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Metabolic disturbances in patients with cerebral palsy and gastrointestinal disorders
Clinical Nutrition ESPEN 11 (2016) e67ee69
Contents lists available at ScienceDirect
Clinical Nutrition ESPEN journal homepage: http://www.clinicalnutritionespen.com
Short communication
Metabolic disturbances in patients with cerebral palsy and gastrointestinal disorders Catalina Jaramillo a, Abiodun Johnson b, Ruchi Singh c, Tetyana L. Vasylyeva d, * a
Pediatric Resident (PGY-3), Department of Pediatrics, Texas Tech University Health Sciences Center, Amarillo, USA Pediatric Gastroenterology, Department of Pediatrics, Texas Tech University Health Sciences Center, Amarillo, USA c Department of Pediatrics, Texas Tech University Health Sciences Center, Amarillo, USA d Pediatric Nephrology, Department of Pediatrics, Texas Tech University Health Sciences Center, Amarillo, USA b
a r t i c l e i n f o
s u m m a r y
Article history: Received 25 March 2015 Accepted 12 August 2015
Under nutrition and growth failure are common findings in children with cerebral palsy (CP) and neurologically impairments. Electrolyte and micronutrient abnormalities have also been documented. Gastrointestinal (GI) diseases like gastro esophageal reflux disease (GERD), feeding difficulties and constipation have been associated with increased frequency of these derangements. The goal of this study was to determine the prevalence of malnutrition, metabolic and electrolyte abnormalities in pediatric patients with cerebral palsy and gastrointestinal disorders. A retrospective review of 172 medical records was performed out of which 45 subjects did not have any GI problem, 69 patients had constipation and 58 patients either had GERD, esophagitis, gastrostomy and feeding difficulties. Data collected included: weight, length and body mass index, pre-albumin, albumin, vitamin D, potassium, chloride, bicarbonate, calcium, magnesium (Mg), phosphorus. The results demonstrate a significant difference (p ¼ 0.0126) in the values of albumin in children with CP with GI disorders vs. those without. Additionally, a significant difference (p ¼ 0.0129) was found in Mg levels between CP children with constipation vs. GERD/esophagitis/feeding issues/gastrostomy. Results suggest that children with CP and GI disorders have decreased levels of albumin, but normal pre-albumin. The mechanism for this is not completely clear and although we acknowledge importance of nutritional intake for albumin level support, other mechanisms such as low grade chronic inflammation and increased gut and vascular permeability may play a role. The lower levels of Mg in children with CP and constipation could be secondary to the use of laxatives. Further prospective studies looking at nutritional protein intake, gut and vascular permeability and laxative use in this patient population are important for future optimization of health care management. © 2015 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights reserved.
Keywords: Cerebral Palsy Malnutrition Gastrointestinal disorders Albumin Magnesium
1. Introduction Under nutrition and growth failure are common findings in children with cerebral palsy (CP) and neurological impairments [1]. As a group, children with CP are smaller and poorly nourished compared with their typically developing peers [2]. These differences between affected and non-affected children are more noticeable with increasing age and severity of motor impairment
* Corresponding author. Department of Pediatrics, Nephrology Section, Texas Tech University Health Sciences Center, 1400 South Coulter Street, Amarillo, TX 79106, USA. E-mail address: [email protected] (T.L. Vasylyeva).
[2]. The most significant factor affecting the nutritional status of children with CP is inadequate intake to meet metabolic demands [3]. In addition, gastrointestinal (GI) diseases like gastroesophageal reflux disease (GERD) and constipation have been associated with increased frequency of these derangements. Under nutrition and growth failure in neurologically impaired children seem to be related to inappropriate caloric intake, altered nutrient needs, inability to self-feed and oral motor dysfunction. Up to one-third of pediatric patients have associated growth disorder and nutritional deficits [4]. Additionally, malnutrition affects quality of life and is associated with increased health care use. Although in the past under nutrition was considered as a natural spectrum of disease of neurologically impaired children, it is now recognized that adequate nutrition in these patients is essential [5].
http://dx.doi.org/10.1016/j.clnesp.2015.08.003 2405-4577/© 2015 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights reserved.
