Study Settings
The study was conducted inSultan Bin Abdulaziz Humanitarian City (SBAHC), Riyadh Saudi Arabia in 2015. SBAHC is 400-bedded medical and rehabilitation center which caters medical and rehabilitation care outpatients and inpatients. Having an interdisciplinary approach and an integrated organizational structure, the patients are treated in a more specialized manner according to patients’ needs and disabilities.
Ethical approval
The study design for the current study was approved by the Research Ethics Committee at College of Applied Medical Science, King Saud University, Riyadh, Saudi Arabia (CAM525/3334). Written consents for participation in the study were obtained from the parents or guardians of children with CP prior to the commencement of the study.
Location, size, and selection of the sample
Children with CP, aged 1-12 years admitted to SBAHC, who met the CP diagnosis criteria [16, 17], were consecutively recruited from children visiting the CP clinic. Briefly, children diagnosed CP on the basis of their gross motor function, brain imaging and/or cranial ultrasound supported by additional tests (vision, hearing, speech, intellect, development, movement etc) by the specialized doctors were included. These diagnosis parameters are part of routine practice of SBAHC. Given the limitations of time and resource, the study used a convenience sample and recruited children with CP admitted between January, 2015 to August, 2015. Initially, 101 children met the eligibility criteria, but consent was only obtained from the caregivers of 80 children. Final data could be completed on 74 children as 6 children dropped out due to various reasons mainly because most (5 out of 6) of them had a documented medical history of low birth weight (<2.5 Kg), while one child was dropped because of premature birth. Information about the socio‐demographic and clinical characteristics of the study population are presented in Table 1.
Study Design
In this cross-sectional study, all assessments were made in three steps as reported elsewhere [8]. Briefly, all children were diagnosed and confirmed as ‘cerebral palsy’ by a developmental pediatrician and/or neurologist at the center. In step 1, a ‘Ten Question Screen’ was used for initial screening [13]. . In the second step, a physiotherapist further assessed the patients following the decision tree for identification of cerebral palsy [14]. In the third and final step, the developmental pediatrician and/or neurologist confirmed CP and classified it using the Gross Motor Function Classification System (GMFCS) level I-V as mentioned elsewhere [18]. Briefly, GMFCS is a validated 5-level scale that classifies the severity of motor impairment in children with cerebral palsy. Gross motor functions are based on developmental milestones, and the items of the scale are distributed among 5 dimensions (A = lying, rolling; B = sitting; C = crawling, kneeling; D = standing; E = walking, running, and jumping). As a routine practice of SBAHC, Gross Motor Function Measure (GMFM-88) tool, which is the original tool used in routine practice of SBAHC, was used for the assessment. The GMFCS level was classified by the child's physiotherapist under the supervision of pediatrician. The medical records of the participants eligible for the study demonstrated the diagnoses of CP had been made when the patient was more than 6 months of age and all required diagnosis relating to mental retardation or other developmental delays were primarily completed by the school personnel or the developmental pediatricians.
The exclusion criteria were not to consider those children with CP who had history of low birth weight or premature birth, metabolic, genetic, or neuro-degenerative diseases or with any medical infections known to affect nutritional and growth status in any way. Also, children with CP fed through enteral or parenteral routes or children with CP receiving corticosteroids or other medication/drugs known to have an influence on growth were excluded [7].
Data Collection: Data were collected in the following distinct stages [8]:
- Structured Interviews. The caregivers were interviewed using a well-structured questionnaire. Questions were included to get information on diet intake, feeding problems and other associated factors that could contribute to nutritional status [7].
- Physical and Cognitive Examination. Gross and fine moor functions were assessed based on the child ability to sit, to grasp and on self-initiated walking and fine moor function [18-21]. Cognitive impairment assessment was performed as a routine clinical practice. Data on cognitive assessment were collected from the patients’ hospital file. In general, all children were assessed for cognitive impairment by a neurologist on a Mini-Mental State Examination (MMSE) adapted and validated by Jain and Passi [20] for children on the basis of a system of scores for cognitive impairments. This instrument assesses the mental functions of language, temporal and spatial orientations, attention, constructive praxis and memory [20]. The test comprehensively assess the visual/verbal attention and visual/verbal short/long term memory. Jain and Passi [20] defined a cutoff point for cognitive deficit of two standard deviations below the mean.
