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Journal of the American College of Nutrition, Vol. 27, No. 1, 177-183 (2008)
Published by the American College of Nutrition

Effect of Diet and Physical Exercise Treatment on Insulin Resistance Syndrome of Schoolchildren

Anna Szamosi, MD, Antal Czinner, MD, PhD, Tamas Szamosi, MD, PhD, Ágnes Sallai, MD, Mensud Hatunic, MD, Zita Berla, MD, Erika Tomsits, MD, PhD, Zsuzsa Almássy, MD and John J. Nolan, MD, PhD

Second Pediatric Department (T.S., Á.S., Z.B., E.T.)
Ophthalmologic Department (A.S.)
Med. Fac, Semmelweis University, Heim Pal Pediatric Hospital (A.C., Z.A.)
Budapest, HUNGARY, Metabolic Research Unit, Hospital 5, St. James Hospital, Dublin, IRELAND (M.H., J.J.N.)

Address reprint requests to: Tamas Szamosi MD, PhD, 2nd Department of Pediatrics, Medical Faculty, Semmelweis University, H-1094 Budapest Tüzoltóu., 7, HUNGARY. E-mail: szatam{at}gyer2.sote.hu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 DESIGN AND METHODS
 RESULTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Background: Insulin resistance syndrome (IRS) of schoolchildren may contribute to cardiovascular diseases (CVD) of young adults. The investigation of different steps, baseline screening parameters and treatment of IRS may help the prevention.

Methods: Schoolchildren (53 boys and 61 girls age 5–17 years) because of adverse family history of CVD, hypertension, and obesity were investigated.

Patients were divided into 3 groups according to baseline plasma glucose level (PGL) 120 and 180 min. after glucose consumption (GC): (1) PGL ≤ 5.5 mmol/L 180 min. after GC, (2) PGL ≥ 5.5 mmol/L 180 min. but ≤ 7.8 mmol/L 120 min. after GC (3) PGL ≥ 7.8 mmol/L 120 min. after GC. Body mass index (BMI), blood pressure (BP) and parameters of glucose and lipid metabolism were measured at baseline and after two year's lifestyle modification.

Results: No significant diference was found in the prevalence of cardiovascular risk factors (CRF) between groups 2 and 3. Fasting PGL > 5.5 mmol/L was found in 1, 2, and 6 cases; HOMA index > 4.4 in 7 (24%), 21 (37%), and 9 (35%) subjects; OGIS index < 400 in 3(10%), 29(51%) and 11 (42%) schoolchildren of groups 1, 2, 3, respectively. Lifestyle modification significantly improved BMI, systolic BP, serum triglyceride and HDL-cholesterol levels and insulin sensitivity.

Conclusions: PGL measured 180 minutes after GC may define an important subgroup of pre-diabetic children. The similar prevalance of CRF in both praediabetic groups underlines the importance of this subgroup. Lifestyle modification for two years improves CRF in this population.

Key words: glucose metabolism, high cardiovascular risk, schoolchildren, insulin resistance, lifestyle intervention


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
DESIGN AND METHODS
 RESULTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Cardiovascular disease is the leading cause of death in developed countries [1]. Numerous risk factors are involved in atherosclerotic process in adulthood [2]. Evidence is accumulating that atherosclerosis starts in childhood and adolescence [3]. The extent of atherosclerotic change in adults can be correlated with the presence of the same risk factors identified in children and adolescents [4].

Atherosclerosis risk factors such as hypertriglyceridaemia, hypertension, low serum high density lipoprotein cholesterol (HDLC) level and obesity are components of the metabolic syndrome (MS) originally described by Reaven [5] and more recently the subject of a range of different definitions. In adults and children these factors together with hyperinsulinaemia have been described as the insulin resistance syndrome (IRS). The natural progression from high risk status in childhood to type 2 diabetes and cardiovascular disease has not been clearly defined to date, but compelling evidence points to an association with overt disease in adults [6]. About 25% of obese children have been reported to have impaired glucose tolerance (IGT) [7]. More detailed study of the IRS in childhood and adolescence is of clinical and epidemiological importance.