e68
C. Jaramillo et al. / Clinical Nutrition ESPEN 11 (2016) e67ee69
Electrolyte and micronutrient deficiencies are also documented in children with cerebral palsy. Iron, zinc, essential fatty acids and vitamins C, D and E were reported to be deficient in 15e50% of these children. Dietary calcium, vitamin D and phosphorus intakes are below the Daily Reference Intake in 50e80% of these children [6]. In a cross-sectional observational study performed to assess the adequacy of sodium, potassium, phosphorus and fluid intakes in children with cerebral palsy, it was shown that 60% of children were sodium deficient [7]. There were no deficiencies in potassium and only one child in the study was considered to have possible inadequate phosphorus intake [7]. The goal of this study was to determine whether GI disorders complicated CP impact children's development and metabolic status.
2. Materials and methods The charts of patients with CP followed in the specialized pediatric clinic, at Texas Tech University Health Science Center (TTUHSC, Amarillo) were retrospectively reviewed after IRB approval. TTUHSC clinic for special need children has three designated providers for CP patients, who followed standardized nutritional protocols and evaluated growth parameters with every visit. CP patients with and without GI disorder received the same or similar professional care. Patients were followed at least every three months with close attention to nutrition and growth. In general, younger children with gastrostomy tubes were on PediaSure® or if growth delay was noticed, on PediaSure® 1.5 Cal (AbbottNutrition). Older children with gastrostomy tubes were on Ensure® (AbbottNutrition), Peptamen Junior®/Peptamen Junior® Health Sciences), or Jevity®/Jevity® 1.2 Cal/Jevity® 1.5 Cal 1.5 (Nestle (AbbottNutrition). Formula preferences and caloric supplements were individually determined by clinical and social (availability, insurance coverage preferences) factors. Patients with adequate growth, who were able tolerate oral feeding were prescribed diet appropriate for age; if the growth curve plateaued or declined, they received additional caloric supplements. A total of the 268 medical records of pediatric patients under 18 years of age with diagnosis of neurologic impairments were reviewed. Ninety-six patients were excluded due to either absence of CP or insufficient data. Demographic data collected included weight in percentile (%p), length (%p) and body mass index (BMI, % p) (Table 1). The most resent laboratory data from were collected: pre-albumin, albumin, sodium (Na), potassium (K), chloride (Cl), bicarbonate (HCO3), calcium (Ca), magnesium (Mg), phosphorus (Phos) and vitamin D (Table 2).
Table 1 Demographics and gastrointestinal (GI) problems in children with cerebral palsy.
Mean age (years) Weight (%p) Length/height (%p) BMI (%p) Gender (n) Male Female GI problems Constipation (n) GERD (n) Esophagitis (n) Gastrostomy (n) Feeding difficulties (n)
GI disorder
No GI disorder
9.01 ± 0.36 31 ± 2.8 25.3 ± 2.7 43.6 ± 3.1
9.51 32.9 34.9 35.6
68 70
34 11
e e
69 24 11 43 13
e e e e e
e e e e e
± ± ± ±
0.74 4.9 4.5 4.9
p Value 0.19NS 0.60NS 0.12NS 0.19NS
Age, weight, length/height and BMI data is represented as Mean ± SEM; n ¼ total number; % p, percentile value; GI, gastrointestinal; GERD, gastro esophageal reflux disorder; NS, no significant.
Table 2 Lab chemistries of patients with Cerebral Palsy. Lab chemistries
GI disorder
Na (mM/L) K (mM/L) Cl (mM/L) HCO3 (mM/L) Ca (mg/dL) Mg (mg/dL) Phos (mg/dL) Vit D (mg/dL) Albumin (mg/dL) Pre-albumin (mg/dL)
138.7 4 116.4 24.4 9.6 2.1 4.7 40.4 3.9 19
± ± ± ± ± ± ± ± ± ±
0.4 0.1 13.6 0.4 0.05 0.03 0.1 2.9 0.05 0.9
No GI disorder
p value
± ± ± ± ± ± ± ± ± ±
0.85 0.34 0.2 0.98 0.66 0.15 0.79 0.09 0.0126* 0.57
138.6 4.2 105.4 23.5 9.6 2.1 5.1 33 4.1 18.4
0.5 0.1 0.5 0.4 0.1 0.06 0.2 2.7 0.06 1
Na; Sodium, K; Potassium, Cl; Chloride, HCO3; bicarbonate, Ca; calcium, Mg; magnesium, Phos; phosphorus, Vit D; Vitamin D, mM/L; millimolar/liter, mg/dL; milligram/deciliter. Data is represented as Mean ± SEM. *Statistical significance p ¼ <0.05.
