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The Importance of Good Nutrition in Children with Cerebral Palsy

  • Gina Rempel
    Correspondence
    Rehabilitation Centre for Children, Inc, 633 Wellington Crescent, Winnipeg, Manitoba R3M 0A8, Canada.
    Affiliations
    Rehabilitation Centre for Children, Inc, 633 Wellington Crescent, Winnipeg, Manitoba R3M 0A8, Canada

    Children’s Hospital, AE 303, 840 Sherbrook Street, Winnipeg, Manitoba R1A 1S1, Canada
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      Keywords

      Key points

      • In children with cerebral palsy (CP), undernutrition has significant negative consequences.
      • Poor oral-feeding skills are the primary cause of inadequate nutrition in children with CP.
      • Understanding the causes of poor nutrition guides nutritional intervention.
      • Overcoming the challenges inherent in the physical measurement of children with CP by using heights extrapolated from segmental measures and triceps skin fold, together with weights, weight gain velocity, and monitoring these measures on appropriate growth charts, informs care providers about the need for nutritional rehabilitation and helps monitor the progress toward collaboratively established nutrition goals.
      • Understanding the multidimensional aspects of oral feeding and the timing of enteral nutrition support are important elements in the nutrition rehabilitation toolkit.

      Introduction

      Nature of the Problem

      Cerebral palsy (CP) describes “a group of persisting, nonprogressive conditions in the development of motor control that appear very early in life.”
      • Rosenbaum P.
      • Rosenbloom L.
      Cerebral palsy: from diagnosis to adult life.
      “The motor disorders of CP are often accompanied by disturbances of sensation, perception, cognition, communication, and behavior; by epilepsy; and by secondary musculoskeletal problems.”

      Rosenbaum P, Paneth M, Leviton A, et al. Definition and classification document. In: The definition and classification of cerebral palsy. Baxter P, editor. Dev Med Child Neurol Suppl 2007;109:8–14.

      Although the primary problems associated with CP are neurodevelopmental in nature, challenges with growth and nutrition are also common in affected children.
      • Stallings V.A.
      • Cronk C.E.
      • Zemel B.S.
      • et al.
      Body composition in children with spastic quadriplegic cerebral palsy.
      • Stevenson R.
      • Hayes R.
      • Cater L.
      • et al.
      Clinical correlates of linear growth in children with cerebral palsy.
      • Dahlseng M.
      • Finbraten A.
      • Juliusson R.
      • et al.
      Feeding problems, growth and nutritional status in children with cerebral palsy.
      As a group, children with CP are smaller and more poorly nourished than their typically developing peers. These differences between affected and nonaffected children are more marked with increasing age and with the severity of the motor impairment.
      • Kuperminc M.
      • Stevenson R.
      Growth and nutrition disorders in children with cerebral palsy.
      A complex interplay of these factors and other nutritional and non-nutritional factors impacts the growth and nutritional status of children with CP.
      • Andrew M.J.
      • Sullivan P.B.
      Growth in cerebral palsy.
      Good nutrition is the cornerstone of health and well-being for all children, whether affected by CP or not. Weight gain and growth along predicted trajectories, reassure families and care providers that a child is thriving and is healthy. The same holds true for children with CP, but in these children the measuring and monitoring of growth is fraught with challenges that must be overcome to be able to interpret nutritional adequacy.
      • Kuperminc M.
      • Stevenson R.
      Growth and nutrition disorders in children with cerebral palsy.
      • Rogers B.
      Feeding method and health outcome of children with cerebral palsy.
      Understanding when a child’s nutritional status is faltering is important because poor nutrition has serious consequences and is potentially remediable.
      • Samson-Fang L.
      • Fung E.
      • Stallings V.A.
      • et al.
      Relationship of nutritional status to health and societal participation in children with cerebral palsy.
      • Brooks J.
      • Day S.
      • Shavelle R.
      • et al.
      Low weight, morbidity and mortality in children with cerebral palsy: new clinical growth charts.

      Factors affecting nutrition and growth in children with cerebral palsy

      The children with CP who are at the greatest risk of having significant nutritional problems are those who present with poor weight gain at a young age,
      • Samson-Fang L.
      • Stevenson R.
      Linear growth velocity in children with cerebral palsy.
      • Dahl M.
      • Thommessen M.
      • Rasmussen M.
      • et al.
      Feeding and nutritional characteristics in children with moderate or severe cerebral palsy.
      who have significant motor impairments,
      • Liptak G.S.
      • O’Donnell M.
      • Conaway M.
      • et al.
      Health status of children with moderate to severe cerebral palsy.
      and who have feeding and swallowing problems.
      • Samson-Fang L.
      • Fung E.
      • Stallings V.A.
      • et al.
      Relationship of nutritional status to health and societal participation in children with cerebral palsy.
      • Karagiozoglu-Lampoudi T.
      • Daskalou E.
      • Vargiami E.
      • et al.
      Identification of feeding risk factors for impaired nutrition status in paediatric patients with cerebral palsy.
      • Stevenson R.D.
      • Conaway M.
      • Chumlea W.C.
      • et al.
      Growth and health in children with moderate-to-severe cerebral palsy.
      Other factors affecting nutrition are detailed in Box 1.
      Factors affecting growth and nutrition in children with cerebral palsy

        Nutritional factors:

      • Inadequate intake primarily related to feeding dysfunction
      • Increased calorie losses
      • Increased calorie use

        Non-nutritional factors:

      • Age
      • Genetic factors
      • Physical factors related to the child’s neurologic condition
        • Neurotrophic factors
        • Lack of weight bearing and mechanical stress on the long bones
      • Endocrine factors

