Clinical and Basic Research | 263

CliniCal & basiC researCh

Sultan Qaboos University Med J, May 2013, Vol. 13, Iss. 2, pp. 263-268 Epub. 9th May 13
Submitted 18TH Jun 12
Revision Req. 15TH Dec 12, Revision Recd. 29TH Dec 12
Accepted 21ST Jan 13

1Paediatric and 2Biochemistry Departments, Minia University, Minia, Egypt
*Corresponding Author e-mail: basmaelmoez@yahoo.com

دراسة األديبونكتني يف األطفال الذين يعانون من مرض السكري
ب�شمة عبد املعز علي، دعاء حممد حمرو�ض، اأحالم حممد عبد اهلل و مينا جرج�ض فكري ق�شم طب الأطفال، الكيمياء احليوية

و  وال�شكري  بالبدانة  عالقة  له  و  الدهنيه  اخلاليا  من  فقط  ويفرز  الدهني  الن�شيج  بوا�شطة   يفرز  هرمون  الأديبونكتني  الهدف:  امللخ�ص: 
بالإ�شابة   ترابطه  ومدي  والثاين  الأول  بنوعيه  ال�شكري  بداء  امل�شابني  الأطفال  يف  الأديبونكتني  م�شتوي  تقييم  الهدف:  م�شاعفاتهما. 
مب�شاعفات الأي�ض يف مر�شي ال�شكري. الطريقه: اأجريت هذه الدرا�شة بعيادة الغدد ال�شماء مب�شت�شفى الأطفال اجلامعي - جامعة املنيا 
خالل الفرتة من اأبريل 2011 حتى يوليو 2011 و�شملت 314 طفل ترتاوح اأعمارهم من 2 اإىل 18 �شنة.ومت تق�شيم احلالت اإىل جمموعتني 
:املجموعة الأوىل: ت�شتمل على 164 مري�ض مت ت�شخي�شهم م�شبقا كمر�شى بداء ال�شكري ثم ق�شمت هذه املجموعة اإىل جمموعتني فرعيتني: 
- املجموعة الأوىل اأ: ت�شتمل على 142 مري�ض بداء ال�شكري من النوع الأول.- املجموعة الأوىل ب: ت�شتمل على 22 مري�ض بداء ال�شكري من 
النوع الثاين واملجموعة الثانية: ت�شتمل على 150 طفل اأ�شحاء ظاهريا ومتماثلني يف ال�شن واجلن�ض .وقد خ�شعت كلتا املجموعتني اإيل: 
اخذ التاريخ املر�شى املف�شل، الفح�ض الإكلينيكي والختبارات املعملية وت�شمل ن�شبة الهيموجلوبني ال�شكري، وقيا�ض م�شتوي الكول�شرتول 
والدهون الثالثية واأي�شا ن�شبة الأديبونكتني وال�شي-ببتيد( يف الدم. النتائج: وجد اأن ن�شبة الأديبونكتني بالدم مل تختلف كثريا يف الأطفال 
املجموعة  عن  ال�شكري  مر�شى  يف  اأعلى  لكنها  و  الثاين.  النوع  ال�شكري  بداء  امل�شابني  الأطفال  عن  الأول  النوع  ال�شكري  بداء  امل�شابني 
ال�شابطة ومن حيث عالقة الأديبونكتني بالعوامل الأخرى وجد انه توجد عالقة تنا�شب طردية ذات دللة اإح�شائية مل�شتوى الأديبونكتني 
بالدم مع حميط الو�شط وفرتة الإ�شابة باملر�ض يف الأطفال امل�شابني بداء ال�شكري من النوع الأول وكذلك عالقة تنا�شب طردية ذات دللة 
اإح�شائية مل�شتوى الأديبونكتني بالدم مع جرعة الأن�شولني اليومية يف الأطفال امل�شابني بداء ال�شكري من النوع الثاين ومن ناحية اأخرى 
مت اإيجاد عالقة تنا�شب عك�شية ذات دللة اإح�شائية مل�شتوى الأديبونكتني بالدم مع كل من ن�شبة الكول�شرتول وال�شي-ببتيد بالدم و �شغط 
الدم النب�شاطي يف الأطفال امل�شابني بداء ال�شكري من النوع الثاين اخلال�شة : نتوقع من نتائج هذا  البحث ان الأديبونكتني له اأهمية  يف 

