Physical activity and sports participation in children and adolescents with type 1 diabetes mellitus

Nutrition, Metabolism & Cardiovascular Diseases (2007) 17, 376e382

www.elsevier.com/locate/nmcd

Physical activity and sports participation in children and adolescents with type 1 diabetes mellitus Giuliana Valerio a,*, Maria Immacolata Spagnuolo b, Francesca Lombardi b, Raffaella Spadaro b, Maria Siano b, Adriana Franzese b a

School of Movement Sciences (DiSISTe), Parthenope University, Via Ammiraglio Acton 38, 80133 Naples, Italy b Department of Paediatrics, Federico II University, Naples, Italy Received 23 June 2005; received in revised form 20 October 2005; accepted 28 October 2005

KEYWORDS Adolescent; Glycosylated haemoglobin; Physical activity; Type 1 diabetes

Abstract Background and aim: Regular physical activity is of great importance in the management of type 1 diabetes mellitus (T1DM). We investigate here the levels of moderate/vigorous physical activity (MVPA) and participation in sporting activity in a sample of children and adolescents with T1DM and analyse whether they differed from healthy subjects. The family variables associated with MVPA or sports participation and the influence of exercise on metabolic parameters are also explored. Methods and results: In this cross-sectional case control study, 138 children and adolescents with T1DM (of which 67 were boys, age 13.6  4.1 years; duration of diabetes 6.1  3.8 years) and 269 (of which 120 were boys) healthy controls were studied. Weekly levels of MVPA and sports participation were investigated using a questionnaire. Body mass index standard deviation score (BMI-SDS) values, plasma total cholesterol, serum triglycerides and the mean glycated haemoglobin (A1c) levels over the past year were assessed in T1DM subjects. MVPA scores in T1DM patients were lower than in controls (p ¼ 0.0004). MVPA was higher in boys than in girls, both in diabetic and control subjects; T1DM girls were less frequently engaged in MVPA than control girls. MVPA scores were significantly and independently correlated with sex, age and diabetic status. Lower triglyceride levels and fewer subjects with poor metabolic control were found more among physically active patients (MVPA > 5 days/week) than in inactive patients (weekly MVPA ¼ 0). Sports participation was lower in T1DM patients than in controls (p ¼ 0.002) and was

* Corresponding author. Tel.: þ39 081 547 5747; fax: þ39 081 545 1278. E-mail address: [email protected] (G. Valerio). 0939-4753/$ - see front matter ª 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.numecd.2005.10.012

Physical activity in type 1 diabetes

377

significantly and independently correlated with sex, father’s education level and diabetic status. Triglyceride levels and the percentage of subjects with poor metabolic control were significantly lower in sports participants than in nonparticipants. Conclusions: Children and adolescents with T1DM appeared to spend less time in physical activity than their non-diabetic peers. Regular physical activity was associated with better metabolic control and lipid profile. Adolescents, particularly the girls, tended to be less active. Further efforts should be made to motivate patients with type 1 diabetes. ª 2005 Elsevier B.V. All rights reserved.

Introduction Type 1 diabetes mellitus (T1DM) greatly influences physical and emotional development. Effective management requires continuous attention to food intake, multiple daily injections of insulin, and glycaemic self-monitoring. Obtaining good metabolic control, preventing long-term complications and promoting social competence and selfworth are the targets of management in young patients with diabetes [1]. The importance of regular physical activity in the management of children and adolescents with T1DM has been highlighted in recent years [2]. Despite the beneficial effects of exercise, the level of physical activity generally undertaken by diabetic patients remains an issue of concern. Limited information exists about physical activity and sporting habits of young patients with T1DM. Several studies have failed to show an independent effect of exercise on improving glycaemic control in T1DM patients [3], while it was demonstrated that exercise reduces known risk factors for atherosclerosis (excess weight, dyslipidemia and hypertension) [4]. In addition, organised activity programmes, including sporting activities, contribute to improved socialisation, social integration and self-esteem in subjects with diabetes, allowing them to take part in different activities just as their peers do [5]. According to the American Department of Health and Human Services ‘‘Healthy People 2010’’ recommendations, adults should practise a moderate physical activity for at least 30 min nearly every day and an intense activity for at least 20 min three times a week [6]. The guidelines for young people do not greatly differ from this and suggest participating in at least 60 min per day of moderate/intense activity for most of the week. Levels of physical activity in healthy children, and particularly in adolescents, are surprisingly low [7]. Determinants of childhood levels of physical activity are complex and vary according to individual characteristics, parental and environmental influences [8]. A low educational level of