      Nutritional Factors

      Inadequate intake

      The most significant factor affecting the nutritional status of children with CP is inadequate intake to meet metabolic demands.
      • Stallings V.A.
      • Zemel B.S.
      • Davies J.C.
      • et al.
      Energy expenditure of children and adolescents with severe disabilities: a cerebral palsy model.
      In turn, food processing and swallowing problems, which affect 30% to 40% of children with CP, are the primary reasons for inadequate intake.
      • Dahlseng M.
      • Finbraten A.
      • Juliusson R.
      • et al.
      Feeding problems, growth and nutritional status in children with cerebral palsy.
      • Rogers B.
      Feeding method and health outcome of children with cerebral palsy.
      • Andrew M.
      • Parr J.
      • Sullivan P.
      Feeding difficulties in children with CP.
      Box 2 describes the feeding problems that are common in children with CP.
      Common feeding problems in children with cerebral palsy that hamper adequate food intake
      • Oral motor/food-processing problems
      • Swallowing difficulties and airway protection problems
      • Positioning difficulties
      • Requiring assistance with feeding
      • Prolonged feeding times
      In general, children with more significant motor impairments have more challenges with oral feeding and have poorer nutritional outcomes. Even mild feeding skill deficits can have a significant impact on the quantity of food consumed. For example, children with CP who require only minor modification of their food texture or viscosity to aid in food processing and swallowing have decreased fat stores, suggesting that they have inadequate energy intake.
      • Sullivan R.B.
      • Lambert B.
      • Rose M.
      • et al.
      Prevalence and severity of feeding and nutritional problems in children with neurological impairment: Oxford Feeding Study.
      • Troughton K.E.
      • Hill A.E.
      Relation between objectively measured feeding competence and nutrition in children with cerebral palsy.
      • Fung E.
      • Samson-Fang L.
      • Stallings V.
      • et al.
      Feeding dysfunction is associated with poor growth and health status in children with cerebral palsy.
      Other factors affecting food intake are detailed in Box 3.
      Other factors that may result in inadequate energy and nutrient intake
      • Sensory factors related to the texture and taste of foods can result in the consumption of a limited repertoire of foods that may be nutritionally incomplete
      • Fatigue before a meal or resulting from the increased effort of eating
      • Prolonged mealtimes cause stress and fatigue in parents and children and spoil the enjoyment of the meal
        • Sullivan P.B.
        • Juszczak E.
        • Lambert B.R.
        • et al.
        Impact of feeding problems on nutritional intake and growth: Oxford feeding study II.
      • Negative feeding behaviors related to mealtime stress or discomfort
      • Disturbances in the sensation of hunger and satiety
        • Andrew M.J.
        • Sullivan P.B.
        Growth in cerebral palsy.
      • Inability to communicate nutritional needs due to speech impediments or intellectual disabilities
      • Secondary health conditions, such as gastroesophageal reflux and constipation,
        • Sullivan R.B.
        • Lambert B.
        • Rose M.
        • et al.
        Prevalence and severity of feeding and nutritional problems in children with neurological impairment: Oxford Feeding Study.
        cause discomfort and therefore impact oral intake
      • Dental caries and dental malocclusion affect the quantity of food consumed

      Increased losses

      Children with CP can have significant calorie losses from gastroesophageal reflux (GER). GER in children with CP is in part related to foregut motility problems related to an interaction of the enteric and the central nervous system and to positioning challenges, increased intra-abdominal pressure secondary to chronic constipation, spasticity, or musculoskeletal deformity.
      • Sullivan P.B.
      Gastrointestinal disorders in children with neurodevelopmental disabilities.
      Aside from its impact on nutritional status, GER can result in esophageal inflammation and dental erosions, and can increase the risk of aspiration.
      • Andrew M.
      • Parr J.
      • Sullivan P.
      Feeding difficulties in children with CP.
      • Sullivan P.B.
      • Juszczak E.
      • Lambert B.R.
      • et al.
      Impact of feeding problems on nutritional intake and growth: Oxford feeding study II.

      Energy expenditure

      Ambulant children with CP have similar energy expenditures to their age-matched peers, whereas those who are marginally ambulant or nonambulant have significantly lower energy expenditures. This is largely due to decreased activity levels.
      • Stallings V.A.
      • Zemel B.S.
      • Davies J.C.
      • et al.
      Energy expenditure of children and adolescents with severe disabilities: a cerebral palsy model.
      • Walker J.
      • Bell K.
      • Boyd R.
      • et al.
      Energy requirements in preschool-age children with CP.
      • Bell K.L.
      • Samson-Fang L.
      Nutritional management of children with cerebral palsy.
      • Rieken R.
      • Goudoever J.
      • Schierbeek H.
      • et al.
      Measuring body composition and energy expenditure in children with severe neurologic impairment and intellectual disability.
      There has been considerable debate about the influence of muscle inefficiency, spasticity, and dyskinesia on the energy requirements of children with CP.
      • Krick J.
      • Murphy P.E.
      • Markham J.F.
      • et al.
      A proposed formula for calculating energy needs of children with cerebral palsy.
      These factors were once thought to increase energy expenditure; however, they may not have as large an influence as was previously thought. At the very least, the contribution of these factors to energy expenditure is subject to considerable variability among children, even when they are matched for motor abilities.
      • Walker J.
      • Bell K.
      • Boyd R.
      • et al.
      Energy requirements in preschool-age children with CP.
      • Arrowsmith F.R.
      • Allen J.K.
      • Gaskin K.G.
      • et al.
      Nutritional rehabilitation increases the resting energy expenditure of malnourished children with severe cerebral palsy.
      Energy requirements in children with CP may increase if their activity levels increase during intensive therapy sessions or if they have an increased respiratory rate and effort. Among other things, the latter can be related to upper airway obstruction or chronic chest infections.
      • Andrew M.
      • Parr J.
      • Sullivan P.
      Feeding difficulties in children with CP.

      Non-nutritional Factors Affecting Growth and Nutrition in Children with Cerebral Palsy

      In general, nutritional factors have a greater impact on children’s weight, whereas non-nutritional factors have a larger influence on their stature.
      • Andrew M.J.
      • Sullivan P.B.
      Growth in cerebral palsy.
      Growth may be impacted by the direct effects of the negative neurotrophic factors related to the children’s underlying condition or the indirect effects of immobility and lack of weight bearing.
      • Samson-Fang L.
      • Stevenson R.
      Linear growth velocity in children with cerebral palsy.
      • Stevenson R.D.
      • Roberts C.D.
      • Vogtle L.
      The effects of non-nutritional factors on growth in cerebral palsy.
      • Oeffinger D.
      • Conaway M.
      • Stevenson R.
      • et al.
      Tibial length growth curves for ambulatory children and adolescents with cerebral palsy.
      Children with asymmetric involvement of CP have decreased growth and fat mass on the more affected side, even in the face of good nutritional status and typical stature for age. This supports the impact of non-nutritional, nonendocrine factors on growth in children with CP.
      • Stevenson R.D.
      • Roberts C.D.
      • Vogtle L.
      The effects of non-nutritional factors on growth in cerebral palsy.
      In contrast, the decline in growth with age in children with CP, even when they are well nourished,
      • Stevenson R.
      • Hayes R.
      • Cater L.
      • et al.
      Clinical correlates of linear growth in children with cerebral palsy.
      and the lack of growth spurt accompanying puberty in children with severe motor impairment, speaks to the contributions of endocrine factors affecting growth. These variations in growth may be related to alterations in growth hormone and the hypothalamic pituitary axis.
      • Coniglio S.
      • Stevenson R.
      • Rogol A.
      Apparent growth hormone deficiency in children with cerebral palsy.
      • Kuperminc M.
      • Gurka M.
      • Houlihan C.M.
      • et al.
      Puberty, statural growth, and growth hormone release in children with cerebral palsy.
      The hypothalamus has an important role in modulating satiety, appetite control, and energy homeostasis and thereby influences growth and nutritional status.
      • Andrew M.J.
      • Sullivan P.B.
      Growth in cerebral palsy.

