Etiological Patterns of Protein-Energy Malnutrition in a Pediatric Clinic in China

Introduction

Malnutrition refers to deficiencies, excesses, or imbalances in a person’s intake of energy and/or nutrients [1]. The 2023 levels and trends in child malnutrition published by the United Nations International Children’s Emergency Fund (UNICEF) and the World Health Organization [2] show that the triple burden of malnutrition – stunting, wasting, and overweight – continues to threaten children’s health. Stunting affects 22.0% of children under the age of 5 worldwide, and nearly 52.0% of the affected children live in Asia. About 6.8% of the children under 5 years of age have wasting. There are now 37 million children under 5 years of age living with overweight globally. Malnutrition is a crucial determinant of morbidity and mortality in infants and young children, with about half of deaths among children under the age of 5 years being related to malnutrition [2]. Protein-energy malnutrition (PEM) is a common form that primarily affects children under the age of 5. The clinical manifestations of PEM include a lack of weight gain, or weight loss, progressive wasting or generalized edema, and reduced or absent subcutaneous fat, which are often accompanied by varying degrees of organ dysfunction and metabolic abnormalities. In this study, we focused mainly on children with undernutrition, which includes wasting (low weight-for-height), stunting (low height-for-age), and underweight (low weight-for-age).

In China, a 2013 analysis of the nutritional status of children aged 0–5 years revealed a PEM incidence of 12.6%, particularly in impoverished rural areas [3]. The Chinese government has launched a series of national nutrition intervention measures to improve malnutrition among children [4]. China updated the 2022 Dietary Reference Intakes (DRIs) and launched the 2023 Dietary Guidelines. Since 2015, the Chinese Nutrition Society has been organizing National Nutrition Week, which takes place in the third week of May each year. This week features various national nutrition education and action activities, with different themes each year. Additionally, China has implemented the Healthy China Initiative (2019–2030) and the National Nutrition Plan (2017–2030). Despite significant improvements in child nutrition due to socioeconomic development, higher living standards, and increased health awareness, clinical PEM cases are still observed.

It is crucial to distinguish between primary and secondary PEM. Primary PEM typically results from inadequate nutrition, often due to insufficient caloric and protein intake, which can stem from factors such as poor feeding practices and/or poor dietary habits in children, such as picky eating [5]. These factors were found to be more likely to result in mild and early-stage PEM in our study. The symptoms and signs of mild and early-stage PEM are atypical and can be easily overlooked clinically. Diagnosis requires a detailed medical history, thorough physical examination, and laboratory tests. Child health clinics primarily provide growth and development monitoring and counseling services, enabling comprehensive medical history information collection and regular follow-up [6]. This helps in early detection of abnormal growth and development or underlying diseases, allowing timely intervention. Regular monitoring helps prevent delays in treatment or serious consequences resulting from prolonged inadequate nutrition, which can necessitate hospitalization [7].

In contrast, secondary PEM arises from underlying medical conditions that impair nutrient intake, absorption, or utilization. Severe PEM is now rare in China and is often secondary to certain chronic diseases or other contributing factors, such as intrauterine growth retardation leading to low birth weight, premature birth, and congenital conditions such as congenital esophageal stenosis and congenital heart disease. Understanding how these chronic conditions contribute to or exacerbate PEM is essential for effective treatment.

Congenital esophageal stenosis leads to narrowing of the esophagus, making it difficult for individuals to swallow, which can result in inadequate nutrient intake. Similarly, congenital heart disease can increase the metabolic demands on the body, requiring more energy and protein to support normal growth and development [8]. These conditions can create a cycle where the individual’s nutritional needs are heightened while their ability to meet those needs is compromised, leading to a worsening of malnutrition. Intrauterine growth retardation and low birth weight can also predispose infants to PEM. Babies born at low birth weights often have lower fat and muscle stores, increasing their vulnerability to malnutrition, especially if they face feeding difficulties or have increased energy needs due to health complications. Premature birth can further complicate this situation, as preterm infants may have underdeveloped organs and require specialized nutritional support to thrive.

Understanding this distinction is vital for tailoring treatment approaches. Primary PEM can be addressed primarily through dietary interventions, including increased caloric and protein intake, supplementation, and education about nutrition. Secondary PEM requires strategies that not only focus on nutritional support but also address underlying health issues. By recognizing the complexities associated with both types of PEM, healthcare providers can develop more effective strategies to combat malnutrition and improve patient outcomes.

