PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of pchealthPaediatrics and Child Health HomepageCurrent IssueSubscription PageSubmissions Pagewww.pulsus.comPaediatrics and Child Health
 
Paediatr Child Health. 2009 Jul-Aug; 14(6): 395–401.
PMCID: PMC2735385

Language: English | French

Nutrition in neurologically impaired children

Abstract

Malnutrition, either under- or overnutrition, is a common condition among neurologically impaired children. Energy needs are difficult to define in this heterogeneous population, and there is a lack of information on what normal growth should be in these children. Non-nutritional factors may influence growth, but nutritional factors such as insufficient caloric intake, excessive nutrient losses and abnormal energy metabolism also contribute to growth failure. Malnutrition is associated with significant morbidity, while nutritional rehabilitation improves overall health. Nutritional support should be an integral part of the management of neurologically impaired children, and should focus not only on improving nutritional status but also on improving quality of life for patients and their families. When considering nutritional intervention, oromotor dysfunction, gastroesophageal reflux and pulmonary aspiration must be addressed and a multidisciplinary team should be involved. Children at risk for nutrition-related problems should be identified early. An assessment of nutritional status should be performed at least yearly, and more frequently in infants and young children, or in children at risk for malnutrition. Oral intake should be optimized if safe, but enteral tube feedings should be initiated in children with oromotor dysfunction, leading to clinically significant aspiration, or in children unable to maintain an adequate nutritional status with oral intake. Nasogastric tube feeding should be used for short-term intervention, but if long-term nutritional intervention is required, a gastrostomy should be considered. Antireflux procedures should be reserved for children with significant gastroesophageal reflux. The patient’s response to nutritional intervention should be carefully monitored to avoid excessive weight gain after initiation of enteral nutrition, and paediatric formulas should be used to avoid micronutrient deficiencies.

Keywords: Cerebral palsy, Growth, Neurologically impaired, Nutrition

Résumé

La malnutrition, qu’il s’agisse de sous-alimentation ou de suralimentation, est courante chez les enfants ayant une déficience neurologique. Les besoins en énergie sont difficiles à définir au sein de cette population hétérogène. De plus, on manque d’information sur ce qui constitue la croissance normale chez ces enfants. Des facteurs non nutritionnels peuvent influer sur la croissance, mais des facteurs nutritionnels, tels qu’un apport calorique insuffisant, des pertes excessives d’éléments nutritifs et un métabolisme énergétique anormal, contribuent également au retard de croissance de ces enfants. La malnutrition est liée à une importante morbidité, tandis que la réadaptation nutritionnelle améliore l’état de santé global. Le soutien nutritionnel doit faire partie intégrante de la prise en charge des enfants ayant une déficience nutritionnelle et viser non seulement à améliorer l’état nutritionnel, mais également la qualité de vie des patients et de leur famille. Au moment d’envisager une intervention nutritionnelle, il faut tenir compte du dysfonctionnement oromoteur, du reflux gastro-œsophagien et de l’aspiration pulmonaire, et une équipe multidisciplinaire doit se concerter. Il faut repérer rapidement les enfants vulnérables à des troubles nutritionnels et procéder à une évaluation de leur état nutritionnel au moins une fois par année, et plus souvent chez les nourrissons et les jeunes enfants ou chez les enfants qui risquent de souffrir de malnutrition. Il faut optimiser l’apport oral s’il est sécuritaire, mais entreprendre une alimentation entérale chez les enfants ayant un dysfonctionnement oromoteur qui provoque une aspiration marquée ou chez ceux qui sont incapables de maintenir un état nutritionnel suffisant au moyen de l’apport oral. Il faut réserver l’alimentation par sonde nasogastrique aux interventions à court terme, mais si une intervention nutritionnelle prolongée s’impose, il faut envisager la gastrostomie. Il faut réserver les mesures antireflux aux enfants présentant un reflux gastro-œsophagien considérable. Il faut surveiller étroitement la réponse du patient à l’intervention nutritionnelle afin d’éviter une prise de poids excessive après l’amorce de l’alimentation entérale, et privilégier les préparations pédiatriques afin d’éviter les carences en micronutriments.

Chronic diseases have a significant impact on nutritional status. In neurologically impaired (NI) patients, malnutrition negatively affects quality of life and is associated with increased health care use and impaired participation in various activities (1). Nutritional rehabilitation has been associated with improved overall health, improved peripheral circulation, healing of decubitus ulcers, decreased spasticity, decreased irritability and improved gastroesophageal reflux in patients with neurodevelopmental disabilities (25). A significant proportion of children with neurodevelopmental disabilities are undernourished (69). This state of malnutrition may have been once considered to be part of the disease, but there is now a better recognition of the importance of nutrition in this population. Nutritional care of children with neurodevelopmental disabilities has improved with the advent of less invasive enteral access methods and better tolerated enteral formulas. We need to provide these often complicated patients with appropriate nutritional support by involving a multidisciplinary team of physicians, nurses, dietitians, speech and occupational therapists, and psychologists working to improve the child’s and the family’s quality of life.