      Undernutrition is a remediable condition

      With the increased use of enteral nutrition support has come the understanding that malnutrition is remediable and not intrinsic to CP.
      • Kuperminc M.
      • Stevenson R.
      Growth and nutrition disorders in children with cerebral palsy.
      Weight gain is generally noted early after the introduction of enteral nutrition support in children with CP, although increases in length often lag behind the improvements in weight. Growth is generally better the earlier nutrition is optimized, suggesting a critical window during which nutritional rehabilitation will have the most beneficial effect on growth.
      • Stallings V.A.
      • Charney E.G.
      • Davies J.C.
      • et al.
      Nutrition-related growth failure of children with quadriplegic cerebral palsy.
      • Rempel G.R.
      • Colwell S.O.
      • Nelson R.P.
      Growth in children with cerebral palsy fed via gastrostomy.

      The importance of good nutrition for children with cerebral palsy

      Good Nutrition Improves General Health and Participation

      In any child, poor nutrition can negatively affect growth, development, and muscle strength, immune function, and wound healing.
      • Kuperminc M.
      • Stevenson R.
      Growth and nutrition disorders in children with cerebral palsy.
      • Andrew M.J.
      • Sullivan P.B.
      Growth in cerebral palsy.
      • Mehta N.
      • Corkins M.
      • Lyman B.
      • et al.
      Defining pediatric malnutrition: a paradigm shift toward etiology-related definitions.
      There is little direct evidence of the relationship between specific health concerns and poor nutrition in children with CP, but its effects on unaffected individuals are also applicable to undernourished children with CP.
      • Kuperminc M.
      • Stevenson R.
      Growth and nutrition disorders in children with cerebral palsy.
      For example, because poor nutrition is associated with decreased muscle strength, poorly nourished children with CP may have respiratory muscle weakness and decreased coughing strength, making them vulnerable to lower respiratory tract infections.
      • Andrew M.
      • Parr J.
      • Sullivan P.
      Feeding difficulties in children with CP.
      Moreover, malnutrition may hamper the resolution of these infections because of decreased immune function. Furthermore, the impaired wound healing that generally accompanies malnutrition takes on special significance in children with CP who are undergoing surgical procedures.
      • Kuperminc M.
      • Stevenson R.
      Growth and nutrition disorders in children with cerebral palsy.
      In these children, delayed wound healing may negatively impact their surgical outcomes and prolong their hospital admissions.
      Given the negative impact of inadequate nutrition in children in general, there has been considerable interest in determining the specific consequences of poor nutritional status in children with CP. Brooks and colleagues
      • Brooks J.
      • Day S.
      • Shavelle R.
      • et al.
      Low weight, morbidity and mortality in children with cerebral palsy: new clinical growth charts.
      demonstrated that poorly nourished children with CP at all levels of severity have a greater number of secondary and chronic health conditions than children who are better nourished. Similarly, researchers in the North American Growth in Cerebral Palsy Research Collaborative
      • Stevenson R.D.
      • Conaway M.
      • Chumlea W.C.
      • et al.
      Growth and health in children with moderate-to-severe cerebral palsy.
      found correlations between general health and nutritional status in children with CP.
      • Fung E.
      • Samson-Fang L.
      • Stallings V.
      • et al.
      Feeding dysfunction is associated with poor growth and health status in children with cerebral palsy.
      They noted that not only do undernourished children with CP who have low muscle mass have poorer general health, but those with low fat reserves have increased health care utilization and decreased participation in school and family activities.
      • Samson-Fang L.
      • Fung E.
      • Stallings V.A.
      • et al.
      Relationship of nutritional status to health and societal participation in children with cerebral palsy.

      Good Nutrition Improves Brain Growth and Neurodevelopmental Outcomes

      Poor nutrition can negatively impact brain growth, which leads to adverse neurodevelopmental outcomes in infants.
      • Cheong J.
      • Hunt R.
      • Anderson P.
      • et al.
      Head growth in preterm infants: correlation with magnetic resonance imaging and neurodevelopmental outcome.
      Conversely, nutritional rehabilitation may have neuroprotective effects in children with a perinatal brain injury. If these children are given a diet enhanced in calories and protein early in life, they demonstrate better brain growth, which has a positive effect on their neurodevelopmental outcomes.
      • Dabydeen L.
      • Thomas J.E.
      • Aston T.J.
      • et al.
      High-energy and -protein diet increases brain and corticospinal tract growth in term and preterm infants after perinatal brain injury.
      Nutritional rehabilitation also enhances motor skill development,
      • Campanozzi A.
      • Capano G.
      • Miele E.
      • et al.
      Impact of malnutrition on gastrointestinal disorders and gross motor abilities in children with cerebral palsy.
      which in turn, increases a child’s exploratory behavior and learning from their environment.

      Good Nutrition Impacts Bone Health

      Children with CP who are nonambulant are at increased risk of having bone demineralization,
      • Henderson R.
      • Kairalla J.
      • Abbas A.
      • et al.
      Predicting low bone density in children and young adults with quadriplegic cerebral palsy.
      which is compounded by inadequate nutrition, decreased exposure to sunlight, and anticonvulsant use.
      • Marchand V.
      • Motil K.
      • NASPGHAN Committee on Nutrition
      Nutrition support for neurologically impaired children: a clinical report of the North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition.
      However, in contrast to other secondary health conditions, which are worsened by underweight status, it is the children with CP who have an increased fat mass and those who are fed via gastrostomy tubes who are at greatest risk of osteopenia-related fractures.
      • Stevenson R.
      • Conaway M.
      • Barrington M.K.
      • et al.
      Fracture rate in children with cerebral palsy.
      This could be related to
      • More rapid accrual of body fat than bone minerals
      • A direct effect of the excess weight on the bone
      • The impact of the fat mass itself on the bone mineral density.
        • Stevenson R.
        • Conaway M.
        • Barrington M.K.
        • et al.
        Fracture rate in children with cerebral palsy.

