Journal of The Arab Society for Medical Research

ORIGINAL ARTICLE
Year
: 2018  |  Volume : 13  |  Issue : 2  |  Page : 79--88

‘Infectobesity’ in egyptian adolescent women and its relations to carotid intima–media thickness


Sahar A El-Masry1, Hanan A El Gamal2, Muhammad Al-Tohamy1, Ayman Nada2, Amany H Abdelrahman3, Mohamed Kh. Metkees1, Amany Ebrahim4, Walaa Saad1,  
1 Biological Anthropology Department, Medical Research Division, National Research Centre, Cairo University, Giza, Egypt
2 Medical Studies Department, Faculty of Postgraduate Childhood Studies, Cairo University, Giza, Egypt
3 Clinical Pathology Department, Medical Research Division, National Research Centre, Cairo University, Giza, Egypt
4 Diabetes and Endocrinology Unit, Pediatrics Department, Cairo University, Giza, Egypt

Correspondence Address:
Sahar A El-Masry
Biological Anthropology Department, National Research Centre, El-Bohooth Street, Dokki, Giza 12622, Cairo
Egypt

Abstract

Background ‘Infectobesity’ is a new term to describe obesity of infectious origin, such as infection by human adenovirus-36 (Adv36). It appears to be a new concept, evolved over the past 20 years. Visceral obesity is associated with a higher risk of cardiovascular disease. Increased carotid intima–media thickness (CIMT), a marker of early-onset atherosclerosis, has been observed in obese children and adolescents. The present study aims to investigate the relationship between visceral obesity, CIMT, and Adv36 in female Egyptian adolescents. Patients and methods The present study included 90 women aged 12–15 years. It was conducted at the Medical Excellence Research Center of the National Research Centre, Cairo, Egypt, during the period between September 2016 and November 2017. Anthropometric assessment was done. Fasting blood samples were withdrawn for the measurement of Qualitative Human Adv36 antibody using a sandwich enzyme-linked immunosorbent assay. Fasting plasma glucose was determined calorimetrically, by the glucose oxidase method and insulin level using the solid-phase enzyme-linked immunosorbent assay and lipid profile. Visceral obesity was measured by an abdominal ultrasound. CIMT for both carotid arteries were measured by high-resolution echo Doppler. Results Girls with visceral obesity (n=26) had higher frequency of increased CIMT at left (96.2 vs. 75%), right carotid artery (84.6 vs. 73.4%) and Adv36 sero-positive antibody (69.2 vs. 56.2%) than among those without visceral obesity (n=64). Among the total samples, visceral obesity had significant positive correlations with BMI, waist and hip circumference, while it had insignificant correlations with age, blood pressure (BP), CIMT at right and left carotid arteries, adenovirus and laboratory findings. CIMT had a significant positive correlation with each other, insulin resistance and total cholesterol, and significant negative correlations with high-density lipoprotein and waist circumference. Adv36 had significant negative correlations with BP (both systolic and diastolic) and significant positive correlation with insulin level. Adv36 and CIMT had insignificant correlations with each other and with the anthropometric measurements, BP, visceral obesity, triglycerides, and low density lipoprotein. Conclusion The frequency of Adv36 and increased CIMT at left carotid artery were higher among girls with visceral obesity than among those without visceral obesity. However, visceral obesity, CIMT at both right and left carotid arteries, and Adv36 had insignificant correlations with each other.



How to cite this article:
El-Masry SA, El Gamal HA, Al-Tohamy M, Nada A, Abdelrahman AH, Metkees MK, Ebrahim A, Saad W. ‘Infectobesity’ in egyptian adolescent women and its relations to carotid intima–media thickness.J Arab Soc Med Res 2018;13:79-88


How to cite this URL:
El-Masry SA, El Gamal HA, Al-Tohamy M, Nada A, Abdelrahman AH, Metkees MK, Ebrahim A, Saad W. ‘Infectobesity’ in egyptian adolescent women and its relations to carotid intima–media thickness. J Arab Soc Med Res [serial online] 2018 [cited 2019 Feb 20 ];13:79-88
Available from: http://www.new.asmr.eg.net/text.asp?2018/13/2/79/248983


Full Text

 Introduction



‘Infectobesity’, the new term that has evolved over the last 30 years, refers to obesity caused by infectious agents. Among 10 different pathogens caused obesity in mice, chicken, and in nonhuman organisms, only adenovirus 36 (Adv36) has been clearly related to cause human obesity [1].

Adenoviruses are considered one of the most popular viral infections in early childhood, responsible for nearly one-third of upper respiratory tract infections; which leads to mild and mostly self-limiting diseases [2]. Adv36 is the only one of the human adenoviruses that was found to have correlations with obesity in human beings [3].

Obesity in the adolescence period of life has major importance not only for the affected adolescents, but also for their society. Adolescents who has obesity, specially visceral, during this period of their life usually will have obesity tracking into the adulthood, which leads to many medical health problems resulting in early death [4]. Vijayakumar et al. [5] have described the secular trends in children’s and adolescent’s physical growth, and reported an increased prevalence of overweight/obese in all age groups and in both sexes.