METHODS

Members of the Canadian Paediatric Society’s Nutrition and Gastroenterology Committee, most of whom are involved in caring for children with neurodevelopmental disabilities, reviewed and interpreted the literature and developed the present position statement on the basis of their experience and research activity. It replaces the previous position statement published in 1994 (10).

NUTRITIONAL STATUS OF CHILDREN WITH NEURODEVELOPMENTAL DISABILITY

Height, weight and weight-for-height of children with neurodevelopmental disabilities are significantly below standards, and other indicators of nutritional status, such as triceps skinfold thickness and mid-arm circumference, are also affected (3,69,11). While most children with cerebral palsy (CP) are undernourished, 8% to 14% are overweight (7).

PREDICTORS OF POOR NUTRITIONAL STATUS

The incidence and the severity of malnutrition in NI children increases with the duration and the severity of neurological impairment (7,11,12). Growth of children with spastic quadriplegia is more severely affected, but children with diplegia or hemiplegia also have altered growth (7). The presence of oromotor dysfunction correlates with a greater risk of malnutrition (1320). Physicians should identify severely affected patients with oromotor dysfunction and monitor them very closely because they are the ones most likely to require enteral nutrition support.

CAUSES OF MALNUTRITION

Inadequate intake

The caloric intake of children with CP is lower than that of age-matched controls (21,22). Some patients are able to feed themselves independently but lack hand-mouth coordination and may, therefore, spill an excessive amount of food. These children may also eat more slowly than other members of the household or require more time to eat than is allowed by the school schedule. As a result, regular family or school mealtime may be too short for them to ingest a sufficient amount of food. Severely affected children are dependent on a caregiver at mealtime and are often unable to communicate hunger and satiety. The caregiver regulates their food intake. This may lead to underfeeding because it has been shown that the caregiver often overestimates the time spent feeding the child and also overestimates the child’s caloric intake (22,23). Increasing caloric intake with tube feedings improves nutritional status in NI children (4,2426).

Increased losses

Gastroesophageal reflux affects a significant proportion of children with CP (27,28). Frequent emesis and regurgitation may be a source of caloric loss. Reflux esophagitis may cause discomfort leading to food refusal and further decreasing food intake.

Altered metabolism

The resting energy expenditure is lower in children with CP than in controls matched for age and weight (22,29,30). Children who are hypotonic and nonambulatory require few calories above the resting energy expenditure to thrive (31). However, children with increased muscle tone or with athetoid forms of CP may require an increased amount of calories (32). Children with mild to moderate diplegic or hemiplegic CP who can ambulate often require more calories to perform daily activities than their normal counterparts (33,34).

Oromotor dysfunction

Oromotor dysfunction affects up to 90% of patients with CP (23), and is a major contributor to malnutrition in NI children (13,14,1620). Parents often report poor suck, breastfeeding difficulties, problems with the introduction of solid food and choking or coughing associated with feedings, even before the diagnosis of CP is made (21,23). Eighty per cent of these children have been fed nonorally at least once as infants (23). Children with oromotor dysfunction have a greater risk of malnutrition and often have lower weight, height and weight-for-height Z-scores than children with normal oromotor function (13,14,1620). Inadequate sucking, dysfunctional swallowing, persistent extrusion reflex, drooling due to inadequate lip closure and reduced ability to chew make oral feeding difficult. Prolonged mealtimes, sometimes 3 h per day to 6 h per day, may not even be sufficient to compensate for the child’s feeding inefficiency resulting in inadequate caloric intake (15,35).

NONNUTRITIONAL FACTORS AFFECTING GROWTH

Although malnutrition plays a major role in linear growth failure, other factors may affect growth in the NI population because height Z-scores decrease with age independently of weight Z-scores (36). Neurological disease itself may affect linear growth because linear growth failure correlates with the severity of cognitive defect and with ambulatory status (7,11,36). In children with hemiplegia, the affected side is usually shorter and smaller than the nonaffected side, thus demonstrating the effect of the neurological disease on growth (36). Other non-nutritional factors affecting linear growth include specific syndromes, endocrine dysfunction, ethnicity, genetic potential and pubertal status.

NUTRITIONAL ASSESSMENT

Clinical observation

Nutritional history

The child’s nutritional history should review not only the type (purees, liquids and solid food) and the amount of food that the child eats, but the degree of dependency on a caregiver and the length of a typical meal. If the child is able to self-feed, the amount of spilling should be assessed. Signs of oromotor dysfunction such as drooling, persistent extrusion reflex, spilling and delayed swallowing, and symptoms of aspiration, such as choking and coughing, should be sought. Besides these functional considerations, the stress associated with meals and the quality of the interaction between the caregiver, the child and the family at mealtime should be explored. Caring for NI children is very demanding and some children may be neglected.

Observation of a meal may be useful to determine the amount of food offered, spilled and ingested and to assess the parent-child interaction. Measuring oxygen saturation during a meal will detect desaturation that may result from aspiration (37).