      Good Nutritional Status Improves Survival

      Good nutrition is a powerful prognosticator of survival in children with CP. At all levels of motor involvement, children with CP who are poorly nourished are at increased risk of mortality.
      • Brooks J.
      • Day S.
      • Shavelle R.
      • et al.
      Low weight, morbidity and mortality in children with cerebral palsy: new clinical growth charts.
      • Strauss D.J.
      • Shavelle R.M.
      • Anderson T.W.
      Life expectancy of children with cerebral palsy.
      Overall, survivorship in children and adults with CP has increased in the past few decades, which is also the period during which use of gastrostomy tube feeding has increased.
      • Strauss D.
      • Brooks J.
      • Rosenbloom L.
      • et al.
      Life expectancy in cerebral palsy: an update.
      • Strauss D.
      • Shavelle R.
      • Reynolds R.
      • et al.
      Survival in cerebral palsy in the last 20 years: signs of improvement?.
      Some have speculated that the increased survival in people affected by CP is at least in part related to a better understanding of the nutrient requirements and more aggressive management of nutrition.
      • Strauss D.
      • Shavelle R.
      • Reynolds R.
      • et al.
      Survival in cerebral palsy in the last 20 years: signs of improvement?.

      Assessment of nutritional status

      Health care providers can acquire valuable information about the child’s nutrition by obtaining a detailed history of the primary and secondary health conditions affecting the child and specific information related to the child’s feeding, as outlined in Box 4.
      Information useful in understanding a child’s feeding challenges
      • WHO: Persons involved with feeding; differences in feeding styles
      • WHAT: The type, texture, viscosity, quantity, and quality of the food consumed
      • WHEN: The timing, frequency, and duration of meals
      • WHERE: The feeding environment, distractions
      • HOW: The feeding routine, technique, adaptive equipment, positioning
      Examining the child and observing a typical meal provides valuable insight into the child’s oro-motor skills, aspiration risk, nutritional status, and fat reserves and the feeding interaction and technique. Assessing the children for micronutrient deficiencies may be important if their diets are very limited in quantity and repertoire.
      All of the information obtained from the history, observation, and evaluation of the child should to be assessed within the context of the child’s family. Understanding the importance of feeding as a time of nurturance for the child and his or her family, regardless of the stress that mealtime may bring, helps to establish feeding goals and nutritional rehabilitation plans. These plans are often multilayered, reflecting the multidimensional nature of the task of feeding and the expertise on many levels, which different team members, including family members, bring to the table.
      • Sullivan P.B.
      • Juszczak E.
      • Lambert B.R.
      • et al.
      Impact of feeding problems on nutritional intake and growth: Oxford feeding study II.

      Anthropometric Measurements in Children with Cerebral Palsy

      To evaluate the nutritional status of a child, anthropometric measurements, both individually and in comparison with each other and with those of other children, are key.
      Height and weight are the most basic of the anthropometric measurements. Monitoring weight is relatively easy in children with CP, especially if a wheelchair scale is available on which children can sit or can be weighed indirectly in and out of their chairs. However, the determination of height is not straightforward in children with CP, who are difficult to measure due to the presence of joint contractures, scoliosis, variations in tone, and inability to stand.
      When a standing height cannot be obtained, segmental measurements that are widely accepted as valid proxies for height in children with CP can be used.
      • Stevenson R.D.
      Use of segmental measure to estimate stature in children with cerebral palsy.
      Accurate measurement is essential, as any errors are magnified by the equation that is needed to translate the segmental measurements into estimated lengths (Table 1).
      Table 1Segmental measurements of height in children with CP who are unable to stand
      MeasurementAgeEquipmentTechniqueCalculation
      • Oeffinger D.
      • Conaway M.
      • Stevenson R.
      • et al.
      Tibial length growth curves for ambulatory children and adolescents with cerebral palsy.
      • Stevenson R.D.
      Use of segmental measure to estimate stature in children with cerebral palsy.
      • Chumlea W.C.
      Prediction of stature from knee height for black and white adults and children with application to mobility-impaired or handicapped persons.
      KHAll agesKH calipersWith the child sitting, the flat blade of the caliper is placed under the child’s heel. With the knee and ankle joint at 90°, the top blade of the caliper is positioned 2 cm behind the patella over the femoral condyles. The KH (cm) is the distance between the blades of the caliper.For children 12 y and younger
      For individuals over 12 years of age refer to the tables in by Chumlea.45


      Estimated height = (2.69) × KH (cm) + 24.2
      TL2–12 yTape measureThe tibia is measured on the medial side. With the child sitting or supine, find and mark the joint space between the tibia and the femur. Then mark the distal edge of the medial malleolus. The TL is the distance between these points in centimeters.Estimated height = 3.26 × TL (cm) + 30.8
      Abbreviations: CP, cerebral palsy; KH, knee height; TL, tibial length.
      For individuals over 12 years of age refer to the tables in by Chumlea.
      • Chumlea W.C.
      Prediction of stature from knee height for black and white adults and children with application to mobility-impaired or handicapped persons.
      Once the height is calculated from the segmental measurements, it can be used in comparison with weight and with age and can be plotted on standard growth charts. Although there are challenges in interpretation in the measurements in children with CP compared with unaffected children, the measurements nonetheless allow for trending of weight and height in individual children and can assist in identifying faltering growth over time.