Visceral fat accumulation causes a lot of metabolic disorders like insulin resistance (IR) and hypertension, through decreasing levels of adipocytokines which lead to cardiovascular risks and premature death due to early atherosclerosis [6]. However, subclinical atherosclerosis starts in early childhood, then progress into the adult life [7].

Increased carotid intima–media thickness (CIMT) and aortic stiffness, as markers of arterial atherosclerosis, have been greatly related (in both children and adults) to the occurrence of cardiovascular risk factors [8]. CIMT is a mirror reflecting an image of remodeling and smooth muscle cell hypertrophy due to increased blood pressures (BPs), one of the most important cardiovascular risk factor [9].

So, the aim of the current study was to investigate the relationship between visceral obesity, CIMT, and Adv36 among Egyptian adolescent women.

 Patients and methods



Patients

This cross-sectional study included 90 adolescent girls in an age range of 12–15 years. It was conducted at the ‘Medical Excellence Research Center’ of the ‘National Research Centre’, during the period between September 2016 and November 2017.

Every girl included in the study was evaluated by the following methods: a full history taking, thorough clinical general and local examination, anthropometric assessment, abdominal ultrasound (US), and carotid artery US and laboratory investigations.

Ethical approvals

The ethical approvals were obtained from both the Ethics Committee of ‘Faculty of Postgraduate Childhood Studies’ and from the ‘National Research Centre’ (approval no.15089). A verbal approval was taken from every girl participated in the current study, in addition to a written informed consent from one of her parents, after explanation of the aim of the study, as well as its possible benefits in avoiding the hazardous health effects of obesity.

Methods

The full history was taken from apparently healthy participants. It included presence of any present disease and past family history [history of obesity, previous infection, hypertension, cardiovascular diseases (CVD), and diabetes].

Thorough clinical general and local examination was done to exclude organic or genetic disorders that might interfere with the individual’s normal growth.

Blood pressure measurements

Triplicate BP measurements were performed in the sitting posture after 5 min rest and with at least 1 min between recordings, using validated (in pediatric population) semiautomated devices (Omron 705IT). An appropriate cuff was used according to the individual’s arm circumference (inflatable bladder size, 13×23, or 15×30 cm2 were appropriate). The average of the last two measurements was used in the analysis. BP was evaluated according to age and sex. A participant was considered hypertensive if her systolic blood pressure (SBP) and/or diastolic blood pressure (DBP) was at least 90th percentile for age and sex. Then according to her BP, the participants were classified into normal (120/80 mmHg), prehypertensive (125/85 mmHg), and hypertensive (130/85 mmHg), according to Lurbe et al. [10].

Anthropometric measurements

For every participant girl, the following anthropometric measurements were taken: body weight, height, waist circumference (WC), and hip circumference (HC). Then, BMI, waist/height ratio, and waist/hip ratio were calculated. All measurements were taken by a well-trained researcher and her assistant, using standardized equipment and following the recommendations of the International Biological Program, and then the mean of three consecutive measurements was recorded [11].

Body height was measured to the nearest 0.1 cm using a Holtain portable anthropometer (The Harpenden Portable Stadiometer, Wales, UK). Body weight was determined to the nearest 0.01 kg using the Seca scale (Seca Balance Beam Scale Model 700, Seca Deutschland Medical Scales and Measuring Systems; Seca GmbH and Co., Hamburg, Germany), with the individual dressed in minimum clothes and no shoes. BMI was calculated as weight (in kg) divided by height (in m) squared. WC was measured at the level of the umbilicus with the girl standing and breathing normally. HC was measured, while the participant girl was wearing light clothing; at the widest level over the greater trochanters in a standing position and by the same examiner. Circumferences were measured, using nonstretchable plastic tape, to the nearest 0.1 cm. The normal WC value for women is 88 cm=35 inches [12].

Abdominal ultrasound

US examination, to every girl, was done to evaluate visceral fat at the umbilicus ultra sound visceral fat (USVF) in cm. Intra-abdominal fat thickness measurement was obtained using the ‘Medison SonoAce X8’ Ultrasonographic equipment. For the visceral fat, a 3.5 MHz transducer was transversely positioned 1 cm above the umbilical scar on the abdominal midline, without exerting any pressure over the abdomen. The visceral fat thickness attempted corresponding to the measurement in centimeters between the internal surface of the abdominal rectus muscle and the posterior aortic wall in the abdominal midline, during expiration. Subcutaneous fat (S) − distance from the skin to the linea alba, measured on the hemisterna line, 1 cm above the umbilical scar, utilizing the linear transducer in a longitudinal section. Umbilical fat normal value is 4.47 cm, and girls with higher values were considered to have visceral obesity [13].

