ORIGINAL ARTICLES / Prace oryginalne Pediatric Endocrinology, Diabetes and Metabolism 2009, 15, 4, 240-245 ISSN 1234-625X Blood pressure in children and adolescents with type 1 diabetes mellitus the influence of body mass index and fat mass Ciśnienie tętnicze u dzieci i młodzieży z cukrzycą typu 1 wpływ wskaźnika masy ciała i masy tkanki tłuszczowej Iwona Pietrzak, Beata Mianowska, Anna Gadzicka, Wojciech Młynarski, Agnieszka Szadkowska Department of Pediatrics, Oncology, Hematology and Diabetology Medical University of Lodz, Poland Klinika Pediatrii, Onkologii, Hematologii i Diabetologii Uniwersytetu Medycznego w Łodzi Address for correspondence: Iwona Pietrzak MD, PhD Klinika Pediatrii, Onkologii, Hematologii i Diabetologi, I Katedra Pediatrii Uniwersytetu Medycznego w Łodzi ul. Sporna 36/50; 91-738 Łódź; Poland; tel.: (+48 42) 617 77 50; e-mail: iwona.pietrzak@vp.pl Abstract Introduction: Prevalence of arterial hypertension and prehypertension in children and adolescents with type 1 diabetes mellitus is higher than in healthy people, even when diabetic nephropathy symptoms (microalbuminuria) in these patients are not detected. Aim of the study: To estimate the influence of body mass and body composition on blood pressure in children and adolescents with type 1 diabetes mellitus. Material and methods: In 164 patients (M 92, F 72), aged 14.8±2.4 years, with diabetes duration 6.0±4.2 years, body weight, height, casual blood pressure, and c level were measured. Body composition (fat mass %FAT) was determined by bioimpedance analysis. Body mass index (BMI) and daily dose of insulin were calculated. Results: Based on BMI value obesity was diagnosed in 8 (4.9%) and overweight in 37 (22.6%) patients. In multivariate analysis we a found positive correlation between systolic blood pressure (SBP) with BMI and %FAT and between diastolic blood pressure (DBP) with BMI and %FAT. Patients with BMI within normal range had the lowest value of SBP. DBP in patients with normal BMI value was lower than in overweight subjects. No differences of SBP and DBP between overweight and obese patients were noted. DBP value increased from the lower to the upper quartile of %FAT. No significant correlation was found between SBP and the quartile value of %FAT. Conclusion: There is a significant association between body mass index and body fat mass with blood pressure level in children and adolescents with type 1 diabetes mellitus. KEY WORDS: type 1 diabetes mellitus, blood pressure, fat mass, children Streszczenie Wprowadzenie: Występowanie cukrzycy typu 1 u dzieci i młodzieży związane jest z wyższymi wartościami ciśnienia tętniczego oraz częstszym występowaniem nadciśnienia tętniczego i stanu przednadciśnieniowego, nawet przy braku mikroalbuminurii uznanego wskaźnika cukrzycowej choroby nerek. Cel pracy: Ocena wpływu zawartości tkanki tłuszczowej na kształtowanie się wartości ciśnienia tętniczego u dzieci i młodzieży z cukrzycą typu 1. Materiał i metody: Badaniami objęto 164 (72 dziewczynki, 92 chłopców) chorych na cukrzycę typu 1 w wieku średnio 14,8±2,4 roku i z czasem trwania choroby średnio 6,0±4,2 roku. Zmierzono wzrost i masę ciała, obliczono wskaźnik masy ciała (BMI). Oznaczono zawartość tkanki tłuszczowej (%FAT) metodą bioimpedancji elektrycznej. Przeprowadzono pomiar ciśnienia tętniczego automatycznym manometrem i oznaczenie odsetka c metodą wysokociśnieniowej chromatografii przepływowej. Obliczono dobowe zapotrzebowanie na insulinę. Wyniki: W oparciu o wartość BMI otyłość rozpoznano u 8 (4,9%), a nadwagę u 37 (22,7%) badanych. 119 (72,4%) pacjentów miało prawidłową masę ciała. Po adjustacji do wieku i płci odnotowano dodatnią korelację pomiędzy średnimi wartościami skurczowego ciśnienia tętniczego (SBP) i rozkurczowego ciśnienia tętniczego (DBP) a BMI i %FAT. Średnia wartość SBP była najniższa wśród osób z prawidłową masą ciała. Chorzy z otyłością nie różnili się statystycznie istotnie od pacjentów z nadwagą pod względem średnich wartości SBP. Osoby z prawidłową masą ciała cechowały się niższą średnią wartością DBP niż osoby z nadmierną masą ciała. Nie odnotowano statystycznie istotnej różnicy pod względem średniej wartości DBP między grupą z otyłością i grupą z nadwagą. Średnia wartość SBP wykazywała tendencję wzrostową w kierunku od najniższego do najwyższego kwartyla %FAT, różnica między poszczególnymi kwartylami nie była jednak istotna statystycznie. Średnia wartość DBP rosła wraz ze wzrostem kwartyla %FAT i była statystycznie istotnie niższa w najniższym kwartylu niż w kwartylu najwyższym. Wnioski: U dzieci i młodzieży z cukrzycą typu 1 wartość ciśnienia tętniczego zależy od wskaźnika masy ciała i odsetka tkanki tłuszczowej w organizmie. SŁOWA KLUCZOWE: cukrzyca typu 1, ciśnienie tętnicze, tkanka tłuszczowa, dzieci 240 Introduction Hypertension and diabetes are the most common diseases, they often occur together. High blood pressure, occurring in about a half of diabetic patients, worsens prognosis and is an important risk factor of their early death. In the type 1 diabetic patients, high blood pressure occurs in most of cases due to diabetic renal disease; primary hypertension is very rare (1, 2).