Medical history

The medical history should include an assessment of gastroesophageal reflux symptoms such as emesis, regurgitation, pain or food refusal. The physician should also look for chronic respiratory problems, recurrent pneumonia and respiratory symptoms suggestive of chronic aspirations. Aspiration due to swallowing dysfunction usually presents with coughing or choking associated with meals. Reflux-related aspiration episodes are often accompanied by regurgitation of gastric contents or frank emesis. In many children, the two problems overlap. Aspiration may also be asymptomatic. Progressive fatigue toward the end of the meal may be suggestive of desaturation. Among other aspects of the medical history that should be investigated are recurrent infections, decubitus ulcers and constipation. A review of the child’s medication is important because some drugs, particularly anticonvulsants such as valproic acid and topiramate, may affect appetite and, therefore, growth.

Growth history

Birth weight, length and head circumference and all previous weight, length and head circumference measurements should be obtained and plotted on a Centers for Disease Control and Prevention/National Center for Health Statistics (USA) growth chart. This will help determine whether there is a decrease in growth velocity. Midparental height may be useful to estimate growth potential.

Physical examination

The most important part of the physical examination is measurement of weight and length. They should be obtained with the proper technique on an adequately calibrated scale. The child should be wearing little or no clothing. Older children who are unable to stand may be weighed while held by a parent, and the difference should be calculated, or a wheelchair scale should be used. The supine length should be obtained in children younger than two years of age and in older children unable to stand. In children with skeletal deformities (scoliosis or contractures), alternative measures, such as lower leg length or upper arm length, may be obtained (38,39). References are available for these alternative measurements (39). Head circumference should also be obtained. Triceps skinfold thickness and mid-arm circumference are often helpful in assessing nutritional status and may even be more accurate than weight-for-height to detect malnutrition (40). Subscapular skinfold is often less affected than triceps skinfold in malnourished NI children (9).

The physical examination should detect signs of malnutrition such as decubitus ulcers and peripheral edema. Contractures, scoliosis, increased or decreased muscle tone as well as choreoathetoid movements should be assessed. Careful examination of the teeth and mouth are important because gingival hyperplasia and poor oral health may cause discomfort, interfering with oral intake. Auscultation of the lungs may reveal signs of chronic aspiration. Examining for digital clubbing, and assessing oxygen saturation may be helpful. Abdominal examination and, if needed, a rectal examination, may reveal constipation.

Investigation

Extensive bloodwork is usually not necessary. A complete blood count may help detect iron deficiency. Serum albumin may reflect nutritional status, but is not very reliable in this population (41). Electrolytes are usually normal. Phosphorus, calcium, alkaline phosphatase and vitamin D levels may be measured in patients with suspected osteoporosis and may be combined with a bone density scan.

For children with suspected oromotor dysfunction, a good clinical evaluation by an experienced clinician may be sufficient to detect fluid aspiration. A swallowing study using different food and liquid textures may be helpful to assess the efficiency and safety of the swallowing process, and may provide the physician with information regarding the child’s risk for aspiration. The swallowing study can also guide recommendations with respect to position for feeds and possible texture restrictions. However, the reproducibility of the swallowing study may be questioned, and the clinician should also consider clinical symptoms of aspiration displayed by the child and be cautious about making decisions based solely on the swallowing study.

The diagnosis of gastroesophageal reflux is often made based on symptoms. An upper gastrointestinal series may be indicated to diagnose possible anatomical abnormalities, such as superior mesenteric artery syndrome, which is frequent in children with scoliosis or who have rapid weight loss. In children with chronic aspiration, a 24 h esophageal pH probe study may help determine whether aspiration is secondary to gastroesophageal reflux. A gastric emptying scan is useful in diagnosing delayed gastric emptying and possibly pulmonary aspiration of gastric content.

PROBLEMS FREQUENTLY ENCOUNTERED IN THE NI POPULATION

Gastroesophageal reflux

Gastroesophageal reflux affects a large portion of children with CP (27,28). Delayed gastric emptying may also be seen. Consequences of gastroesophageal reflux include emesis resulting in increased nutrient losses; reflux esophagitis, which may lead to food refusal; and pulmonary aspiration of gastric contents. Gastroesophageal reflux should be treated aggressively with proton pump inhibitors or H2 blockers. Prokinetics may also be useful in some cases. Some children with severe gastroesophageal reflux that is unresponsive to medical therapy may require a surgical antireflux procedure (ARP). However, patients should be selected carefully because the NI population is known to have more complications after this type of surgery than the general population (4245).

Pulmonary aspiration

Pulmonary aspiration may be the result of swallowing dysfunction with aspiration of saliva and/or aspiration of gastric contents in patients with gastroesophageal reflux. It is important to differentiate between these two entities to treat the patient adequately.

Additionally, respiratory symptoms of viral origin and respiratory symptoms from aspiration may be difficult to differentiate. Community-acquired pneumonia in an NI child may be mistakenly diagnosed as ‘aspiration pneumonia’, leading to investigation and intervention that may not always be warranted.

