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Impact of malnutrition on gastrointestinal disorders and gross motor abilities in children with cerebral palsy
Brain & Development 29 (2007) 25–29 www.elsevier.com/locate/braindev
Impact of malnutrition on gastrointestinal disorders and gross motor abilities in children with cerebral palsy Angelo Campanozzi a,b, Guglielmo Capano a, Erasmo Miele a, Alfonso Romano a, Goffredo Scuccimarra c, Ennio Del Giudice a, Caterina Strisciuglio a, Roberto Militerni c, Annamaria Staiano a,* a
Department of Pediatrics, University of Naples ‘‘Federico II’’, Via S. Pansini 5, 80131 Naples, Italy b Unit of Pediatrics, University of Foggia, Italy c Child Neurology, Second University of Naples, Italy Received 15 October 2005; received in revised form 18 May 2006; accepted 29 May 2006
Abstract Children with cerebral palsy (CP) often demonstrate abnormal feeding behaviours, leading to reduced food consumption and malnutrition. Moreover, most of them present with gastrointestinal disorders, such as gastroesophageal reflux disease (GERD) and/or chronic constipation (CC), and poor motor function rehabilitation. The aim of our study was to assess the possible relationship between malnutrition and gastrointestinal problems and to evaluate the role of nutrition on their gross motor abilities in a population of children with CP and mental retardation. Patients: Twenty-one consecutive children (10 boys; mean age: 5.8 ± 4.7 years; range: 1–14 years) with CP and severe mental retardation. Methods: Nutritional assessment included the measurement of body mass index (BMI = W/H2), fat body mass (FBM) and fat free mass (FFM). Children with symptoms suggesting GERD underwent prolonged 24 h intraesophageal pH monitoring and/or upper GI endoscopy with biopsies before and after a 6 months of pharmaceutical (omeprazole) and nutritional (20% increment of daily caloric intake) treatments. The motor function was evaluated by ‘‘The Gross Motor Function Measure’’ (GMFM) before and after the 6 months on nutritional rehabilitation. Results: BMI for age was 65° percentile in 11 children (52%) and FBM was 680% of ideal value for height in 15 (71%). GERD was present in 14 children (67%), 9 of them were affected by both GERD and CC. Among children with FBM 6 80%, GERD was present in 11 (73%) and CC in 9 (60%). Considering the group of patients with BMI 6 5° percentile, 9 out of 11 children had GERD (82%) and 7 had CC (64%). Fourteen malnourished children (FBM 6 80%) completed the 6 months nutritional trial. Their starting and final means ± SD BMI were 13.56 ± 1.31 and 14.15 ± 1.85 (p = 0.08), respectively. GMFM values were significantly (p < 0.05) improved in 9/14 pts (Group A), while it remained unchanged in 5/14 pts (Group B). Nine children with GERD and malnutrition completed the 6 months of pharmaceutical and nutritional treatments. Their initial mean ± SD weight was 10.1 ± 2.9 kg, whereas the final mean ± SD weight was 12.7 ± 4 kg (p < 0.05). A marked improvement of GERD was noted in four of nine (44.4%) children. Despite successful nutritional rehabilitation with a BMI achievement of P25° percentile, five of nine (55.5%) patients had persistent GERD when they were taken off the medication. Conclusions: Malnutrition and gastrointestinal disorders are very common in children with cerebral palsy. Improved nutritional status, particularly fat free mass gain, appears to have an impact on motor function in children with CP. Ó 2006 Elsevier B.V. All rights reserved. Keywords: Cerebral palsy; Body composition; Children; Nutrition
*
Corresponding author.Tel.: +39 081 7462679; fax: +39 081 5469811.
0387-7604/$ - see front matter Ó 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.braindev.2006.05.008
26
A. Campanozzi et al. / Brain & Development 29 (2007) 25–29
1. Introduction Cerebral palsy (CP) is a severe disability that is associated with abnormal physical activity, body composition and poor nutritional status. Its prevalence is approximately 2.5/1000 live births and in recent years there is a moderate rise of this value, which is the result of increased survival of very low birth weight infants [1]. Apart from the neuropsychiatric problems, there has been an increased awareness that children with CP are at increased risk of developing feeding problems and a strong association has been found between the presence of oral-motor dysfunction and undernutrition [2]. According to previous data from our group [3], 92% of children with CP have clinically significant gastrointestinal symptoms [3]. Approximately a one-third of children with CP are undernourished and many exhibit the consequences of malnutrition [4]. The energy intake issue is critical in patients with associated mental retardation considering their inability to clearly communicate hunger, satiety and pain, which leaves them dependent on a variety of caregivers to define and provide optimal intake without disease-specific dietary guidelines. Nutritional disorders in these children are not as frequently recognized and treated as they are in children with other chronic pediatric diseases. Moreover, it is not clear whether gastrointestinal symptoms have an additional negative effect on the already impaired nutritional status of children with CP and little is known about the importance of wasting as a cofactor of muscle spasticity and reduced motor function. In addition, the impact of nutritional rehabilitation on gross motor function has never been documented. Thus the aim of our study was to assess the possible relationship between malnutrition and gastrointestinal problems, and to evaluate the role of nutrition on their gross motor abilities in a population of children with CP and mental retardation.