2.1. Statistical analysis Initially the data for patients with and without GI disease were compared and subsequently a subgroup analysis by GI diagnosis was also done. Normality was checked and the variables that meet normality were analyzed by parametric t-test and ANOVA. The remaining variables were analyzed by non-parametric tests (ManneWhitney). “p values” less than or equal to 0.05 were considered as significant. The analysis was done by using Prismgraphpad (GraphPad Software, Inc.®, La Jolla, CA) software. 3. Results A total of 172 patients were included of which 45 did not have any GI co-morbidity, 69 patients had constipation and 58 had either GERD, esophagitis, gastrostomy and feeding difficulties (Table 1). There was a significant difference (p ¼ 0.0126) in the values of albumin levels in children with CP with and without gastrointestinal disorders. Group without GI comorbidity had higher albumin levels (Table 2). After a subgroup analysis, a significant difference (p ¼ 0.0129) was found in magnesium levels between children with CP and constipation and children with CP and GERD, esophagitis, feeding issues and/or gastrostomy. There were no other statistically significant differences in the main comparison groups or subgroups (Table 2). 4. Discussion This study showed a significant difference in the albumin levels in children with CP and GI disorders vs. those without. There were no differences in pre-albumin values between the groups, which makes inadequate intake less likely cause of this finding. Previous studies have determined that albumin and pre-albumin are less reliable indicators of nutritional status as it reflects the body's physiologic response to illness [6]. Although the low levels albumin in the GI group was statistically significant, it was not low enough to show immediate clinical impacts. The mechanism is not completely clear and although we acknowledge importance of nutritional intake for albumin level support, other mechanisms such as low grade chronic inflammation and increased gut and vascular permeability may play a role in patients with GI problems independently from CP. Lower caloric intake, lack of hand-mouth coordination and increased feeding times in patients who are unable to self-feed was a concern expressed in the previous publications and thought to contribute to insufficient intake [1,2,6]. Severely neurologically impaired patients are unable to communicate hunger and depend
C. Jaramillo et al. / Clinical Nutrition ESPEN 11 (2016) e67ee69
on caregiver, who may over or underestimate his/her caloric needs. Energy needs of children with cerebral palsy who ambulate and have athetosis are higher than those who do not, but in wellnourished, non-ambulatory children resting energy expenditure is significantly lower [6]. Also, higher severity of motor impairment has been associated with more feeding dysfunction, which itself is associated with poor nutritional status [2]. We did not have sufficient data on the degree of motor impairment, but focused on GI problems as a factor, which made difference in patients' management. Malnutrition affects the quality of life and is associated with increased health care use. Although in the past, under-nutrition was considered as a natural spectrum of disease of neurologically impaired children, it is now recognized that adequate nutrition in these patients is essential [5]. High caloric and adopted formulas, as we use in our clinic, might well accommodate nutritional needs of patients with CP with and without GI problems. Although we did not find any significant differences in anthropometric measurements in our patients, what we attributed to vigorous nutritional support and frequent follow up in our specialized clinic, undernutrition and growth failure are common findings in studies on neurologically impaired children and seem to be related to inappropriate caloric intake, altered nutrient needs, inability to selffeed and oral motor dysfunction [4,5]. Up to one-third of pediatric patients have associated growth disorder and nutritional deficits [4]. Evaluation of malnutrition in these children should include accurate growth and anthropometric measurements, a complete physical examination and biochemical metabolic studies. Height and length can be difficult to obtain due to contractures or scoliosis, but valid alternatives include upper arm length or lower leg length. It is difficult to overestimate needs for adequate nutrition for patients with CP whether they have GI problems or not: malnutrition has many adverse effects on the overall health of these patients. Decreased muscle strength can lead to cardiopulmonary complications due to weakness of pulmonary musculature and diminished cardiac work capacity. Reduced cerebral growth and delayed cognitive development are some of the neurological consequences. Furthermore, these children present with severe gastro esophageal reflux which is difficult to control [2]. High rates of poor oral intake, chronic esophagitis and suppurative lung disease have also been reported in developmentally disabled patients who present with feeding and nutritional issues [2]. In Campanozzi et al. study, which addressed impact of malnutrition on gastrointestinal disorders and gross motor abilities in children with CP, 33% had acute malnutrition grade I and 19% had acute malnutrition grade II [8]. Gastrostomy tube feeding has been shown to lead to improved weight gain. This is indicated in children with CP who have an unsafe swallow, unable to maintain a satisfactory nutritional state by oral feeding alone, are have exceedingly long oral feeding time and are dependent on nasogastric or gastrostomy tube feeding [9]. Children who have gastrostomies placed within the first year of life are more likely to exceed the fifth percentile for height and weight [6]. There were no significant differences in our CP patients with and without gastrostomy, indicating that timely gastrostomy tube placement could make a significant difference in a child development.