Carotid artery ultrasonography

This examination was performed using a high-resolution echo-Doppler device with a 7 MHz linear transducer. All participants in the study were examined in the supine position, with the head overextended and turned 45° away from the examined side. Both carotid arteries were visualized longitudinally, so that the CIMT of their distal wall was apparent. The best images of the distal wall were used to calculate the CIMT of the common and internal carotid arteries. The value of the CIMT was defined as the mean value of measurements between the right and left carotid arteries, calculated from 10 measurements on each side, 10 mm from the bifurcation of the common carotids [14].

Among women aged less than 30 years, CIMT values of at least 75th per centile were considered high and indicative of increased CVD risk, whereas values between 25th and 75th percentile were considered average and indicative of unchanged CVD risk. Values up to 25th percentile were considered lower CVD risk [15]:Cutoff point for right common carotid artery=0.39–0.43 (25th to 75th percentile).Cutoff point for left common carotid artery=0.30–0.47 (25th to 75th percentile).

Laboratory investigations

Venous blood samples (5 ml) were obtained in the morning by venipuncture after 12-h overnight fasting. The blood samples were left to clot, and then sera were separated by centrifugation for ∼20 min at 1000g (or 3000 rpm) within 30 min after collection. Serum was then divided into two parts, one part of them stored at −80°C for Adv36 and insulin tests and the other part was tested for fasting glucose and lipid profile tests.

Qualitative human Adv36 antibody was measured using a sandwich enzyme-linked immunosorbent assay (ELISA), to qualitatively analyze human Adv36 antibody [16] using ELISA kit of MyBioSource Inc. (USA).

Serum insulin was measured using ELISA immunoassay kit of Immunospec Corporation (Livonia, Michigan, USA), according to the method of Kurtoglu et al. [17].

Fasting blood glucose was determined calorimetrically, by the glucose oxidase method [18]. Homeostasis model assessment for insulin resistance (HOMA-IR) was calculated as [fasting glucose (mg/dl)×fasting insulin (lU/ml)/405], according to Shashaj et al. [19].

Plasma total cholesterol (TC) level [20], triglycerides (TG) [21], and high-density lipoprotein cholesterol (HDL-C) [22] were measured using commercially available kits provided by Stanbio Laboratory Inc. (Boerne, Texas, USA). Low-density lipoprotein cholesterol (LDL-C) was calculated according to the equation developed by Friedewald et al. [23] as follows:

[INLINE:1]

Statistical analysis

It was performed using the computer program statistical package software for Windows, version 16 (SSPS Inc., Chicago, Illinois, USA). Visceral fat; at umbilicus; cutoff point of 4.47 cm was used to classify the girls under study into two groups: those above 4.47 cm were considered to have visceral obesity, while those with up to 4.47 cm were considered without visceral obesity. Descriptive statistics (mean±SD) was calculated for the anthropometric and laboratory assessment and the ultrasound findings. Student’s t-test was used to compare the two groups. Frequency distribution of the high-risk groups was presented as number and percentage. χ2-Test was used to compare the qualitative data. Pearson’s correlation was used to assess the association between CIMT and anthropometric measurements, as well as the laboratory findings (quantitative data). Spearman’s correlation was used to assess the association between adenovirus (qualitative data) and other variables. Standards of probability were set to P value of less than 0.01; which is considered highly significant and P value of less than 0.05 which is considered statistically significant, in all analyses.

 Results



The participants under investigation were classified into two group: girls with (n=26) or without (n=64) visceral obesity.

Adv36 was detected among 56.2% (36/64) of girls without visceral obesity versus 69.2% (18/26) of those with visceral obesity, revealing significant differences between the two groups using the χ2-test ([Figure 1]).{Figure 1}

Girls with visceral obesity had the highest significant values for most of the anthropometric parameters (weight, BMI, WC, HC), visceral fat at umbilicus (P<0.05), and the lowest significant value in HDL. There were insignificant differences between the two groups in SBP, DBP, CIMT at right and left carotid, and for most of the laboratory investigations (fasting blood glucose, insulin, HOMA, TC, TG, and LDL) ([Table 1]).{Table 1}

Moreover, girls with visceral obesity had highly significant higher frequency of wide WC (76.9 vs. 34.4%), significantly higher frequency of decreased HDL (50 vs. 37.5%) and increased CIMT at left carotid artery (96.2 vs.75%) and insignificant higher frequency of hypertension; both DBP (34.6 vs. 31.2%) and SBP (19.2 vs. 7.8%), and SBP prehypertension (38.5 vs. 25%), and increased right CIMT (84.6 vs. 73.4%), increased plasma insulin (30.8 vs. 20.3%), HOMA-IR (46.2 vs. 40.6%) and fasting blood glucose (19.2 vs. 6.2%) than those without visceral obesity. While girls without visceral obesity had significantly higher frequency of increased LDL (26.6 vs. 7.7%) and insignificantly higher frequency of increased plasma TC (6.2 vs. 3.8%) and TG (7.8 vs. 3.8%; [Table 2]).{Table 2}

Visceral obesity at umbilicus, among the total sample, had significant positive correlations with body weight, BMI, WC, and HC, while it had insignificant correlations with age, BP, body height, CIMT at both right and left carotid arteries, laboratory finding and adenovirus ([Table 3] and [Table 4]).{Table 3}{Table 4}

Adenovirus had significant negative correlations with BP both SBP and DBP; among total sample and among girls with visceral obesity; and with fasting blood glucose among girls with visceral obesity. It had significant positive correlation with insulin level among the total samples. It had insignificant correlations with age, anthropometric measurements, visceral obesity at umbilicus, and CIMT at both right and left carotid arteries, HOMA, cholesterol, TG, HDL, and LDL ([Table 3] and [Table 4]).

