Skip to main content
American Academy of Pediatrics Selective Deposit logoLink to American Academy of Pediatrics Selective Deposit
. 2020 Dec;10(12):1087–1095. doi: 10.1542/hpeds.2020-0177

The Impact of Malnutrition on Hospitalized Children With Cerebral Palsy

Byron Alexander Foster 1,, Jennifer E Lane 1, Elizabeth Massey 1, Michelle Noelck 1, Sarah Green 1, Jared P Austin 1
PMCID: PMC7684553  PMID: 33154081

Abstract

Children with cerebral palsy (CP) and other medical complexity comprise an outsized proportion of health care use. In this review, we describe the current science of assessment of nutritional status for children with CP, outline a systematic approach to assessing their nutritional status, delineate ramifications of malnutrition on hospitalization-associated outcomes, and identify knowledge gaps and means of addressing those gaps using quality improvement and clinical research tools. Methods to accurately assess body composition and adiposity in this population by using skinfolds, age, sex, and activity level are available but are not widely used. There are limitations in our current method of estimating energy needs in children with CP, who are at higher risk of both obesity and micronutrient deficiencies. There is some evidence of an association between malnutrition, defined as either underweight or obesity, and hospitalization-associated outcomes in children generally, although we lack specific data for CP. The gaps in our current understanding of optimal nutritional status and between current science and practice need to be addressed to improve health outcomes for this vulnerable patient population.


Children with medical complexity account for a significant and increasing proportion of acute care hospitalizations, and they have unique nutritional needs.1,2 Improving our understanding of their nutritional status and how to optimize nutritional intake may help reduce unnecessary hospitalizations, reduce morbidity during hospitalizations, and improve clinical outcomes for these children. The time period of a hospitalization provides a critical window in which to optimize and potentially change the trajectory of their nutritional status. In this review, we propose an approach to addressing the nutritional status of children with medical complexity, identify knowledge gaps and potential means of addressing those gaps using quality improvement and clinical research tools, and, finally, describe the potential ramifications of both under- and overnutrition on hospitalization. We used the literature on children with cerebral palsy (CP) as a proxy for the broader group of children with medical complexity.

CP is a motor impairment caused by a brain injury or malformation during development.3 Not all children with CP are medically complex. The Gross Motor Function Classification System (GMFCS) uses a I to V scale that corresponds to increasing levels of motor impairment, and, for many children, this level is also used to approximate their degree of medical complexity.4 Some children with CP, particularly those with a higher GMFCS, have impaired oral-motor function, placing them at increased risk of malnutrition and associated morbidities.5 The increased use of gastrostomy tubes (G-tubes) and other enteral feeding tubes for providing nutrition to children with impaired oral-motor function has improved their health-related quality of life.6 More recently, excess adiposity has been recognized as a potential risk for children receiving supplemental nutrition,7 and adults with CP are increasingly recognized as having a higher risk of obesity-associated chronic diseases.8

Nutrition affects health via critical immunologic and biochemical pathways. There are several mechanisms by which nutritional status may affect acute hospitalization outcomes in this population. Protein calorie malnutrition impairs the cellular immune system, puts the child at an increased risk of infection and morbidity associated with infectious diseases, and decreases the response to vaccinations.9 Obesity influences the immune system via multiple mechanisms, including endocrine effects of leptin on T-cell metabolism and function.10,11 Micronutrient deficiencies have clinical effects ranging from hematologic (eg, folate) to more wide ranging (fatigue, muscle pain [eg, carnitine]).12,13 Secondary to their impaired oral-motor function and reliance on enteral feeds, children with more severe CP have an increased risk of malnutrition and these clinical sequelae.

Recommended Clinical Approach to Hospitalized Children With CP

History

Nutrition in children with CP is complicated by varying levels of function, ability to eat by mouth, and tolerance of different food types and textures. The feeding history should include, but is not limited to, route of food administration (oral versus G-tube or other enteral feeding tubes); type, texture, and concentration of food or formula, along with any fluid supplementation; vitamin and mineral supplementation; medications and caregiver report of usual dietary intake by 24 hour recall, diet log, or daily tube-feeding regimen with interruptions in regimen noted. Caregivers may inaccurately report energy intake in children with CP, and meticulous attention to detail in the feeding history is critical.14 Patients with epilepsy and, in particular, those taking valproic acid should be asked about carnitine supplementation. Obtaining specific information on multivitamin and supplement use can be helpful in assisting a dietitian in their assessment, given the heterogeneity in components. Bowel function and the medicines caregivers use to address any dysfunction are important because they may affect absorption and transit time.

Physical Examination Findings

An overall assessment of muscle and fat stores and specific signs of micronutrient deficiency should be noted on a thorough physical examination (Table 1). The American Society for Parenteral and Enteral Nutrition and the Academy of Nutrition and Dietetics propose the use of nutrition-focused physical examination techniques to assess for micronutrient deficiencies as well as overall muscle and fat stores. A general inspection of the patient should be done, noting if there is evidence of significant weight change demonstrated by signs of muscle mass loss or subcutaneous fat loss: areas of the body to focus on for fat loss include the face, arms, chest, and buttocks. For muscle wasting, areas of focus include the temple, clavicle, shoulder, scapula, thigh, knee, and calf.12 In Table 1, we identify additional clinical findings of nutritional deficiencies.

TABLE 1.