2. Patients and methods Nutritional status, gastrointestinal symptoms and Gross Motor Function were evaluated in 21 consecutive children (M/F: 11/10) with CP and severe mental retardation referred to the Unit of NeuroGastroenterology of the Department of Pediatrics – University ‘‘Federico II’’ of Naples (Italy). Their ages, at study, ranged from 1 to 14 years (mean ± SD: 5.8 ± 4.7 years). On admission each child underwent a clinical, neurological and nutritional examination. Nutritional assessment included the measurement of the following anthropometric variables: weight (W), length (H), weight for length (W/H) and body mass index (BMI). Fat free mass (FFM) and fat body mass
(FBM) were obtained by the same investigator with the multiple skinfold anthropometry procedure (MSA). Weight was determined to the nearest 0.1 kg on a standard physician scale, with the child dressed only in light underwear and without shoes. Length was measured to the nearest 0.5 cm while lying in a measuring board. BMI was calculated as weight divided by length squared (Kg/m2). Skinfold thickness was determined to the nearest millimeter at the left biceps, triceps, subscapular and soprailiac sites with an Holtain skinfold caliper calibrated to exert a constant pressure of 10 gr/ mm2 (Holtain Ltd, Crymych, UK). Triplicate readings were made at each site to improve the accuracy and the reproducibility of the measurements. The generalized equations of Brook and Durnin, in accordance with different ages, for predicting body density were used in this study [5,6]. FBM was derived according to Siri [7]. FFM was calculated as the difference between bodyweight and FBM. Gastrointestinal assessment. A questionnaire was filled out for each patient to evaluate the presence of gastrointestinal symptoms, defined according to previous reports from our group [3,8]. Eighteen children (86%) had a clinical history suggesting gastroesophageal reflux disease (GERD), because of frequent regurgitation and/or recurrent pneumonia and/or insomnia and/or unmotivated crying and/or refusal of alimentation. Twelve patients out of eighteen underwent prolonged 24 h intraesophageal pH monitoring and 6 of 18 underwent upper GI endoscopy with biopsies. Esophageal pH was performed according to the method previously reported [9]. Children were considered affected by GERD in case of endoscopically and histologically documented oesophagitis or if esophageal pH scoring showed that the total time of esophageal acid exposure was >4% of total recording time [9]. Malnourished-children received a 6 month nutritional rehabilitation based on a 20% increment of daily caloric intake, by using a cow’s standard milk based polymeric formula, through nasogastric tube feeding. ‘‘The Gross Motor Function Measure’’ (GMFM), an instrument comprising dimensions devised by Russell [10] to measure basic gross motor activities in children with CP or brain damage, was administered to monitor changes in their performance status before and after nutritional rehabilitation. Patients affected by both malnutrition and GERD underwent a course treatment with omeprazole (2 mg/ kg/day for the first 3 months and 1 mg/kg/day for 3 additional months) in addition to nutritional rehabilitation and, after 6 months of medical and nutritional treatments, they underwent a re-evaluation of their nutritional status and GERD. Pre-dietary and post-dietary caloric intake, weight gain, FFM, FBM, BMI and GMFM were compared using the Student’s T test for paired data and a p value
A. Campanozzi et al. / Brain & Development 29 (2007) 25–29
<0.05 was considered significant. Percentages were rounded to the nearest whole numbers. The study was approved by the local institutional review board. In each case informed consent for participating in the study was obtained from the children’s parents.
Table 2 Prevalence of gastrointestinal problems in malnourished patients
Patients with FBM 6 80% Patients with BMI 6 5° pc
GERD No. (%)
CC No. (%)
11 (73) 9 (81.8)
9 (60) 7 (64)
Table 3 Six months nutritional rehabilitation in 14 CP children with FBM 6 80%
3. Results Nutritional status is reported in Table 1. W/H 6 80% of ideal value was present in 4 out of 21 (19%) children affected by cerebral palsy and H/age was <5° pc in 13 (62%). BMI/age was 65° percentile in 11 children (52%). FBM and FFM were 680% of their ideal values for height in 15 (71%) and 2 (9%) patients, respectively. Nineteen out of 21 (90%) patients showed gastrointestinal disorders. Gastroesophageal reflux disease (GERD) was found in a group of 14 children (67%): in 10 patients by 24 h-pHmetry which documented a total time of esophageal acid exposure >4% of total recording time; in four patients by upper GI endoscopy which revealed a mild to moderate esophagitis. Chronic constipation was found in 14 children (67%), nine of them (43%) were affected by both GERD and CC. The prevalence of GI problems in malnourished patients is reported in Table 2. Patients who were malnourished at presentation (FBM 6 80% or BMI 6 5° percentile) underwent nutritional rehabilitation receiving an increment of their mean energy intake from 72.3 ± 11.5 kcal/kg/day to 99.9 ± 20.4 kcal/kg/day (p < 0.05). Fourteen malnourished children (mean age: 6.4 ± 3.9 years; M/F: 11/3), among those with a fat body mass 680%, completed the 6 months nutritional trial. Their starting and final (mean ± SD) BMI was 13.56 ± 1.31 and 14.15 ± 1.85 (p = 0.08), respectively. As reported in Table 3, (mean ± SD) GMFM values were significantly improved in 9/14 (64%) pts (Group A) from 9.9 ± 6.7% to 13.7 ± 7.1%, while it remained unchanged in 5/14 pts (36%) (Group B). Mean ± SD FFM gains in Group A and B were, respectively, 1.2 ± 0.59 kg (p < 0.005 between starting and final FFM in Group A) and 0.62 ± 0.57 kg (p = NS between starting and final FFM in Group B); FBM gains in Group A and B were 0.49 ± 0.74 kg and 0.95 ± 0.97 kg, respectively (p < 0.05 between starting and final FBM in both groups).