The causes of PEM in children attending child health clinics show unique characteristics [9]. This study examines the specific etiological factors contributing to PEM in children attending pediatric health clinics. By analyzing these cases, we aim to provide insights that can improve PEM diagnosis and treatment, with an emphasis on early intervention and prevention. Understanding the unique characteristics of PEM in this setting may inform more effective strategies for managing malnutrition among vulnerable child populations.

Material and Methods

ETHICS APPROVAL:

This study was conducted in accordance with the Declaration of Helsinki. Ethical approval of this study was obtained from the Medical Ethics Committee of West China Second University Hospital, Sichuan University [2023 Medical Scientific Research for Ethical Approval No. (372)]. Because this was a retrospective study, written informed consent was waived upon the approval of the Medical Ethics Committee of West China Second University Hospital, Sichuan University.

DATA SOURCE AND SAMPLE:

According to the sample size calculation formula

Za2 represents the two-sided Z value at the specified significance level α, δ is the allowable error, and π is the overall rate (the estimated proportion of a single etiology). We set α=0.05, δ=6%, and π=50%. The required sample size was 267 cases. Assuming a dropout rate of 15%, the required sample size increased to 286 cases. We used the random number table method for simple random sampling. Ultimately, the study included 286 children with PEM who visited the West China Second University Hospital Child Healthcare for Xinchuan West China Center for Child Development and Excellence from January to December 2022.

Among these patients, 231 (80.8%) had mild PEM, 49 (17.1%) had moderate PEM, and 6 (2.1%) had severe PEM. There were 143 male (50.0%) and 143 female (50.0%) patients. Severe PEM patients (only 6 patients) were not grouped separately in this study because of the small sample size. Instead, patients were categorized into mild PEM (n=231) and moderate PEM (n=49) groups only.

RELEVANT DIAGNOSTIC CRITERIA:

PEM Diagnostic Criteria: According to the diagnostic criteria for PEM established by the World Health Organization, PEM in children is clinically diagnosed using one of the following 3 criteria. The severity of PEM is assessed based on the most severe of these 3 criteria [1]. 1) Underweight: Children are categorized as mildly, moderately, or severely underweight if their weight falls below the average for normal children of the same age and sex by 1 SD to 2 SD, 2 SD to 3 SD, or more than 3 SD, respectively. 2) Stunted growth: Children are categorized as having mild, moderate, or severe stunted growth if their height is lower than the average for normal children of the same age and sex by 1 SD to 2 SD, 2 SD to 3 SD, or more than 3 SD, respectively. 3) Wasting: Children are considered to have mild, moderate, or severe wasting if their weight is lower than the average for normal children of the same height by 1 SD to 2 SD, 2 SD to 3 SD, or more than 3 SD, respectively. Small for gestational age (SGA) diagnostic criteria: A newborn is diagnosed as SGA if birth weight is below the 10th percentile for babies of the same gestational age [12].

Premature infant diagnostic criteria: An infant is diagnosed as premature if born before 37 weeks of gestation [13].

Diagnosis of dietary behavior problems in children: Dietary behavior problems are diagnosed using the Identification and Management of Feeding Difficulties (IMFeD) [14]. Dietary behavior problems refer to abnormalities in feeding behavior, eating behavior, food selection, and the eating environment.

Diagnosis of Recurrent Respiratory Tract Infection (RRTI): A child with 7 upper respiratory tract infections per year between the ages of 0 and 2 years, 6 upper respiratory tract infections per year between the ages of 2 and 5 years, or 2 to 3 lower respiratory tract infections per year between the ages of 0 and 2 years, and 2 lower respiratory tract infections per year between the ages of 2 and 5 years is diagnosed with RRTI [15].

Clinical Diagnosis of Food Allergy (FA): Food allergy (FA) is clinically diagnosed primarily based on detailed medical history, family history, and physical examination results, especially the relationship between the quantity of potentially allergenic foods consumed and the timing and clinical presentation of allergic reactions. Additional tests include serum-specific IgE testing, allergen skin prick tests, total eosinophil count, patch tests, and endoscopy. A criterion standard involves a trial of diet avoidance followed by an oral food challenge. When this cannot be routinely used in clinical practice, allergens should be avoided for 2 to 4 weeks, and improvements in symptoms and signs should be observed. Significant improvement suggests the presence of FA [16,17].