Physical Examination Findings of Nutritional Deficiencies and Prevalence of Deficiencies Identified in Children With CP

Nutritional Deficiency Site Physical Examination Finding Prevalence of Deficiency
Iron54 54%–60%13,19,55
Skin Pallor
Nails Beau lines, koilonychia (spoon-nails), onychomadesis, loss of nail
Zinc12,54,56 0%–56%13,55
Hair Alopecia, poor hair quality
Skin Diaper dermatitis that affects the perineum, acral surfaces, chins, and cheeks but spares the upper lip
Copper56,57 0%–86%19,58, 59
Hair Abnormally formed hair
Skin Depigmentation of the skin
Bones Spontaneous rib fracture
Neuro Myelopathy, spastic gait, sensory ataxia
Vitamin A12,54 20%–74%13,55
Hair Corkscrew hair
Skin Phrynoderma (follicular hyperkeratosis)
Eyes Bitot’s spots
Vitamin C12,54,56 5%–29%13,55
Hair Corkscrew hair
Skin Perifollicular petechiae, hemorrhages, pallor
Bones Long bone tenderness
Mucosa Gingival bleeding, epistaxis
Selenium12,56 57%–62%19,55
Hair Loss of hair pigment, alopecia
Muscle Skeletal muscle tenderness

Dietitian Consultation

Dietitians are nutrition experts uniquely trained to evaluate adequacy of growth, body composition, and nutritional intake. Early screening for nutritional risk is crucial for timely intervention and nutrition management. Some hospitals do not have standardized protocols or indices for dietitian consultation. In one study, the frequency and reason for dietitian consult was evaluated with 39 patients with CP identified at potential for nutrition risk, and only 58% received a dietitian consultation, and the average time to see a dietitian was >5 days.15

The European Society for Pediatric Gastroenterology Hepatology and Nutrition (ESPAGN) has suggested the use of 5 risk factors to identify children with neurologic impairment at high risk of malnutrition.16 These risk factors include (1) physical signs of underweight, including a physical examination of skin and peripheral circulation; (2) weight-for-age z scores <−2 SDs on standard growth charts; (3) triceps skinfold thickness <10th percentile for age and sex; (4) mid–upper arm fat or muscle area <10th percentile; and (5) faltering weight and/or failure to thrive. Increasing GMFCS is associated with a greater number of risk indicators.17 Risk of low weight for age was increased with a history of using antiepileptic drugs, dysphagia, and the presence of a gastrostomy tube. Other nutritional risk factors include rapid weight gain, overweight (defined as BMI ≥85th percentile), obesity (defined as BMI ≥95th percentile), or excess adiposity found either by physical examination, skinfold thickness, or abdominal circumference.18 In another study, we found that children with CP identified as having at least 1 ESPAGN nutrition risk factor suffered from weight loss 6 months after follow-up, indicating that risk factors were not addressed in clinical practice.17

We recommend implementation of a risk factor–based approach to quickly identify hospitalized children at risk to facilitate timely consultation with a dietitian, similar to the approach proposed by ESPAGN, with the additional inclusion of obesity in addition to inadequate adiposity as a risk factor. The measurement of obesity should not use BMI; instead, use weight-for-age charts specific to CP in the short-term while the emerging research on skinfold-based equations to estimate percentage of body fat outlined in Table 2 are being examined. Although this review is focused on CP, all children with medical complexity could benefit from a standardized approach.

TABLE 2.

