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 Table of Contents  
Year : 2021  |  Volume : 16  |  Issue : 2  |  Page : 91-99

Possible risk factors that may play a role in augmenting the liability and intensity of coronavirus disease 2019 infection in obese and nonobese Egyptian children

1 Department of Biological Anthropology, Medical Research Division, Giza, Egypt
2 Department of Pediatrics, Faculty of Post Graduate Childhood Studies, Ain-Shams University, Cairo, Egypt
3 Department of Nutrition and Food Science, National Research Centre, Giza, Egypt
4 Department of Clinical Pathology, Medical Research Division, Giza, Egypt

Date of Submission04-May-2021
Date of Decision12-Jul-2021
Date of Acceptance27-Jul-2021
Date of Web Publication31-Dec-2021

Correspondence Address:
Sahar Abd El-Raufe El-Masry
Department of Biological Anthropology, National Research Centre, 33 El-Bohooth Street, Dokki, Giza, Cairo 12622
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jasmr.jasmr_13_21

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Background/aim Obesity, insulin resistance (IR), dyslipidemia, and decreased consumption of essential micronutrients are factors that can compromise the immune response to coronavirus disease 2019 (COVID-19) infection, leading to increased morbidity and mortality among children. The aim of this study was a detection of possible risk factors that may play a role in augmenting the liability and intensity of COVID-19 infection in Egyptian obese and normal-weight children.
Patients and methods This study was a retrospective observational cross-sectional review including 120 obese children (group 1), in addition to 61 age-matched and sex-matched controls (group 2) from children attending ‘the Management of Visceral Obesity and Growth Disturbances Unit’ at the Medical Research Excellence Center (MERC), National Research Centre, Egypt. All children were exposed to medical assessment, anthropometric evaluation, and a three 24-h dietary recall for assessment of micronutrient intake. Laboratory assessment of fasting serum blood glucose, insulin, triglycerides, total cholesterol, high-density lipoprotein, and low-density lipoprotein was done and IR was calculated.
Results Obese children showed higher significant values than the control group regarding all anthropometric measurements with increased blood pressure, waist circumference, and waist-to-hip ratio. Laboratory assessment revealed elevated fasting levels of glucose and Homeostatic Model Assessment for Insulin Resistance denoting IR together with the presence of triglycerides and high-density lipoprotein levels within the high-risk range showing tendency toward dyslipidemia. The intake of vitamins A, D, folic acid, and calcium was lower than the recommended dietary allowances in both groups.
Conclusion Obesity and its consequent complications, including dyslipidemia and IR together with decreased consumption of vitamins A, D, folic acid, and calcium, were the most prominent risk factors found among the studied sample of Egyptian children that can affect their immune response and predispose to increased severity of COVID-19 infection.

Keywords: children, coronavirus disease 2019, obesity, risk factors

How to cite this article:
Hassan NE, El-Masry SA, El Hussieny MS, ElKhayat SH, Ahmed NH, Aboud HT, Mostafa MI, Kamal AN. Possible risk factors that may play a role in augmenting the liability and intensity of coronavirus disease 2019 infection in obese and nonobese Egyptian children. J Arab Soc Med Res 2021;16:91-9

How to cite this URL:
Hassan NE, El-Masry SA, El Hussieny MS, ElKhayat SH, Ahmed NH, Aboud HT, Mostafa MI, Kamal AN. Possible risk factors that may play a role in augmenting the liability and intensity of coronavirus disease 2019 infection in obese and nonobese Egyptian children. J Arab Soc Med Res [serial online] 2021 [cited 2022 Jun 26];16:91-9. Available from: http://www.new.asmr.eg.net/text.asp?2021/16/2/91/334640

  Introduction Top

Since December 2019, the world has been suffering from a severe pandemic generated by a sentimental type of coronavirus infection. It was transmitted expeditiously throughout countries causing severe pneumonia .The disease was termed coronavirus disease 2019 (COVID-19) [1]. It was found to affect almost all age groups but less frequently the pediatric group with less severity and mortality when compared with adults [2].

Obesity was found to be a crucial risk factor determining the necessity of respiratory support among children infected with COVID-19 [3]. The World Obesity Federation predicted obesity to reach 158 million all over the world in the age group from 5- to 19-year olds [4]. In Egypt, a cross-sectional study, including 1000 primary school students (6–12 years) in 2019, found that the overall prevalence of obesity and overweight was 13.9 and 16.2%, respectively [5].

In a study done by Hassan et al. [6] among obese Egyptian school children aged 7–11 years found several cardiometabolic risk factors indicated by elevated total cholesterol and low-density lipoprotein (LDL) together with increased fasting glucose level and waist circumferences among obese children in comparison with the control group.