Osteoporosis

Osteopenia and osteoporosis are frequently encountered in the NI population (46,47). Among the factors contributing to this problem are reduced ambulation and weight-bearing activity, malnutrition, limited sun exposure and the use of anticonvulsant medication, which alters vitamin D metabolism (4852). Dietary intake of vitamin D, phosphorus and calcium are insufficient in a significant proportion of these children (53,54). This may be exacerbated by using an adult type formula with a calorie-to-nutrient ratio that is inadequate for a growing child.

It may be difficult to evaluate bone mineral density in these patients because of skeletal deformities and the inability to stay still. While bone densitometry remains the gold standard, bone quantitative ultrasonography may be easier to perform in these children and may become a useful test in the future (55).

Pathological fractures may be very debilitating, and osteoporosis should be prevented with an adequate intake of dietary calcium, phosphorus and vitamin D. Biphosphonates have been used in these children with good results (56).

NUTRITIONAL INTERVENTION

Determine energy needs

Energy needs are difficult to define in this heterogeneous population. Most methods used to determine energy requirements tend to overestimate the needs of NI children (30,31). Energy requirements must be individualized to take into account mobility, muscle tone, activity level, altered metabolism and growth. Indirect calorimetry may be used, but is not available everywhere. Different methods to calculate energy needs are summarized in Table 1. However, the best way to ensure adequate intake is to monitor weight gain in response to dietary therapy.

TABLE 1
Calculating energy needs of neurologically impaired patients

Improve oral intake

The easiest and least invasive method to increase energy intake is to improve oral intake. Adequate positioning of the child during meals is very important. Oromotor skills may be improved with therapy, although results may be disappointing (5759). Food consistency may be adjusted with thickening agents to provide the best consistency for the patient as determined by a swallowing study. Food caloric density may be increased with the help of a dietitian, by adding modular nutrients, modifying recipes or using high-calorie formulas. Oral intake can be maintained as long as there is no risk of aspiration, the child is growing well and the time required to feed the child remains within acceptable limits.

Enteral nutrition

When oral intake is unsafe, insufficient or too time consuming, enteral nutrition should be initiated.

Enteral access

The type of enteral access will depend on the anticipated duration of enteral nutrition support as well as the clinical status of the child.

Nasogastric tubes are minimally invasive but are easily dislodged and have local complications (sinusitis, congestion, otitis and skin irritation). Generally, nasogastric feeds should only be used for short-term nutritional support (less than three months). They may be useful to use for a nutrition challenge to assess tolerance and efficacy.

For long-term enteral nutrition support (more than three months), a gastrostomy should be considered. Gastrostomies are more invasive, but are also more convenient and esthetically acceptable. The gastrostomy may be performed by open surgery, laparoscopic surgery, endoscopy (percutaneous endoscopic gastrostomy) or interventional radiology. The decision needs to take into account the institutional expertise and the need for a concomitant ARP. Children with symptoms of reflux who do not respond to medical therapy or with evidence of pulmonary aspiration caused by their reflux should undergo a surgical gastrostomy along with an ARP. In children without symptoms of reflux or with mild reflux responding well to medical treatment, a percutaneous approach, either endoscopic or radiological, may be used. There is no role for a prophylactic ARP (6063). The choice between a gastrostomy with or without an ARP has to be carefully evaluated because the failure rate and the incidence of major complications following ARP are high in NI children (4244,64,65). In difficult cases, it may be useful to attempt a trial of nasogastric feeds for one month to assess tolerance before making a decision. This is particularly true in patients for whom the indication of ARP is recurrent aspiration pneumonia because it is often difficult to differentiate aspiration from swallowing dysfunction and aspiration from gastroesophageal reflux. Some children may develop gastroesophageal reflux after a gastrostomy. It is unclear whether this is a consequence of the change in volume, consistency and composition of the feeds or a consequence of the procedure. If this problem occurs, medical treatment with prokinetics and changes in the formula or in the rate and volume of feeds should be attempted before resorting to an ARP.

In some cases, patients may require jejunal feeds. Nasojejunal feeds should be used for short-term enteral nutrition in patients with gastroesophageal reflux or gastric dysmotility. Long-term gastrojejunal feeds should only be used in patients with reflux who are poor candidates for ARP. Gastrojejunal tubes often migrate back into the stomach and need to be repositioned under fluoroscopic guidance. In addition, these tubes tend to be of smaller calibre and are more likely to get obstructed. A jejunostomy may be an option in selected cases.

Enteral formulas

Before 12 months of age, an infant formula should be used. In patients with high-caloric needs or with poor tolerance to increased formula volume, the formula may be concentrated and/or modular nutrients, such as glucose polymer or lipids, may be added. The addition of modular nutrients should be made with the help of a dietician to ensure that the final composition of the diet is adequate, and to avoid preparation errors. Casein hydrolysates and amino acid-based formulas may be used in selected patients.

After 12 months of age, a paediatric 1 kcal/mL formula is preferred. A 1.5 kcal/mL formula may be used with careful monitoring of hydration status. Fibre-containing formulas are often used to alleviate constipation. Adult formulas should be avoided because the calorie-to-nutrient ratio is inadequate for children. Their use may result in calcium, phosphorus and vitamin deficiency, especially in patients with low-caloric needs. Most children will tolerate a polymeric formula, but some children may require a semielemental or elemental formula (66).