Measures for Nutritional Assessment in Children With CP

Normal Parameters Data Specific to Children With CP Pros and Cons
Anthropometrics
 BMI Normal between fifth and 85th percentile for age and sex60 Poor association with percentage of body fat in children with CP18 Challenging to measure height accurately; does not differentiate fat mass and fat-free mass
 Wt-for-age growth charts for CP Normal between 20th and 80th percentile for sex and GMFCS level Derived from >25 000 children with CP at various levels; examined mortality associated with growth strata46 Represents how children with CP grew, rather than ideal growth patterns; stratified by GMFCS level and by tube feeding for GMFCS V
 DXA 10%–25% body fat for boys; 15%–30% body fat for girls (typically developing reference) 47%–64% of children with CP had excess body fat29,31; 4% had low body fat Criterion standard for body composition; challenging to measure in hospital; also dependent on fat-free mass, elevating the percentage of fat
 BIA Body fat percentage as above; total body water: 53%–63% for ages 6 mo to 11 y (typically developing children) Kushner and Fjeld equations are valid for estimating total body water in children with CP.61,62 Quick and noninvasive; lack of equipment available in most hospitals; requires accurate height measures; relies on total body water and hydration status
 Tibia length Estimated stature = (3.26 × tibia length [in centimeters]) + 30.8 Data revealing strong correlation (0.97) with height in children <12 y of age27,28 Easy to measure; measured from superomedial aspect of tibia to inferior aspect of medial malleolus
 MUAC CDC normal values based on NHANES data60 95% sensitivity of MUAC <10th percentile for severe malnutrition64; poor correlation with DXA in CP Easy to measure; not widely used in current practice
 FMI30: fat mass (rather than total body mass) adjusted for height squared No clear standards yet established Limited data; higher FMI in CP compared to typical development30 Benefit of not overestimating fat percentage, given the lower muscle mass in CP
 Body composition equations by using skinfolds31,40,65 Slaughter equation uses the subscapular and triceps skin folds; Gurka equations correct for CP, sex, and level of motor impairment. Slaughter equation significantly underestimates body fat. Correction with the Gurka equation improved estimation of body fat with only a 0.8% mean difference from DXA. Gurka equation allows you to correct for CP, sex, and level of motor impairment. Gurka equation has data for a population from 8 to 18 y old.
Laboratory tests
 Prealbumin and albumin Prealbumin; low: <16 mg/d; borderline: 16–20 mg/dL; adequate: >20 mg/dL Prealbumin and albumin do not have a significant relationship with anthropometric measures of nutritional status (including height, midarm fat, and skinfolds).66 Indicator of overall illness, rather than specific to nutritional status6668
 Vitamin D69 25(OH)D levels; deficient: ≤12 ng/mL; insufficient: 12–20 ng/mL; sufficient: >20 Children with CP are at risk for vitamin D deficiency, with researchers identifying 34% of participants having Vitamin D deficiency. Children with CP and being nonambulatory, with epilepsy, intellectual delay, teeth problems, or growth retardation are at higher risk of deficiency.
 Ferritin and iron13,55 Low iron stores: <12 µg/L ferritin Approximately one-half of patients with CP have low iron stores or inadequate iron intake when compared with estimated average requirement. Easy to measure and to replenish with oral supplement. Many participants’ highest proportion of energy source came from milk or a milk-based drink, which was a poor source of iron.
 Copper58,59,70 All ages: 0.7–1.5 mg/L Copper serum levels were lower in children with CP compared with controls in one study from Ghana; no deficiencies were noted in two US studies. Copper is a vital cofactor for enzyme antioxidants in defense against reactive oxygen species, and copper deficiency has been shown to lead to lower defense against oxidative stress.
 Folate13,71 Children: 4–20 ng/mL25 Children with CP who are tube fed have higher levels of folate compared with those who are not. Children with CP on antiepileptic drugs are at increased risk of folate deficiency, which may result in increased homocysteine levels. Folate supplementation for children with CP on AEDs may prevent elevated homocysteine and resulting health risks.24
 Selenium59,70 All ages: 7–15 mg/L Asmah et al59 found selenium levels higher in children with CP, compared with controls. Hals et al19 found selenium levels low in 62% of their cohort. High selenium levels have been associated with increased oxidative stress.
 Thiamine13 All ages: 55–125 nmol/L Children with CP who take a multivitamin have higher thiamine levels and are less likely to be deficient. Easy to supplement with a multivitamin
 Vitamin B1213 Infant: 160–1300 pg/mL; child: 200–835 pg/mL25 Children with CP who take a multivitamin supplement have higher B12 levels and are less likely to be deficient. Children with CP on antiepileptic medications are at increased risk of B12 deficiency. Easy to supplement with multivitamin; B12 supplementation for children with CP on AEDs may prevent elevated homocysteine and, thus, the risk for cerebrovascular events or heart disease.
 Zinc59 All ages: 70–120 ug/dL72 Zinc levels were detected at lower levels in the blood in children 0–5 y of age with CP compared with controls. Zinc deficiency leads to lower defense against oxidative stress. High daily zinc intake risks inhibiting intestinal absorption of copper, leading to copper deficiency.

FMI, fat mass index; MUAC, mean upper arm circumference; NHANES, National Health and Nutrition Examination Survey.

Laboratory Testing and Findings

Prealbumin has been used as a measure of nutritional status. The data that this metric lacks value as an indicator of nutrition are now strong. Along with albumin, low levels of prealbumin reflect disease severity and intercompartmental shifts, rather than reduced protein synthesis capacity due to malnutrition (Table 2).

Measurement of adequate intake of important micronutrients can be estimated both by a dietary intake report and laboratory testing.13,19 In few studies have researchers examined micronutrient assessment by laboratory testing in children with CP. The data we do have suggest that multivitamin supplementation and G-tube feeding are associated with fewer deficiencies, in both B vitamins and trace minerals such as selenium.13 Children with CP and epilepsy should have a free carnitine level measured and, if deficient, carnitine supplementation provided in consultation with a dietitian. This population has been found to be at risk for carnitine deficiency, particularly for those taking valproic acid or with multiple anti-epileptic drugs (AEDs), those on enteral formula only, and those with a low body weight.2022

Low bone mineral density in children with CP may be driven by immobility, antiepileptic drugs, and vitamin D deficiency. In a systematic review published in 2011 to develop evidence-based clinical practice guidelines for children with CP and low bone mineral density, researchers recommended vitamin D supplementation on the basis of baseline vitamin D laboratory testing (25-hydroxyvitamin D).23 There is a rich scientific debate on what a target vitamin D concentration should be, ranging from >12 ng/mL to >20 or even 30 ng/mL.24,25 Given the multiple risk factors most children with CP, particularly those with immobility, have for low bone mineral density, we recommend a target of at least 20 ng/mL, with attention to appropriate dosing because, although low, the potential for toxicity does exist.26

Supplementation with an age-appropriate multivitamin should be strongly considered in children with CP, given their higher likelihood of these deficiencies, given a lack of variety in their diet and potentially reduced formula intake due to lower energy needs. We recommend that clinicians should consider testing for folate, calcium, and vitamin D deficiencies in children who are not taking an age-appropriate multivitamin. Testing children with abnormal skin and hair findings (Table 1) for micronutrients such as selenium or copper should also be considered.

Body Composition

BMI has significant flaws, given the lower fat-free mass in children with CP and significant challenges in accurate measurement of height. Tibia lengths show a strong correlation with height and can be used to estimate height,27,28 although the limitations of BMI remain. In the current growth charts specific for CP, past trends, rather than ideal growth, are described: in other words, how they have grown rather than how they should grow.

Dual-energy radiograph absorptiometry (DXA) is the standard for body composition analyses (see Table 2 for a comparison of anthropometric indicators). In a study of children with GMFCS III to V, investigators showed that all of the other individual anthropometric indicators had a poor correlation with percentage of body fat using DXA.29 Bioelectric impedance analysis (BIA) uses a small current passed between the hands or feet to estimate the percentage of fat given the known variation in resistance by the percent of body fat. DXA and BIA are not readily available for all hospitalized children and are, currently, primarily research modalities. Another emerging area of research is the use of a fat mass index, which has the benefit of not overestimating the percentage of fat with lower muscle mass.30

We recommend the use of estimating equations using both skinfold measurements and other variables, such as age and sex, developed by Oeffinger et al.31 These have shown good agreement with DXA, the functional gold standard.31 The widespread use of electronic medical records makes the widespread use of complex skinfold-based equations easier.