Table 1 Nutritional status in 21 children with cerebral palsy No. (%) Height/age <5° pc Weight/height >80% <90% Weight/height 680%
27
13 (62) 7 (33) 4 (19)
Number of patients
Group A 9/14
Group B 5/14
Age (years) Starting GMFM (%) Final GMFM (%) Starting weight (kg) Final weight (kg) Starting FFM (kg) Final FFM (kg) Starting FBM (kg) Final FBM (kg)
6.11 ± 4.45 9.9 ± 6.7a 13.7 ± 7.1a 14 ± 7.6b 15.7 ± 8.3b 12.8 ± 6.8b 13.9 ± 7b 1.3 ± 1.1a 1.8 ± 1.4a
7 ± 3.1 4.14 ± 1.71c 4.13 ± 1.71c 15.5 ± 5.4a 17.1 ± 6.8a 13.7 ± 4.5c 14.1 ± 4.5c 1.8 ± 1.6a 2.9 ± 2a
a b c
p < 0.05. p < 0.005. NS.
Nine children with GERD and malnutrition (mean ± SD age: 3.7 ± 2.3 years; M/F: 3/6) completed the 6 months pharmaceutical and nutritional treatments. Their initial mean ± SD BMI was 13.6 ± 0.5 (<5°) and a significant gain was achieved at the end of the 6 months (15.9 ± 1, >25°; p < 0.05). A marked improvement of GERD was noted in four of nine (44%) children. Despite successful nutritional rehabilitation with a BMI achievement of P25° percentile, five of nine (56%) patients had persistent GERD, when they were taken off the medication. Therefore in these five CP patients medical therapy was reinstituted and significant clinical improvement was noted in two of five (40%). The remaining three patients, unresponsive to a second course of medical treatment, underwent Nissen fundoplication. 4. Discussion Our results indicate that malnutrition and gastrointestinal disorders are very common in infants with cerebral palsy and mental retardation, and this is in agreement with previous papers [2,3]. The peculiarity of the present study is that improved nutritional status, particularly fat free mass gain, appears to have an impact on motor function in neurologically impaired children, while it is not clear its role on GERD. A marked improvement of GERD was noted in only four of six (44.4%) children, suggesting that GERD could contribute to malnutrition in CP children much more than be a consequence of it, not supporting the hypothesis previously reported by Lewis et al. [11].
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A. Campanozzi et al. / Brain & Development 29 (2007) 25–29
Most children with neurologic disabilities have progressive weight loss due to fat loss, while skeletal muscle and visceral protein are maintained for a longer period [12]. Our data suggest that the final goal of nutrition to obtain a muscular functional gain in terms of motor activities, as measured by GMFM score, is to increase fat free mass compartments of the body, as the only group of children (Group A) presenting an increase in GMFM was the one with a significant FFM gain. The problem could be now to understand why some children (Group B) did not present any FFM gain in spite of a general increase in whole body weight. A possible explanation could be that adequate nutritional management should be started before neurological disorders produce muscular denervation. According to Waterlow criteria [13], acute malnutrition was expressed in terms of weight for height and BMI, taking into consideration the length deficit caused by stunting. Thirty-three percent of children, presenting 80%–90% of W/H, were classified as having evidence of acute malnutrition grade I. Whereas, 19% of children, presenting a 70%–80% of W/H, had grade II acute malnutrition. In our study, anthropometric data were analyzed to describe the current nutritional status of children with CP relatively to healthy children and not to evaluate their growth potential. To estimate nutritional reserves and to avoid problems related to the aberrant distribution of body fat in children without any motor activity, the MSA procedure was preferred to the simple triceps skinfold thickness measurements [5]. Although this estimate does not quantify precisely the size of the body fat stores, in the hands of a trained examiner it provides a reasonable measure of nutritional status and can be obtained repeatedly. Too often the wasted appearance and poor growth patterns of these children have been identified as primary features or complications of the underlying neurologic disorder, without consideration that other causal relationships may exist. In the past it has been postulated that increased energy expenditure could be associated with spasticity, athetosis and stereotypic motor movements, but more recently it has been shown that total energy expenditure (measured by the doubly labelled water method) was lower in CP children than in a control group; leading to the concept that CPmalnutrition is not related to excessive energy expenditure but to inadequate energy intake [14]. Ninety percent (19/21) of our population had evidence of GI disorders that could be related to poor nutritional conditions, as suggested by the prevalence of GERD and CC in both children with FBM 6 80% and BMI 6 5° pc. It is possible that vomiting and rumination, frequently thought to be neurologic in origin, could be clinical signs of GERD and hyperextention of the head and neck, seen in many of these patients, are not always a manifestation of a primary neuromus-