      Weight for height and body mass index

      In typically growing children, assessing weight in relation to height is a universally accepted concept for assessing nutritional status
      • Stevenson R.D.
      • Conaway M.R.
      Weight and mortality rater: “Gomez classification” for children with cerebral palsy?.
      ; however, in children with CP, weight for height or body mass index (BMI) calculations are of little clinical use because they lack clinical sensitivity due to the children’s altered body composition and growth:
      • Weight for height measures fail to identify depleted fat stores in half of children with CP
        • Samson-Fang L.
        • Stevenson R.
        Identification of malnutrition in children with cerebral palsy: poor performance of weight-for-height centiles.
      • Measurement errors are magnified by the BMI calculations
      • Microcephaly or macrocephaly can skew the weight for height measurements of the children.
      For example, a child with a very small head may appear poorly nourished on the weight for height measurement of a standard growth chart because the typical contribution of the weight of the head to the child’s overall weight is small. Examining the child and using measurements other than the standard weight for height or BMI are required in this circumstance to assess whether or not the child is adequately nourished.

      Triceps skin fold measurement

      Because weight for height and BMI do not identify children with CP who are undernourished, other measurements to enhance the interpretation of their nutritional status are required. The clinical measurement that performs best as a screening test for depleted fat stores in children with CP is a triceps skin fold (TSF) measurement less than the 10th percentile for age as measured on standard charts.
      • Samson-Fang L.
      • Stevenson R.
      Identification of malnutrition in children with cerebral palsy: poor performance of weight-for-height centiles.
      • Frisancho A.T.
      New norms of upper limb fat and muscle areas for assessment of nutritional status.

      World Health Organization. Growth charts. Available at: http://www.who.int/childgrowth/standards/ac_for_age/en/. Accessed April 28, 2014.

      The TSF can be easily measured without causing distress, as outlined in Box 5.
      Measuring a triceps skin fold (TSF)
      • Identify the point halfway between the acromion and distal end of the humerus
      • Using the thumb and forefinger, lift the fat overlying the triceps muscle away from the muscle
      • Measure the width of the fat fold in millimeters with appropriate calipers
      The TSF measurement generally underestimates the fat stores in a child with CP, in whom considerable fat is stored internally and is therefore inaccessible to fat-fold measurements.
      • Samson-Fang L.
      • Stevenson R.
      Identification of malnutrition in children with cerebral palsy: poor performance of weight-for-height centiles.
      This fact must be taken in to consideration during nutritional rehabilitation. Targeting a goal TSF between the 10th and 25th percentiles and not the more usual 50th percentile for age is appropriate for children with CP because of the differences in fat distribution.
      Although the TSF is a valuable screening tool for fat depletion, it cannot be used in isolation to calculate overall body fat. To calculate body fat (see “Body composition” section, later in this article), indirect or direct measurements of body composition are required. However, as these are often inaccessible in clinical practice, computing the total body fat measurements using the subscapular fat fold and the TSF in CP-specific equations developed by Gurka and colleagues,
      • Gurka M.
      • Kuperminc M.
      • Busby M.
      • et al.
      Assessment and correction of skinfold thickness equations in estimating body fat in children with cerebral palsy.
      is a good predictor of total body fat, especially in children with CP who are ambulant.
      • Oeffinger D.
      • Gurka M.
      • Kuperminc M.
      • et al.
      Accuracy of skinfold and bioelectrical impedance assessment of body fat percentage in ambulatory individuals with cerebral palsy.

      Mid-arm circumference

      Interest in using mid-arm circumference (MAC) measurements in the children with malnutrition has increased recently.
      • Mehta N.
      • Corkins M.
      • Lyman B.
      • et al.
      Defining pediatric malnutrition: a paradigm shift toward etiology-related definitions.
      The MAC is a measure of the child’s muscle mass, and bone and fat reserves, and, therefore, like other measurements in children with CP, is affected by differences in body composition and growth compared with typical children. However, like TSF measurements, it is reproducible and can be compared with other children on the MAC chart developed either by Frisancho
      • Frisancho A.T.
      New norms of upper limb fat and muscle areas for assessment of nutritional status.
      or the World Health Organization (WHO).

      World Health Organization. Growth charts. Available at: http://www.who.int/childgrowth/standards/ac_for_age/en/. Accessed April 28, 2014.

      Box 6 illustrates an example of using the MAC and TSF measurements.
      Using the mid-arm circumference (MAC) and TSF measurements in nutritional assessments
      Using the MAC in combination with the TSF provides valuable information to share with the children’s families when planning nutritional rehabilitation. For example, if a child who appears to be very lean has a TSF measurement at the 25th percentile for age but the MAC measurement is only at the 5th percentile for age, it suggests that the child has adequate calorie intake but appears very lean because of low muscle (lean body) mass. If both the MAC and the TSF are low, muscle depletion and low body fat reserves may be present.
      All of the anthropometric measurements (weight, height, TSF, and MAC) can be repeatedly measured and compared to monitor overall growth. Weight gain velocity between visits in grams per day helps to demonstrate weight plateaus. Expressing the growth parameters as standard deviations (z-scores) allows for comparison of actual numbers. This has an advantage over trying to gauge the trajectories on percentile charts, especially when the children plot far from the expected percentiles on standard growth charts. For example, if the weight is plotted on a standard growth chart and is always well below the third percentile, it is difficult to gauge changes over time. But if one knows that the z-score was −3.19 at the last clinic visit and now is −2.98, this is an improvement, which may not be seen on a standard percentile plot.