CIMT at the left carotid artery had significant positive correlation with CIMT at right carotid artery, HOMA-IR among total sample and among girls with visceral obesity, and TC among the total samples only. It had significant negative correlations with HDL and WC among the total samples only. CIMT had insignificant correlations with the other anthropometric measurements such as age, BP, visceral obesity at umbilicus, insulin, glucose, TG, and LDL ([Table 3] and [Table 4]).

 Discussion



Measurement of CIMT, which is a noninvasive, feasible, reliable, and inexpensive tool to diagnose early vascular damage, is considered as a marker for increased cardiovascular risk and development of subclinical atherosclerosis in adults, as well as in children [24].

In the current study, girls with visceral obesity had the highest significant values in BMI, WC, HC, and visceral fat at the umbilicus, compared with those without visceral obesity. Moreover, girls with visceral obesity had highly significantly higher frequency of wide WC, and insignificantly higher frequency of hypertension, both DBP and SBP, SBP prehypertension, than those without visceral obesity. This agrees with the studies of Al-Hazzaa et al. [25] in Saudi Arabia; Kankana et al. [26] in India; and El-Kassas and Ziade [27] in Lebanon; who found that adolescent girls with visceral obesity had higher BMI, HC, and wide WC. McGrowder [28] in Brazil and Manios et al. [29] in Greece have reported that visceral obese adolescents had a significant increase in both SBP and DBP than normal-weight adolescents. Wyszyńska et al. [30] studied 568 adolescents with mild intellectual disabilities and assessed visceral obesity by WC, observed that increased risk of hypertension was more than three-fold higher in adolescents with visceral obesity than in participants with normal WC. Also, the hypertension values were increased stridently in girls with WC of at least 90 percentile.

In the current study, girls with visceral obesity had significantly higher frequency of decreased HDL than those without visceral obesity, while girls without visceral obesity had significantly higher frequency of increased LDL. In agreement with the current results, Kankana et al. [26] found that visceral obese adolescent girls had increased risk to have chronic heart disease later on in the future. Sato et al. [6] in Japan reported that participants, from both sexes, with visceral obesity had significantly low HDL-C; but in contrast to current results, they had higher serum TG level and higher fasting blood glucose level than patients without visceral obesity, and with no effect on serum LDL-C.

The present study revealed that girls with visceral obesity had significantly higher risk of increased CIMT at the left carotid artery, but insignificant at the right one than in girls without visceral obesity. In agreement with the current study, Baroncini et al. [31] in Brazil observed that CIMT is constant in healthy children at age less than 10 years, regardless of sex or BMI, while CIMT increased after that age in all the study samples. Turer et al. [32] studied 2893 adolescents aged 12–18 year, from four studies (Cardiovascular Risk in Young Finns, Childhood Determinants of Adult Health, Bogalusa Heart, and Insulin Studies). They reported that obesity is an important risk factor which was strongly associated with increased CIMT. Gooty et al. [7] observed that the association between obesity and increased CIMT was stronger in adolescents than in young children. In the study of Atherosclerosis Risk in Young Adults in the Netherlands, Eikendal et al. [9] studied adolescents and young adults where the mean age of adolescents was 13.5 years and young adults was 28.4 years. They found that obese adolescents with high SBP had experienced increased CIMT in their young adulthood life. Kollias et al. [33] studied 448 children and adolescents from both sexes (aged 10–18 years) from a semirural area in Greece, and found that visceral adiposity, as well as SBP was related to increased CIMT values in healthy adolescents. The CIMT values in the left side were higher than on the right side, thus defining the cardiovascular risk (SBP).

The current study revealed that visceral obesity at umbilicus had insignificant correlations with BP, CIMT at both right and left carotid arteries, and Adv36. Reviewing literature, we found that the relations between visceral obesity, CIMT, and Adv36 were not discussed before. In concordance with the current results, Berger et al. [34] found no association between Adv36 and visceral obesity.