cular degenerative disorder, being sometimes secondary to the patient’s effort to find a position that will alleviate the symptoms of GERD (Sandifer’s syndrome). Because of immobility and pureed foods poor in fiber, children with neurologic disabilities are at higher risk of CC, which might be exacerbated by medication and reduced amount of water intake. It is important to note that chronic constipation may result in persistently increased intraabdominal pressure, which could contribute to the development of GERD [15], and is frequently associated to early satiety. It could explain why 43% of subjects in our population were affected by both GERD and CC and a 60% prevalence of CC was observed among malnourished patients. How much gastrointestinal disorders contribute or are due to malnutrition in children with cerebral palsy has been, for long time, a matter of debate. We observed that, in spite of a significant weight gain and a BMI attaining the 25° pc for age and sex, five of nine patients continued having persistent GERD at the end of a 6 months course of omeprazole treatment, leading to the concept that improved nutritional status has no impact on the severity of GERD. This finding is supported by Sulaeman et al. [16], and in agreement with Grunow et al. [17], who showed with pre- and post-PEG pH studies that 6 of 10 children without GERD before PEG had GERD after PEG and nutritional rehabilitation. In conclusion GERD and CC are common in malnourished children with CP. Our data obtained suggest that GERD contributes to alter the nutritional status in neurologically impaired children and it is not true the contrary since a course of nasogastric feeding seems to improve nutrition without affecting the severity of GERD. Finally, we have been able to show for the first time that improved nutritional status, particularly FFM gain, appears to have an impact on motor function in these children. Nutritional and GI problems should be always considered together with neurological and neuromuscular impairment, to take better care of CP patients.
References [1] Bhushon V, Paneth N, Kiely JL. Impact of improved survival of very low birth weight infants on recent secular trends in the prevalence of cerebral palsy. Pediatrics 1993;91:1094–100. [2] Dahl M, Thommessen M, Rasmussen M, Selberg T. Feeding and nutritional characteristics in children with moderate or severe cerebral palsy. Acta Pediatr 1996;85:697–701. [3] Del Giudice E, Staiano A, Capano G, Romano A, Florimonte L, Miele E, et al. Gastrointestinal manifestations in children with cerebral palsy. Brain Dev 1999;21:307–11. [4] Stallings VA, Cronk CE, Zemel BS, Charney EB. Body composition in children with spastic quadriplegic cerebral palsy. J Pediatr 1995;126:833–9. [5] Durnin JV, Rahaman MM. The assessment of the amount of fat in the human body from the measurements of skinfold thickness. Br J Nutr 1967;21:681–9.
A. Campanozzi et al. / Brain & Development 29 (2007) 25–29 [6] Brook CG. Determination of body composition of children from skinfold measurements. Arch Dis Child 1971;46:182–4. [7] Siri W. Body composition from fluid spaces and density: analysis of methods. In: Brozek J, Hanschels A, editors. Techniques for measuring body composition. Washinghton DC: National Academy of Sciences; 1961. p. 223–44. [8] Corazziari E, Cucchiara S, Staiano A, Romaniello G, Tamburini O, Torsoli A, et al. Gastrointestinal transit time, frequency of defecation and anorectal manometry in healthy and constipated children. J Pediatr 1985;106:379–82. [9] Cucchiara S, Staiano A, Gobio Casali L, Boccieri A, Paone FM. Value of the 24 hour intraoesophageal pH monitoring in children. Gut 1990;31:129–33. [10] Russell DJ, Rosenbaum PL, Cadman DT, Growland C, Hardy S, Jarvis S. The gross motor function measure: a mean to evaluate the effects of physical therapy. Dev Med Child Neurol 1989;31:341–52. [11] Lewis D, Khoshoo V, Pencharz PB, Golladay ES. Impact of nutritional rehabilitation on gastroesophageal reflux in neurologically impaired children. J Pediatr Surg 1994;29:167–9.
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[12] Bandini LG, Schoeller DA, Fukagawa NK, Wykes LJ, Dietz WH. Body composition and energy expenditure in adolescents with cerebral palsy or myelodysplasia. Pediatr Res 1991;29:70–7. [13] Waterlow JC. Note on the assessment and classification of protein-energy malnutrition in children. Lancet 1973;2:87–9. [14] Stallings VA, Zemel BS, Davies JC, Cronk CE, Charney EB. Energy expenditure of children and adolescents with severe disabilities: a cerebral palsy model. Am J Clin Nutr 1996;64:627–34. [15] Wesley JR, Coran AG, Sarahan TM, Klein MD, White SJ. The need for evaluation of gastroesophageal reflux in brain-damaged children referred for feeding gastrostomy. J Pediatr Surg 1981;16:866–71. [16] Sulaeman E, Udall Jr JN, Brown RF, Mannick EE, Loe WA, Hill CB, et al. Gastroesophageal reflux and Nissen fundoplication following percutaneous endoscopic gastrostomy in children. J Pediatr Gastroenterol Nutr 1998;26:269–73. [17] Grunow JE, al-Hafidh A, Tunell WP. Gastroesophageal reflux following percutaneous endoscopic gastrostomy in children. J Pediatr Surg 1989;24:42–4.
