A Cross-Sectional Study Examining the Relationship Between Malnutrition and Gross Motor Function in Cerebral Palsy

Introduction Cerebral palsy (CP) characterizes a range of permanent, nonprogressive symptoms of postural and motor dysfunction caused by an insult to the developing central nervous system in a fetus or an infant. CP manifests early in life, often within the first two to three years of age. CP is associated with poor growth, that is the deviation from the normal growth parameters. The prevalence of CP ranges from 2.0 to 3.5 per 1000 live births in high-income countries which is comparable to the estimates from low-income countries. Antenatal and perinatal insults are among the most commonly reported causes of CP; however, a large number of cases do not have an identifiable etiology of CP. The current study aims to examine the relationship between malnutrition and gross motor function in children with CP. Materials and Methods This study was conducted at the Department of Pediatrics and Neonatology, Nehru Hospital, Baba Raghav Das (BRD) Medical College, Gorakhpur (UP) over a period of one year (August 2020 to July 2021) after obtaining ethical clearance from the College Research Council. Children of age 1-15 years with CP attending the pediatric outpatient and inpatient departments were enrolled as the study participants after obtaining informed consent from a legal guardian. Assessment of motor function was done using the gross motor function classification system (GMFCS). Associations of malnutrition across levels of gross motor function were tested using Chi-square or Fisher’s exact test whichever was applicable. Statistical significance was set at p < 0.05 as significant. Data was analyzed using IBM SPSS Statistics for Windows, Version 21 (Released 2012; IBM Corp., Armonk, New York, United States). Result We analyzed 110 children with a diagnosis of CP (median age 6.5 years, interquartile range (IQR) 4.4-9.0 years). The majority (65/110; 59%) of the patients were male, and 68 (61.8%) delivered at term gestation. The most common presenting symptom among children with CP was seizures (79/110; 72.3%), the second most common being delayed milestones among 73 (66.8%), followed by difficulty in breathing among 63 (57.5%). The association between the anthropometric index of participants and GMFCS was found to be highly significant. Conclusion Most CP patients were facing gross motor disturbances. Spastic type of CP was most frequent, and more than half of the patients experienced feeding difficulty. A statistically significant association was found between gross motor functioning and the prevalence of malnutrition and stunting.


Introduction
Cerebral palsy (CP) characterizes a range of permanent, nonprogressive symptoms of postural and motor dysfunction caused by an insult to the developing central nervous system in a fetus or an infant [1].The motor disorders of CP are often accompanied by disturbances of sensation, cognition, communication, perception, and/or behavior and/or by a seizure disorder [2].The prevalence of CP ranges from 2.0 to 3.5 per 1000 live births in high-income countries which is comparable to the estimates from low-income countries [3].CP manifests early in life, often within the first two to three years of age.CP is a complex of symptoms rather than a specific disease.CP is the leading cause of childhood disability [4].It is well recognized that CP is related to poor growth and the deviation from the routine growth parameter values increases with increasing levels of gross motor dysfunction [5,6].A multidisciplinary team involving a dedicated pediatrician, pediatric neurologist, physiotherapist, occupational therapist, child psychologist, and social worker is needed to evaluate a child with CP.The pathophysiologic processes behind the majority of the CP symptoms are still poorly understood.Antenatal and perinatal insults are among the most commonly reported causes of CP; however, a large number of cases do not have identifiable etiology of CP [7].Risk factors for CP may include but are not limited to low birth weight or preterm birth, multiple gestations, infertility treatments, infections during pregnancy, fever during pregnancy, Rh incompatibility, and exposure to toxic chemicals.Some maternal medical conditions like abnormal thyroid function, intellectual and developmental disability, seizures, complicated labor and delivery, jaundice, preterm or low birthweight, birth injury, etc., may also lead to CP. Malnutrition during the initial days of life may result in a delay in developmental milestones with early and remote consequences [8].
CP is a complex neuromuscular disorder known to impact gross motor function adversely [9,10].Damage to the developing brain disrupts motor control and may generate spasticity, leading to diminished strength and aberrant musculoskeletal loading, further resulting in joint contractures and bone abnormalities.CP is nonprogressive in course, but secondary effects can continue and may worsen with maturation [11].Children with CP and malnutrition are at increased risk of adverse outcome [12,13].Malnutrition and growth impairment are associated both with nutritional and nonnutritional factors, including poor oral-motor function, gastric reflux, aspiration pneumonia, adverse neurotropic effects, and endocrine malfunctions [14,15].Nutritional status and prognosis in children with CP are also found to be associated with socioeconomic factors.In low-income countries, poverty is a strong determinant which might aggravate the vulnerability of these children.The accurate assessment of nutritional status in children with CP is difficult.A reliable measurement of basic data such as weight, height, and body mass index (BMI) and their correct interpretation and analysis is required to identify children with nutritional risk and proper management.The present study was conducted to find out the association between malnutrition and gross motor function in children with CP using the gross motor function classification system (GMFCS).