      Specialized growth charts

      As mentioned previously, comparing children with CP with typically growing children on standard growth charts is fraught with challenges because of alterations in body composition and structure in children with CP. However, growth charts on which the individual weights of children with similar motor impairments can be compared has more utility. Such growth charts have been developed using a large sample of children whose information is captured in the Life Expectancy Project.
      • Brooks J.
      • Day S.
      • Shavelle R.
      • et al.
      Low weight, morbidity and mortality in children with cerebral palsy: new clinical growth charts.
      Brooks and colleagues developed multiple CP-specific growth charts stratified by tube feeding status and functional severity using the well-validated clinical algorithm, the Gross Motor Function Classification Scale (GMFCS).
      • Palisano R.
      • Rosenbaum P.
      • Walter S.
      • et al.
      Development and reliability of a system to classify gross motor function in children with cerebral palsy.
      The 5 GMFCS levels group children in age-bands and define trajectories of motor function over time. Children in level 1 have the best motor function and are able to walk without limitation, whereas those in level 5 have little independent mobility and are transported by others in manual wheelchairs. As there are significant differences in the children’s weight and growth in relation to motor function, separate growth charts for each level provide important information about the weight of children compared with other children with a similar level of motor function. Children who are classified as GMFCS 5, are not only very different in motor function compared with children in other groups, but they are also more likely to have fragile and complex health status, grow more poorly, and require enteral nutrition support more often than children in other groups.
      The CP-specific growth charts
      • Brooks J.
      • Day S.
      • Shavelle R.
      • et al.
      Low weight, morbidity and mortality in children with cerebral palsy: new clinical growth charts.
      describe not only the weight gain and growth characteristics of children at various levels of function, they also identify the weight-for-age percentile (20th percentile), at which point the children are at increased risk of morbidity and mortality. Thus, a single measurement can be used to provide some insight into a child’s nutritional risk. This is important, because even though validated measurements appropriate for children with CP, as described previously, are available, they are still not widely applied in clinical settings.
      These growth charts are population-based and will have to be validated in clinical settings. Further research also is required to see if nutritional rehabilitation will mitigate the increased risk of mortality identified in the children who plot in the “zone of concern” on the CP-specific growth charts.
      • Stevenson R.D.
      • Conaway M.R.
      Weight and mortality rater: “Gomez classification” for children with cerebral palsy?.
      These charts are valuable tools in opening the discussions regarding nutritional rehabilitation with families, as parents can see how their child is fairing compared with children with similar motor challenges.
      • Stevenson R.D.
      • Conaway M.R.
      Weight and mortality rater: “Gomez classification” for children with cerebral palsy?.
      If a child’s weight for age is consistently plotting below the 20th percentile, health care providers knowing the significance of this, at least on a population level, can reinforce the importance of improving the nutrition to avoid the morbidity and mortality risk associated with this low weight for age.

      Body composition

      Measures of body composition quantify body fat, muscle, and bone mass and total body water. In children with CP, body composition is altered due to decreased muscle and bone mass related to decreased activity levels, as well as malnutrition and neurologic impairment. Although it was once thought that children with CP had a decreased overall fat mass,
      • Stallings V.A.
      • Cronk C.E.
      • Zemel B.S.
      • et al.
      Body composition in children with spastic quadriplegic cerebral palsy.
      more recent information suggests that children with CP have similar fat mass to children without chronic health conditions.
      • Kuperminc M.
      • Gurka M.
      • Bennis J.
      • et al.
      Anthropometric measures: poor predictors of body fat in children with moderate to severe cerebral palsy.
      An understanding of this is important, because the children may appear very thin because of low lean body mass, but actually have an appropriate fat mass.
      Reliable measurements of body composition that are easy to perform in the clinical setting would provide valuable insight into a child’s nutritional status. However, at this point, there is little consensus in the literature as to the best approach to measure body composition. Research has focused on direct measures of underwater weighing, deuterium-dilution technique, dual x-ray absorptiometry (DXA), and an indirect measure, namely, bioelectrical impedance (BIA). Of these methods, BIA holds promise as a technique to measure body composition that can be incorporated into clinical practice because of ease of use and its noninvasive technique.
      • Bell K.L.
      • Boyd R.N.
      • Walker J.K.
      • et al.
      The use of bioelectrical impedance analysis to estimate total body water in young children with cerebral palsy.
      BIA correlates quite well with DXA in the assessment of fat mass, as does the computing of fat mass by using the TSF and subscapular fat-fold measurements in the CP-specific equations.
      • Gurka M.
      • Kuperminc M.
      • Busby M.
      • et al.
      Assessment and correction of skinfold thickness equations in estimating body fat in children with cerebral palsy.
      • Oeffinger D.
      • Gurka M.
      • Kuperminc M.
      • et al.
      Accuracy of skinfold and bioelectrical impedance assessment of body fat percentage in ambulatory individuals with cerebral palsy.
      At this point, the other methods are largely used on a research basis because of time constraints and lack of availability of equipment.
      • Kuperminc M.
      • Gurka M.
      • Bennis J.
      • et al.
      Anthropometric measures: poor predictors of body fat in children with moderate to severe cerebral palsy.

      Nutritional intervention

      Enhancing Oral Nutrition

      Once families and care providers decide that a concerted nutritional intervention is required for a child because of poor weight gain, depleted fat reserves, or faltering growth, a plan can be developed that focuses on improving all aspects of oral feeding, incorporates the families’ priorities for feeding, and defines time frames for evaluating the efficacy of the oral nutritional rehabilitation plan (Table 2).
      Table 2Goals of nutrition rehabilitation
      • Nutrition rehabilitation goals for children with poor nutritional status:
        • Safe, comfortable, pleasurable intake to meet nutritional and energy requirements
      Nutrients
      • Protein and micronutrients similar to requirements of age-matched peers
      • Meet age-appropriate calcium and vitamin D requirements
      • There are no clear standards for energy requirements but they are lower in children who are not ambulant than in typically growing children
      Triceps skin foldAim for 10th–25th percentile for age
      WeightMonitor weight at 2–4-wk intervals
      Weight gain velocityAim for 4–7 g per day in children >1 y (adjust as needed depending on degree of malnutrition)
      Weight for age on cerebral palsy growth chart
      • Brooks J.
      • Day S.
      • Shavelle R.
      • et al.
      Low weight, morbidity and mortality in children with cerebral palsy: new clinical growth charts.
      Aim for a weight >20th percentile which is above the “zone of concern”
      The next step is to establish specific nutrient requirements. The protein and micronutrient requirements of children with CP are similar to their age-matched peers. Special attention should be given to meeting vitamin D and calcium requirements for bone health reasons, especially for children who are not ambulant. There are, however, no standard methods for determining energy requirements for children with CP. This is in large part because of the heterogeneity of the children with CP, the high variability in motor activity, and the variations in body composition.
      • Rieken R.
      • Goudoever J.
      • Schierbeek H.
      • et al.
      Measuring body composition and energy expenditure in children with severe neurologic impairment and intellectual disability.
      As a starting point in oral nutrition rehabilitation, care providers may want to consider increasing the caloric intake by 10% above the children’s current intake. Then the anthropometric measurements can be monitored and adjustments made with the family, nutrition goals, and the time frames taken into consideration.
      Food records are not useful for calculating exact intakes, because families frequently overestimate the child’s intake and underestimate the amount of food lost from the child’s mouth.
      • Walker J.
      • Bell K.
      • Caristo F.
      • et al.
      A review of energy intake measures used in young children with cerebral palsy.
      However, food records may be useful in identifying opportunities for improving the calorie and nutrient content of foods listed in the food record with nutrient-dense and high-energy food stuffs, especially fats, dairy products, sugars, and glucose polymers, commercial meal replacements, or supplements.
      Oral nutritional rehabilitation involves increasing a child’s caloric and nutrient intake and improving the entire feeding process. Members of the multidisciplinary team can advise families about feeding safety and efficiency
      • Snider L.
      • Majnemer A.
      • Darsaklis V.
      Feeding interventions for children with cerebral palsy: a review of the evidence.
      and about other aspects of feeding, as noted in Box 7.
      Other interventions for oral nutritional rehabilitation
      • Positioning for optimal feeding
      • Adjusting the consistency and viscosity of foods/liquids to best suit the child’s skills and sensorimotor requirements
      • Pacing of the feeding
      • Balancing fatigue with the pleasure of eating
      • The appropriate use of adaptive equipment
      Unfortunately, improving the nutritional status of children with significant motor impairment by oral means alone is challenging even when attention is paid to all aspects of the feeding process. Nutrition support via gastrostomy tube (GT) feeding has become widely accepted if nutrition goals cannot be met by oral means. Box 8 describes factors to consider before GT placement.
      Factors that warrant consideration of gastrostomy tube (GT) placement
      • Prolonged meal times are limiting the child’s participation in school and community activities
      • Stress with the oral-feeding process is present for the child and the family
      • Aspiration during feeding is interfering with pleasure of eating or is contributing to recurrent respiratory illnesses
      • Ongoing poor weight gain and growth despite attempts at oral nutritional rehabilitation