e69
Electrolyte and micronutrient deficiencies have also been documented in children with cerebral palsy. Iron, zinc, essential fatty acids and vitamins C, D and E were reported to be deficient in 15e50% of these children [6]. In a cross-sectional observational study, which was done to assess the adequacy of sodium, potassium, phosphorus and fluid intakes in children with CP, it was shown that 60% of children were sodium deficient. There were no deficiencies in potassium and only one child in the study was considered to have possible inadequate phosphorus intake [7]. In our subgroup analysis we found that children with CP and constipation have lower levels of Mg in comparison to those with CP and GERD, esophagitis, feeding issues and/or gastrostomy. The altered Mg levels we attributed to laxative use in patients with CP and persistent constipation. Mg levels need to be followed regularly in all patients with vigorously treated constipation to avoid hypomagnesemia. 5. Conclusions Further prospective studies looking at nutritional protein intake, gut and vascular permeability and laxative use in this patient population are important for optimization of future health care management. Conflict of interest None. References [1] Rempel G. The importance of good nutrition in children with cerebral palsy. Phys Med Rehab Clin N. Am 2015;26(1):39e56. http://dx.doi.org/10.1016/ j.pmr.2014.09.001. PubMed PMID: 25479778. [2] Kuperminc MN, Stevenson RD. Growth and nutrition disorders in children with cerebral palsy. Dev Disabil Res Rev 2008;14(2):137e46. http://dx.doi.org/ 10.1002/ddrr.14. PubMed PMID: 18646022; PubMed Central PMCID: PMC2830751. [3] 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(4):627e34. PubMed PMID: 8839510. [4] Karagiozoglou-Lampoudi T, Daskalou E, Vargiami E, Zafeiriou D. Identification of feeding risk factors for impaired nutrition status in paediatric patients with cerebral palsy. Acta Paediatr 2012;101(6):649e54. http://dx.doi.org/10.1111/ j.1651-2227.2012.02641.x. PubMed PMID: 22404086. [5] Nutrition in neurologically impaired children. Paediatr Child Health 2009;14(6):395e401. PubMed PMID: 20592978; PubMed Central PMCID: PMC2735385. [6] Marchand V, Motil KJ. Nutrition NCo. Nutrition support for neurologically impaired children: a clinical report of the North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition. J Pediatr Gastroenterol Nutr 2006;43(1):123e35. http://dx.doi.org/10.1097/01.mpg.0000228124.93841.ea. PubMed PMID: 16819391. [7] McGowan JE, Fenton TR, Wade AW, Branton JL, Robertson M. An exploratory study of sodium, potassium, and fluid nutrition status of tube-fed nonambulatory children with severe cerebral palsy. Appl Physiol Nutr Metab Physiologie appliquee, nutrition et metabolisme 2012;37(4):715e23. http:// dx.doi.org/10.1139/h2012-050. PubMed PMID: 22667347. [8] Campanozzi A, Capano G, Miele E, Romano A, Scuccimarra G, Del Giudice E, et al. Impact of malnutrition on gastrointestinal disorders and gross motor abilities in children with cerebral palsy. Brain Dev 2007;29(1):25e9. http:// dx.doi.org/10.1016/j.braindev.2006.05.008. PubMed PMID: 16843628. [9] Sullivan PB. Gastrointestinal disorders in children with neurodevelopmental disabilities. Dev Disabil Res Rev 2008;14(2):128e36. http://dx.doi.org/10.1002/ ddrr.18. PubMed PMID: 18646021.