Impact of malnutrition on gastrointestinal disorders and gross motor abilities in children with cerebral palsy Angelo Campanozzi a,b, Guglielmo Capano a, Erasmo Miele a, Alfonso Romano a, Goffredo Scuccimarra c, Ennio Del Giudice a, Caterina Strisciuglio a, Roberto Militerni c, Annamaria Staiano a,* a
Department of Pediatrics, University of Naples ‘‘Federico II’’, Via S. Pansini 5, 80131 Naples, Italy b Unit of Pediatrics, University of Foggia, Italy c Child Neurology, Second University of Naples, Italy Received 15 October 2005; received in revised form 18 May 2006; accepted 29 May 2006
Abstract Children with cerebral palsy (CP) often demonstrate abnormal feeding behaviours, leading to reduced food consumption and malnutrition. Moreover, most of them present with gastrointestinal disorders, such as gastroesophageal reflux disease (GERD) and/or chronic constipation (CC), and poor motor function rehabilitation. The aim of our study was to assess the possible relationship between malnutrition and gastrointestinal problems and to evaluate the role of nutrition on their gross motor abilities in a population of children with CP and mental retardation. Patients: Twenty-one consecutive children (10 boys; mean age: 5.8 ± 4.7 years; range: 1–14 years) with CP and severe mental retardation. Methods: Nutritional assessment included the measurement of body mass index (BMI = W/H2), fat body mass (FBM) and fat free mass (FFM). Children with symptoms suggesting GERD underwent prolonged 24 h intraesophageal pH monitoring and/or upper GI endoscopy with biopsies before and after a 6 months of pharmaceutical (omeprazole) and nutritional (20% increment of daily caloric intake) treatments. The motor function was evaluated by ‘‘The Gross Motor Function Measure’’ (GMFM) before and after the 6 months on nutritional rehabilitation. Results: BMI for age was 65° percentile in 11 children (52%) and FBM was 680% of ideal value for height in 15 (71%). GERD was present in 14 children (67%), 9 of them were affected by both GERD and CC. Among children with FBM 6 80%, GERD was present in 11 (73%) and CC in 9 (60%). Considering the group of patients with BMI 6 5° percentile, 9 out of 11 children had GERD (82%) and 7 had CC (64%). Fourteen malnourished children (FBM 6 80%) completed the 6 months nutritional trial. Their starting and final means ± SD BMI were 13.56 ± 1.31 and 14.15 ± 1.85 (p = 0.08), respectively. GMFM values were significantly (p < 0.05) improved in 9/14 pts (Group A), while it remained unchanged in 5/14 pts (Group B). Nine children with GERD and malnutrition completed the 6 months of pharmaceutical and nutritional treatments. Their initial mean ± SD weight was 10.1 ± 2.9 kg, whereas the final mean ± SD weight was 12.7 ± 4 kg (p < 0.05). A marked improvement of GERD was noted in four of nine (44.4%) children. Despite successful nutritional rehabilitation with a BMI achievement of P25° percentile, five of nine (55.5%) patients had persistent GERD when they were taken off the medication. Conclusions: Malnutrition and gastrointestinal disorders are very common in children with cerebral palsy. Improved nutritional status, particularly fat free mass gain, appears to have an impact on motor function in children with CP. Ó 2006 Elsevier B.V. All rights reserved. Keywords: Cerebral palsy; Body composition; Children; Nutrition
*
Corresponding author.Tel.: +39 081 7462679; fax: +39 081 5469811.
0387-7604/$ - see front matter Ó 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.braindev.2006.05.008
26
A. Campanozzi et al. / Brain & Development 29 (2007) 25–29
1. Introduction Cerebral palsy (CP) is a severe disability that is associated with abnormal physical activity, body composition and poor nutritional status. Its prevalence is approximately 2.5/1000 live births and in recent years there is a moderate rise of this value, which is the result of increased survival of very low birth weight infants [1]. Apart from the neuropsychiatric problems, there has been an increased awareness that children with CP are at increased risk of developing feeding problems and a strong association has been found between the presence of oral-motor dysfunction and undernutrition [2]. According to previous data from our group [3], 92% of children with CP have clinically significant gastrointestinal symptoms [3]. Approximately a one-third of children with CP are undernourished and many exhibit the consequences of malnutrition [4]. The energy intake issue is critical in patients with associated mental retardation considering their inability to clearly communicate hunger, satiety and pain, which leaves them dependent on a variety of caregivers to define and provide optimal intake without disease-specific dietary guidelines. Nutritional disorders in these children are not as frequently recognized and treated as they are in children with other chronic pediatric diseases. Moreover, it is not clear whether gastrointestinal symptoms have an additional negative effect on the already impaired nutritional status of children with CP and little is known about the importance of wasting as a cofactor of muscle spasticity and reduced motor function. In addition, the impact of nutritional rehabilitation on gross motor function has never been documented. Thus the aim of our study was to assess the possible relationship between malnutrition and gastrointestinal problems, and to evaluate the role of nutrition on their gross motor abilities in a population of children with CP and mental retardation.