      Gastrostomy Tube Feeding

      Expertise in the management of enteral feeding via GTs and the availability of appropriate devices and nutritional formulas, have contributed to the improved ability to provide nutritional rehabilitation to children with CP. However, families experience considerable decisional uncertainty regarding GT placement, because they and their children often value oral feeding despite the significant challenges that may accompany it. Box 9 details factors that help decrease a family’s decisional uncertainty about GT placement.
      Factors facilitating decision-making regarding GT placement for families
      • Providing information without exerting pressure to make a decision
      • Reassuring parents that some oral feeding can continue after GT placement
      • Education about the GT simply as an adaptive device to facilitate feeding
      Although families often have considerable uncertainty about GT placement initially, they generally experience high satisfaction rates and the children generally have improved nutritional indicators and better health after GT placement (Box 10).
      Findings after GT placement

        Parents experience the following:

      • High satisfaction rates with enteral feeding
      • Decreased stress
      • Decreased time spent feeding
        • Sullivan P.B.
        • Juszczak E.
        • Bachlet A.
        • et al.
        Gastrostomy tube feeding in children with cerebral palsy: a prospective longitudinal study.
      • Improved perception of their child’s health
        • Sullivan P.B.
        • Juszczak E.
        • Bachlet A.
        • et al.
        Gastrostomy tube feeding in children with cerebral palsy: a prospective longitudinal study.
        • Mahant S.
        • Friedman J.N.
        • Connolly B.
        • et al.
        Tube feeding and quality of life in children with severe neurological impairment.

        Children demonstrate the following:

      • Improvement in nutritional indicators
      • Improved health
      • Decreased hospitalization rates for pneumonia
        • Sullivan P.B.
        • Morrice J.S.
        • Vernon-Roberts A.
        • et al.
        Does gastrostomy tube feeding in children with cerebral palsy increase the risk of respiratory morbidity?.
      Despite the challenges with weight gain seen in children with CP who are orally fed, GT feeding can lead to an unexpectedly rapid weight gain.
      • Sullivan P.B.
      • Alder N.
      • Bachlet A.M.
      • et al.
      Gastrostomy feeding in cerebral palsy: too much of a good thing?.
      Overnourishing children with CP puts them at a mechanical disadvantage, decreasing their already limited mobility and increasing their respiratory effort, as they have to breathe against an increased fat mass. In addition, their families experience increased strain on their backs and joints.
      • Sullivan P.B.
      • Alder N.
      • Bachlet A.M.
      • et al.
      Gastrostomy feeding in cerebral palsy: too much of a good thing?.
      • Vernon-Roberts A.
      • Wells J.
      • Grant H.
      • et al.
      Gastrostomy feeding in cerebral palsy: enough and no more.
      Frequent monitoring of the children’s weight, weight gain velocity, and TSF after GT placement ensures that the child’s overall growth and nutritional status is improved
      • Andrew M.J.
      • Sullivan P.B.
      Growth in cerebral palsy.
      while avoiding the negative consequences of overnutrition.
      Calculating calorie requirements after GT placement in children with CP can be a challenge. In general, children who require GT placement have significant motor impairments, and thus have lower energy requirements than children who are unaffected. After GT placement, some clinicians estimate caloric requirements of a child with CP to be 50% to 70%
      • Walker J.
      • Bell K.
      • Boyd R.
      • et al.
      Energy requirements in preschool-age children with CP.
      • Vernon-Roberts A.
      • Wells J.
      • Grant H.
      • et al.
      Gastrostomy feeding in cerebral palsy: enough and no more.
      of those a typically growing child of the same age may require. Energy requirements, as published by various national bodies

      Office of Disease Prevention and Health Promotion. Dietary guidelines for Americans. Available at: www.health.gov/dietaryguidelines/. Accessed May 27, 2014.

      Health Canada: estimated caloric requirements. Available at: http://www.hc-sc.gc.ca/fn-an/food-guide-aliment/basics-base/1_1_1-eng.php. Accessed May 27, 2014.

      or by WHO

      World Health Organization. Human energy and protein requirements: report of a Joint FAO/WHO/UNU Expert Consultation. Available at: http://www.who.int/nutrition/publications/nutrientrequirements/9251052123/en/. Accessed May 27, 2014.

      for typically growing children, can be used for these calculations. Starting with a low caloric intake, which can be increased depending on weight gain velocity and carefully monitored anthropometric measurements (see Table 2), has the advantage that the tube feeding may be better tolerated from the onset and that weight gain will not be excessive. Weighing the children within 2 weeks of GT placement and then monthly until the dietary requirements become clear, allows frequent fine-tuning of the nutrient intake. Dietary changes should be made by 5% to 10% increments of the total caloric intake, always ensuring the protein, vitamin D, and micronutrient intake is adequate. This can be challenging when very low caloric intakes are required. Once the appropriate nutritional goals have been achieved, monitoring of the children’s nutritional status with complete anthropometric measurements should occur every 6 to 12 months.