- Anthropometric Measurements. Anthropometric measurements included weight, height, arm circumference (AC), arm muscle circumference (AMC), and triceps skinfold thickness (TST).Weight (kg) and height (cm) were measured as reported elsewhere [7,8]. Weight was recorded on Scale-Tronix model 2002 single scale (Dynamic Scales, Inc. 1466 South 8th Street Terre Haute, IN 47802, USA). For children who could stand easily and erectly, the height was measured with a scale with a fixed and attached stadiometer (SECA 789, Hamburg, Germany). In case it was not possible or difficult to measure the standing height because of the inherent contractures or scoliosis, height was estimated from the knee-height using available authenticated equations [6]:(see Equation 1 in the Supplementary Files)
The procedure for measuring knee-height was completed while the patient was in the supine position. The common stretchable measuring tape was used for the measurement. All measurements were done in triplicate and the average was considered. All measurements were done in the morning by the same experienced examiner.
AC was measured using non-elastic measuring tape. TST was measured with skinfold caliper (Lange®;; Power Systems, Inc., Tennessee, USA). AMC was calculated using an equation [22] as: (See Equation 2 in the Supplementary Files
All measurements were done in duplicate by the same person and the mean values were used for final analysis.
- Dietary. Dietary data were obtained by 3-days dietary records, kept by parents/caregivers or nurses of cerebral palsy children. Prior to data collection, the parents/caregivers or nurses were educated on how to measure food quantities according to the food materials that were used in the diet clinic. Nutrients were calculated from the contents of the 3-day food diaries using the Arab food analysis program (HBCN; health balance for clinical nutrition, Riyadh, Saudi Arabia) diet analysis software. The calorie and protein intake of cerebral palsy children were used for assessment of nutrient-specific demands and percentage of nutrient intake based on the WHO estimated average intake as reference (23).
- Assessment of feeding problems of children with CP. A speech and swallowing therapists assessed the feeding problems of CP children. Questions were also asked to know feeding problems (yes/no) and appetite status of the children (normal/fair vs. poor) from the parents/caregivers. For this purpose, a questionnaire, based on recommendations from previously published reports [8-13] was designed in such a way to identify the most common feeding problems including inability to self-feed, inadequate/absence of tongue lateralization, chewing problem, swallowing problem, cough/choking during feed, drooling, hypertonic tongue, inability to take solid food, constipation, sucking problem, vomiting/regurgitation, non-closure of lips around spoon, Inappropriate wide mouth opening and cry/extensor dystonia during feeding.
- Laboratory Investigations. Under aseptic conditions, 5 ml blood was drawn and serum creatinine was quantified using the ethylene-diamine-tetraacetic acid tubes. Hemoglobin, red blood cells (RBC) and hematocrit were quantified using gel tubes. All parameters were measured using routine laboratory procedures. Normal ranges for Hb, creatinine, RBC and hematocrit were used to classify the children ‘within normal range’ and ‘within abnormal range’ (see Additional File 1).
Data Handling
BMI was calculated from the weight and height of the patient (BMI = weight [kg]/height [m2]).Weight, height, and BMI values were used to calculate the sex and age normalized z-scores using the reference data for normal and healthy children [23]. Sex and age normalized z-scores were calculated using WHO Anthro- (2010) and AnthroPlus (2009). Children with extreme z‐scores were excluded from the final calculations (8). The weight‐for‐age z‐score was only calculated for children up to 10 years of age and the weight‐for‐height z‐score for those up to 5 years of age [8]. Nutritional status of each child was assessed on the basis of z-scores. For the purpose of interpretation, a weight-for-age z-score <-2 was defined as ‘underweight’; height-for-age z-score <-2 was defined as ‘stunting’; weight-for-height z-score <-2 was defined as ‘wasting’ whereas BMI-for-age z-score<- 2 was defined as ‘thinness’ as previously reported [3,8]. Classification of nutritional status was also performed using arm anthropometrics, i.e. AC, AMC, and TSF. Reference values proposed by Frisancho [24] (for children older than 1 year of age) and Jelliffe [25] (for those younger than 1 year) were used. Definitions of anthropometric indicators and normal ranges for Hb, creatinine, RBC and hematocrit are summarized in additional file (see Additional File 1).Adequate energy and protein intakes were evaluated according to the Dietary Reference Intake (DRI) values of WHO.
Statistical Analysis
Statistical Package for Social Sciences database (IBM, SPSS, version 23, USA) was used for the analyses of the data that were expressed as percentages and mean (SD). Pearson's correlation co-efficient was calculated to determine any association between the factors considered and the dependent variables of stunting, underweight, wasting and thinness with p value ≤ 0.05 as significant. . Co-occurrence of more than two indicators of nutritional status in a single child was depicted using a Venn diagram and consequent correlation between nutritional indicators were calculated based on Venn diagram as reported previously [8]. Factors such as age and type of cerebral palsy were categorized, and the adjusted odds ratios (aORs) with corresponding 95% confidence intervals (CIs) were computed. A p-value <0.05 was considered significant.