The prevalence of type 2 diabetes and IRS has been increasing rapidly. Evidence is growing that this is likely to be linked to current obesity epidemic. Diabetes and insulin resistance are associated with early atherosclerosis and premature cardiovascular diseases (CVD) [8].

Since most children have neither symptoms nor signs of atherosclerosis, screening of high risk children (the offspring of parents and grandparents with premature CVD, children with obesity, hypertension or dyslipidemia) is of clinical importance. Fasting plasma glucose (FPG) is one of the advised parameters for screening [3] according to results of the Bogalusa study [9]. Not all studies, however, agree with this recomendation [10]. Fasting plasma insulin level (FPI) has been used by some groups as a marker of IRS [11].

Increased physical activity and weight reduction improved glucose tolerance and attenuated the progression to diabetes in one of several adult preventive studies [12]. The importance of lifestyle modification and family compliance for the treatment of childhood obesity, hypertension and dyslipidemia have been described previously by other authors [13–16]. Observation period used these authors was different from 6 weeks to more than ten years. Recently, the new dietary recommendation of American Heart Association was published according to results of these studies [17].

The aim of this study was to investigate different steps of insulin resistance syndrome, to evaluate the usefulness of baseline screening parameters and to analyze the effect of a two year's lifestyle modification on cardiovascular risk factors in schoolchildren across a full range of normal to pre-diabetic glucose metabolism.


   DESIGN AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 DESIGN AND METHODS
RESULTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Study Population
Schoolchildren (53 boys and 61 girls age 5–17 years) referred by family doctors because of adverse family history of cardiovascular disease, and/or the presence of hypertension and/or obesity, were investigated. All subjects were initially referred to the Second Pediatric Department of Medical Faculty, Semmelweis University or Heim Pál Hospital. Subjects with hepatologic, nephrologic or other serious chronic illnesses causing secondary lipid and carbohydrate metabolic disorders were excluded from the study. The protocol was approved by the local Research Ethics Committee and written informed consent was obtained.

Clinical Measurements
These measurements were performed at the start, and 2, 8, 14, 20, 24 months after the start of the 2 years long care.

Subjects attended on one morning at 08:00 for initial investigations. They underwent a full history and physical examination. Weight, height and body mass index (BMI) were determined.

Systolic (SBP) and diastolic (DBP) blood pressure were measured occasionally in the sitting position after five minutes rest and by 24 hour ambulatory blood pressure monitoring (ABPM) using a Meditech 004 type monitor in the cases in which hypertension was suspected. Patients were deemed to have elevated SBP, or DBP if more than 10% of their SBP, or DBP ABPM values and the 3 times repeated occasional measurements resulted BP higher than the 95th centile of values measured in the Hungarian population according to the age and height. The fundus of the eye of these patients was investigated by the same paediatric ophthalmologist used a Topcon fundus camera connected with a personal computer (PC) in which the software showed the width of ciliary veins and arteries measured in 4–4 places within a two disc circle from the optic disc. Hypertensive retinopathy grade 1 was detected where the mean vein: mean artery width ratio was <0.6.

Blood was collected from cubital vein. FPG, serum total cholesterol (TC), HDLC and total triglyceride (TG) levels were measured automatically using Hitachi 912 machine. Low density lipoprotein cholesterol LDLC level was calculated by the Friedewald equation [18] because no serum TG level above 400mg/dL was detected in any patients.

A standard three hour oral glucose tolerance test (OGTT) was performed after a 12 hour fast and blood samples were taken at 0, 30, 60, 90, 120, 150, 180 minutes after the consumption of 1.75g glucose/kg body weight, (or 75g glucose in those subjects who weighed >42 kg). Plasma insulin level (PIL) was measured by the IMX (Abbott) fully automatic method. Homeostasis model assessment (HOMA) indices were derived from the FPG and FPI [19]. The oral glucose insulin sensitivity (OGIS) index was calculated as described previously [20].