Contents lists available at ScienceDirect
Clinical Nutrition ESPEN journal homepage: http://www.clinicalnutritionespen.com
Short communication
Metabolic disturbances in patients with cerebral palsy and gastrointestinal disorders Catalina Jaramillo a, Abiodun Johnson b, Ruchi Singh c, Tetyana L. Vasylyeva d, * a
Pediatric Resident (PGY-3), Department of Pediatrics, Texas Tech University Health Sciences Center, Amarillo, USA Pediatric Gastroenterology, Department of Pediatrics, Texas Tech University Health Sciences Center, Amarillo, USA c Department of Pediatrics, Texas Tech University Health Sciences Center, Amarillo, USA d Pediatric Nephrology, Department of Pediatrics, Texas Tech University Health Sciences Center, Amarillo, USA b
a r t i c l e i n f o
s u m m a r y
Article history: Received 25 March 2015 Accepted 12 August 2015
Under nutrition and growth failure are common findings in children with cerebral palsy (CP) and neurologically impairments. Electrolyte and micronutrient abnormalities have also been documented. Gastrointestinal (GI) diseases like gastro esophageal reflux disease (GERD), feeding difficulties and constipation have been associated with increased frequency of these derangements. The goal of this study was to determine the prevalence of malnutrition, metabolic and electrolyte abnormalities in pediatric patients with cerebral palsy and gastrointestinal disorders. A retrospective review of 172 medical records was performed out of which 45 subjects did not have any GI problem, 69 patients had constipation and 58 patients either had GERD, esophagitis, gastrostomy and feeding difficulties. Data collected included: weight, length and body mass index, pre-albumin, albumin, vitamin D, potassium, chloride, bicarbonate, calcium, magnesium (Mg), phosphorus. The results demonstrate a significant difference (p ¼ 0.0126) in the values of albumin in children with CP with GI disorders vs. those without. Additionally, a significant difference (p ¼ 0.0129) was found in Mg levels between CP children with constipation vs. GERD/esophagitis/feeding issues/gastrostomy. Results suggest that children with CP and GI disorders have decreased levels of albumin, but normal pre-albumin. The mechanism for this is not completely clear and although we acknowledge importance of nutritional intake for albumin level support, other mechanisms such as low grade chronic inflammation and increased gut and vascular permeability may play a role. The lower levels of Mg in children with CP and constipation could be secondary to the use of laxatives. Further prospective studies looking at nutritional protein intake, gut and vascular permeability and laxative use in this patient population are important for future optimization of health care management. © 2015 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights reserved.
Keywords: Cerebral Palsy Malnutrition Gastrointestinal disorders Albumin Magnesium
1. Introduction Under nutrition and growth failure are common findings in children with cerebral palsy (CP) and neurological impairments [1]. As a group, children with CP are smaller and poorly nourished compared with their typically developing peers [2]. These differences between affected and non-affected children are more noticeable with increasing age and severity of motor impairment
* Corresponding author. Department of Pediatrics, Nephrology Section, Texas Tech University Health Sciences Center, 1400 South Coulter Street, Amarillo, TX 79106, USA. E-mail address: [email protected] (T.L. Vasylyeva).
[2]. The most significant factor affecting the nutritional status of children with CP is inadequate intake to meet metabolic demands [3]. In addition, gastrointestinal (GI) diseases like gastroesophageal reflux disease (GERD) and constipation have been associated with increased frequency of these derangements. Under nutrition and growth failure in neurologically impaired children seem to be related to inappropriate caloric intake, altered nutrient needs, inability to self-feed and oral motor dysfunction. Up to one-third of pediatric patients have associated growth disorder and nutritional deficits [4]. Additionally, malnutrition affects quality of life and is associated with increased health care use. Although in the past under nutrition was considered as a natural spectrum of disease of neurologically impaired children, it is now recognized that adequate nutrition in these patients is essential [5].
http://dx.doi.org/10.1016/j.clnesp.2015.08.003 2405-4577/© 2015 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights reserved.
e68
C. Jaramillo et al. / Clinical Nutrition ESPEN 11 (2016) e67ee69
Electrolyte and micronutrient deficiencies are also documented in children with cerebral palsy. Iron, zinc, essential fatty acids and vitamins C, D and E were reported to be deficient in 15e50% of these children. Dietary calcium, vitamin D and phosphorus intakes are below the Daily Reference Intake in 50e80% of these children [6]. In a cross-sectional observational study performed to assess the adequacy of sodium, potassium, phosphorus and fluid intakes in children with cerebral palsy, it was shown that 60% of children were sodium deficient [7]. There were no deficiencies in potassium and only one child in the study was considered to have possible inadequate phosphorus intake [7]. The goal of this study was to determine whether GI disorders complicated CP impact children's development and metabolic status.