In childhood and adolescence, the relatively high pancreatic reserve of insulin allows hyperinsulinism to occur as a result of obesity-associated hyperglycemia [7]. Although hyperinsulinism keeps blood glucose within normal levels, it can also cause several health consequences, such as dyslipidemia, nonalcoholic fatty hepatitis, arterial hypertension, micronutrient shortage, enhanced oxidative stress, and increased uric acid level [8].

In circumstances of extreme metabolic activity, such as during immune reaction to coronavirus infection, beta cells secrete increased amount of insulin, which may not be accomplished when they are already working at their ceiling as in obesity. SARS-CoV-2 can also cause beta cells to rupture by the interaction with angiotensin-converting enzyme-2 (ACE2), which further aggravates this process [8]. Insulin resistance (IR) can also cause impairment of the vasoprotective and anti-inflammatory effects of nitric oxide as a result of reduction in phosphoinositide 3-kinase [9].

Dyslipidemias are highly prevalent among obese children and adolescents. Decreased level of high-density lipoprotein (HDL) cholesterol and increased LDL cholesterol are certified risk factors for advancement of endothelial dysfunction and atherosclerosis that may provoke COVID-19 vascular complications [7].

A sufficient intake of iron, zinc, and vitamins A, D, C, B6, and B12 is essential for maintaining the immune function. The presence of nutritional deficiencies of these micronutrients among obese children would lead to depressed immune function and increased susceptibility to COVID-19 infection [10].

The present study aims to detect the possible risk factors that may play a role in augmenting the liability and intensity of COVID-19 infection in obese and nonobese Egyptian children.

  Patients and methods Top

Patients and study design

This study is a retrospective observational cross-sectional study that comprised 120 prepubertal obese (exogenous obesity) children aged 6–less than 12 years old of both sexes (54 males and 66 females) with BMI more than or equal to 95th percentile (Egyptian growth curves 2002) (group 1), in addition to 61 age-matched and sex-matched controls (31 males and 30 females) with BMI=15–less than 85 percentile (group 2). Children with other causes of obesity, congenital anomalies, chronic diseases, or taking medications that can affect their normal growth were excluded. The study was carried out in the Management of Visceral Obesity and Growth Disturbances Unit at ‘Medical Excellence Research Center,’ which is a part of the ‘National Research Centre’ during the period from January to November 2019.

Ethical approval

All experiments were approved by the Ethical Committee of the National Research Centre with approval number 16/448, in accordance with the Declaration of Helsinki. A written informed consent was taken from one of the parents of the participated children.


Anthropometric measurements

All children were subjected to clinical examination and anthropometric assessment, including body weight, height, and waist and hip circumferences following the recommendation of International Biological Program [11]. Then, BMI [(weight (kg)/height2 (m)], waist-to-hip ratio and waist-to-height ratio were calculated. Dietary history was taken, including 24 h of average food recall of the last 3 days. Portions consumed were estimated according to Ferguson et al. [12]. The total dietary intake was analyzed using the Nutrisurvey computer program to convert the food taken into micronutrients [13], and compared with the recommended dietary intake of micronutrients in children of same age [14].

Nutritional characteristic methods

Children were asked to recall their dietary intakes of the previous 24 h for 3 days and average intake was recorded, any snacks taken between meals were also recorded, and portion sizes consumed were estimated according to Ferguson et al. [12].

The total dietary intake was analyzed using the Nutrisurvey for Windows computer program to convert the food taken into micronutrients [13]. The average daily intake was then compared with the recommended dietary allowances (RDA) of micronutrients in children of same age [14].

Sampling and biochemical analysis

A 5-ml sample of venous blood was obtained from each child after 12 h of fasting for laboratory assessment. The blood samples were centrifuged and the serum was separated and kept at −8°C for batch assessment.

Fasting blood glucose was assessed immediately after taking blood samples by enzymatic colorimetric method, using kits of Chemelex S.A. (Barcelona, Spain) according to the method of Tietz [15]. Values less than 100 mg/dl were categorized as normal fasting glucose; values between 100 and 125 mg/dl are categorized as impaired fasting glucose. Values above 126 mg/dl are categorized as prediabetes or provisional diabetes if persistent on repeated testing, according to ISPAD Clinical Practice Consensus Guidelines 2018 [16]. Serum insulin was assessed using enzyme immunoassay test of Immunospec Corporation (9428 Eton Ave, Unit O, Chatsworth, California, USA) according to the method of Burtis et al. [17]. Fasting insulin values less than 25 mIU/l are classified as desirable and values equal to or more than 25 mIU/l are classified as high risk [18].