The present study showed that CIMT at left carotid artery had significant positive correlation with CIMT at right carotid artery, HOMA-IR and TC, and significant negative correlations with HDL. It had insignificant correlations with other anthropometric measurements, BP visceral obesity at umbilicus, insulin, glucose, TG, and LDL. In agreement with the current study, Epifanio et al. [35] in Brazil reported that CIMT on the right side was positively correlated with HOMA-IR, but had insignificant correlations with TG, LDL, glucose, insulin, and HDL. Silva et al. [36] in Brazil observed that CIMT was positively correlated with HOMA-IR, a weak positive correlation with LDL, and was inversely correlated with HDL in adolescents. Ryder et al. [37] in Minnesota found that CIMT was significantly positively related to IR. Kupfer et al. [38] in Brazil also found that there was insignificant correlation between CIMT and TG and LDL. Önal et al. [39] found an insignificant correlation between serum triglyceride, LDL, and CIMT. Gao et al. [40] in Cincinnati studied 784 African-American adolescents aged 10–24 years and they found that CIMT was negatively correlated with HDL, but positively correlated with cholesterol. In disagreement with our results, they found positive correlations between CIMT with SBP and DBP, LDL, TG, and fasting glucose. Silva et al. [36] in Brazil observed that CIMT was positively correlated with BMI and WC among adolescents. Ryder et al. [37] in Minnesota found that CIMT was significantly positively related to visceral obesity. Önal et al. [39] found insignificant correlation between serum cholesterol and CIMTs. Vijayakumar et al. [5] found that CIMT was positively correlated with visceral obesity and WC as one of the important abdominal fat indices. Ge et al. [41] in South Asians found that the WC was correlated to CIMT. Rumińska et al. [42] showed no correlation between CIMT and IR. Kupfer et al. [38] in Brazil found insignificant correlation between CIMT and WC, cholesterol, and HDL.

The present study showed that the frequency of Adv36 was significantly higher among girls with visceral obesity (69.2%) than among girls without visceral obesity (56.2%). Our results agree with many studies, for example, Parra-Rojas et al. [43] in Mexico and Cakmakliogullari et al. [44], Karamese et al. [45], and Kocazeybek et al. [46] in Turkey. They found significantly higher frequency of Adv36 sero-positive antibody among obese adolescents than normal peers. In a study in USA, Broderick et al. [47] studied US military personnel, and they found a significant association between Adv36 positivity and female sex; and attributed this to estrogens that may play an important role in increasing the susceptibility to Adv36 infection. Moreover, Atkinson et al. [48] and Gabbert et al. [49] found a significantly greater WC as a marker of visceral obesity in Adv36-positive obese Italian children, although Na et al. [50] did not find the same relation.

In this study, Adv36 had significant negative correlations with BP both SBP and DBP and fasting blood glucose, and significant positive correlation with insulin level, but it had insignificant correlations with WC, HC, visceral obesity at umbilicus, and CIMT at both right and left carotid arteries, HOMA, cholesterol, TG, HDL, and LDL. This coincided with the study of Rogers et al. [51] which found that human Adv36 infections in adult White women was associated with significantly lower fasting glucose levels; in addition, Adv36 proteins may provide novel therapeutic targets for the treatment of diabetes mellitus. Ergin et al. [52] and Karamese et al. [45] in Turkey found an insignificant difference in cholesterol and triglyceride levels between the Adv36-positive antibodies patients and normal ones. Yamada et al. [53] found that sero-positive patients (adults and children) with Adv36 are associated with the risk of obesity and increased body weight, with no association with visceral obesity (WC). Na et al. [50] and Aldhoon-Hainerova et al. [54] did not find a correlation between visceral obesity and Adv36-positive antibodies. Almgren et al. [55] found that blood lipid profile levels (TG, TC, and LDL-C) did not differ between Adv36-positive and Adv36-negative Swedish overweight/obese children.In contrast to our results, Parra-Rojas et al. [43] found that adolescents with Adv36-positive serum antibodies had higher TC, TG, LDL-C, HOMA, and lower HDL-C levels than in the Adv36-negative group. Trovato et al. [56] reported that women with sero-positive Adv36 antibodies had positive correlation with BMI, DBP, HOMA, and TG, while having negative correlation with HDL cholesterol. Na et al. [50] in Korea found that obese Adv36-positive children had significantly increased levels of TG, TC, and LDL-C related to Adv36-negative children. In a cross-sectional study, Zarkesh et al. [57] found that infection with human Adv36 had positive correlation with TG, TC, LDL-C, and SBP and lower HDL-C levels. Atkinson et al. [48] reported a reduction in lipid levels in the presence of Adv36 infection. They demonstrated that Adv36 induced an obese state while paradoxically the serum levels of TG and cholesterol will reduce significantly. Sohrab et al. [58] found that Adv36 sero-positive populations had a reduction of total serum cholesterol and TG which in turn increased their body weight and shifting of HDL to LDL cholesterol. Adv36 affected the enzymatic functions mediated in the lipid and glucose uptake. It also reduced the expression and secretion of leptin leading to an increase in appetite, and TG accumulation of fat tissue.