Risk Factor Criteria
For each parameter, simple risk thresholds were established, as follows: FPG level above 5.5 mmol/L, serum TC above 5.0 mmol/L, and LDLC above 3.5 mmol/L were considered to be elevated in all scholchildren, TG was considered to be elevated when above 1.1 mmol/L before 10 years of age, and above 1.5 mmol/L after 10 years of age. Serum HDLC level was considered to be reduced when below 0.9 mmol/L according to decisions of the Hungarian Consensus Conference about pediatric prevention of atherosclerosis held in Sept. 26, 2004 Budapest. FPI level was considered to be elevated above 20 µU/L [21]. HOMA index above 4.4 and OGIS index below 400 were considered to be abnormal and consistent with insulin resistance.

The co-existence of cardiometabolic risk factors was defined as IRS in the presence of 3 or more of the following:

  1. hypertension (SBP > 95th centile).
  2. hyperinsulinaemia (FPI > 20 µU/L).
  3. obesity (BMI > 95th centile corrected for age).
  4. hypertriglyceridaemia (serum TG level > 1.1 mmol/L prior to 10 years of age and > 1.5 mmol/L in those aged 10 and over).
  5. low serum HDLC level (< 0.9 mmol/L).

Patients were sub-divided into 3 groups according to their plasma glucose 120 and 180 minutes after oral glucose administration in the following way:

Group 1 (lean and obese schoolchildren who were referred because of their adverse family history of atherosclerosis - parents and/or grandparents-, or mild obesity and/or SBP higher than 95 centiles): Plasma glucose < 5.5 mmol/L 180 minutes after OGTT

Group 2 (‘praediabetic group’ containing lean and obese schoolchildren with abnormal glucose level but not IGT): Plasma glucose > 5.5 mmol/L at 180 minutes and < 7.8 mmol/L at 120 min after the OGTT,

Group 3 (IGT group containing obese schoolchildren): Plasma glucose > 5.5 mmol/L at 180 min and > 7.8 mmol/L at 120 minutes after OGTT.

1 person with Type 2 diabetes mellitus and 1 patient with impaired fasting glucose (IFG) was not included in any group.

15 obese children (2 from group 1, 5 from group 2, 7 from group 3 and 1 with IFG) refused the participation in the intervention study. Their parameters were measured only at the start and the end of study.

Lifestyle Intervention
A two year lifestyle modification was performed during which some patients had minor upper respiratory tract infections but no other significant illnesses. Advice regarding to the diet, physical activity and the cessation of the active and passive smoking was given under supervision of a pediatrician in cooperation with dietetician, psychologist and exercise physiologist, family doctors and nurses. Problems of patients and their families were discussed locally biweekly by family doctors and/or special nurses used 24 hours recall. Physical activity changes (inactivity and sedentary life hours, mild or high activity) were asked in these discussions and a diet accomodation was performed. Bimonthly meetings were held in lipid centers when lifestyle modification methods were discussed and the necessary personal modifications of the lifestyle intervention were made. Following advice - applied mostly by others [17], too - regarding to the lifestyle modifications were given:

  1. the use of the sunflower oil instead of pork fat during cooking,
  2. serving vegetables, legumes without ketchup and mayonnaise instead of cooking with roux (a fat and flour rich material usually mixed with greens and soups in Hungary). Fruit 5 times/day, whole grains.
  3. giving soups without roux,
  4. changing the fatty meats to poultry, lean meats and fish in the daily diet (seafish two times a week, mostly canned light tuna)
  5. no fat containing material to be used on bread
  6. 0.1% yoghurt with fruits and 0.5 L of 0.8–1.5% milk/daily,
  7. self-made fruit drink instead of any drink bought in a store,
  8. more spices instead of salt, low sugar, low fat diet,
  9. daily physical activity until the T shirt of patient became wet,
  10. cessation of smoking of relatives in the home and naturally smoking of the patients if they were smokers earlier.

Statistical Analysis
Data are presented as means with standard error of the mean in parenthesis. The significance of prevalence was calculated by chi-quadrat probe. The significance of the difference of means was tested by t-test for independent variables. A two-tailed model was used and a p value < 0.05 was considered to be statistically significant. Office SBP and DBP taken according to ISH recommendations were used for the statistical analysis.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 DESIGN AND METHODS
 RESULTS
ACKNOWLEDGMENTS
 REFERENCES
 
Baseline Characteristics
Number of patients belonging to different groups is outlined in Table 1.