Estimated Energy Requirements and Macronutrient Needs

To reduce the risk of over- and underfeeding, careful determination of energy requirements is essential. Evaluating the energy needs of children with CP is challenging, and individual needs vary depending on the severity of disability. In general, total energy expenditure, in calories per day, is determined first by estimating resting energy expenditure (REE) and then by using adjustment factors that take into account activity level.

Predictive equations for REE, such as the Schofield, Harris-Benedict, or World Health Organization (WHO) equations, are used in typically developing children; these equations are dependent on age, sex, and accurate measurements of weight and height. It has been shown that the energy needs of children with CP differ from those of typically developing children.32,33 In a recent study, researchers compared the WHO, Harris-Benedict, and Schofield equations, among others, with indirect calorimetry in children with spastic CP and found that these commonly used equations are inaccurate in this population.34 Lee et al35 compared measured energy expenditure by indirect calorimetry with predicted energy expenditure and found that predictive equations significantly overestimated energy needs in children with spastic CP. Children with athetoid CP may have an increased REE.

Attempts at developing equations specific to children with CP have been made.34,36,37 Culley and Middleton36 suggested a method of estimation based on height and the presence of motor dysfunction using a range of 11 to 15 kcal/cm; this method remains stable regardless of age or sex.38 The use of this equation is dependent on accurate height measurement, which is difficult to obtain in the presence of muscle contractures, inability to stand independently, and scoliosis. Using tibia measurements to approximate height and then applying those estimates in this method has not been examined. BIA may be a reliable and accurate method for estimating REE and total energy expenditure in comparison with indirect calorimetry, although, at this time, it requires further study and has some practical barriers to widespread implementation.38

The current recommendation of expert groups, such as the American Society for Parenteral and Enteral Nutrition and the European Society for Paediatric Gastroenterology, Hepatology and Nutrition, is to use reference equations for typically developing children, adjusting for differences in mobility, muscle tone and body composition, activity level, and growth requirements, as needed for weight gain or loss. These estimates should be used as a starting point for dietary intervention, and frequent monitoring of weight and body composition for reassessment is required.16,39 Understanding that these equations tend to overestimate the needs of children with CP is important. When reducing caloric intake, especially in children exclusively tube fed, there should be careful consideration of protein, essential fatty acids, and micronutrients to prevent deficiency.

We agree with this recommendation of using reference equations for typically developing children, with adjustments as described, with one additional caveat. Using more accurate estimates of body composition, such as the Gurka et al40 equations, would provide a better metric of identifying whether those estimates are over- or underestimating energy requirements for the individual child.

Challenges and the Path Forward

There are several challenges to optimizing nutrition for children with CP who are hospitalized and, by extension, other children with medical complexity. Optimal nutrition can be defined as the dietary intake that results in the optimal growth and development of the individual child while also reducing the risk of disease.41 The inherent circularity of this basic definition presents challenges if optimal growth and development are not fully understood or defined. We need more research, and there are several tangible steps that pediatric hospital medicine as a field can make (Table 3). These children make up a significant proportion of the children we serve, and addressing their nutritional needs can affect their hospitalization outcomes.

TABLE 3.

Current State and Recommendations Going Forward for Improving Nutrition for Hospitalized Children With CP

Current State Recommendations Tools Needed To Implement
Lack of a uniform and standardized approach to involving dieticians in the care of hospitalized patients with CP Develop a standardized approach for involving dieticians in the care of hospitalized children with CP by using a risk factor–based approach that incorporates measures of both insufficient and excess adiposity. Risk factor identification by using EMR tools
Dietician available for consultation
Skinfold calipers and training
Lack of an accurate and accessible measure of body habitus for children with CP Implementation of evidence-based measures of body habitus for children with CP; do not use BMI with typically developing children as the reference for this population. Estimating equations from skinfold measurements
Quality improvement for implementation
Imperfect understanding of optimal energy requirements for children across the spectrum of impairment with CP Using reference equations for typically developing children with strong caveat of adjusting on the basis of accurate assessment of body composition; clinical research examining optimal energy requirements Dietitian partnerships
Medical record adaptation
Quality improvement for implementation
Lack of uniform data collection across hospital systems for nutritional status of children with CP Examine data on patients with CP to determine the impact of under- and overnutrition on hospital-based outcomes, morbidity, and mortality. Steps above need to be completed to have better metrics to examine

EMR, electronic medical record.

Prevalence of Malnutrition (Both Underweight and Obesity)

Estimates of the prevalence of underweight and obesity in children vary as a function of both method of measurement and degree of motor impairment. In studies, researchers using BMI, which has significant limitations as outlined above, as the measure of underweight have found estimates ranging between 7% and 14% of children with CP.4244 In a retrospective cohort study of 587 children with CP GMFCS levels I to III, researchers found that ∼7% of their cohort was underweight according to CDC-based BMI z scores, 74% were healthy, and 19% were either overweight or obese.44 Of note, children with greater motor impairment (higher GMFCS) were more likely to have obesity. In a single center study from a Shriners Hospital in South Carolina, researchers identified a prevalence of 16.5% for obesity in children with CP at GMFCS levels I to III in 2003 to 2004, with an increase from 7.7% in the 1990s.45

Using a more accurate method, a DXA scanner, a study of 300 children with CP from Germany revealed a prevalence of 17% for excess body fat, with nearly twice the prevalence (20%) in GMFCS level III or V children compared with GMFCS level I or II children (10%).18,44 Using DXA scans in children with GMFCS III or V, a multi-site study from the United States revealed that 64% of children with CP had excess body fat (defined as >25% for boys and >30% for girls).29 Similarly, using height estimated from knee height for children with GMFCS I to III and the same body fat definitions as above, Oeffinger et al31 identified 47% of children as having excess body fat and 4% as having inadequate body fat using DXA.