parents has been associated with an unhealthy lifestyle and increased future risk of cardiovascular disease in their offspring [9]. Important barriers to physical activity include television viewing and computer use [10]. The presence of a chronic disease, such as type 1 diabetes, may additionally interfere with participation in physical activities, for the risk felt by parents and children of acute metabolic complications, such as hypoglycaemic crises [11,12]. Therefore, levels of physical activity may not meet guidelines particularly in diabetic children. The aim of this study was to investigate the levels of moderate/vigorous physical activity (MVPA) and participation in sporting activities in a sample of children and adolescents with T1DM. The influence of parental educational level on MVPA or sports participation and the influence of exercise on metabolic parameters were also explored.

Methods In this cross-sectional case control study, 138 children and adolescents with type 1 diabetes mellitus (67 boys, 71 girls) were recruited at the Diabetes Unit, Department of Paediatrics, Federico II University of Naples, from October 2002 to January 2003. Mean age was 13.6  4.1 years (range 5.9e20 years); duration of diabetes was 6.1  3.8 years (range 1e17 years). They were treated with recombinant human insulin (mean 0.86  0.22 U/kg), divided into 3e4 daily doses, and performed self-monitoring of glycaemic control; a balanced normocaloric diet was prescribed. Only patients free of any diabetic complication were enrolled. Height was measured by Harpenden stadiometer and weight by SECA scale; body mass index (BMI) was calculated (weight/height2). Limits for overweight and obesity were represented by the Italian centiles [13] having at 18 years the value of 25 and 30 kg/m2, according to the method proposed by Cole et al. [14]. Thirty-two patients were overweight (23.2%) and 4 obese (2.9%).

378 Since BMI values are sex- and age-dependent, the standard deviation scores of BMI (BMI-SDS) were also calculated by Cole’s LMS method, using the Italian standards [13]. Two hundred and sixtynine healthy schoolchildren and adolescents (120 boys, 149 girls), mean age 12.9  3.5 years (range 6e19 years), were the control group. They were recruited from five classes (grades 1e5) randomly selected from one elementary school, three classes (grades 1e3) from one middle school and five classes (grades 1e5) from one high school in the district of Naples. No anthropometric measurement was taken in the control group. All subjects and their parents gave their informed consent to participate in the investigation. A questionnaire was used to obtain information about parents’ educational level. Length of school attendance was calculated and coded as 0 for no education, 5 years for primary school, 8 years for lower secondary education, 13 years for upper secondary education and 17 years and over for post secondary education. Children and adolescents reported the following information about their own lifestyle: engagement in moderate/vigorous physical activity (MVPA) in spare time, number and kind of sports played in the last 12 months and weekly hours spent training. A score of MVPA was assessed by calculating the number of days in which subjects had accumulated 60 min of MVPA during the previous days and for a typical week. This was achieved using a structured questionnaire, the reliability and validity of which had been previously assessed [15]. MVPA scores significantly correlated with the data provided by an accelerometer, an electronic device that objectively measures frequency and intensity of physical activity. The following two questions were asked: (1) ‘‘Over the past 7 days, on how many days were you physically active for a total of at least 60 min per day (min. 0emax. 7 days)?’’; (2) ‘‘Over a typical or usual week, on how many days are you physically active for a total of at least 60 min per day (min. 0emax. 7 days)?’’. The measure defined physical activity broadly as an activity that ‘‘increases your heart rate and makes you get out of breath some of the time’’ and did not specify intensity; some examples of physical activity were reported as running, brisk walking, rollerblading, biking, dancing, skateboarding, swimming, soccer and basketball. A composite average of the two items yielded a score of the number of days per week during which the subject accumulated 60 min of MVPA. Subjects were considered ‘‘inactive’’ if they did not report any MVPA over the week, ‘‘moderately active’’ if they were participating in MVPA 1e4 times/week and ‘‘active’’ if they

G. Valerio et al. Table 1

Demographic characteristics of participants T1DM patients Controls

Number Male/Female Age (years) Elementary school, n (%) Middle school, n (%) High school, n (%) Father’s school years Mother’s school years

138 67/71 13.6  4.1 33 (23.9) 36 (26.1) 69 (50.0) 10.3  3.5 9.6  3.8

269 120/149 12.9  3.5 69 (25.6) 66 (24.5) 134 (49.9) 9.8  3.7 9.5  3.9

were participating 5 or more times/week. Demographic characteristics of the participants are shown in Table 1.