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  		Table 1. Number of Patients Belonging to Different Groups (Age Range 5–17 Years)

 
IRS was not observed in group 1, and no significant difference in the prevalence of IRS between groups 2 (70.2%) and 3 (57.7%) was found (Table 2).


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  		Table 2. Baseline Prevalence of IRS in the Different Groups

 
Baseline SBP higher than 95 centiles of age matched Hungarian population was found in 47 patients (Fig. 1). Funduscopy showed grade 1 hypertensive retinopathy in 18 patients from patients with high SBP (Fig. 2).


Figure 1
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  		Fig. 1. ABPM results of a 14 years old children with BP higher than 95 centiles.

 

Figure 2
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  		Fig. 2. Fundus hypertonicus grad I. detected by objective funduscopy.

 
FPG ≥ 5.5 mmol/L was detected in 1, 2, 6 patients belonging to group 1, 2, 3, respectively. (Significance was not calculated because of the small sample size). High FPI was found in 12 (41%), 28 (49%) and 12 (46%) patients belonging to group 1, 2, and 3, respectively. High HOMA index was observed in 7 (24%), 21 (37%) and 9 (35%) patients belonging to group 1, 2, and 3, respectively. The frequency of high FPI, or high HOMA index in groups 2 and 3 was not significantly different from that in group 1. Patients with IFG and T2DM had high FPI and HOMA index. Low OGIS index was found in 3 (10%), 29 (51%), and 11 (42%) patients belonging to group 1, 2, and 3 respectively. The frequency of low OGIS index in both groups 2 and 3 was significantly different from that in group 1 (Table 3). The single patient with T2DM had a low OGIS index: 333.11.


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  		Table 3. Glucose Metabolism and Insulin Resistance at Baseline

 
No significant differences were found between parameters for boys and girls, or patients with or without high family risk of atherosclerosis.

Response to Lifestyle Intervention
Favourable changes in a range of risk markers were noted after the two years lifestyle intervention. Thus BMI, SBP, TG levels and HOMA index all decreased, serum HDLC level and OGIS index increased significantly after two years. TC and LDLC levels were unchanged. No similar significant differences were found in patients who refused to take part in the study (Table 4). The effectiveness of the intervention was compared in groups subdivided according to baseline BMI. (group 3 was not subdivided, because only 3 persons in this group were lean). Mean serum HDLC increased significantly after the 2 years in all groups regardless of BMI. (Table 4). Significant decrease (14–19%) of BMI was observed in all baseline obese sub-groups together with the decrease of SBP. The close connection between BMI and SBP changes was found in baseline non- obese patients belonging to group 2 whose BMI decreased significantly (9%) together with a decrease of SBP, too. Mean serum TG level decreased significantly in the obese subjects (but not in the lean subjects regardless of BMI changes) in each group. Serum TC level decreased significantly in group 3 only (Table 5). No patients with pathologic fundus of the eye was detected after the intervention.


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  		Table 4. Whole Group Measurements Pre and Post Lifestyle Intervention (n = 114)

 

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  		Table 5. Sub-Group Risk Factors Pre and Post Lifestyle Intervention

 
Lifestyle modification was associated with the following changes in glucose metabolism in the different groups (Table 6): (1) No significant change in FPG was found, (2) 120 min. after OGTT a significant decrease in plasma glucose was observed in obese subjects of group 2 and in group 3, but not in lean subjects of group 2 and obese subjects of group 1 inspite of their significant weight loss, (3) a significant decrease of plasma glucose 180 min. after the OGTT was observed in both lean and obese subjects of group 2 and 3, but not in obese subjects of group 1 inspite of their significant weight loss, (4) a significant decrease of the FPI level was found in obese children of group 1, only, (5) HOMA index was reduced in group 2 and obese subjects from group 1, but not in group 3, inspite of the significant weight loss observed in children belonging to this group after the care, (6) the OGIS index significantly increased in groups 2 and 3.