In agreement with our study, a meta-analysis of 10 studies was done from different countries all over the world. This included those of Na et al. [50] in Korea and Yamada et al. [53], who reported that the risk of obesity and overweight was associated with infection by human Adv36, although being not associated with waist circumstance, suggesting that virus infection is generally related to obesity rather than visceral obesity.

 Conclusion



The frequency of Adv36 and increased CIMT at left carotid artery were higher among girls with visceral obesity than among those without visceral obesity. However, visceral obesity, CIMT at both right and left carotid arteries, and Adv36 had insignificant correlations with each other.

Acknowledgements

The authors acknowledge the National Research Centre, Egypt without the support of which this study could not have been possible. They also acknowledge the participants of this study for their cooperation, without whose help, this study could not have been completed.

Sahar A. El-Masry and Hanan A. El Gamal conceived and designed the study. Sahar A. El-Masry analyzed and interpreted the data. Muhammad Al-Tohamy was responsible for the anthropometric assessment. Amany H. Abdelrahman was responsible for laboratory investigations. Mohamed Kh. Metkees was responsible for radiological examination. Ayman Nada shared in drafting the article. Amany Ebrahim and Walaa Saad collected the data. All authors contributed to the collection of references, drafting of the article, and final approval of the version to be submitted. All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1Voss JD, Dhurandhar NV. Viral infections and obesity. Curr Obes Rep 2017; 6:28–37.
2Nakamura H, Fujisawa T, Suga S, Taniguchi K, Nagao M, Ito M et al. Species differences in circulation and inflammatory responses in children with common respiratory adenovirus infections. J Med Virol 2018; 90:873–880.
3Chappell CL, Dickerson M, Day RS, Dubuisson O, Dhurandhar NV. Adenovirus 36 antibody detection: Improving the standard serum neutralization assay. J Virol Methods 2017; 239:69–74.
4Reinehr T. Long-term effects of adolescent obesity: time to act. Nat Rev Endocrinol 2018; 14:183–188.
5Vijayakumar P, Wheelock KM, Kobes S, Nelson RG, Hanson RL, Knowler WC, Sinha M. Secular changes in physical growth and obesity among southwestern American Indian children over four decades. Pediatr Obes 2018; 13:94–102.
6Sato F, Maeda N, Yamada T, Namazui H, Fukuda S, Natsukawa T et al. Association of epicardial, visceral, and subcutaneous fat with cardiometabolic diseases. Circ J 2018; 82:502–508.
7Gooty VD, Sinaiko AR, Ryder JR, Dengel DR, Jacobs DRJr, Steinberger J. Association between carotid intima-media thickness, age, and cardiovascular risk factors in children and adolescents. Metab Syndr Relat Disord 2018; 16:122–126.
8Mendizábal B, Urbina EM. Subclinical atherosclerosis in youth: relation to obesity, insulin resistance, and polycystic ovary syndrome. J Pediatr 2017; 190:14–20.
9Eikendal AL, Groenewegen KA, Bots ML, Peters SA, Uiterwaal CS, den Ruijter HM. Relation between adolescent cardiovascular risk factors and carotid intima-media echogenicity in healthy young adults: the atherosclerosis risk in young adults (ARYA) study. J Am Heart Assoc 2016; 5:e002941.
10Lurbe E, Agabiti-Rosei E, Cruickshank JK, Dominiczak A, Erdine S, Hirth A et al. 2016 European Society of Hypertension guidelines for the management of high blood pressure in children and adolescents. J Hypertens 2016; 34:1887–1920.
11Hiernaux J, Tanner JM. Growth and physical studies. In: Human biology: a guide to field methods. Weiner JS, Lourie SA, editors. Oxford, UK: IBP. London, Blackwell Scientific Publications; 1969.
12Bischoff SC, Boirie Y, Cederholm T, Chourdakis M, Cuerda C, Delzenne NM et al. Towards a multidisciplinary approach to understand and manage obesity and related diseases. Clin Nutr 2017; 36:917–938.
13Grotti Clemente AP, Molin Netto BD, Ganen AD, Tock L, Arisa Caranti D, de Mello MT et al. Cut-off values of visceral adiposity to predict NAFLD in Brazilian obese adolescents. J Nutr Metab 2013; 2013:724781.
14Ho SS. Current status of carotid ultrasound in atherosclerosis. Quant Imaging Med Surg 2016; 6:285–296.