Feeding regimen

The choice of feeding regimen will be based on the child’s enteral access, activities, caloric needs and tolerance to feeds. In children with poor tolerance to gastric feeds, continuous feeds may be necessary. They may also be necessary for children with dumping syndrome. Continuous feeds should always be used when the child has a gastrojejunal tube. For ambulatory children who have scheduled daily activities, bolus feeds are preferred because they allow more freedom. A child with high-caloric needs or with poor tolerance to volume may benefit from a combination of daytime boluses and nocturnal continuous feeds.

Monitor response to nutritional intervention

NI children are often unable to communicate hunger and satiety. In tube-fed children, this may lead to overfeeding; some children become overweight after initiation of gastrostomy feedings (26). Because these children are often wheelchair bound and dependent on a caregiver for most of their transfers, it is important to avoid excessive weight gain. These children often have a decreased lean body mass, and excess weight gain is mostly fat mass. In children younger than three years of age and in children with normal activity level, weight-for-height should be in the 50th percentile. For older children who are wheelchair bound but able to accomplish transfers, weight-for-height should be in the 25th percentile. For the bedridden patient, the 10th percentile may be sufficient (32).

ETHICAL AND SOCIAL CONSIDERATIONS

Providing adequate nutrition should be a priority when taking care of NI children. The goal should be to improve their quality of life. Many NI children will ultimately need a gastrostomy. Although there is no randomized controlled trial comparing oral versus gastrostomy feedings in NI children, gastrostomies have been shown to improve nutritional status, to reduce the time spent feeding the child and to improve quality of life (2426,59,6771). For parents, however, a gastrostomy may be difficult to accept because they may see it as a failure on their part to feed their child adequately. The physician should respect the parents’ wishes and the gastrostomy should be performed when the parents are ready, unless continuing oral feeds is compromising the child’s health or nutritional status. Excellent communication and the support of the whole caregiving team are important (72).

CONCLUSION

Malnutrition should not be considered normal in NI children. Nutritional intervention should be provided by a multidisciplinary team of professionals to ensure adequate growth, improve quality of life and optimize functional status. Early nutritional intervention, appropriate support and continuing follow-up are necessary to ensure success.

RECOMMENDATIONS

  • Nutritional support should be an integral part of the management of NI children.
  • A multidisciplinary team should be involved in the nutritional care of NI children.
  • Children at risk of nutrition-related problems should be identified early.
  • Assessment of nutritional status should be performed at least annually in NI children, and more frequently in infants and young children or in children at risk.
  • Oral intake should be optimized if safe for the child.
  • Enteral tube feedings should be initiated in children with oromotor dysfunction leading to clinically significant aspiration or in children unable to maintain adequate nutritional status with oral intake.
  • Nasogastric tube feeding should be used for short-term (less than three months) intervention.
  • For the child requiring long-term nutritional intervention, a gastrostomy should be considered.
  • ARPs should be reserved for children with significant gastroesophageal reflux.
  • Response to nutritional intervention should be carefully monitored to avoid excessive weight gain after initiation of enteral nutrition.
  • Paediatric formulas should be used to avoid micronutrient deficiencies.

ACKNOWLEDGEMENTS

This position statement was reviewed by the Canadian Paediatric Society’s Community Paediatrics and Psychosocial Paediatric Committees.

Footnotes

NUTRITION AND GASTROENTEROLOGY COMMITTEE

Members: Drs Margaret Boland, Children’s Hospital of Eastern Ontario, Ottawa, Ontario; Jeff Critch, Janeway Child Health Centre, St John’s, Newfoundland; Jae Hong Kim, UCSD Medical Center, San Diego, California, USA; Valérie Marchand, Sainte-Justine UHC, Montreal, Quebec (chair); Theodore Prince, Calgary, Alberta (board representative); Marli Ann Robertson, Alberta Children’s Hospital, Calgary, Alberta

Liaisons: Dr George Davidson, BC Children’s Hospital, Vancouver, British Columbia (Human Milk Banking Association); Ms Joanne Gilmore, Toronto Public Health, Toronto, Ontario (Breastfeeding Committee for Canada); Dr Frank Greer, Madison, Wisconsin, USA (American Academy of Pediatrics, Committee on Nutrition); Ms Jennifer McCrea, Ottawa, Ontario (Office of Nutrition Policy and Promotion, Health Canada); Ms Eunice Misskey, Regina, Saskatchewan (Dietitians of Canada); Ms Christina Zehaluk, Ottawa, Ontario (Bureau of Nutritional Sciences, Health Canada)

Principal author: Dr Valérie Marchand, Sainte-Justine UHC, Montreal, Quebec

The recommendations in this statement do not indicate an exclusive course of treatment or procedure to be followed. Variations, taking into account individual circumstances, may be appropriate.

All Canadian Paediatric Society position statements/notes are reviewed, revised or retired as needed on a regular basis.

For the current version, please consult the “Position Statements” section of the CPS Web site (www.cps.ca/english/publications/statementsindex.htm).

La version française intégrale est accessible à www.cps.ca/francais/publications/Nutrition.htm.