Biochemical assessments Blood samples were collected in the morning only from diabetic patients using venipuncture after a 12-h overnight fast. Total cholesterol and triglycerides were measured by enzymatic assays (Roche/Hitachi 747). As an indicator of metabolic control, the mean A1c level of the last 3e4 determinations performed over the past year was calculated. A1c measurements (immunoassay) were taken by an Ames DCA-2000 Analyser (normal range: 4.2e6.5%).

Statistical analyses Power calculation was done before the study, using McNemar’s test of equality of paired proportion with a 0.05 two-sided significance level. It was found that a sample size of 115 pairs would have 80% power to detect a difference in proportion of 0.200, while the proportion of discordant pairs was expected to be 0.600. The following parametric and non-parametric tests have been used when appropriate: Student’s unpaired t-test or the ManneWhitney test were used to compare the means between two groups (diabetic patients versus healthy controls, sports participants versus non-participants), while ANOVA or KruskalleWallis tests were used to compare the means among groups with different MVPA levels. Associations between MVPA levels or sports participation and diabetic status were explored using the Fisher exact test for categorical variables. Multiple and logistic linear regression analyses were performed to determine the relationships between individual and family variables on children’s MVPA or sports participation. The dependent variables were, respectively, MVPA scores and sports participation, while the independent variables were gender

Physical activity in type 1 diabetes (coded as 1 for boys and 2 for girls), age, father’s and mother’s education level and diabetic status (coded as 0 for absent and 1 for present). Data are shown as mean  standard deviation (SD). Analysis was performed by SPSS 10.0 release. A p value of less than 0.05 was considered significant.

Results Measure of MVPA and associated variables Scores of MVPA were widely distributed in the population (range 0e7 days), with a mean of 2.8  2.5 days/week in T1DM patients and 3.6  1.9 days/week in controls (p ¼ 0.0001). Mean MVPA score was higher for boys than for girls, either when diabetic subjects (3.5  2.6 vs. 2.1  2.3, respectively, p ¼ 0.001) or controls (3.9  1.8 vs. 3.3  1.9, respectively, p ¼ 0.003) were considered. Diabetic girls were less frequently engaged in MVPA than control girls (p ¼ 0.0001), while no significant difference was found between diabetic and control boys. According to the classification based upon the number of days per week on which the subject participated in MVPA, 34 patients (24.6%) were inactive, 70 (50.7%) were moderately active and 34 (24.6%) were active. This distribution was significantly different from that found in the control group, where only 21 subjects were inactive (7.8%), 149 (55.4%) were moderately active and 99 (36.8%) were active (p < 0.0001). In order to analyse factors influencing the MVPA score, multiple regression analysis was performed in the whole population of patients and controls. MVPA score was the dependent variable, while gender, age, father’s and mother’s education

379 level, diabetic status and sporting practice were the independent variables. MVPA was significantly and independently correlated with sex, age and diabetic status (Table 2). BMI-SDS values did not differ among the different groups of MVPA (inactive 0.52  0.67, moderately active 0.49  0.94 and active 0.63  0.92). Triglyceride serum levels in inactive diabetic patients were higher than in active patients (inactive 73  28 mg/dl, moderately active 66  23 mg/dl and active 59  21 mg/dl, p ¼ 0.035), while no significant difference was found regarding total cholesterol levels (inactive 177  33 mg/dl, moderately active 164  30 mg/dl and active 165  31 mg/dl). Prevalence of patients with poor metabolic control (A1c > 8.5%) was higher in inactive patients than in those who were moderately active or active (Fig. 1).