IR was calculated according to Matthews et al. [19], using the following equation:

IR=fasting glucose (mg/dl)×fasting insulin (µIU/ml)/405. The cut-off point in children was defined as more than or equal to 3.16. Results up to l5 were considered as moderate IR. Results higher than 5 were considered as severe IR [20].

In addition, lipid profile (total cholesterol, triglycerides, HDL cholesterol, and LDL cholesterol) was assayed by standard enzymatic procedures according to Tietz [15]. However, serum triglycerides were assessed using the kit of Chemelex S.A.. Serum triglyceride values less than 75 mg/dl are classified as desirable, values between 75 and 99 mg/dl as borderline risk, and values equal to or more than 100 mg/dl as high risk for 6–9-year-old children. Values less than 90 mg/dl are classified as desirable, values between 90 and 129 mg/dl as borderline risk, and values equal to or more than 130 mg/dl as high risk for 10–less than 12-year-old children [21].

Serum total cholesterol was assessed using the kit of Chrono Lab Systems (Barcelona, Spain). Total cholesterol values less than 170 mg/dl are classified as desirable, values between 170 and 199 mg/dl as borderline risk, and values starting from 200 mg/dl as high risk [21].

HDL was assessed using the kit of Chemelex S.A.. HDL values less than 40 mg/dl are classified as major heart-disease risk factor, values between 40 and 45 mg/dl as borderline risk, while values more than 45 mg/dl were considered as low risk against heart disease [21]. LDL was assessed using the kit of Quimica Clinica Aplicada S.A. (Spain). According to polvinylsulfate method of Demacker et al. [22], LDL values less than 110 mg/dl are classified as desirable, values between 110 and 129 mg/dl are classified as borderline risk, and values from 130 mg/dl and above as high risk [21].

Statistical analysis

Data were analyzed using the Statistical Package for Social Sciences (SPSS/Windows, Version 18; SPSS Inc., Chicago, Illinois, USA). The total dietary intake was analyzed using the Nutrisurvey computer program to convert the food taken into micronutrients. Normality of data was tested using the Kolmogorov–Smirnov test. The data were normally distributed. The parametric data were expressed as mean±SD, where the qualitative ones were expressed as number and percentage. Student’s t test was used to compare between two parametric groups, and χ2 test was used to compare between groups with qualitative data. Standards of probability were set to P value less than 0.01, which was considered highly significant and P value less than 0.05 was considered statistically significant.

  Results Top

Comparisons between obese and controls regarding blood pressure and the studied anthropometric parameters are shown in [Table 1]. The mean systolic and diastolic blood pressure were higher in the obese children than in children of the control group with a highly significant difference (P=0.000). All anthropometric parameters showed a highly significant difference, being higher in obese children than control ones.
Table 1 Clinical and anthropometric characteristics of the obese and control (nonobese) groups

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Laboratory comparison between obese and control is presented in [Table 2]. The mean fasting insulin levels showed a highly significant difference between the two groups being higher in obese children (P=0.000). The mean fasting insulin levels of both groups were within the desirable range. The mean fasting blood glucose of the obese group was 152.16±20.31 mg/dl, which was above the desirable range carrying the risk of diabetes (if persistent on two separate occasions). The mean fasting blood glucose of the control group was 85.24±7.61 mg/dl, which was within the desirable range with a highly significant difference (P=0.000) in comparison with obese group. Homeostatic Model Assessment for Insulin Resistance (HOMA-IR) was higher in obese children than in controls with a highly significant difference (P=0.000). The mean value of HOMA-IR in the obese group was 4.50±0.79, which was above the cut-off value for IR, while the mean value of HOMA-IR in the control group was 1.68±0.22, which was within the normal range.
Table 2 Laboratory characteristics of the obese and control (nonobese) groups

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Regarding the lipid profile of our obese and control children, the mean values of cholesterol, triglycerides, and LDL showed statistically significant higher levels in obese children compared with their controls. The mean values of cholesterol and LDL were within the desirable low-risk range in both groups. The mean values of HDL and triglycerides in obese children lied within the high-risk range.