REFERENCES

1. Samson-Fang L, Fung E, Stallings VA, et al. Relationship of nutritional status to health and societal participation in children with cerebral palsy. J Pediatr. 2002;141:637–43. [PubMed]
2. Patrick J, Boland M, Stoski D, Murray GE. Rapid correction of wasting in children with cerebral palsy. Dev Med Child Neurol. 1986;28:734–9. [PubMed]
3. Shapiro BK, Green P, Krick J, Allen D, Capute AJ. Growth of severely impaired children: Neurological versus nutritional factors. Dev Child Neurol. 1986;28:729–33. [PubMed]
4. Sanders KD, Cox K, Cannon R, et al. Growth response to enteral feeding by children with cerebral palsy. J Parenter Enteral Nutr. 1990;14:23–6. [PubMed]
5. 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. [PubMed]
6. Krick J, Murphy-Miller P, Zeger S, Wright E. Pattern of growth in children with cerebral palsy. J Am Diet Assoc. 1996;96:680–5. [PubMed]
7. Stallings VA, Charney EB, Davies JC, Cronk CE. Nutritional status and growth of children with diplegic or hemiplegic cerebral palsy. Dev Med Child Neurol. 1993;35:997–1006. [PubMed]
8. Stallings VA, Cronk CE, Zemel BS, Charney EB. Body composition in children with spastic quadriplegic cerebral palsy. J Pediatr. 1995;126:833–9. [PubMed]
9. Stallings VA, Charney EB, Davies JC, Cronk CE. Nutrition-related growth failure of children with quadriplegic cerebral palsy. Dev Med Child Neurol. 1993;35:126–38. [PubMed]
10. Canadian Paediatric Society, Nutrition Committee [Principal authors: J Patrick, P Pencharz] Undernutrition in children with a neurodevelopmental disability. CMAJ. 1994;151:753–9. [PMC free article] [PubMed]
11. Stevenson RD, Hayes RP, Cater LV, Blackman JA. Clinical correlates of linear growth in children with cerebral palsy. Dev Med Child Neurol. 1994;36:135–42. [PubMed]
12. Sánchez-Lastres J, Eirís-Puñal J, Otero-Cepeda JL, Pavón-Belinchón P, Castro-Gago M. Nutritional status of mentally retarded children in north-west Spain. I. Anthropometric indicators. Acta Paediatr. 2003;92:747–53. [PubMed]
13. Fung EB, Samson-Fang L, Stallings VA, et al. Feeding dysfunction is associated with poor growth and health status in children with cerebral palsy. J Am Diet Assoc. 2002;102:361–73. [PubMed]
14. Thommessen M, Riis G, Kase BF, Larsen S, Heiberg A. Energy and nutrient intakes of disabled children: Do feeding problems make a difference? J Am Diet Assoc. 1991;91:1522–5. [PubMed]
15. Sullivan PB, Lambert B, Rose M, Ford-Adams M, Johnson A, Griffiths P. Prevalence and severity of feeding and nutritional problems in children with neurological impairment: Oxford Feeding Study. Dev Med Child Neurol. 2000;42:674–80. [PubMed]
16. Sullivan PB, Juszczak E, Lambert BR, Rose M, Ford-Adams ME, Johnson A. Impact of feeding problems on nutritional intake and growth: Oxford Feeding Study II. Dev Med Child Neurol. 2002;44:461–7. [PubMed]
17. Troughton KE, Hill AE. Relation between objectively measured feeding competence and nutrition in children with cerebral palsy. Dev Med Child Neurol. 2001;43:187–90. [PubMed]
18. Thommessen M, Heiberg A, Kase BF, Larsen S, Riis G. Feeding problems, height and weight in different groups of disabled children. Acta Paediatr Scand. 1991;80:527–33. [PubMed]
19. Motion S, Northstone K, Emond A, Stucke S, Golding J. Early feeding problems in children with cerebral palsy: Weight and neurodevelopmental outcomes. Dev Med Child Neurol. 2002;44:40–3. [PubMed]
20. Krick J, Van Duyn MA. The relationship between oral-motor involvement and growth: A pilot study in a pediatric population with cerebral palsy. J Am Diet Assoc. 1984;84:555–9. [PubMed]
21. Reilly S, Skuse D. Characteristics and management of feeding problems of young children with cerebral palsy. Dev Med Child Neurol. 1992;34:379–88. [PubMed]
22. 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. [PubMed]
23. Reilly S, Skuse D, Poblete X. Prevalence of feeding problems and oral motor dysfunction in children with cerebral palsy: A community survey. J Pediatr. 1996;129:877–82. [PubMed]
24. Kong CK, Wong HS. Weight-for-height values and limb anthropometric composition of tube-fed children with quadriplegic cerebral palsy. Pediatrics. 2005;116:e839–45. [PubMed]
25. Corwin DS, Isaacs JS, Georgeson KE, Bartolucci AA, Cloud HH, Craig CB. Weight and length increases in children after gastrostomy placement. J Am Diet Assoc. 1996;96:874–9. [PubMed]