2. Materials and methods The charts of patients with CP followed in the specialized pediatric clinic, at Texas Tech University Health Science Center (TTUHSC, Amarillo) were retrospectively reviewed after IRB approval. TTUHSC clinic for special need children has three designated providers for CP patients, who followed standardized nutritional protocols and evaluated growth parameters with every visit. CP patients with and without GI disorder received the same or similar professional care. Patients were followed at least every three months with close attention to nutrition and growth. In general, younger children with gastrostomy tubes were on PediaSure® or if growth delay was noticed, on PediaSure® 1.5 Cal (AbbottNutrition). Older children with gastrostomy tubes were on Ensure® (AbbottNutrition), Peptamen Junior®/Peptamen Junior® Health Sciences), or Jevity®/Jevity® 1.2 Cal/Jevity® 1.5 Cal 1.5 (Nestle (AbbottNutrition). Formula preferences and caloric supplements were individually determined by clinical and social (availability, insurance coverage preferences) factors. Patients with adequate growth, who were able tolerate oral feeding were prescribed diet appropriate for age; if the growth curve plateaued or declined, they received additional caloric supplements. A total of the 268 medical records of pediatric patients under 18 years of age with diagnosis of neurologic impairments were reviewed. Ninety-six patients were excluded due to either absence of CP or insufficient data. Demographic data collected included weight in percentile (%p), length (%p) and body mass index (BMI, % p) (Table 1). The most resent laboratory data from were collected: pre-albumin, albumin, sodium (Na), potassium (K), chloride (Cl), bicarbonate (HCO3), calcium (Ca), magnesium (Mg), phosphorus (Phos) and vitamin D (Table 2).
Table 1 Demographics and gastrointestinal (GI) problems in children with cerebral palsy.
Mean age (years) Weight (%p) Length/height (%p) BMI (%p) Gender (n) Male Female GI problems Constipation (n) GERD (n) Esophagitis (n) Gastrostomy (n) Feeding difficulties (n)
GI disorder
No GI disorder
9.01 ± 0.36 31 ± 2.8 25.3 ± 2.7 43.6 ± 3.1
9.51 32.9 34.9 35.6
68 70
34 11
e e
69 24 11 43 13
e e e e e
e e e e e
± ± ± ±
0.74 4.9 4.5 4.9
p Value 0.19NS 0.60NS 0.12NS 0.19NS
Age, weight, length/height and BMI data is represented as Mean ± SEM; n ¼ total number; % p, percentile value; GI, gastrointestinal; GERD, gastro esophageal reflux disorder; NS, no significant.
Table 2 Lab chemistries of patients with Cerebral Palsy. Lab chemistries
GI disorder
Na (mM/L) K (mM/L) Cl (mM/L) HCO3 (mM/L) Ca (mg/dL) Mg (mg/dL) Phos (mg/dL) Vit D (mg/dL) Albumin (mg/dL) Pre-albumin (mg/dL)
138.7 4 116.4 24.4 9.6 2.1 4.7 40.4 3.9 19
± ± ± ± ± ± ± ± ± ±
0.4 0.1 13.6 0.4 0.05 0.03 0.1 2.9 0.05 0.9
No GI disorder
p value
± ± ± ± ± ± ± ± ± ±
0.85 0.34 0.2 0.98 0.66 0.15 0.79 0.09 0.0126* 0.57
138.6 4.2 105.4 23.5 9.6 2.1 5.1 33 4.1 18.4
0.5 0.1 0.5 0.4 0.1 0.06 0.2 2.7 0.06 1
Na; Sodium, K; Potassium, Cl; Chloride, HCO3; bicarbonate, Ca; calcium, Mg; magnesium, Phos; phosphorus, Vit D; Vitamin D, mM/L; millimolar/liter, mg/dL; milligram/deciliter. Data is represented as Mean ± SEM. *Statistical significance p ¼ <0.05.