Underweight and Health Outcomes in Hospitalized Children With CP

We found few studies in which researchers look specifically at the effects of nutritional status on health outcomes in hospitalized children with CP who were underweight. Brooks et al46 conducted a large retrospective analysis of >25 000 outpatient children with CP. They found that children with a weight for age <20th percentile were more likely to have comorbid chronic conditions and a higher risk of death than those with weights >20th percentile, after stratifying by GMFCS level.

These results are supported by a study in 2019 by Kim et al.47 In this large birth cohort study, individuals with CP showed a higher mortality rate than the general population. When taking into account patients whose weight for age was less than the third percentile by using WHO growth charts, the mortality rate was 2 to 5 times higher in a combined population of patients with CP and the general population. They did not conduct a specific analysis within the CP group.

Obesity and Health Outcomes in Hospitalized Children With Medical Complexity

For children generally, the data indicate an increased risk of morbidity and mortality with obesity. In a systematic review through 2012, researchers identified 28 cohort or case-control studies in which the associations between obesity and outcomes of mortality, length of stay, and hospital-acquired infections, including all hospitalized children, were examined.48 Although they identified a significant variation in quality of the studies, larger and higher quality studies revealed an association between obesity and worse outcomes.

Studies in which researchers use administrative data have revealed an association between obesity and morbidity during hospitalizations for children for outcomes of all infections49 and, specifically, lower respiratory tract infections.50 Bechard et al51 showed that malnutrition, defined as either underweight or obesity, was associated with poorer outcomes in all patients in an analysis of 2 large multi-PICU studies. In a retrospective analysis of data from the virtual PICU systems database, it was found that being overweight (defined by using equally distributed BMI z score intervals) was independently associated with increased PICU mortality, after controlling for preexisting conditions and disease severity.52 In this study, researchers also found an increased mortality risk for underweight children; however, this did not hold true after controlling for comorbidities and disease severity.52 This study had a large cohort of children, but, in the analysis only those patients who had weight and height values reported were included, thus potentially not capturing a large proportion of patients at risk with nonambulatory CP. Children with CP are at increased risk of sleep apnea secondary to abnormal muscle tone and control, and excess adiposity would potentially increase the risk of obstructive sleep apnea as well.

In 1 study, researchers looking at postoperative complications in children with CP after orthopedic procedures found that underweight status was an independent predictor of increased complications, whereas no increased risk was found in the overweight or obese cohorts.53 In this study, researchers used BMI as a measurement of patient nutritional status and did not take individual functional status into account. Brooks et al46 found no increased risk of overall mortality for patients with CP whose weight was >80th percentile in their outpatient cohort.

Conclusions

Drawing on the limited data we do have on patients with CP and extrapolating from other populations of patients with medical complexity, we postulate that malnutrition, including both underweight and obesity, contribute to worse outcomes, including more frequent and prolonged hospitalizations. Given the potential benefit for individual children’s morbidity and the outsized impact these children have on the medical system, it is imperative that we address the lack of uniformity of data collection, conduct quality improvement projects targeting improved hospital dietitian assessments and implementing more accurate body composition assessments, and address the scientific gaps in our understanding of energy expenditure for these children.

Footnotes

Dr Foster contributed to the conceptualization of the article, conducted the literature search, and drafted the initial manuscript and revisions; Dr Lane contributed to the initial draft, conducted a literature search, and edited several revisions and the tables; Ms Massey conducted a literature search and contributed to the initial draft and several revisions; Dr Noelck revised several versions of the manuscript and conducted a literature search for subsections; Dr Green contributed to the organization of the article, edited several drafts, and assisted with figure and table development; Dr Austin contributed to the literature search and conceptual organization of the article and edited several revisions; and all authors approved the final manuscript as submitted.

FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.

FUNDING: The National Institutes of Health provided funding to Dr Foster via grant K23 DK109199. Funded by the National Institutes of Health (NIH).

POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.