26. Rempel GR, Colwell SO, Nelson RP. Growth in children with cerebral palsy fed via gastrostomy. Pediatrics. 1988;82:857–62. [PubMed]
27. Ravelli AM, Milla PJ. Vomiting and gastroesophageal motor activity in children with disorders of the central nervous system. J Pediatr Gastroenterol Nutr. 1998;26:56–63. [PubMed]
28. Sondheimer JM, Morris BA. Gastroesophageal reflux among severely retarded children. J Pediatr. 1979;94:710–4. [PubMed]
29. Azcue MP, Zello GA, Levy LD, Pencharz PB. Energy expenditure and body composition in children with spastic quadriplegic cerebral palsy. J Pediatr. 1996;129:870–6. [PubMed]
30. Bandini LG, Puelzl-Quinn H, Morelli JA, Fukagawa NK. Estimation of energy requirements in persons with severe central nervous system impairment. J Pediatr. 1995;126:828–32. [PubMed]
31. Hogan SE. Energy requirements of children with cerebral palsy. Can J Diet Pract Res. 2004;65:124–30. [PubMed]
32. Krick J, Murphy PE, Markham JF, Shapiro BK. A proposed formula for calculating energy needs of children with cerebral palsy. Dev Med Child Neurol. 1992;34:481–7. [PubMed]
33. Rose J, Medeiros JM, Parker R. Energy cost index as an estimate of energy expenditure of cerebral-palsied children during assisted ambulation. Dev Med Child Neurol. 1985;27:485–90. [PubMed]
34. Rose J, Gamble JG, Burgos A, Medeiros J, Haskell WL. Energy expenditure index of walking for normal children and for children with cerebral palsy. Dev Med Child Neurol. 1990;32:333–40. [PubMed]
35. Gisel EG, Patrick J. Identification of children with cerebral palsy unable to maintain a normal nutritional state. Lancet. 1988:283–6. [PubMed]
36. Stevenson RD, Roberts CD, Vogtle L. The effect of non-nutritional factors on growth in cerebral palsy. Dev Med Child Neurol. 1995;37:124–30. [PubMed]
37. Rogers BT, Arvedson J, Msall M, Demerath RR. Hypoxemia during oral feeding of children with severe cerebral palsy. Dev Med Child Neurol. 1993;35:3–10. [PubMed]
38. Hogan SE. Knee height as a predictor of recumbent length for individuals with mobility-impaired cerebral palsy. J Am Coll Nutr. 1999;18:201–5. [PubMed]
39. Spender QW, Cronk CE, Charney EB, Stallings VA. Assessment of linear growth of children with cerebral palsy: Use of alternative measures to height or length. Dev Med Child Neurol. 1989;31:206–14. [PubMed]
40. Samson-Fang LJ, Stevenson RD. Identification of malnutrition in children with cerebral palsy: Poor performance of weight-for-height centiles. Dev Med Child Neurol. 2000;42:162–8. [PubMed]
41. Lark RK, Williams CL, Stadler D, et al. Serum prealbumin and albumin concentrations do not reflect nutritional state in children with cerebral palsy. J Pediatr. 2005;147:695–7. [PubMed]
42. Richards CA, Andrews PL, Spitz L, Milla PJ. Nissen fundoplication may induce gastric myoelectrical disturbance in children. J Pediatr Surg. 1998;33:1801–5. [PubMed]
43. Martinez DA, Ginn-Pease ME, Caniano DA. Sequelae of antireflux surgery in profoundly disabled children. J Pediatr Surg. 1992;27:267–71. [PubMed]
44. Pearl RH, Robie DK, Ein SH, et al. Complications of gastroesophageal antireflux surgery in neurologically impaired versus neurologically normal children. J Pediatr Surg. 1990;25:1169–73. [PubMed]
45. Kimber C, Kiely EM, Spitz L. The failure rate of surgery for gastro-oesophageal reflux. J Pediatr Surg. 1998;33:64–6. [PubMed]
46. Henderson RC, Kairalla JA, Barrington JW, Abbas A, Stevenson RD. Longitudinal changes in bone density in children and adolescents with moderate to severe cerebral palsy. J Pediatr. 2005;146:769–75. [PubMed]
47. Henderson RC, Lark RK, Gurka MJ, et al. Bone density and metabolism in children and adolescents with moderate to severe cerebral palsy. Pediatrics. 2002;110:e5. [PubMed]
48. Henderson RC, Kairalla J, Abbas A, Stevenson RD. Predicting low bone density in children and young adults with quadriplegic cerebral palsy. Dev Med Child Neurol. 2004;46:416–9. [PubMed]
49. Bischof F, Basu D, Pettifor JM. Pathological long-bone fractures in residents with cerebral palsy in a long-term care facility in South Africa. Dev Med Child Neurol. 2002;44:119–22. [PubMed]
50. Morijiri Y, Sato T. Factors causing rickets in institutionalised handicapped children on anticonvulsant therapy. Arch Dis Child. 1981;56:446–9. [PMC free article] [PubMed]