Sports participation and associated variables Sports participation was reported by 65 diabetic patients (of which 34, or 47.1%, were boys) and 170 controls (of which 86, or 63.2%, were boys) (p ¼ 0.002). Weekly time spent in training was similar between groups (2.53  0.6 and 2.51  0.6 h/ week, respectively). Generally, participation in individual sports outnumbered participation in team sports in the patient group (46 individual sports versus 19 team sports), while they were evenly distributed in the control group (96 individual sports versus 74 team sports). In order to analyse factors influencing sports participation, a logistic regression analysis was performed on the whole population of patients and controls. Sports participation was the dependent variable. Gender, age, father’s and mother’s

Table 2 Variables independently associated with MVPA (model 1) or sports participation (model 2) by multiple and logistic regression analyses in the whole sample of subjects (patients and controls) Independent variable

Dependent variables

Beta (SE)

Standardised beta

p

Gender Age Father’s education Mother’s education Diabetic status

0.98 0.19 0.004 0.01 0.74

(0.22) (0.03) (0.04) (0.04) (0.22)

0.225 0.299 0.065 0.021 0.164

0.0001 0.0001 0.341 0.754 0.001

Gender Age Father’s education Mother’s education Diabetic status

0.18 0.004 0.02 0.003 0.18

(0.06) (0.01) (0.01) (0.01) (0.06)

0.152 0.023 0.151 0.020 0.154

0.004 0.674 0.035 0.777 0.004

Model 1: MVPA

Model 2: Sports participation

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G. Valerio et al. 45 38.2

40

chi2 for trend 0.017

35

% cases

30 25 20.0 20 14.7

15 10 5 0 inactive

moderately active

active

Figure 1 Percentage of subjects with poor glycaemic control (HbA1c > 8.5%) stratified according to days of MVPA per week.

education level and diabetic status were the independent variables. Sports participation was significantly and independently correlated with sex, father’s educational level and diabetic status (Table 2). By comparing sports participants and nonparticipants among the diabetic subjects, no difference was found regarding BMI-SDS (0.58  0.85 vs. 0.49  0.89, p > 0.05), daily insulin dosage (0.9  0.2 vs. 0.9  0.2 U/kg, p > 0.05), mean A1c (7.8  0.9 vs. 7.9  1.0%, p > 0.05) and total cholesterol (168  33 vs. 167  30 mg/dl, p > 0.05). On the contrary, triglyceride serum levels were significantly lower in sports participants than in non-participants (61.5  19.9 vs. 70.8  26.9 mg/dl, p ¼ 0.037). In agreement with the above, the percentage of subjects with poor metabolic control was lower in patients reporting sports participation (10 of 65 or 15.4%) than that found in patients who did not report any sports participation (22 of 73 or 30.1%, p ¼ 0.045).

Discussion Regular physical activity is associated with immediate and long-term health benefits [16]. It therefore represents a critical component of diabetes management. According to ADA guidelines, ‘‘all patients with diabetes should be given the opportunity to benefit from the many effects of exercise’’ [2]. Every kind of physical exercise, including competitive sports, should be made available to diabetic children, who should never feel different from their non-diabetic peers. Appropriate adjustment of insulin dosage, frequent

glucose self-monitoring, more careful dietary management before starting physical activity and programming the right time for exercise are the indispensable recommendations. In this survey, weekly time engaged in MVPA and participation in sports were investigated in a wide sample of children and adolescents with type 1 diabetes using a structured questionnaire. Scores of MVPA obtained through this questionnaire have been proposed as an easy measure for assessing participation in overall physical activity and for assessing conformance to current guidelines. This study has limitations that need to be considered before interpreting the findings. The measure used to assess levels of physical activity was brief and based on self-report, and thus bias may be present as children and adolescents may tend to respond in a socially desirable manner by over-reporting their physical behaviour. Despite health recommendations, many young people in industrialised countries have already adopted a sedentary life-style by the age of 13 years; girls, furthermore, being more inactive than boys [17,18]. According to previous reports using the same measure of moderatevigorous physical activity that we used, between 26.8% and 53% U.S. adolescents meet the ‘‘Healthy People 2010’’ recommendations [15,19]. No previous data exist regarding the Italian population. In our sample, only 25% of patients reached good levels of physical activity compared to 37% of healthy controls. Scores of MVPA were lower in diabetic patients than in controls, indicating the influence that diabetic status has on the levels of physical activity. In particular, multiple regression analysis indicated that low levels of MVPA were independently associated not only with diabetic status but also with female gender and older age, confirming that, as many children develop into adolescence, their physical activity levels decline [20]. Similarly, participation in sports was significantly lower in patients than in controls (47% vs. 63%). Again no published data exists for the Italian population, apart from the survey released by the Italian Institute of Statistics in 2003, indicating that about 59% of youth between 6 and 17 years of age regularly or occasionally engage in one or more sporting activities. In our sample, multiple regression analysis indicated that male gender and higher paternal education levels were independently associated with sports participation. Education is often used as an indirect measure of socioeconomic status in studies aimed at investigating the effect of socioeconomic inequalities in health research [21]. Higher parental educational level, and consequently higher socioeconomic status (SES), may provide better support for sporting