احلمايه من م�شاعفات الأي�ض يف مر�شي ال�شكري.
مفتاح الكلمات: ال�شكري؛ الأديبونيكتني؛ مقاومة الأن�شولينز؛ م�رس.

abstract: Objectives: Adiponectin is a hormone produced by adipose tissue. It is secreted exclusively 
by adipocytes and appears to play a role in the pathophysiology of obesity, diabetes mellitus (DM), and its co-
morbidities. The aim of this study was to assess adiponectin levels in diabetic children with type 1 DM (T1DM) and 
type 2 DM (T2DM), and to detect its prognostic role in them. Methods: This study was undertaken from April to July 
2011 at Minia University Children’s Hospital, Egypt, and included  314 children aged 2–18 years divided into  two 
patient groups. Group I consisted of 164 pre-diagnosed diabetic patients, further subdivided into Group Ia which 
included 142 patients with T1DM and Group Ib, 22 patients with T2DM; Group 2 included 150 apparently healthy 
children as a controls; they were age- and sex-matched to the diseased group. Patients were subjected to a thorough 
history taking, clinical examination, and laboratory investigations including assessment of HbA1c percentages, 
fasting C-peptide levels, lipid profiles and fasting serum adiponectin levels. Results: Adiponectin levels did not 
differ significantly between patients with T1DM and T2DM, but it was significantly higher in diabetic patients 
than in the controls. In T1DM, adiponectin had positive significant correlations with the duration of the disease 
and waist circumference, while in T2DM, it had a positive significant correlation with the dose of insulin given and 
negative significant associations with diastolic blood pressure, cholesterol, and C-peptide levels. Conclusion: The 
results of the study suggest that adiponectin can play a protective role against the metabolic complications of DM.  

Keywords: Diabetes mellitus; Adiponectin; Insulin resistance; Egypt.

A Study of Adiponectin in Children with 
Diabetes Mellitus

*Basma A. Ali,1 Doaa M. Mahrous,1 Ahlam M. Abdallah,2 Mina Fikri1

Advances in knowledge 
- Adiponectin, a hormone produced and secreted by adipocytes, is present in the blood in high circulating concentrations suggesting an 

important physiological role. 
- An indirect regulator of glucose metabolism, adiponectin increases insulin sensitivity, improves glucose tolerance, and inhibits 

inflammation. 
- Adiponectin is emerging as a risk factor for health problems such as diabetes, hypertension, and heart disease, yet there is very limited 

information on the distribution of this hormone in some populations, especially in children.



A Study of Adiponectin in Children with Diabetes Mellitus

264 | SQU Medical Journal, May 2013, Volume 13, Issue 2

Egypt has one of the world’s ten highest rates of diabetes mellitus (DM) and impaired glucose tolerance.1 The ageing 
population together with socioeconomic and 
lifestyle changes has resulted in a dramatic increase 
in the prevalence of DM.1 In DM, the improper 
regulation of glucose and lipid metabolism due to 
the lack of insulin leads to an increased lipolysis rate 
and decreased stored fat tissue, which is reversible 
after insulin administration. 

Adiponectin is a hormone produced by 
the adipose tissue.2 It is secreted exclusively by 
adipocytes, circulates at relatively high levels 
in the blood stream, and appears to play a role 
in the pathophysiology of obesity, DM, and its 
comorbidities.2 This is because of its involvement 
in the regulation of carbohydrate and fat 
metabolism, as demonstrated in several animal 
and in vitro studies.3 By acting through two distinct 
membrane receptors, adiponectin receptors 1 
and 2 (which utilise 5-adinosine monophosphate-
activated protein kinase phosphorylation, p38 
mitogen-activated protein kinase, and peroxisome 
proliferator-activated receptor alpha as key cell-
signalling elements), increase hepatic and skeletal 
muscle sensitivity to insulin, enhance fatty 
acid oxidation, suppress monocyte-endothelial 
interaction, support endothelial cell growth, lower 
blood pressure, and moderate adipose tissue 
growth. The secretion of adiponectin can be 
suppressed by adipose factors, which are turned on 
once fat cell mass increases, such as cytokines, the 
adipose renin-angiotensin system, and increased 
oxidative stress. Inhibition of adiponectin secretion 
results in the loss of an array of mechanisms which, 
under normal conditions of fat cell homeostasis, 
provide protection from insulin resistance, DM, 
and atherosclerosis.4 The aim of this study was to 
assess adiponectin levels in diabetic children with 
type 1 DM (T1DM) and type 2 DM (T2DM), and to 
detect their role as a prognostic factor. 