51. Baer MT, Kozlowski BW, Blyler EM, Trahms CM, Taylor ML, Hogan MP. Vitamin D, calcium, and bone status in children with developmental delay in relation to anticonvulsant use and ambulatory status. Am J Clin Nutr. 1997;65:1042–51. [PubMed]
52. Tolman KG, Jubiz W, Sannella JJ, et al. Osteomalacia associated with anticonvulsant drug therapy in mentally retarded children. Pediatrics. 1975;56:45–50. [PubMed]
53. Duncan B, Barton LL, Lloyd J, Marks-Katz M. Dietary considerations in osteopenia in tube-fed nonambulatory children with cerebral palsy. Clin Pediatr (Phila) 1999;38:133–7. [PubMed]
54. Fried MD, Pencharz PB. Energy and nutrient intakes of children with spastic quadriplegia. J Pediatr. 1991;119:947–9. [PubMed]
55. Hartman C, Brik R, Tamir A, Merrick J, Shamir R. Bone quantitative ultrasound and nutritional status in severely handicapped institutionalized children and adolescents. Clin Nutr. 2004;23:89–98. [PubMed]
56. Henderson RC, Lark RK, Kecskemethy HH, Miller F, Harcke HT, Bachrach SJ. Biphosphonates to treat osteopenia in children with quadriplegic cerebral palsy: A randomized, placebo-controlled clinical trial. J Pediatr. 2002;141:644–51. [PubMed]
57. Gisel EG. Effect of oral sensorimotor treatment on measures of growth and efficiency of eating in the moderately eating-impaired child with cerebral palsy. Dysphagia. 1996;11:48–58. [PubMed]
58. Pinnington L, Hegarty J. Effects of consistent food presentation on oral-motor skill acquisition in children with severe neurological impairment. Dysphagia. 2000;15:213–23. [PubMed]
59. Rogers B. Feeding method and health outcomes of children with cerebral palsy. J Pediatr. 2004;145:S28–32. [PubMed]
60. Sulaeman E, Udall JN, Jr, Brown RF, et al. Gastroesophageal reflux and Nissen fundoplication following percutaneous endoscopic gastrostomy in children. J Pediatr Gastroenterol Nutr. 1998;26:269–73. [PubMed]
61. Byrne WJ. A reevaluation of the role of antireflux procedures in severely neurologically handicapped children requiring a gastrostomy for feeding. J Pediatr Gastroenterol Nutr. 1990;11:141. [PubMed]
62. Isch JA, Rescorla FJ, Scherer LR, III, West KW, Grosfeld JL. The development of gastroesophageal reflux after percutaneous endoscopic gastrostomy. J Pediatr Surg. 1997;32:321–2. [PubMed]
63. Khattak IU, Kimber C, Kiely EM, Spitz L. Percutaneous endoscopic gastrostomy in paediatric practice: Complications and outcome. J Pediatr Surg. 1998;33:67–72. [PubMed]
64. Spitz L, Roth K, Kiely EM, Brereton RJ, Drake DP, Milla PJ. Operation for gastro-oesophageal reflux associated with severe mental retardation. Arch Dis Child. 1993;68:347–51. [PMC free article] [PubMed]
65. Borgstein ES, Heij HA, Beugelaar JD, Ekkelkamp S, Vos A. Risks and benefits of antireflux operations in neurologically impaired children. Eur J Pediatr. 1994;153:248–51. [PubMed]
66. Miele E, Staiano A, Tozzi A, Auricchio R, Paparo F, Troncone R. Clinical response to amino acid-based formula in neurologically impaired children with refractory esophagitis. J Pediatr Gastroenterol Nutr. 2002;35:314–9. [PubMed]
67. Sullivan PB, Juszczak E, Bachlet AM, et al. Gastrostomy tube feeding in children with cerebral palsy: A prospective, longitudinal study. Dev Med Child Neurol. 2005;47:77–85. [PubMed]
68. Sullivan PB, Juszczak E, Bachlet AM, et al. Impact of gastrostomy tube feeding on the quality of life of carers of children with cerebral palsy. Dev Med Child Neurol. 2004;46:796–800. [PubMed]
69. Smith SW, Camfield C, Camfield P. Living with cerebral palsy and tube feeding: A population-based follow-up study. J Pediatr. 1999;135:307–10. [PubMed]
70. Samson-Fang L, Butler C, O’Donnell M. AACPDM. Effects of gastrostomy feeding in children with cerebral palsy: An AACPDM evidence report. Dev Med Child Neurol. 2003;45:415–26. [PubMed]
71. Sleigh G, Brocklehurst P. Gastrostomy feeding in cerebral palsy: A systematic review. Arch Dis Child. 2004;89:534–9. [PMC free article] [PubMed]
72. Craig GM, Scambler G, Spitz L. Why parents of children with neurodevelopmental disabilities requiring gastrostomy feeding need more support. Dev Med Child Neurol. 2003;45:183–8. [PubMed]
73. Culley WJ, Middleton TO. Caloric requirements of mentally retarded children with and without motor dysfunction. J Pediatr. 1969;75:380–4. [PubMed]

Articles from Paediatrics & Child Health are provided here courtesy of Pulsus Group