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  		Table 6. Sub-Group Glucose Metabolism and Insulin Resistance in Response to Lifestyle Intervention

 
As a summary of results regarding to effectivity of lifestyle modification treatment on glucose metabolism of our patients plasma glucose level measured 120 and 180 min. after OGTT decreased significantly in baseline overweight subjects and the significant increase of OGIS index of lean and obese subjects in both prediabetic groups showed the favourable changes of insulin resistance. SBP changes only showed in every sub-group close connection with weight loss.


   DISCUSSION
 
IRS was detected in most of obese patients in both group 2 (patients with abnormal glucose metabolism but without IGT) and group 3 (patients with IGT), but not in subjects in group 1 (patients with PGL ≤ 5.5 mmol/L 180 min. after OGTT) even though 59% of subjects in this group were obese. IRS appears to be present when obesity coexists with even minor abnormalities of glucose tolerance. The prevalence of IGT in our obese population was similar (29%) to that reported by others [7].

The presence of IRS is thought to indicate higher risk for later CVD [8]. The lack of the difference in IRS frequency of patients belonging to group 2 or 3 in the current study underlines the importance of the detection of patients with abnormal glucose metabolism below the threshold for IGT. In this sub-group, the plasma glucose 180 min. after OGTT is higher than 5.5mmol/L but the plasma glucose 120 min. after OGTT is below 7.8 mmol/L, thus below the currently defined threshold for IGT. Our data support the inclusion of this cohort of children as another variant of pre-diabetes, at an earlier step in the natural progression to Type 2 diabetes. The OGIS index seems to be an useful aid to investigate this population. Further follow up investigations in this cohort and similar larger cohorts will be required to better define the exact metabolic and cardiovascular prognosis for this sub-category of glucose metabolism.

Hypertensive retinopathy grade 1 is a well known consequence of hypertension [22]. The presence of this condition shows the importance of the mild hypertension observed in our patients. The possibility of the improvement of this condition has been described previously by others [23] and the lack of any pathologic fundus changes after lifestyle intervention supports the benefits of the intervention in this population of children.

FPG has been suggested as useful parameter for the detection of the abnormal glucose metabolism during screening for atherosclerosis risk factors in the pediatric practice [3,9] but in follow up studies the tracking of FPG was not observed. Other authors [11] reported an association between FPI and other parameters of MS in adolescents. Measurement of FPG alone confirms overt cases of type 2 diabetes and impaired fasting glucose, however, according to the statement of the American Heart Association [6] will miss those cases of Type 2 diabetes with normal FPG but abnormal post-challenge glucose after two hours. Neither the determination of FPG nor the measurement of FPI alone provided sufficient information or risk categorisation in most of the patients investigated by us. Half or more of the "prediabetic’ and IGT cases were not confirmed even with the calculation of HOMA and OGIS indices. For this reason we and other authors [12] recommend the three hour OGTT in obesity and any other cases when IRS is suspected. The measurement of the plasma glucose 180 min after the OGTT is of proven value based on our findings in children and adolescents in the current study.

The Finnish Diabetes Prevention Study and other prevention studies have confirmed the favourable effect of lifestyle modification in treatment of IGT [12, 24]. The efficacy of lifestyle modification on BMI and SBP in seriously obese children has been described by numerous authors [12,14,15]. A 6 weeks lifestyle modification appeared to be of insufficient duration [16]. Falkner at al [25] performed a two years lifestyle modification in an adolescent girl with MS and high risk family background and observed similar improvements in glucose metabolism, SBP, TG and HDL as those reported by us in the current study.

In schoolchildren at different stages of abnormal glucose metabolism the prevalance of cardiovascular risk factors is similar. Plasma glucose measured 180 minutes after glucose consumption may define an important subgroup of pre-diabetic children with abnormal glucose metabolism. Lifestyle modification for two years improves cardiovascular and metabolic risk factors and is highly effective in this population.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 INTRODUCTION
 DESIGN AND METHODS
 RESULTS
 ACKNOWLEDGMENTS
REFERENCES
 
Authors thank the technical assistance of Mrs Erika B Mathe.

Received September 15, 2006. Accepted April 30, 2007.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 DESIGN AND METHODS
 RESULTS
 ACKNOWLEDGMENTS
 REFERENCES
 

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