2. Patients and methods Nutritional status, gastrointestinal symptoms and Gross Motor Function were evaluated in 21 consecutive children (M/F: 11/10) with CP and severe mental retardation referred to the Unit of NeuroGastroenterology of the Department of Pediatrics – University ‘‘Federico II’’ of Naples (Italy). Their ages, at study, ranged from 1 to 14 years (mean ± SD: 5.8 ± 4.7 years). On admission each child underwent a clinical, neurological and nutritional examination. Nutritional assessment included the measurement of the following anthropometric variables: weight (W), length (H), weight for length (W/H) and body mass index (BMI). Fat free mass (FFM) and fat body mass
(FBM) were obtained by the same investigator with the multiple skinfold anthropometry procedure (MSA). Weight was determined to the nearest 0.1 kg on a standard physician scale, with the child dressed only in light underwear and without shoes. Length was measured to the nearest 0.5 cm while lying in a measuring board. BMI was calculated as weight divided by length squared (Kg/m2). Skinfold thickness was determined to the nearest millimeter at the left biceps, triceps, subscapular and soprailiac sites with an Holtain skinfold caliper calibrated to exert a constant pressure of 10 gr/ mm2 (Holtain Ltd, Crymych, UK). Triplicate readings were made at each site to improve the accuracy and the reproducibility of the measurements. The generalized equations of Brook and Durnin, in accordance with different ages, for predicting body density were used in this study [5,6]. FBM was derived according to Siri [7]. FFM was calculated as the difference between bodyweight and FBM. Gastrointestinal assessment. A questionnaire was filled out for each patient to evaluate the presence of gastrointestinal symptoms, defined according to previous reports from our group [3,8]. Eighteen children (86%) had a clinical history suggesting gastroesophageal reflux disease (GERD), because of frequent regurgitation and/or recurrent pneumonia and/or insomnia and/or unmotivated crying and/or refusal of alimentation. Twelve patients out of eighteen underwent prolonged 24 h intraesophageal pH monitoring and 6 of 18 underwent upper GI endoscopy with biopsies. Esophageal pH was performed according to the method previously reported [9]. Children were considered affected by GERD in case of endoscopically and histologically documented oesophagitis or if esophageal pH scoring showed that the total time of esophageal acid exposure was >4% of total recording time [9]. Malnourished-children received a 6 month nutritional rehabilitation based on a 20% increment of daily caloric intake, by using a cow’s standard milk based polymeric formula, through nasogastric tube feeding. ‘‘The Gross Motor Function Measure’’ (GMFM), an instrument comprising dimensions devised by Russell [10] to measure basic gross motor activities in children with CP or brain damage, was administered to monitor changes in their performance status before and after nutritional rehabilitation. Patients affected by both malnutrition and GERD underwent a course treatment with omeprazole (2 mg/ kg/day for the first 3 months and 1 mg/kg/day for 3 additional months) in addition to nutritional rehabilitation and, after 6 months of medical and nutritional treatments, they underwent a re-evaluation of their nutritional status and GERD. Pre-dietary and post-dietary caloric intake, weight gain, FFM, FBM, BMI and GMFM were compared using the Student’s T test for paired data and a p value
A. Campanozzi et al. / Brain & Development 29 (2007) 25–29
<0.05 was considered significant. Percentages were rounded to the nearest whole numbers. The study was approved by the local institutional review board. In each case informed consent for participating in the study was obtained from the children’s parents.
Table 2 Prevalence of gastrointestinal problems in malnourished patients
Patients with FBM 6 80% Patients with BMI 6 5° pc
GERD No. (%)
CC No. (%)
11 (73) 9 (81.8)
9 (60) 7 (64)
Table 3 Six months nutritional rehabilitation in 14 CP children with FBM 6 80%
3. Results Nutritional status is reported in Table 1. W/H 6 80% of ideal value was present in 4 out of 21 (19%) children affected by cerebral palsy and H/age was <5° pc in 13 (62%). BMI/age was 65° percentile in 11 children (52%). FBM and FFM were 680% of their ideal values for height in 15 (71%) and 2 (9%) patients, respectively. Nineteen out of 21 (90%) patients showed gastrointestinal disorders. Gastroesophageal reflux disease (GERD) was found in a group of 14 children (67%): in 10 patients by 24 h-pHmetry which documented a total time of esophageal acid exposure >4% of total recording time; in four patients by upper GI endoscopy which revealed a mild to moderate esophagitis. Chronic constipation was found in 14 children (67%), nine of them (43%) were affected by both GERD and CC. The prevalence of GI problems in malnourished patients is reported in Table 2. Patients who were malnourished at presentation (FBM 6 80% or BMI 6 5° percentile) underwent nutritional rehabilitation receiving an increment of their mean energy intake from 72.3 ± 11.5 kcal/kg/day to 99.9 ± 20.4 kcal/kg/day (p < 0.05). Fourteen malnourished children (mean age: 6.4 ± 3.9 years; M/F: 11/3), among those with a fat body mass 680%, completed the 6 months nutritional trial. Their starting and final (mean ± SD) BMI was 13.56 ± 1.31 and 14.15 ± 1.85 (p = 0.08), respectively. As reported in Table 3, (mean ± SD) GMFM values were significantly improved in 9/14 (64%) pts (Group A) from 9.9 ± 6.7% to 13.7 ± 7.1%, while it remained unchanged in 5/14 pts (36%) (Group B). Mean ± SD FFM gains in Group A and B were, respectively, 1.2 ± 0.59 kg (p < 0.005 between starting and final FFM in Group A) and 0.62 ± 0.57 kg (p = NS between starting and final FFM in Group B); FBM gains in Group A and B were 0.49 ± 0.74 kg and 0.95 ± 0.97 kg, respectively (p < 0.05 between starting and final FBM in both groups).