15Onut R, Balanescu AP, Constantinescu D, Calmac L, Marinescu M, Dorobantu PM. Imaging atherosclerosis by carotid intima-media thickness in vivo: how to, where and in whom? Maedica (Buchar) 2012; 7:153–162.
16Atkinson RL, Dhurandhar NV, Allison DB, Bowen RL, Israel BA, Albu JB, Augustus AS. Human adenovirus-36 is associated with increased body weight and paradoxical reduction of serum lipids. Int J Obes (Lond) 2005; 29:281–286.
17Kurtoğlu S, Hatipoğlu N, Mazıcıoğlu M, Kendirci M, Keskin M, Kondolot M. Insulin resistance in obese children and adolescents: HOMA-IR cut-off levels in the prepubertal and pubertal periods. J Clin Res Pediatr Endocrinol 2010; 2:100–106.
18Manco M. metabolic syndrome in childhood from impaired carbohydrate metabolism to nonalcoholic fatty liver disease. J Am Coll Nutr 2011; 30:295–303.
19Shashaj B, Luciano R, Contoli B, Morino GS, Spreghini MR, Rustico C et al. Reference ranges of HOMA-IR in normal-weight and obese young Caucasians. Acta Diabetol 2016; 53:251–260.
20Abe Y, Okada T, Sugiura R, Yamauchi K, Murata M. Reference ranges for the non-high-density lipoprotein cholesterol levels in Japanese children and adolescents. J Atheroscler Thromb 2015; 22:669–675.
21Burtis CA, Ashwood ER, Bruns DE. Tietz textbook of clinical chemisty and molecular diagnostics. 5th ed. St. Louis, USA: Elsevier; 2012. pp. 2238, 909 illustrations. ISBN: 978-1-4160-6164-9.
22Burstein M, Scholnick HR, Morfin R. Rapid method for the isolation of lipoproteins from human serum by precipitation with polyanions. J Lipid Res 1970; 11:583–595.
23Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972; 18:499–502.
24Baroncini LAV, Sylvestre LC, Baroncini CV, Pecoits RF. Assessment of carotid intima-media thickness as an early marker of vascular damage in hypertensive children. Arq Bras Cardiol 2017; 108:452–457.
25Al-Hazzaa HM, Abahussain NA, Al-Sobayel HI, Qahwaji DM, Alsulaiman NA, Musaiger AO. Prevalence of overweight, obesity, and abdominal obesity among urban Saudi adolescents: gender and regional variations. J Health Popul Nutr 2014; 32:634–645.
26KanKana D. Waist circumference, waist-hip ratio and body mass index in assessing nutritional status and central obesity of adolescent. Glob J Arch Anthropol 2017; 1:552–555.
27El-Kassas G, Ziade F. Exploration of the risk factors of generalized and central obesity among adolescents in North Lebanon. J Environ Public Health 2017; 2017:2879075.
28McGrowder DA. Biochemical parameters as cardiovascular risk factors in obese children and adults. J Endocrinol Diabetes Obes 2018; 6:1115.
29Manios Y, Karatzi K, Protogerou AD, Moschonis G, Tsirimiagou C, Androutsos O et al. Prevalence of childhood hypertension and hypertension phenotypes by weight status and waist circumference: the Healthy Growth Study. Eur J Nutr 2018; 57:1147–1155.
30Wyszyńska J, Podgórska-Bednarz J, Dereń K, Mazur A. Association between waist circumference and hypertension in children and adolescents with intellectual disabilities. J Intellect Dev Disabil 2018. DOI: 10.3109/13668250.2018.1425964
31Baroncini LA, Sylvestre Lde C, Pecoits Filho R. Assessment of intima–media thickness in healthy children aged 1 to 15 years. Arq Bras Cardiol 2016; 106:327–332.
32Turer CB, Brady TM, de Ferranti SD. Obesity, hypertension, and dyslipidemia in childhood are key modifiable antecedents of adult cardiovascular disease: a call to action. Circulation 2018; 137:1256–1259.
33Kollias A, Psilopatis I, Karagiaouri E, Glaraki M, Grammatikos E, Grammatikos EE et al. Adiposity, blood pressure, and carotid intima–media thickness in greek adolescents. Obesity (Silver Spring) 2013; 21:1013–1017.
34Berger PK, Pollock NK, Laing EM, Warden SJ, Hill Gallant KM, Hausman DB et al. Association of adenovirus 36 infection with adiposity and inflammatory-related markers in children. J Clin Endocrinol Metab 2014; 99:3240–3246.
35Epifanio M, Baldisserotto M, Sarria EE, Lazaretti A, Mattiello R. Ultrasound evaluation of carotid intima-media thickness in children. J Atheroscler Thromb 2015; 22:1141–1147.
36Silva LR, Cavaglieri C, Lopes WA, Pizzi J, Coelho-e-Silva MJ, Leite N. Endothelial wall thickness, cardiorespiratory fitness and inflammatory markers in obese and non-obese adolescents. Braz J Phys Ther 2014; 18:47–55.
37Ryder JR, Dengel DR, Jacobs DR Jr, Sinaiko AR, Kelly AS, Steinberger J. Relations among adiposity and insulin resistance with flow-mediated dilation, carotid intima-media thickness, and arterial stiffness in children. J Pediatr 2016; 168:205–211.