Methods
This study included 164 patients with DM, 70 males 
(42.7%) and 94 females (57.3%); information on 
them was collected from April to July 2011 and 
they were classified as Group I. They had regular 
follow-up in the paediatric endocrinology 
outpatient clinic of Minia University Children’s 
Hospital, Minia, Egypt. Informed consent was 
obtained from every subject after the study received 
the approval of the ethical committee of the Faculty 
of Medicine of Minia University. Participants were 
further subdivided into two groups. Group Ia 
(T1DM) consisted of 142 patients (86.6 %) with a 
mean of age of 10.9 ± 4.2 years. In this group, there 
were 64 males (45.1%) and 78 females (54.9%) with a 
mean duration of illness of 40.2 ± 12 months. Group 
Ib (T2DM) consisted of 22 patients (13.4 %) with a 
mean of age 14.5 ± 2.7 years. In this group, there 
were 6 males (27.3%) and 12 females (72.7%), with 
a mean duration of illness of 82.1 ± 39.6 months.  
Another 150 children (Group II) acted as a 
control group which was age- and sex-matched 
to the study group. Both groups underwent a 
thorough history taking. A clinical examination 
included anthropometric measurements, including 
weight, height, body mass index (BMI), and waist 
circumference (WC). Each measurement was 
taken as the mean of three consecutive readings. 
Laboratory investigations included a measure of 
glycosylated haemoglobin (HbA1c%), cholesterol, 
and triglycerides (TG).5,6 Three ml venous blood 
samples were taken in the morning after 12 hours 
overnight using a complete aseptic technique. 
They were then centrifuged at 1000 rpm for 5 
minutes. The sera were separated and stored 
at -20° C until an assay of C-peptide levels by 
enzyme-linked immunosorbent assay (ELISA) 
technique was performed. This was carried out 
using C-peptide ELISA kits (InterMedical, Villarica, 
Italy). Adiponectin levels were also determined by 
immunoassay technique using Quantikine (Human 
Total Adiponectin/Acrp30 Immunoassay) DRP300 
kits (R&D Systems, Minneapolis, Minnesota, 
USA).7,8 

Application to Patient Care
- The use of intensive insulin therapy in the management of type 2 diabetes mellitus might be protective as it improves insulin sensitivity 

by increasing adiponectin levels and normalising C-peptide, while adiponectin could also provide protection by affecting metabolic 
complications in the form of dyslipidaemia and hypertension.



Basma A. Ali, Doaa M. Mahrous, Ahlam M. Abdallah and Mina Fikri

Clinical and Basic Research | 265

The data were coded and verified prior to data 
entry. All statistical analyses were carried out using 
the Statistical Package for Social Sciences (SPSS), 
Version 19.0 (IBM, Inc., Chicago, Illinois, USA). 
For descriptive statistics, continuous variables 
were presented as mean followed by standard 
deviation (SD), and categorical variables were 
presented as frequency and percentage. In regards 
to analytical statistics, for qualitative data Pearson’s 
chi-square test (χ2) was used; for quantitative data, 
an independent samples t-test (for two groups) 
and a one-way analysis of variance (ANOVA) test 
and post hoc multiple comparisons with the least 
significant difference (LSD) equal variance assumed 
(for three groups), were used. Two-tailed partial 
correlation coefficients (r), adjusted for age, sex, and 
BMI were used to assess the relationships between 
adiponectin and other variables. A P value <0.05 
was considered significant.9