References

  • 1.Burns KH, Casey PH, Lyle RE, Bird TM, Fussell JJ, Robbins JM. Increasing prevalence of medically complex children in US hospitals. Pediatrics. 2010;126(4):638–646 [DOI] [PubMed] [Google Scholar]
  • 2.Berry JG, Ash AS, Cohen E, Hasan F, Feudtner C, Hall M. Contributions of children with multiple chronic conditions to pediatric hospitalizations in the United States: a retrospective cohort analysis. Hosp Pediatr. 2017;7(7):365–372 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Rosenbaum P, Paneth N, Leviton A, et al. A report: the definition and classification of cerebral palsy April 2006. [published correction appears in Dev Med Child Neurol. 2007;49(6):480]. Dev Med Child Neurol Suppl. 2007;109:8–14 [PubMed] [Google Scholar]
  • 4.Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39(4):214–223 [DOI] [PubMed] [Google Scholar]
  • 5.Kuperminc MN, Stevenson RD. Growth and nutrition disorders in children with cerebral palsy. Dev Disabil Res Rev. 2008;14(2):137–146 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Sullivan PB, Juszczak E, Bachlet AME, et al. Gastrostomy tube feeding in children with cerebral palsy: a prospective, longitudinal study. Dev Med Child Neurol. 2005;47(2):77–85 [DOI] [PubMed] [Google Scholar]
  • 7.Sullivan PB, Alder N, Bachlet AME, et al. Gastrostomy feeding in cerebral palsy: too much of a good thing? Dev Med Child Neurol. 2006;48(11):877–882 [DOI] [PubMed] [Google Scholar]
  • 8.Ryan JM, Allen E, Gormley J, Hurvitz EA, Peterson MD. The risk, burden, and management of non-communicable diseases in cerebral palsy: a scoping review. Dev Med Child Neurol. 2018;60(8):753–764 [DOI] [PubMed] [Google Scholar]
  • 9.Cunningham-Rundles S, McNeeley DF, Moon A. Mechanisms of nutrient modulation of the immune response. J Allergy Clin Immunol. 2005;115(6):1119–1128; quiz 1129 [DOI] [PubMed] [Google Scholar]
  • 10.Alwarawrah Y, Kiernan K, MacIver NJ. Changes in nutritional status impact immune cell metabolism and function. Front Immunol. 2018;9:1055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Andersen CJ, Murphy KE, Fernandez ML. Impact of obesity and metabolic syndrome on immunity. Adv Nutr. 2016;7(1):66–75 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Corkins KG. Nutrition-focused physical examination in pediatric patients. Nutr Clin Pract. 2015;30(2):203–209 [DOI] [PubMed] [Google Scholar]
  • 13.Hillesund E, Skranes J, Trygg KU, Bøhmer T. Micronutrient status in children with cerebral palsy. Acta Paediatr. 2007;96(8):1195–1198 [DOI] [PubMed] [Google Scholar]
  • 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(4):627–634 [DOI] [PubMed] [Google Scholar]
  • 15.Larsen BM, Luchak M, Prenoslo L, Wood KB, Mazurak V. Indicators of pediatric malnutrition in a tertiary care hospital. Can J Diet Pract Res. 2014;75(3):157–159 [DOI] [PubMed] [Google Scholar]
  • 16.Romano C, van Wynckel M, Hulst J, et al. European Society for Paediatric Gastroenterology, Hepatology and Nutrition guidelines for the evaluation and treatment of gastrointestinal and nutritional complications in children with neurological impairment. J Pediatr Gastroenterol Nutr. 2017;65(2):242–264 [DOI] [PubMed] [Google Scholar]
  • 17.Huysentruyt K, Geeraert F, Allemon H, et al. Nutritional red flags in children with cerebral palsy. Clin Nutr. 2020;39(2):548–553 [DOI] [PubMed] [Google Scholar]
  • 18.Duran I, Schulze J, Martakis K, Stark C, Schoenau E. Diagnostic performance of body mass index to identify excess body fat in children with cerebral palsy. Dev Med Child Neurol. 2018;60(7):680–686 [DOI] [PubMed] [Google Scholar]
  • 19.Hals J, Ek J, Svalastog AG, Nilsen H. Studies on nutrition in severely neurologically disabled children in an institution. Acta Paediatr. 1996;85(12):1469–1475 [DOI] [PubMed] [Google Scholar]
  • 20.Coppola G, Epifanio G, Auricchio G, Federico RR, Resicato G, Pascotto A. Plasma free carnitine in epilepsy children, adolescents and young adults treated with old and new antiepileptic drugs with or without ketogenic diet. Brain Dev. 2006;28(6):358–365 [DOI] [PubMed] [Google Scholar]
  • 21.Anil M, Helvaci M, Ozbal E, Kalenderer O, Anil AB, Dilek M. Serum and muscle carnitine levels in epileptic children receiving sodium valproate. J Child Neurol. 2009;24(1):80–86 [DOI] [PubMed] [Google Scholar]
  • 22.Fukuda M, Kawabe M, Takehara M, et al. Carnitine deficiency: risk factors and incidence in children with epilepsy. Brain Dev. 2015;37(8):790–796 [DOI] [PubMed] [Google Scholar]
  • 23.Fehlings D, Switzer L, Agarwal P, et al. Informing evidence-based clinical practice guidelines for children with cerebral palsy at risk of osteoporosis: a systematic review. Dev Med Child Neurol. 2012;54(2):106–116 [DOI] [PubMed] [Google Scholar]
  • 24.Manson JE, Brannon PM, Rosen CJ, Taylor CL. Vitamin D deficiency - is there really a pandemic? N Engl J Med. 2016;375(19):1817–1820 [DOI] [PubMed] [Google Scholar]
  • 25.Holick MF, Binkley NC, Bischoff-Ferrari HA, et al. ; Endocrine Society. Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. [published correction appears in J Clin Endocrinol Metab. 2011;96(121):3908]. J Clin Endocrinol Metab. 2011;96(7):1911–1930 [DOI] [PubMed] [Google Scholar]