      Case example

      Harley was born at 26 weeks’ gestation and experienced a stormy neonatal course and prolonged hospitalization. He eventually transitioned to oral feeding, but his growth and nutrition remained challenging. At 3 years of age he has CP (GMFCS 5) demonstrating spasticity and very limited mobility. Although he remains in good health and free of lower respiratory tract infections, he is falling farther behind on the conventional growth charts. His day care workers are having increasing difficulty feeding him, noting that he coughs frequently when drinking liquids, which are primarily bottle-fed. Oral food processing is minimal. His parents state that he enjoys eating the pureed foods they feed him and rarely refuses a meal, although they spend up to 6 hours a day feeding him. The food record details that he drinks 16 ounces of whole milk daily, and eats some yogurt, infant cereal, and pureed table foods. The parents estimate that he consumes1500 kilocalories per day, although the mealtime observation shows that the amount eaten is significantly less than reported because of loss of large quantities of food from Harley’s mouth while he is eating. He is quite constipated and regurgitates once weekly, often when coughing. His only medication is vitamin D.
      Harley looks very thin. He is smiling and interactive. His skin and hair are healthy, although there is an area of redness, but no skin breakdown, over the coccyx. Positive physical findings are limited to signs of his underlying disability and dental caries, in part related to the prolonged bottle-feeding and due to his inability to clear his mouth after he swallows, leaving a residue of food on his teeth. His parents are able to position him well in a specialized chair where he is fully supported for feeding. The feeding observation reveals significant oro-motor and swallowing challenges and a prolonged feeding time. Despite this, Harley and his parents clearly enjoy the feeding experience.
      Harley’s anthropometrics reveal a weight of 10 kg and height of 80 cm extrapolated from a knee height measurement of 20.7 cm (20.7 × 2.69 + 24.2). When these are plotted on the WHO growth charts, the weight is at the 0 percentile (z = −3.01) and the height is at the 0 percentile (z = −4.34). Over time, the z-scores of his weight and height show a steady increase in distance from normal z-scores. The percentile charts have always been at or below 0 and thus provide less insight into the deviation of the basic anthropometric measurements from that of typically growing children than the z-scores. The BMI does not contribute to the assessment because it is at the 50th percentile, which is not in keeping with the clinical observation. His TSF is 5 mm, which is less than the third percentile (z = −2) (WHO Child Growth Standards), and his MAC of 135 mm is at the third percentile (z = −2) (WHO Child Growth Standards). On the CP growth charts stratified for age, degree of motor involvement, and tube feeding status, his weight-for-age plots less than the 20th percentile in the “zone of concern,” where increased morbidity and mortality may result because of his nutritional status.
      Harley’s parents accept the information about his feeding challenges and nutrition but state at the outset that their goal is to continue oral feeding. However, together with his community therapists, day care workers, and the multidisciplinary feeding team, they participate in developing a feeding plan that addresses the following:
      • Feeding safety through positioning, thickening of the fluids, pacing the liquid and solid intake, limiting the feeding time to avoid fatigue without jeopardizing intake of calories, and appropriate cup and spoon use
      • Caloric and nutrient density of his foods: infant cereal, high-fat dairy products, high-fat spreads
      • Managing the constipation to improve comfort
      • Dental care to decrease the bacterial burden of the saliva should it be aspirated
      The parents are informed about enteral feeding options, but are reticent about considering them, citing that he has been completely healthy despite the challenges.
      Six weeks later, there is a bit of weight gain (2 g per day where >4 g per day would be expected for age), but the TSF is essentially unchanged, as is the weight for age (z-score now −3.03). But the parents are heartened by the small gain and wish to proceed with oral nutritional rehabilitation for 6 months. Within that time period, Harley gets an intercurrent viral illness with fever and coughing. He refuses oral intake and experiences rapid-onset dehydration and requires hospitalization. At this point, his weight is lower than it was at the start of the nutritional rehabilitation, despite the significant input of time and energy of a number of individuals. The parents become very worried about possible impact of poor nutrition on Harley’s health status and the risk of dehydration because of his tenuous oral intake and consent to GT placement, which takes place when he has recovered from the intercurrent infection.
      Weight gain ensues after GT feeding is initiated, even with only 500 calories per day given enterally, which is only 50% of the calories another child his age may require. Oral feeding is limited to tastes for pleasure and skill maintenance. Weekly weights during the first month after GT placement allow frequent adjustments of calorie and nutrient intake. The team decides on a maximum weight gain velocity of 10 g per day until he has achieved a TSF of the 15th percentile for age (6.25 cm) and weight of 12 kg, at which he no longer plots less than the 20th percentile on the CP growth charts (now using the ones for a boy GMFCS 5 who is tube fed).
      • Brooks J.
      • Day S.
      • Shavelle R.
      • et al.
      Low weight, morbidity and mortality in children with cerebral palsy: new clinical growth charts.
      Although his parents had a difficult time deciding on GT placement, they are pleased with the outcome. They continue to feed him small amounts of pleasurable food, but use the GT for the bulk of his calories. His day care staff is pleased with the decreased coughing at meals because of the smaller intake of oral food and feel that Harley is more interested in his environment and no longer looks as fragile as he did in the past.

      Summary

      Children with CP frequently experience challenges with nutrition and growth, which have a negative impact on their health, neurodevelopmental outcome, and survival. Intervention strategies to remediate the poor nutrition in children with CP are shaped by the following:
      • Understanding of the nutritional and non-nutritional factors affecting nutrition
      • Careful assessment of the nutritional status with appropriate anthropometric measures and growth charts
      • Consideration of the multidimensional aspects of feeding
      • Important contribution of family members in setting goals and carrying out the nutritional intervention
      If nutritional rehabilitation by oral means is not successful, careful consideration must be given to providing enteral nutrition support. The decision to proceed with gastrostomy placement is frequently associated with uncertainty for families, who require considerable support to make informed decisions about the procedure. Although gastrostomy feeding is not a panacea for all nutritional problems, weight gain usually can be achieved in children with malnutrition. Although more research is required regarding nutritional rehabilitation, the hope is that early attention to the nutritional status of children with CP will translate into positive outcomes.

      Acknowledgments

      The author thanks Dr Paul Shelton for his helpful suggestions when reviewing this article.

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