Results
The study group (Group I) had significantly higher 
fasting serum levels of adiponectin than the 
controls (Group II) where P = 0.003 and 0.002, 
respectively. On the other hand, there was a 
non-significant difference between Groups Ia 

and b, where P = 0.4, although patients of Group 
Ib had the highest mean levels of adiponectin of 
all the studied groups [Table 1]. In the different 
laboratory investigations, the current study 
found that there were non-significant differences 
between Groups Ia and b in regards to the HbA1c 
percentage and triglycerides levels, while Group 
Ib had significantly higher levels of C-peptide and 
cholesterol than Group Ia (P = 0.0001 and 0.01, 
respectively) [Table 2]. Finally, concerning different 
correlations, we found that in Group Ia, there 
were significant fair positive correlations between 
mean adiponectin levels and both the duration of 
DM and WC, where r = 0.28 and P = 0.001 and 
r = 0.19 and P = 0.02, respectively. On the other 
hand, in Group Ib, there was a moderate positive 
significant correlation between mean adiponectin 

Table 1: Comparison between the studied groups as regarding the fasting serum level of adiponectin (µg/ml)

Fasting serum 
adiponectin
(µg/ml)

Group Ia 
(T1DM) 
(n =142)

Group Ib 
(T2DM) 
(n = 22)

Group II 
(Control) 
(n = 150)

P value

P† P‡ P§ P¶

Mean ± SD 9.5 ± 4.9 10.4 ± 5.7 4.9 ± 2.3 0.4 0.003* 0.002* 0.006*

Median 8.9 10.3 5.5

range 1.3–18.5 1.1–18.5 1.5–7.9

T1DM = type 1 diabetes mellitus; T2DM = type 2 diabetes mellitus; SD = standard deviation; * = significant; † = difference between Groups Ia and b; 
‡ = difference between Groups Ia and II; § = difference between Groups Ib and II; ¶ = comparison between the studied groups.

Table 2: Laboratory investigations of Groups Ia and b

Laboratory 
investigations

Group Ia Group Ib P 
value

Mean SD Mean SD

HbA1c (%) 7.5 1.4 8.1 0.62 0.06

C-peptide (ng/
ml)

0.26 0.07 0.77 0.8 <0.001*

Cholesterol 
(mg/dl)

168.6 38.9 191.1 52.2 0.01*

triglyceride 
(mg/dl)

131.2 205.3 140 54.2 0.8

SD = standard deviation; HbA1c = glycosylated haemoglobin; 
* = significant.

Table 3: Partial correlation coefficients adjusted for age, 
sex and body mass index between collected data and 
mean adiponectin in diabetic patients

Group Ia Group Ib

r P r P

Insulin dose 
(IU/Kg/day)

-0.08 NS 0.66 0.002*

Duration of DM 
(months)

0.28 0.001* 0.37 NS

Waist 
circumference 
(cm)

0.19 0.02* 0.2 NS

DBP (mmhg) -0.002 NS -0.73 <0.001*

HbA1c (%) 0.03 NS -0.32 NS

Cholesterol 
(mg/dl)

0.14 NS -0.54 0.01*

triglycerides 
(mg/dl)

0.1 NS 0.35 NS

C-peptide (ng/ml) 0.05 NS -0.49 0.03*

NS = not significant; * = significant; DM = diabetes mellitus; DBP = 
diastolic blood pressure; HbA1c = glycosylated haemoglobin.
Grades of r: 0.00 to 0.24 (weak or no association); 0.25 to 0.49 (fair 
association); 0.50 to 0.74 (moderate association); ≥0.75 (strong 
association).



A Study of Adiponectin in Children with Diabetes Mellitus

266 | SQU Medical Journal, May 2013, Volume 13, Issue 2

levels and the doses of insulin, and a moderate 
negative highly-significant correlation with diastolic 
blood pressure (DBP) (r = 0.66 and P = 0.002; 
r = -0.73 and P = 0.0001, respectively). Furthermore, 
there were negative significant correlations between 
the mean adiponectin level and both cholesterol and 
C-peptide, which displayed a moderate relationship 
with the former and a fair relationship with the 
latter (r = -0.45 and P = 0.01; r = -0.49 and P = 0.03, 
respectively) [Table 3].

Discussion
Several experimental studies have shown the anti-
inflammatory and anti-atherosclerotic effects of 
adiponectin.10 Furthermore, there is substantial 
evidence that adiponectin has protective effects 
against the development of atherosclerosis.11 

Therefore, the aim of our study was to assess the 
difference of adiponectin levels in children with 
T1DM and T2DM, and to detect its prognostic role.