Study design and study period
This is a tertiary care hospital-based cross-sectional study.The study was completed over a period of one year (August 2020 to July 2021).

Study center
This study was conducted at the Department of Pediatrics and Neonatology, Nehru Hospital, Baba Raghav Das (BRD) Medical College, Gorakhpur (UP).The study was approved by the College Research Council (CRC) of BRD Medical College, Gorakhpur, Uttar Pradesh, India.

Inclusion criteria and exclusion criteria
Children of age 1-15 years attending the pediatric outpatient department (OPD) and inpatient care with a diagnosis of CP contributed as the study participants.A written informed consent from the parents of the study participants was obtained beforehand.
Patients having a history of congenital malformations that would independently affect food intake, e.g., cleft lip, cleft palate, diagnosis associated with genetic syndromes, and spina bifida were excluded.

Sample size
The sample size was determined using the following formula: n = 4 pq/L2, where n is the required sample size, p is the estimated prevalence of CP at 3.8% (prevalence in India in 2017), q is 100-p, and L is the margin error at 5% (standard value of 0.05).The total calculated sample size was 110.

Nutritional Assessment
Weight was measured on a digital scale in kilograms, with minimum cloths, or by calculating the difference between caretaker's weight with and without the child.Height was measured in centimeters using a stadiometer, with the child in the standing or supine position, in those, who had no major skeletal deformities.In children with deformities, height was measured using the knee height equation, where height = (2.69x knee height) + 24.2.Nutritional status and growth parameters were evaluated according to the WHO sex-specific weight-for-age, height-for-age, and weight-for-height growth charts."Normal" will be considered when values had a z-score between -1.99 and 1.99.Moderate undernutrition was established when z-scores were between -2 and -2.99.Severe undernutrition was considered when z-scores were below -3.Based on the GMFCS, motor function was classified into five levels: level I, walks without limitations; level II, walks with limitations; level III, walks using a handheld mobility device; level IV, self-mobility with limitations, may use powered mobility; and level V, transported in a manual wheelchair) [16].

Statistical analysis
Categorical variables were presented as proportions and percentage.Age was presented as the median and interquartile range (IQR), and all the other continuous variables were presented as means and standard deviations.Normal distribution of all continuous variables was checked by skewness/kurtosis.Associations of malnutrition across levels of gross motor function were tested using Chi-square or Fisher's exact test whichever was applicable.Statistical significance was set at p < 0.05 as significant.Data was analyzed using IBM SPSS Statistics for Windows, Version 21 (Released 2012; IBM Corp., Armonk, New York, United States).

Characteristics of participants
Weight for height of participants    The association between the anthropometric indices of the participants and GMFCS was highly significant (Table 6).