  • 26.Lee JP, Tansey M, Jetton JG, Krasowski MD. Vitamin D toxicity: a 16-year retrospective study at an academic medical center. Lab Med. 2018;49(2):123–129 [DOI] [PubMed] [Google Scholar]
  • 27.Stevenson RD. Use of segmental measures to estimate stature in children with cerebral palsy. Arch Pediatr Adolesc Med. 1995;149(6):658–662 [DOI] [PubMed] [Google Scholar]
  • 28.Gauld LM, Kappers J, Carlin JB, Robertson CF. Height prediction from ulna length. Dev Med Child Neurol. 2004;46(7):475–480 [DOI] [PubMed] [Google Scholar]
  • 29.Kuperminc MN, Gurka MJ, Bennis JA, et al. Anthropometric measures: poor predictors of body fat in children with moderate to severe cerebral palsy. Dev Med Child Neurol. 2010;52(9):824–830 [DOI] [PubMed] [Google Scholar]
  • 30.Whitney DG, Miller F, Pohlig RT, Modlesky CM. BMI does not capture the high fat mass index and low fat-free mass index in children with cerebral palsy and proposed statistical models that improve this accuracy. Int J Obes (Lond). 2019;43(1):82–90 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Oeffinger DJ, Gurka MJ, Kuperminc M, Hassani S, Buhr N, Tylkowski C. Accuracy of skinfold and bioelectrical impedance assessments of body fat percentage in ambulatory individuals with cerebral palsy. Dev Med Child Neurol. 2014;56(5):475–481 [DOI] [PubMed] [Google Scholar]
  • 32.Calis EAC, Veugelers R, Rieken R, Tibboel D, Evenhuis HM, Penning C. Energy intake does not correlate with nutritional state in children with severe generalized cerebral palsy and intellectual disability. Clin Nutr. 2010;29(5):617–621 [DOI] [PubMed] [Google Scholar]
  • 33.Rieken R, van Goudoever JB, Schierbeek H, et al. Measuring body composition and energy expenditure in children with severe neurologic impairment and intellectual disability. Am J Clin Nutr. 2011;94(3):759–766 [DOI] [PubMed] [Google Scholar]
  • 34.Penagini F, Borsani B, Bosetti A, et al. Resting energy expenditure in children with cerebral palsy: accuracy of available prediction formulae and development of a population-specific formula. Clin Nutr ESPEN. 2018;25:44–49 [DOI] [PubMed] [Google Scholar]
  • 35.Lee SPP, Cheung KM, Ko CH, Chiu HC. Is there an accurate method to measure metabolic requirement of institutionalized children with spastic cerebral palsy? JPEN J Parenter Enteral Nutr. 2011;35(4):530–534 [DOI] [PubMed] [Google Scholar]
  • 36.Culley WJ, Middleton TO. Caloric requirements of mentally retarded children with and without motor dysfunction. J Pediatr. 1969;75(3):380–384 [DOI] [PubMed] [Google Scholar]
  • 37.Krick J, Murphy PE, Markham JF, Shapiro BK. A proposed formula for calculating energy needs of children with cerebral palsy. [published correction appears in Dev Med Child Neurol. 1992;34(10):927]. Dev Med Child Neurol. 1992;34(6):481–487 [DOI] [PubMed] [Google Scholar]
  • 38.García Íñiguez JA, Vásquez Garibay EM, García Contreras AA, et al. Energy expenditure is associated with age, anthropometric indicators and body composition in children with spastic cerebral palsy. Nutr Hosp. 2018;35(4):909–913 [DOI] [PubMed] [Google Scholar]
  • 39.Corkins MR, ed. The A.S.P.E.N. Pediatric Nutrition Support Core Curriculum. 2nd ed American Society for Parental and Enteral Nutrition; 2015 [Google Scholar]
  • 40.Gurka MJ, Kuperminc MN, Busby MG, et al. Assessment and correction of skinfold thickness equations in estimating body fat in children with cerebral palsy. Dev Med Child Neurol. 2010;52(2):e35–e41 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Heaney RP. The nutrient problem. Nutr Rev. 2012;70(3):165–169 [DOI] [PubMed] [Google Scholar]
  • 42.Lionti T, Reid SM, Reddihough D, Sabin MA. Monitoring height and weight: findings from a developmental paediatric service. J Paediatr Child Health. 2013;49(12):1063–1068 [DOI] [PubMed] [Google Scholar]
  • 43.Park ES, Chang WH, Park JH, Yoo JK, Kim SM, Rha D-w. Childhood obesity in ambulatory children and adolescents with spastic cerebral palsy in Korea. Neuropediatrics. 2011;42(2):60–66 [DOI] [PubMed] [Google Scholar]
  • 44.Pascoe J, Thomason P, Graham HK, Reddihough D, Sabin MA. Body mass index in ambulatory children with cerebral palsy: a cohort study. J Paediatr Child Health. 2016;52(4):417–421 [DOI] [PubMed] [Google Scholar]
  • 45.Rogozinski BM, Davids JR, Davis RB, et al. Prevalence of obesity in ambulatory children with cerebral palsy. J Bone Joint Surg Am. 2007;89(11):2421–2426 [DOI] [PubMed] [Google Scholar]
  • 46.Brooks J, Day S, Shavelle R, Strauss D. Low weight, morbidity, and mortality in children with cerebral palsy: new clinical growth charts. Pediatrics. 2011;128(2). Available at: www.pediatrics.org/cgi/content/full/128/2/e299 [DOI] [PubMed] [Google Scholar]
  • 47.Kim HJ, Kang TU, Park KY, Kim J, Ahn HS, Yim S-Y. Which growth parameters can affect mortality in cerebral palsy? PLoS One. 2019;14(6):e0218320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Bechard LJ, Rothpletz-Puglia P, Touger-Decker R, Duggan C, Mehta NM. Influence of obesity on clinical outcomes in hospitalized children: a systematic review. JAMA Pediatr. 2013;167(5):476–482 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Maley N, Gebremariam A, Odetola F, Singer K. Influence of obesity diagnosis with organ dysfunction, mortality, and resource use among children hospitalized with infection in the United States. J Intensive Care Med. 2017;32(5):339–345 [DOI] [PubMed] [Google Scholar]