Table 1 Nutritional status in 21 children with cerebral palsy No. (%) Height/age <5° pc Weight/height >80% <90% Weight/height 680%
27
13 (62) 7 (33) 4 (19)
Number of patients
Group A 9/14
Group B 5/14
Age (years) Starting GMFM (%) Final GMFM (%) Starting weight (kg) Final weight (kg) Starting FFM (kg) Final FFM (kg) Starting FBM (kg) Final FBM (kg)
6.11 ± 4.45 9.9 ± 6.7a 13.7 ± 7.1a 14 ± 7.6b 15.7 ± 8.3b 12.8 ± 6.8b 13.9 ± 7b 1.3 ± 1.1a 1.8 ± 1.4a
7 ± 3.1 4.14 ± 1.71c 4.13 ± 1.71c 15.5 ± 5.4a 17.1 ± 6.8a 13.7 ± 4.5c 14.1 ± 4.5c 1.8 ± 1.6a 2.9 ± 2a
a b c
p < 0.05. p < 0.005. NS.
Nine children with GERD and malnutrition (mean ± SD age: 3.7 ± 2.3 years; M/F: 3/6) completed the 6 months pharmaceutical and nutritional treatments. Their initial mean ± SD BMI was 13.6 ± 0.5 (<5°) and a significant gain was achieved at the end of the 6 months (15.9 ± 1, >25°; p < 0.05). A marked improvement of GERD was noted in four of nine (44%) children. Despite successful nutritional rehabilitation with a BMI achievement of P25° percentile, five of nine (56%) patients had persistent GERD, when they were taken off the medication. Therefore in these five CP patients medical therapy was reinstituted and significant clinical improvement was noted in two of five (40%). The remaining three patients, unresponsive to a second course of medical treatment, underwent Nissen fundoplication. 4. Discussion Our results indicate that malnutrition and gastrointestinal disorders are very common in infants with cerebral palsy and mental retardation, and this is in agreement with previous papers [2,3]. The peculiarity of the present study is that improved nutritional status, particularly fat free mass gain, appears to have an impact on motor function in neurologically impaired children, while it is not clear its role on GERD. A marked improvement of GERD was noted in only four of six (44.4%) children, suggesting that GERD could contribute to malnutrition in CP children much more than be a consequence of it, not supporting the hypothesis previously reported by Lewis et al. [11].
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A. Campanozzi et al. / Brain & Development 29 (2007) 25–29
Most children with neurologic disabilities have progressive weight loss due to fat loss, while skeletal muscle and visceral protein are maintained for a longer period [12]. Our data suggest that the final goal of nutrition to obtain a muscular functional gain in terms of motor activities, as measured by GMFM score, is to increase fat free mass compartments of the body, as the only group of children (Group A) presenting an increase in GMFM was the one with a significant FFM gain. The problem could be now to understand why some children (Group B) did not present any FFM gain in spite of a general increase in whole body weight. A possible explanation could be that adequate nutritional management should be started before neurological disorders produce muscular denervation. According to Waterlow criteria [13], acute malnutrition was expressed in terms of weight for height and BMI, taking into consideration the length deficit caused by stunting. Thirty-three percent of children, presenting 80%–90% of W/H, were classified as having evidence of acute malnutrition grade I. Whereas, 19% of children, presenting a 70%–80% of W/H, had grade II acute malnutrition. In our study, anthropometric data were analyzed to describe the current nutritional status of children with CP relatively to healthy children and not to evaluate their growth potential. To estimate nutritional reserves and to avoid problems related to the aberrant distribution of body fat in children without any motor activity, the MSA procedure was preferred to the simple triceps skinfold thickness measurements [5]. Although this estimate does not quantify precisely the size of the body fat stores, in the hands of a trained examiner it provides a reasonable measure of nutritional status and can be obtained repeatedly. Too often the wasted appearance and poor growth patterns of these children have been identified as primary features or complications of the underlying neurologic disorder, without consideration that other causal relationships may exist. In the past it has been postulated that increased energy expenditure could be associated with spasticity, athetosis and stereotypic motor movements, but more recently it has been shown that total energy expenditure (measured by the doubly labelled water method) was lower in CP children than in a control group; leading to the concept that CPmalnutrition is not related to excessive energy expenditure but to inadequate energy intake [14]. Ninety percent (19/21) of our population had evidence of GI disorders that could be related to poor nutritional conditions, as suggested by the prevalence of GERD and CC in both children with FBM 6 80% and BMI 6 5° pc. It is possible that vomiting and rumination, frequently thought to be neurologic in origin, could be clinical signs of GERD and hyperextention of the head and neck, seen in many of these patients, are not always a manifestation of a primary neuromus-