[Table 3] shows comparison between obese and controls regarding daily micronutrient intake and it’s percent to RDA. The intake of vitamin B1, niacin, vitamin B6, B12, folic acid, vitamin C, vitamin D, sodium, magnesium, phosphorus, iron, and zinc is significantly higher in the obese children than control ones. Vitamin B1, B2, niacin, vitamin B6, B12, vitamin C, sodium, magnesium, zinc, and iron intake is higher than the RDA in both groups. Phosphorus intake is higher than the RDA in obese children and lower than the RDA in control ones. The intake of vitamin A, vitamin D, folic acid, and calcium is lower than the RDA in the two groups.
Table 3 Comparison between the obese and control (nonobese) groups regarding their nutritional characteristics

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Regarding the frequency distribution of risk factors for COVID-19 infection among our studied groups in [Table 4], 100% of obese-group hyperglycemia in the prediabetic or diabetic risk range, while only 6.7% of female controls showed the same risk factor. All members of our obese group showed IR and none of our studied groups, either obese or control, showed hyperinsulinemia. Obese males (81.5%) showed elevated serum levels of triglycerides in the high-risk range for age and 90.9% of obese females showed the same risk. Only 6.5% of control males and 20% of control females showed the risk of hypertriglyceridemia. HDL levels were in the high-risk range in 100% of male and female obese children, while 12.9% of male controls and 6.7% of female controls showed the same risk factor. LDL was not elevated to the high-risk range in either of the two groups.
Table 4 Frequency distribution (%) of the high risk among obese and control (nonobese) children by sex

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According to the frequency distribution of decreased intake of vitamins and minerals, vitamin D and calcium intake was deficient among most children of both groups. The deficiency of vitamins B1, B2, B16, B12, folic acid, vitamin C, and minerals, including magnesium, phosphorus, iron, and zinc, was of greater incidence among members of the control group. Vitamin-A intake was lower than the RDA in both groups with no significant difference in deficiency between them ([Table 5]).
Table 5 Frequency distribution (%) of the low intake of recommended dietary allowances (high risk) among obese and control (nonobese) children by sex

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  Discussion Top

The identification of biomarkers for early detection of COVID‐19 severity and progression has still been a global concern. Early classification and treatment of COVID‐19 patients who may advance into the severe crucial stage can result in better prognosis [23].

The WHO described both the COVID‑19 outburst and obesity ‘epidemic’ as global public health emergencies. Although less frequently, COVID-19 affects the pediatric age group, but recent clinical studies observed that COVID-19 can cause more severe symptoms and complications in obese adults [24] and obese children [3] and that obese patients are at higher risk of hospital admittance, irrespective of their viral status [25].

A direct metabolic link was found between the state of inflammation associated with metabolic syndrome and the cytokine storm that causes decline of the respiratory functions in COVID‑19 patients. This metabolic disorder is intensified by preexisting diabetes or hypertension that is usually accompanied by obesity [26]. Obese children tend to have higher blood pressure than normal-weight children of the same age, which increases the potentials for endothelial damage, one of the bases of COVID-19 pathogenesis [27].

Our study involved 120 obese children in addition to 61 age-matched and sex-matched controls aiming for detection of risk factors that can increase liability and severity of COVID-19 infection in obese and normal-weight Egyptian children. Children of the obese group showed increased IR and increased fasting blood glucose in all patients of this group. IR arises from a defect in insulin action on its target tissues, either due to a defect in insulin receptor or more commonly due to disorders in the postreceptor insulin-signaling cascade [28]. This impaired insulin action is associated with increased circulating insulin concentrations [29].

ACE2, which serves as the ligand through which coronaviruses bind to their target cells [30], is an important link between COVID-19 severity and IR. A recent study has confirmed that several diabetes-related traits are associated with increased lung ACE2 expression [31]; another study found that IR and elevated insulin levels result in increased ACE2 expression in lung tissues, leading to aggravating the intensity of the disease [32].

Also, serum levels of cholesterol, triglycerides, and LDL were significantly higher in the obese children than the control ones; however, the means for cholesterol and LDL were in the desirable low-risk range. Serum levels of HDL and triglycerides were in the high-risk range in obese children and were prevalent among most members of the group. Dyslipidemia has a high prevalence among obese children [7] and low levels of HDL cholesterol and increased LDL cholesterol are confirmed risk factors for development of endothelial malfunction and atherosclerosis [33].

In viral infections, high levels of LDL cholesterol interoperate with macrophages in atherosclerotic plaques and increase the secretion of pro-inflammatory cytokines [34]. Additionally, low HDL cholesterol causes disturbance in the intrinsic immune response, which is the first line of defense against COVID-19 infection [35]. Finally, elevated LDL cholesterol or triglycerides can cause endothelial dysfunction, which in turn predisposes to cardiovascular complications with more severe outcomes [36]. A recent review was conducted based on meta-analysis of the relationship between dyslipidemia and COVID-19 infection severity, where patients with dyslipidemia were found to be at risk for severe COVID-19 infections [37].