2.1. Statistical analysis Initially the data for patients with and without GI disease were compared and subsequently a subgroup analysis by GI diagnosis was also done. Normality was checked and the variables that meet normality were analyzed by parametric t-test and ANOVA. The remaining variables were analyzed by non-parametric tests (ManneWhitney). “p values” less than or equal to 0.05 were considered as significant. The analysis was done by using Prismgraphpad (GraphPad Software, Inc.®, La Jolla, CA) software. 3. Results A total of 172 patients were included of which 45 did not have any GI co-morbidity, 69 patients had constipation and 58 had either GERD, esophagitis, gastrostomy and feeding difficulties (Table 1). There was a significant difference (p ¼ 0.0126) in the values of albumin levels in children with CP with and without gastrointestinal disorders. Group without GI comorbidity had higher albumin levels (Table 2). After a subgroup analysis, a significant difference (p ¼ 0.0129) was found in magnesium levels between children with CP and constipation and children with CP and GERD, esophagitis, feeding issues and/or gastrostomy. There were no other statistically significant differences in the main comparison groups or subgroups (Table 2). 4. Discussion This study showed a significant difference in the albumin levels in children with CP and GI disorders vs. those without. There were no differences in pre-albumin values between the groups, which makes inadequate intake less likely cause of this finding. Previous studies have determined that albumin and pre-albumin are less reliable indicators of nutritional status as it reflects the body's physiologic response to illness [6]. Although the low levels albumin in the GI group was statistically significant, it was not low enough to show immediate clinical impacts. The mechanism is not completely clear and although we acknowledge importance of nutritional intake for albumin level support, other mechanisms such as low grade chronic inflammation and increased gut and vascular permeability may play a role in patients with GI problems independently from CP. Lower caloric intake, lack of hand-mouth coordination and increased feeding times in patients who are unable to self-feed was a concern expressed in the previous publications and thought to contribute to insufficient intake [1,2,6]. Severely neurologically impaired patients are unable to communicate hunger and depend
C. Jaramillo et al. / Clinical Nutrition ESPEN 11 (2016) e67ee69
on caregiver, who may over or underestimate his/her caloric needs. Energy needs of children with cerebral palsy who ambulate and have athetosis are higher than those who do not, but in wellnourished, non-ambulatory children resting energy expenditure is significantly lower [6]. Also, higher severity of motor impairment has been associated with more feeding dysfunction, which itself is associated with poor nutritional status [2]. We did not have sufficient data on the degree of motor impairment, but focused on GI problems as a factor, which made difference in patients' management. Malnutrition affects the quality of life and is associated with increased health care use. Although in the past, under-nutrition was considered as a natural spectrum of disease of neurologically impaired children, it is now recognized that adequate nutrition in these patients is essential [5]. High caloric and adopted formulas, as we use in our clinic, might well accommodate nutritional needs of patients with CP with and without GI problems. Although we did not find any significant differences in anthropometric measurements in our patients, what we attributed to vigorous nutritional support and frequent follow up in our specialized clinic, undernutrition and growth failure are common findings in studies on neurologically impaired children and seem to be related to inappropriate caloric intake, altered nutrient needs, inability to selffeed and oral motor dysfunction [4,5]. Up to one-third of pediatric patients have associated growth disorder and nutritional deficits [4]. Evaluation of malnutrition in these children should include accurate growth and anthropometric measurements, a complete physical examination and biochemical metabolic studies. Height and length can be difficult to obtain due to contractures or scoliosis, but valid alternatives include upper arm length or lower leg length. It is difficult to overestimate needs for adequate nutrition for patients with CP whether they have GI problems or not: malnutrition has many adverse effects on the overall health of these patients. Decreased muscle strength can lead to cardiopulmonary complications due to weakness of pulmonary musculature and diminished cardiac work capacity. Reduced cerebral growth and delayed cognitive development are some of the neurological consequences. Furthermore, these children present with severe gastro esophageal reflux which is difficult to control [2]. High rates of poor oral intake, chronic esophagitis and suppurative lung disease have also been reported in developmentally disabled patients who present with feeding and nutritional issues [2]. In Campanozzi et al. study, which addressed impact of malnutrition on gastrointestinal disorders and gross motor abilities in children with CP, 33% had acute malnutrition grade I and 19% had acute malnutrition grade II [8]. Gastrostomy tube feeding has been shown to lead to improved weight gain. This is indicated in children with CP who have an unsafe swallow, unable to maintain a satisfactory nutritional state by oral feeding alone, are have exceedingly long oral feeding time and are dependent on nasogastric or gastrostomy tube feeding [9]. Children who have gastrostomies placed within the first year of life are more likely to exceed the fifth percentile for height and weight [6]. There were no significant differences in our CP patients with and without gastrostomy, indicating that timely gastrostomy tube placement could make a significant difference in a child development.