Physical activity in type 1 diabetes activities in children, increasing the availability of and access to community-based organised sports programmes at and outside school. A direct relationship between father’s occupation and sporting activities has been found also among seventh and eighth grade healthy students [22]. In chronically ill patients, lower educational levels and lower degrees of physical activity were associated with poor metabolic control in adult patients with T1DM [23]. The findings provided by multiple regression analysis in our sample indicate that, while individual features (gender, chronic disease) are important correlates of MVPA levels as well as of sporting activity, social and cultural factors may not affect the free-time playdalthough they may impede participation in organised sports in healthy and chronically ill children. The sporting habits of T1DM patients did not differ from healthy controls in terms of time spent weekly, while a stronger trend towards individual sports was found in diabetic patients. This may be interpreted as difficult socialisation experienced by patients. Since physical exercise can reduce blood glucose levels and insulin resistance [24,25], the hypothesis that regular aerobic exercise can improve metabolic control in T1DM patients has been analysed by several authors. Two crosssectional studies on the levels of physical activity evaluated using a questionnaire did not demonstrate any improvement in their long-term glycaemic control in T1DM adults [26,27]. Short-term trials have been carried out in T1DM children. While results are unequivocal in demonstrating an increase in aerobic capacity or fitness after a programme of physical activity, contrasting data were reported on the capacity of exercise to reduce A1c levels [3,28e31]. These contrasting results can be explained by the fact that several factors, such as variation in caloric intake or insulin dosage, stress or stricter medical monitoring can influence glycaemic status. For instance, increased carbohydrate intake to avoid hypoglycaemia may erroneously occur on days of physical activity, particularly in children, or additional care and/or attention to diet and insulin may be given to the training patients, resulting in a bias in the opposite direction. Our cross-sectional survey precludes the establishment of any causation. However, it suggests that conforming to the physical activity guidelines (at least 5 days of MVPA a week) or attending sports activities was associated with a lower percentage of subjects with bad metabolic control compared to that for inactive patients. Patients with a more active lifestyle are also more motivated to participate in various

381 programmes related to diabetes management, which is not necessarily an effect of training per se. In fact, according to previous findings, selfreported exercise was associated with both a better quality of life and better metabolic control in young T1DM patients [32]. Moreover, sports participation among high school students has been associated with multiple positive health behaviours, including fruit and vegetable consumption and reduced cigarette smoking [33]. Other studies underline the benefit of exercise on lipid profile and cardiovascular risk factors in T1DM patients. In 59 T1DM adolescents, fitness measured by VO2 max during cyclo-ergometry was negatively correlated with A1c levels, insulin dose, triglycerides, total and LDL-cholesterol levels [4]. Lehmann et al. [34] reported that at the end of a 3-month programme of physical exercise performed by 20 T1DM patients under good metabolic control, physical activity levels and the VO2 max increased, while LDL-cholesterol, systolic and diastolic blood pressure, weight and abdominal fat decreased. In agreement with these findings, our data, too, indicated that T1DM patients who met physical activity guidelines or attended sporting activity had triglyceride levels lower than those found in inactive patients. No variation was found in total cholesterol, which indeed is less susceptible to changes than LDL and HDL fractions; unfortunately, these fractions were not measured in our patients. In conclusion, our results indicate that only 25% of young diabetic patients meet the guidelines for healthy physical activity and that less than 50% of them appear to spend time with sporting activity. Participation in organised sports is largely influenced by cultural factors, both in healthy and chronically ill adolescents. Regular practice of moderate to intense physical activity or sports participation is associated with better metabolic control and lipid profile. Within our diabetic adolescent population, particularly the girls are at risk from the effects of low physical activity and should therefore be targeted by educational programmes promoting a more active lifestyle.

Acknowledgements The authors wish to thank Dr Giuseppe Signoriello for his invaluable statistical advice.

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