A suitable nutritional status has been considered as an essential component for immune response against coronavirus infection. A study conducted by Zhang and Lui [38] showed that some nutrients are cardinal for better response to coronavirus, such as vitamins A, C, D, and E, omega-3 fatty acids, and the minerals zinc and iron. In obesity, despite eating above energy needs, the quality of dietary intake may not be adequate, so vitamin or mineral deficiencies may be present in those with excess weight ‘hidden hunger’ [39].

In the current study, vitamin-D intake was lower than the recommended RDA among most children of both obese and control groups. Vitamin D has immune-modulatory effects and also enhances the expression of antimicrobial peptides in neutrophils and monocytes [40]. Furthermore, hypovitaminosis D is found to be interrelated with disorders that have possible influence on COVID-19, such as arterial hypertension, fatty liver, and increased uric acid level [41].

Another finding in our study was the decreased intake of calcium below the RDA in both obese and normal-weight children. SARS‐CoV‐2 E gene encodes a small transmembrane protein with ion-channel activity that is highly synthesized during infection. These channels are penetrable to Ca2+, so the disturbance of calcium homeostasis may stimulate the activation of inflammatory pathways, leading to edema and damage of the lung cell [42]. In contrast to moderately infected cases, severe COVID‐19 patients were found to be more likely to have hypocalcemia even after adjustment by age and comorbidities [43]. An Italian study of 531 patients establishes that hypocalcemia could anticipate the severity and need for hospitalization of COVID‐19 patients [44].Vitamin-A intake was deficient in both our obese and control children with no significant difference in prevalence between the two groups. Vitamin A helps the renewal of the mucosal barriers damaged by infection and helps the protective role of macrophages, neutrophils, and natural killer cells. Vitamin-A deficiency reduces T-helper 2 response, which culminates in a lack of interleukin-4 and fails to induce immunoglobulin A, hindering the response to influenza virus infection [45].

Zinc deficiency was proved to be present among obese children. Zinc takes part in insulin and leptin metabolism, leading to metabolic deregulation in obese children, causing inadequate inflammatory response [46]. However, the mean intake of zinc was above the RDA in both of the current groups, but the prevalence of its deficiency occurred more among the control group. Zinc deficiency has been also related to decreased production of cytokines and interferon, atrophy of the thymus gland and other lymphoid organs, and changes in the ratio of lymphocytes [47].

Folic acid intake was below the RDA in both groups of the current study, but the prevalence of its deficiency was more among controls than the obese children. Studies have shown that folic acid can reduce the replication of COVID-19 virus either by inactivation of furin endoprotease that is essential for the SARS-CoV-2 virus entry to the host cell [48], or by inactivation of protease 3CLpro, which is vital in the replication of all coronaviruses [49]. Clinical evidence suggests that folic acid supplementation can protect against SARS-CoV-2 infection and pregnant women receiving folic acid supplementation seem to have a lower probability forgetting this infection and even those who are infected have a higher chance of being asymptomatic [50].

Finally, the presence of metabolic comorbidities and dyslipidemia among our obese children, together with the presence of nutrient deficiencies among obese and normal-weight children, represents serious risk factors contributing to the severity of COVID-19 infection.

  Conclusion Top

Current piece of research among this sample of Egyptian children gave an idea about ‘What Do We Need to Know about the Risk Factors for COVID-19 Infection among children.’ It was observable that obesity and its metabolic consequences, such as dyslipidemia and IR, accompanied with decreased consumption of vitamins A, D, folic acid, and calcium, were the most noticeable risk factors found among the Egyptian children that can impair their immune response and accelerate serious consequences of COVID-19 infection.


The authors acknowledge the institute ‘National Research Centre; Egypt’; without its fund, this study could not be done. The authors are also grateful to everybody who participated in this study: the children who were the participants of this study, the technicians who helped in the laboratory analysis, and the doctors who participated in collection of the data. Without their help, this study could not have been completed.

Author contribution: Nayera E. Hassan designed the study as well as revised every step and gave conceptual advice; Sahar Abd El-Raufe El-Masry performed the statistical analysis shared in tabulation of the data and publication process; Nihad H. Ahmed was responsible about analysis of the nutritional data; Mohammed I. Mostafa dis laboratory analysis; Mohamed S. El Hussieny, Samer H. ElKhayat, Heba Tala, and Ayat N. Kamal collected the nutritional data from participants and took anthropology measurements; Ayat N. Kamal wrote the draft of the paper. All authors read and approved the final paper.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]


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