E. Williams, MD^

From the *Department of Pharmacy and ^Department of Pediatrics, University of Tennessee Heath Science Center, Memphis; and Arlington Developmental Center, Arlington, Tennessee

Received for publication, August 31, 2001.

Accepted for publication, May 29, 2002.

Correspondence: Dr Roland Dickerson, Department of Pharmacy, University of Tennessee Health Science Center, 26 South Dunlap Street, Memphis, TN 38163.

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