  • 50.Okubo Y, Nochioka K, Testa MA. The impact of pediatric obesity on hospitalized children with lower respiratory tract infections in the United States. Clin Respir J. 2018;12(4):1479–1484 [DOI] [PubMed] [Google Scholar]
  • 51.Bechard LJ, Duggan C, Touger-Decker R, et al. Nutritional status based on body mass index is associated with morbidity and mortality in mechanically ventilated critically ill children in the PICU. Crit Care Med. 2016;44(8):1530–1537 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Ross PA, Newth CJL, Leung D, Wetzel RC, Khemani RG. Obesity and mortality risk in critically ill children. Pediatrics. 2016;137(3):e20152035. [DOI] [PubMed] [Google Scholar]
  • 53.Minhas SV, Chow I, Otsuka NY. The effect of body mass index on postoperative morbidity after orthopaedic surgery in children with cerebral palsy. J Pediatr Orthop. 2016;36(5):505–510 [DOI] [PubMed] [Google Scholar]
  • 54.Yan AC, Jen MV. Skin signs of pediatric nutritional disorders. Curr Probl Pediatr Adolesc Health Care. 2012;42(8):212–217. [DOI] [PubMed] [Google Scholar]
  • 55.Sullivan P, 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(7):461–467 [DOI] [PubMed] [Google Scholar]
  • 56.Haemer MA PL, Krebs NF. Normal childhood nutrition and its disorders. In: Hay JW, Levin MJ, Deterding RR, Abzug MJ, eds. Current Diagnosis & Treatment: Pediatrics. New York, NY: McGraw-Hill. [Google Scholar]
  • 57.Kumar N. Copper deficiency myelopathy (human swayback). Mayo Clin Proc. 2006;81(10):1371–1384 [DOI] [PubMed] [Google Scholar]
  • 58.Bebars GM, Afifi MF, Mahrous DM, Okaily NE, Mounir SM, Mohammed EA. Assessment of some micronutrients serum levels in children with severe acute malnutrition with and without cerebral palsy - a follow up case control study. Clin Nutr Exper. 2019;23:34–43 [Google Scholar]
  • 59.Asmah RH, Anyele A, Asare-Anane H, Brown A, Archampong T, Amegatcher G, Badoe E, Adjei D, Dzudzor B, Ayeh-Kumi P. Micronutrient levels and antioxidant status in pediatric cerebral palsy patients. Oxid Antioxid Med Sci. 2015;4(2):73–77 [Google Scholar]
  • 60.Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, Wei R, Curtin LR, Roche AF, Johnson CL. 2000. CDC growth charts for the United States: methods and development. Vital Health Stat 11 2002(246):1–190 [PubMed] [Google Scholar]
  • 61.Bell KL, Boyd RN, Walker JL, Stevenson RD, Davies PS. The use of bioelectrical impedance analysis to estimate total body water in young children with cerebral palsy. Clin Nutr. 2013;32(4):579. [DOI] [PubMed] [Google Scholar]
  • 62.Snik DAC, de Roos NM. Criterion validity of assessment methods to estimate body composition in children with cerebral palsy: A systematic review. Ann Phys Rehabil Med. 2019 [DOI] [PubMed] [Google Scholar]
  • 63.Fryar CD, Gu Q, Ogden CL. Anthropometric reference data for children and adults: United States, 2007-2010. Vital Health Stat 11 2012(252):1–48 [PubMed] [Google Scholar]
  • 64.Leonard M, Dain E, Pelc K, Dan B, De Laet C. Nutritional status of neurologically impaired children: Impact on comorbidity. Arch Pediatr. 2020;27(2):95–103 [DOI] [PubMed] [Google Scholar]
  • 65.Martinez EE, Smallwood CD, Quinn NL, Ariagno K, Bechard LJ, Duggan CP, Mehta NM. Body composition in children with chronic illness: accuracy of bedside assessment techniques. J Pediatr. 2017;190:56–62 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 66.Lark RK, Williams CL, Stadler D, Simpson SL, Henderson RC, Samson-Fang L, Worley G. Serum prealbumin and albumin concentrations do not reflect nutritional state in children with cerebral palsy. J Pediatr. 2005;147(5):695–697 [DOI] [PubMed] [Google Scholar]
  • 67.Ong C, Han WM, Wong JJ, Lee JH. Nutrition biomarkers and clinical outcomes in critically ill children: A critical appraisal of the literature. Clin Nutr. 2014;33(2):191–197 [DOI] [PubMed] [Google Scholar]
  • 68.Marcason W. Should albumin and prealbumin be used as indicators for malnutrition? J Acad Nutr Diet. 2017;117(7):1144. [DOI] [PubMed] [Google Scholar]
  • 69.Akpinar P. Vitamin D status of children with cerebral palsy: Should vitamin D levels be checked in children with cerebral palsy? North Clin Istanb. 2018;5(4):341–347 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 70.Hals J, Ek J, Svalastog AG, Nilsen H. Studies on nutrition in severely neurologically disabled children in an institution. Acta Paediatr. 1996;85(12):1469–1475 [DOI] [PubMed] [Google Scholar]
  • 71.Xu Y, Zhang N, Xu S, Xu H, Chen S, Xia Z. Effects of phenytoin on serum levels of homocysteine, vitamin B12, folate in patients with epilepsy: A systematic review and meta-analysis (PRISMA-compliant article). Medicine. 2019;98(12): e14844 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Hughes HK KL. Blood Chemistries and Body Fluids. In: The Harriet Lane Handbook. Philadelphia, PA: Elsevier; 2018 [Google Scholar]

Articles from Hospital Pediatrics are provided here courtesy of American Academy of Pediatrics

RESOURCES