Discussion
This study was done to examine the association between malnutrition and gross motor function in children with CP based on the anthropometric assessment done according to growth charts by the WHO and motor assessment done according to the GMFCS.In our study, the majority of the patients were males (59%) with a male-to-female ratio of 1.4:1.Similarly, male predominance was also found in a study conducted by Bax et al. (1.6:1) [2].Based on gestational age, 68 (61.8%) were term and 42 (38.2%)were preterm.We distributed children among three groups according to age 1-5 years, 5-10 years, 10-15 years 55.4%, 34.6%, and 10% in each group, respectively.Most of the children belonged to the age group of 1 to 5 years.The mean age was found to be 3.7 ± 1.4 years.In a study conducted by Singhi et al., the mean age was 3.1 ± 2.6 years (range 2 months to 16 years) [5].
In our study, the most common presenting symptom among children with CP was seizures among 79 (72.3%) of the participants, while the second most common was delayed milestones among 73 (66.8%), followed by difficulty in breathing in 63 (57.5%); other common presenting symptoms were cough, fever, speech impairment, hearing impairment, and abnormal body movements.Pavone et al. also found epilepsy as one of the most frequent comorbidities of CP [17].
Anthropometry assessment is one of the important and well-established methods to screen malnutrition CP children.Assessing the nutritional status of CP children is highly essential.In our study, we found that more than half of children with CP were malnourished.Out of 110 children with CP, 54.5% were severely wasted, 50.0%were severely underweight, and 47.2% were severely stunted.A recent study by Kakooza et al. in 2015, however, reported that 52% of children with CP, who visited clinics, were malnourished [18].In another study by Aydin, the prevalence of malnutrition was 57.2% based on the physicians' clinical judgment [19].
Of the total 110 children with CP, 17.2% were GMFCS level I, 6.3% were GMFCS level II, 12.7% were GMFCS level III, 35.4% were GMFCS level IV, and 28.1% were GMFCS level V.More than half of the children with CP were classified in functional levels IV and V.A cross-sectional study from Colombia, Herrera-Anaya et al. examined 177 children with a diagnosis of CP (median, 6.5 years; IQR, 4.4-9.0years; 59.3% males) [20].There were 70 (39.5%),12 (6.8%), 10 (5.6%), 29 (16.4%), and 56 (31.6%) patients classified in levels I to V of the GMFCS, respectively, and a significantly higher prevalence of malnutrition among patients with lower motor function was found (p < 0.001) [20].The proportion of children in levels IV and V in our study was higher as compared to some international studies [21,22].We also observed that the z-scores of the anthropometric parameters, such as weight for age, height for age, and weight for height, progressively decreased as the levels of the GMFCS increased.
The observed associations may be attributed to the coexistence of gross motor and gastrointestinal dysfunctions in patients with CP.These gastrointestinal dysfunctions may include sucking difficulties, food refusal, sialorrhea, gastroesophageal reflux disease, oro-motor dysfunction, dysphagia, and constipation [23][24][25].Children with malnutrition undergo a slowing down of organ systems owing to physiological and metabolic changes.[26] The presence of increased muscle tone, muscle spasms, and involuntary movements, which increase energy expenditure, might be the additional factors explaining this relationship.

Limitations
Although there were some limitations in our study, the results obtained using the anthropometric data demonstrate that the WHO gold standard may not be suitable for the anthropometric evaluation of children with CP.Using the same growth charts for children with neurological impairment tends to overestimate malnutrition and growth and development in children with CP.Furthermore, nutritional status was measured using the anthropometric measurements rather than the more precise ways, such as dual-energy X-ray absorptiometry.The small sample size is another limitation.

Conclusions
The findings of this study revealed a high burden of malnutrition while also emphasizing the likelihood that malnutrition is overestimated in children with CP when the regular anthropometric assessment was done using the growth charts for the general pediatric population.Spastic type of CP was most frequent, and more than half of the patients experienced feeding difficulty.Most CP patients were facing gross motor disturbances.A statistically significant association was found between gross motor functioning and the prevalence of malnutrition and stunting.These findings emphasize the critical importance of early detection and intervention for malnutrition among children with CP, necessitating a multidisciplinary approach involving pediatricians, nutritionists, and therapists.Future research should focus on developing and validating specific nutritional screening tools tailored to the unique needs of children with CP and conducting longitudinal studies to understand the relationship between gross motor function and nutritional status.

2024
Bharti et al.Cureus 16(3): e55753.DOI 10.7759/cureus.55753 (17.27%) of them required PICU care and 13 (11.81%) of them required respiratory support.Most of the children belonged to the age group of 1 to 5 years with a mean age of 3.7 ± 1.4 years.Other characteristics of study participants are compiled in Table1.
n: number

TABLE 2 : Presenting symptoms of participants with cerebral palsy (n = 110)
n: number

TABLE 4 : Distribution of participants with cerebral palsy according to weight for age
n: number; SD: standard deviation Of the total 110 children, 26 (23.63%) were normal, 32 (29.09%) were moderately stunted, and 32 (47.27%) were severely stunted based on height for age (Table5).

TABLE 5 : Distribution of participants with cerebral palsy according to height for age
n: number; SD: standard deviation

TABLE 6 : Association between the nutritional status (WHO) and gross motor function
GMFCS: gross motor function classification system; n: number; p-value, statistical significance; WHO, World Health Organization