38Kupfer R, Larrúbia MR, Bussade I, Pereira JRD, Lima GAB, Epifanio MA et al. Predictors of subclinical atherosclerosis evaluated by carotid intima-media thickness in asymptomatic young women with type 1 diabetes mellitus. Arch Endocrinol Metab 2017; 61:115–121.
39Önal ZE, Soydan L, Öztürk HE, Sağ Ç, Gürbüz T, Nuhoğlu Ç, Şimşek MM. Carotid intima media thickness in obese children: is there an association with hyperlipidemia? J Pediatr Endocrinol Metab 2016; 29:157–162.
40Gao Y, Xie X, Cianflone K, Lapointe M, Guan J, Bu-jiaer GWB, Ma YT. Ethnic differences in acylation stimulating protein (ASP) in Xinjiang Uygur autonomous region, China. Int J Clin Exp Med 2015; 8:2823–2830.
41Ge W, Parvez F, Wu F, Islam T, Ahmed A, Shaheen I et al. Association between anthropometric measures of obesity and subclinical atherosclerosis in Bangladesh. Atherosclerosis 2014; 232:234–241.
42Rumińska M, Witkowska-Sędek E, Majcher A, Brzewski M, Czerwonogrodzka-Senczyna A, Demkow U, Pyrżak B. Carotid intima-media thickness and metabolic syndrome components in obese children and adolescents. Adv Exp Med Biol 2017; 1021:63–72.
43Parra-Rojas I, Del Moral-Hernández O, Salgado-Bernabé AB, Guzmán-Guzmán IP, Salgado-Goytia L, Muñoz-Valle JF. Adenovirus-36 seropositivity and its relation with obesity and metabolic profile in children. Int J Endocrinol 2013; 2013:463194.
44Cakmakliogullari EK, Sanlidag T, Ersoy B, Akcali S, Var A, Cicek C. Are human adenovirus-5 and 36 associated with obesity in children? J Investig Med 2014; 62:821–824.
45Karamese M, Altoparlak U, Turgut A, Aydogdu S, Karamese SA. The relationship between adenovirus-36 seropositivity, obesity and metabolic profile in Turkish children and adults. Epidemiol Infect 2015; 143:3550–3556.
46Kocazeybek B, Dinc HO, Ergin S, Saribas S, Ozcabi BT, Cizmecigil U et al. Evaluation of adenovirus-36 (Ad-36) antibody seropositivity and adipokine levels in obese children. Microb Pathog 2017; 108:27–31.
47Broderick MP, Hansen CJ, Irvine M, Metzgar D, Campbell K, Baker C, Russell KL. Adenovirus 36 seropositivity is strongly associated with race and gender, but not obesity, among US military personnel. Int J Obes (Lond) 2010; 34:302–308.
48Atkinson RL, Lee I, Shin HJ, He J. Human adenovirus-36 antibody status is associated with obesity in children. Int J Pediatr Obes 2010; 5:157–160.
49Gabbert C, Donohue M, Arnold J, Schwimmer JB. Adenovirus 36 and obesity in children and adolescents. Pediatrics 2010; 126:721–726.
50Na HN, Hong YM, Kim J, Kim HK, Jo I, Nam JH. Association between human adenovirus-36 and lipid disorders in Korean schoolchildren. Int J Obes (Lond) 2010; 34:89–93.
51Rogers PM, Fusinski KA, Rathod MA, Loiler SA, Pasarica M, Shaw MK et al. Human adenovirus Ad-36 induces adipogenesis via its E4 orf-1 gene. Int J Obes (Lond) 2008; 32:397–406.
52Ergin S, Altan E, Pilanci O, Sirekbasan S, Cortuk O, Cizmecigil U et al. The role of adenovirus 36 as a risk factor in obesity: the first clinical study made in the fatty tissues of adults in Turkey. Microb Pathog 2015; 80:57–62.
53Yamada T, Hara K, Kadowaki T. Association of adenovirus 36 infection with obesity and metabolic markers in humans: a meta-analysis of observational studies. PLoS One 2012; 7:e42031.
54Aldhoon-Hainerová I, Zamrazilová H, Atkinson RL, Dušátková L, Sedláčková B, Hlavatý P et al. Clinical and laboratory characteristics of 1179 Czech adolescents evaluated for antibodies to human adenovirus 36. Int J Obes (Lond) 2014; 38:285–291.
55Almgren M, Atkinson RL, Hilding A, He J, Brismar K, Schalling M et al. Human adenovirus-36 is uncommon in type 2 diabetes and is associated with increased insulin sensitivity in adults in Sweden. Ann Med 2014; 46:539–546.
56Trovato GM, Castro A, Tonzuso A, Garozzo A, Martines GF, Pirri C et al. Human obesity relationship with Ad36 adenovirus and insulin resistance. Int J Obes (Lond) 2009; 33:1402–1409.
57Zarkesh M, Daneshpour M, Ehsandar S, Bandehpour M, Alfadhli S, Azizi F, Hedayati M. Association of human adenovirus-36 with dyslipidemia in tehranian children and adolescent. TLGS Scimetr 2015; 3:e23927.
58Sohrab SS, Kamal MA, Atkinson RL, Alawi MM, Azhar EI. Viral infection and obesity: current status and future prospective. Curr Drug Metab 2017; 18:798–807.