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Electrolyte and micronutrient deficiencies have also been documented in children with cerebral palsy. Iron, zinc, essential fatty acids and vitamins C, D and E were reported to be deficient in 15e50% of these children [6]. In a cross-sectional observational study, which was done to assess the adequacy of sodium, potassium, phosphorus and fluid intakes in children with CP, it was shown that 60% of children were sodium deficient. There were no deficiencies in potassium and only one child in the study was considered to have possible inadequate phosphorus intake [7]. In our subgroup analysis we found that children with CP and constipation have lower levels of Mg in comparison to those with CP and GERD, esophagitis, feeding issues and/or gastrostomy. The altered Mg levels we attributed to laxative use in patients with CP and persistent constipation. Mg levels need to be followed regularly in all patients with vigorously treated constipation to avoid hypomagnesemia. 5. Conclusions Further prospective studies looking at nutritional protein intake, gut and vascular permeability and laxative use in this patient population are important for optimization of future health care management. Conflict of interest None. References [1] Rempel G. The importance of good nutrition in children with cerebral palsy. Phys Med Rehab Clin N. Am 2015;26(1):39e56. http://dx.doi.org/10.1016/ j.pmr.2014.09.001. PubMed PMID: 25479778. [2] Kuperminc MN, Stevenson RD. Growth and nutrition disorders in children with cerebral palsy. Dev Disabil Res Rev 2008;14(2):137e46. http://dx.doi.org/ 10.1002/ddrr.14. PubMed PMID: 18646022; PubMed Central PMCID: PMC2830751. [3] 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(4):627e34. PubMed PMID: 8839510. [4] Karagiozoglou-Lampoudi T, Daskalou E, Vargiami E, Zafeiriou D. Identification of feeding risk factors for impaired nutrition status in paediatric patients with cerebral palsy. Acta Paediatr 2012;101(6):649e54. http://dx.doi.org/10.1111/ j.1651-2227.2012.02641.x. PubMed PMID: 22404086. [5] Nutrition in neurologically impaired children. Paediatr Child Health 2009;14(6):395e401. PubMed PMID: 20592978; PubMed Central PMCID: PMC2735385. [6] Marchand V, Motil KJ. Nutrition NCo. Nutrition support for neurologically impaired children: a clinical report of the North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition. J Pediatr Gastroenterol Nutr 2006;43(1):123e35. http://dx.doi.org/10.1097/01.mpg.0000228124.93841.ea. PubMed PMID: 16819391. [7] McGowan JE, Fenton TR, Wade AW, Branton JL, Robertson M. An exploratory study of sodium, potassium, and fluid nutrition status of tube-fed nonambulatory children with severe cerebral palsy. Appl Physiol Nutr Metab Physiologie appliquee, nutrition et metabolisme 2012;37(4):715e23. http:// dx.doi.org/10.1139/h2012-050. PubMed PMID: 22667347. [8] Campanozzi A, Capano G, Miele E, Romano A, Scuccimarra G, Del Giudice E, et al. Impact of malnutrition on gastrointestinal disorders and gross motor abilities in children with cerebral palsy. Brain Dev 2007;29(1):25e9. http:// dx.doi.org/10.1016/j.braindev.2006.05.008. PubMed PMID: 16843628. [9] Sullivan PB. Gastrointestinal disorders in children with neurodevelopmental disabilities. Dev Disabil Res Rev 2008;14(2):128e36. http://dx.doi.org/10.1002/ ddrr.18. PubMed PMID: 18646021.