cular degenerative disorder, being sometimes secondary to the patient’s effort to find a position that will alleviate the symptoms of GERD (Sandifer’s syndrome). Because of immobility and pureed foods poor in fiber, children with neurologic disabilities are at higher risk of CC, which might be exacerbated by medication and reduced amount of water intake. It is important to note that chronic constipation may result in persistently increased intraabdominal pressure, which could contribute to the development of GERD [15], and is frequently associated to early satiety. It could explain why 43% of subjects in our population were affected by both GERD and CC and a 60% prevalence of CC was observed among malnourished patients. How much gastrointestinal disorders contribute or are due to malnutrition in children with cerebral palsy has been, for long time, a matter of debate. We observed that, in spite of a significant weight gain and a BMI attaining the 25° pc for age and sex, five of nine patients continued having persistent GERD at the end of a 6 months course of omeprazole treatment, leading to the concept that improved nutritional status has no impact on the severity of GERD. This finding is supported by Sulaeman et al. [16], and in agreement with Grunow et al. [17], who showed with pre- and post-PEG pH studies that 6 of 10 children without GERD before PEG had GERD after PEG and nutritional rehabilitation. In conclusion GERD and CC are common in malnourished children with CP. Our data obtained suggest that GERD contributes to alter the nutritional status in neurologically impaired children and it is not true the contrary since a course of nasogastric feeding seems to improve nutrition without affecting the severity of GERD. Finally, we have been able to show for the first time that improved nutritional status, particularly FFM gain, appears to have an impact on motor function in these children. Nutritional and GI problems should be always considered together with neurological and neuromuscular impairment, to take better care of CP patients.
References [1] Bhushon V, Paneth N, Kiely JL. Impact of improved survival of very low birth weight infants on recent secular trends in the prevalence of cerebral palsy. Pediatrics 1993;91:1094–100. [2] Dahl M, Thommessen M, Rasmussen M, Selberg T. Feeding and nutritional characteristics in children with moderate or severe cerebral palsy. Acta Pediatr 1996;85:697–701. [3] Del Giudice E, Staiano A, Capano G, Romano A, Florimonte L, Miele E, et al. Gastrointestinal manifestations in children with cerebral palsy. Brain Dev 1999;21:307–11. [4] Stallings VA, Cronk CE, Zemel BS, Charney EB. Body composition in children with spastic quadriplegic cerebral palsy. J Pediatr 1995;126:833–9. [5] Durnin JV, Rahaman MM. The assessment of the amount of fat in the human body from the measurements of skinfold thickness. Br J Nutr 1967;21:681–9.
A. Campanozzi et al. / Brain & Development 29 (2007) 25–29 [6] Brook CG. Determination of body composition of children from skinfold measurements. Arch Dis Child 1971;46:182–4. [7] Siri W. Body composition from fluid spaces and density: analysis of methods. In: Brozek J, Hanschels A, editors. Techniques for measuring body composition. Washinghton DC: National Academy of Sciences; 1961. p. 223–44. [8] Corazziari E, Cucchiara S, Staiano A, Romaniello G, Tamburini O, Torsoli A, et al. Gastrointestinal transit time, frequency of defecation and anorectal manometry in healthy and constipated children. J Pediatr 1985;106:379–82. [9] Cucchiara S, Staiano A, Gobio Casali L, Boccieri A, Paone FM. Value of the 24 hour intraoesophageal pH monitoring in children. Gut 1990;31:129–33. [10] Russell DJ, Rosenbaum PL, Cadman DT, Growland C, Hardy S, Jarvis S. The gross motor function measure: a mean to evaluate the effects of physical therapy. Dev Med Child Neurol 1989;31:341–52. [11] Lewis D, Khoshoo V, Pencharz PB, Golladay ES. Impact of nutritional rehabilitation on gastroesophageal reflux in neurologically impaired children. J Pediatr Surg 1994;29:167–9.
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[12] Bandini LG, Schoeller DA, Fukagawa NK, Wykes LJ, Dietz WH. Body composition and energy expenditure in adolescents with cerebral palsy or myelodysplasia. Pediatr Res 1991;29:70–7. [13] Waterlow JC. Note on the assessment and classification of protein-energy malnutrition in children. Lancet 1973;2:87–9. [14] Stallings VA, Zemel BS, Davies JC, Cronk CE, Charney EB. Energy expenditure of children and adolescents with severe disabilities: a cerebral palsy model. Am J Clin Nutr 1996;64:627–34. [15] Wesley JR, Coran AG, Sarahan TM, Klein MD, White SJ. The need for evaluation of gastroesophageal reflux in brain-damaged children referred for feeding gastrostomy. J Pediatr Surg 1981;16:866–71. [16] Sulaeman E, Udall Jr JN, Brown RF, Mannick EE, Loe WA, Hill CB, et al. Gastroesophageal reflux and Nissen fundoplication following percutaneous endoscopic gastrostomy in children. J Pediatr Gastroenterol Nutr 1998;26:269–73. [17] Grunow JE, al-Hafidh A, Tunell WP. Gastroesophageal reflux following percutaneous endoscopic gastrostomy in children. J Pediatr Surg 1989;24:42–4.