In regards to the results of the current study, 
mean adiponectin levels in T1DM patients did 
not differ significantly from those in patients with 
T2DM (P = 0.4). This may have been due to the 
fact that our paediatric T2DM patients were on 
insulin therapy. Insulin downregulates adiponectin 
receptor expression, and insulin replacement could 
induce adiponectin resistance, making increased 
levels necessary to achieve physiological effects.12 

Also, several authors have observed that intensive 
insulin treatment increases circulating adiponectin 
levels, improving insulin sensitivity.13,14 Moreover, 
the positive highly-significant correlation between 
the mean fasting serum adiponectin level and 
the dose of insulin in patients with T2DM in 
our study supports this result (r = 0.66 and 
P = 0.002). On the other hand, the mean adiponectin 
levels were significantly higher in diabetic patients 
than the controls. This result correlated with the 
results obtained by Furuta et al. who found that 
adiponectin levels increased in conjunction with 
β-cells dysfunction.15 Also, Barnes et al. and Ljubic 
et al. found that adiponectin levels were significantly 
higher in diabetics than in controls.16,17 

Concerning laboratory investigations, the 
current study found that there was an insignificant 
difference between patients in Groups Ia and Ib in 
regards to HbA1c percentage. On the other hand, 
Group Ib had significantly higher mean C-peptide 

levels than Group Ia. Furthermore, they had 
significantly higher cholesterol levels than group 
Ia. It is possible that poor glycaemic control among 
those with T2DM contributed substantially to 
the high lipid profile.18 This result correlated with 
the results obtained by Dabelea et al. and Mayer-
Davis et al., who found that T2DM patients had 
higher C-peptide levels and cholesterol than T1DM 
patients.19,20 Contrary to our results, Wadwa et al. 
found that there was a non-significant difference 
between T1DM and T2DM in regards to cholesterol 
levels.21

Concerning different correlations, in Group 
Ia mean serum adiponectin had a significant fair 
positive correlation with duration of DM. This 
result was in agreement with the result obtained by 
Lindström et al.22 Also, there was a significant weak 
positive correlation between mean adiponectin 
levels and WC. This was possibly due to the fact that 
93% of Group Ia were lean patients. On the other 
hand, in Group Ib there was a moderate positive 
significant correlation between mean adiponectin 
level and dose of insulin. This might be due to 
the fact that insulin therapy increased circulating 
adiponectin levels and decreased insulin resistance 
by increasing the metabolic insulin signal in 
human skeletal muscles.13 Furthermore, there was 
a moderate negative highly significant correlation 
between adiponectin and DBP. This result correlated 
with the results obtained by Degawa-Yamauchi et 
al. in their study of African boys, Weiss et al. in 
their study of French adolescents, and Hassan et 
al. in their study of obese children.23–25 This could 
possibly be due to the beneficial role of adiponectin 
in the management of endothelial dysfunction as 
adiponectin acts directly on vascular endothelial 
cells and exerts salutary effects on endothelial 
function through endolethial nitric oxide synthase 
(eNOS)-dependent and cyclooxygenase-2 (COX-
2) dependent regulatory mechanisms.26 Also, there 
was a moderate negative significant correlation 
between mean adiponectin and total cholesterol 
among Group Ib. This may have been due to the 
anti-inflammatory and anti-atherosclerotic effects 
of adiponectin.27 Finally, there was a fair negative 
significant correlation between serum adiponectin 
levels and C-peptide. This could be explained by 
the adiponectin level increase in conjugation with 
β-cell dysfunction, which was estimated by fasting 
serum C-peptide.



Basma A. Ali, Doaa M. Mahrous, Ahlam M. Abdallah and Mina Fikri

Clinical and Basic Research | 267

Conclusion
Based on the results of this study, we concluded 
that there was a non-significant difference in the 
adiponectin levels between T1DM and T2DM, but 
that diabetic patients had significantly higher levels 
than the control group. The increase in circulating 
adiponectin concentrations in patients with T1DM 
appeared to be associated with a longer duration 
of illness and a greater WC. On the other hand, 
pancreatic β-cell function is a significant regulator 
for serum adiponectin concentrations in T2DM 
patients where serum adiponectin concentrations 
were associated with C-peptide. Also, in T2DM, 
adiponectin had a significant negative association 
with DBP and hypercholesterolaemia, suggesting its 
protective role against the metabolic complications 
of DM. 

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