INCLUSION AND EXCLUSION CRITERIA:

The inclusion criteria for PEM patients were as follows: 1) Children aged 0 to 5 years. 2) Newly diagnosed patients who met the PEM diagnostic criteria [4].

The exclusion criteria were as follows: 1) Patients with a follow-up diagnosis of PEM. 2) Children with short stature for special reasons but with normal weight gain, such as those with growth hormone deficiency or idiopathic short stature.

RESEARCH METHODOLOGY:

We conducted a retrospective analysis of the clinical case data of 286 patients with PEM. The data encompassed several aspects, such as sex, age of onset of PEM, clinical symptoms, feeding history, growth and development history, medical history, family history, comprehensive physical examinations, and results from tests. These tests included routine blood tests, thyroid function tests, electrolytes, IgE tests, allergens, skin prick tests, patch tests, and neurodevelopmental assessment tests, as well as results from genetic metabolic tests, since PEM might be one of the symptoms of some genetic metabolic diseases.

STATISTICAL ANALYSIS:

The data were processed using the SPSS 19.0 statistical software package. For skewed quantitative data, such as the age of children in the 2 groups, the median and interquartile range M (Q₁ and Q₃) were used for representation. The Mann-Whitney U test was used to compare 2 groups. The count data, such as the sex composition ratio of the 2 groups of children and the proportions of PEM causes, such as FA, are expressed as percentages (%). The 2 groups were compared using the chi-square test and continuity-corrected chi-square test. All the statistical tests were two-sided, and a P value less than 0.05 was considered statistically significant.

Results

COMPARISON OF GENERAL CLINICAL DATA BETWEEN THE 2 GROUPS OF CHILDREN:

There were no statistically significant differences in sex distribution or age between the mild and moderate PEM groups (P>0.05), indicating that the groups were comparable in terms of these baseline characteristics.

DISTRIBUTION OF PEM CAUSES IN PEM PATIENTS:

The common causes of PEM among the 286 children included FA (163 cases, 57.0%), SGA children (76 cases, 26.6%), dietary behavior problems (41 cases, 14.3%), premature infants (23 cases, 8.0%), and RRTI (13 cases, 4.5%) (Table 1).

COMPARISON OF PEM CAUSES BETWEEN MILD AND MODERATE PEM GROUPS:

The proportions of children with SGA and patients with RRTI in the moderate PEM group were significantly greater than those in the mild PEM group, and the differences were statistically significant (P<0.05). A comparison of the proportion of FA, premature infants, and dietary behavior problems between the 2 groups of PEM patients revealed no statistically significant differences (P > 0.05) (Table 2).

COMPARISON OF SINGLE AND MULTIPLE ETIOLOGICAL FACTORS BETWEEN MILD PEM GROUP AND MODERATE PEM GROUP:

The proportion of children with 2 or more etiological factors was 48.9% (24/49) in the moderate PEM group, which was significantly greater than the 19.0% (44/231) reported in the mild PEM group (P<0.001). The proportion of children in the mild PEM group with a single etiological factor was 73.6% (170/231), which was significantly greater than the 38.8% (19/49) reported in the moderate PEM group, and this difference was also statistically significant (P<0.001) (Table 3). All 6 patients with severe PEM had 2 or more etiological factors.

Discussion

LIMITATIONS:

This was a single-center study, hence further studies are needed in various regions of China to determine whether local factors in each area play a role.

Conclusions

This analysis of single and multiple etiological factors revealed that the proportion of children with 2 or more etiological factors in the moderate PEM group was significantly greater than in the mild PEM group (P<0.05). The proportion of children with a single etiological factor was significantly greater in the mild group than in the moderate group (P<0.05). Six patients with severe PEM were not included in the comparison because of multiple etiologies. Thus, multiple etiological factors interact and affect each other, exacerbating the severity of PEM. Pediatric health clinicians should focus on timely detection of deviations in the growth and development of disease in infants and children. Routine growth monitoring, dietary counseling for parents, and targeted screening for key risk factors such as food allergies and small for gestational age, should be included. We also encourage clinicians to make these practices a standard part of pediatric care, integrating comprehensive assessment and proactive management strategies into routine visits. This approach not only supports early identification of at-risk children but also helps prevent the progression of PEM, reducing its incidence and severity in pediatric populations.