Pietrzak I., Mianowska B., Gadzicka A. i wsp. Ciśnienie tętnicze u dzieci i młodzieży z cukrzycą typu 1... In diabetic children and adolescents, the relation between diabetes and higher blood pressure values was noted. In the diabetic group of patients the prevalence of hypertension and prehypertension is more frequent than in healthy children (3, 4). Studies conducted in type 1 children and adolescents have showed that the increase in blood pressure values can precede microalbuminuria, appreciated marker of diabetic renal disease (5). Moreover, elevated blood pressure contributes to existence and development of chronic diabetes complications microand macroangiopathy (2, 3, 6). These are the reasons to perform the investigation of hypertension risk factors in type 1 diabetic children and adolescents. It is known that there is the relationship between blood pressure values and fat tissue. The fat tissue may influence by its pressive mechanisms such as hemodynamic disturbances, insulin resistance and hyperinsulinemia, activation of sympathetic system, sodium retention and biologically active adipocytes products (7). Among healthy children, a significant positive correlation between body fat and blood pressure values was found (8-10). Research conducted in diabetic adolescents also shows the role of body fat in the pathogenesis of hypertension. Hypertension occurs more commonly in type 2 diabetic adolescents than in their peers with type 1 diabetes as it is associated with a higher rate of obesity in this group of patients (11). Whereas our own and other authors observations indicate higher body fat indexes in type 1 diabetic children and adolescents than in the general population (12). Body mass index is widely used as an indicator of overweight and obesity. However, it does not let to assess body composition (fat and lean mass). It could be gained with the use of bioimpedance (bioimpedance analysis BIA), a non-invasive, easy method that lets to assess body fat mass (13, 14). There are relatively few studies about the impact of body fat on blood pressure values in type 1 diabetic patients in the developmental age. Aim of the study The estimation of the body fat impact on blood pressure values in type 1 diabetic children and adolescents. Material and methods Study group Type 1 diabetic children and adolescent patients of Diabetology Outpatient Clinic of University Clinical Hospital No. 4 of Medical University of Lodz were examined. All the following patients who came for the follow-up examination to the diabetology department between November 2007-March 2009 and fulfilled inclusion criteria (age 10-18 years, diabetes duration >0.5 year) were included into the study. The patients suffering from acute or chronic diseases that can influence the results of the study were excluded. Moreover, presence of chronic microangiopathic diabetes complications was an exclusion criterion. Data of 164 patients (72 girls and 92 boys) at the mean age of 14.8±2.4 years and with mean diabetes duration 6.2±4.2 years were analyzed. All children were treated by intensive insulin therapy: 96 using a multiple insulin injections regimen, 68 undergoing treatment with continuous subcutaneous insulin infusion. The study protocol was approved by the Ethical Committee of the Medical University of Lodz. Informed consent was obtained from parents and informed assent from the children. Height and weight measurement was performed with medical scales and anthropometer in the morning in fasting state in light clothes. Weight was measured with the 100 g and height with 0.5 cm accuracy. Body mass index (BMI) was calculated. Overweight and obesity were diagnosed according to International Obesity Task Force criteria (15). Fat mass content (FAT) was measured with electrical bioimpedance with the use of eight electrode scales TGF-410GS Body Analyzer (Tanita, Japan). Blood pressure was measured three times after 5-minute rest in the sitting position on both upper limbs with the use of automatic manometer (Omron M4 Plus, Omron Healthcare Europe, Hoofddorp, Holland). The mean value of the second and the third measurement was calculated. The measurements taken on the dominant limb were analyzed. Because the mean blood pressure value from measurements taken during one follow-up visit was calculated we resigned from classifying patients into groups with normal blood pressure, prehypertension and hypertension. c was measured with high-pressure liquid chromatography method (HPLC) with the use of Variant (BioRad Laboratories, Marnes-la-Coquette, Germany). Daily insulin requirement was estimated according to patients medical documentation. Statistical analysis The results were entered into the database and transferred to Statistica 7.0 to perform further analysis. Shapiro-Wilk test was used to determine whether the distribution of preliminary quantity variables was normal. Group comparisons were performed with the use of non-parametric variance analysis (ANOVA). Pearson correlation coefficient was calculated to evaluate the dependence of two quality variables and, in the case of adjustment towards other variables, multiple regression analysis was performed. A p <0.05 was considered statistically significant. Results The characteristics of studied parameters are shown in table I. Lower systolic blood pressure values were observed among girls than boys. Diastolic blood pressure values were comparable in both sexes (tab. II). A positive correlation between diastolic blood pressure (DBP) and patient age and diabetes duration was found. However, systolic blood pressure (SBP) depended only on the patient s age (tab. III). There was no relation between mean blood pressure values and daily insulin requirement and diabetes metabolic control (tab. III). According to BMI obesity was diagnosed in 8 (4.9%) and overweight in 37 (22.7%) patients; 119 (72.4%) individuals had normal body mass. There was a positive correlation between body mass index and body fat (%FAT) (β=0.79; p <0.0001; adjusted to sex and age). Moreover, BMI but not %FAT values correlated positively with the patients age and c (tab. IV). There was no relation between daily insulin dose and any body fat parameter (tab. IV). 241
Szadkowska A., Pietrzak I., Szlawska J. et al. Blood pressure in children and adolescents with type 1 diabetes mellitus... Pediatric Endocrinology, Diabetes and Metabolism 2009, 15, 4 Table I: Clinical characteristics of the study group Table I: Charakterystyka kliniczna badanej grupy Parameter Parametr Mean±SD Średnia±SD Ranges Zakresy Age [years] / Wiek [lata] 14.8±2.4 10.0-18.0 Duration of diabetes [years] Czas trwania cukrzycy [lata] 6.1±4.2 0.5-15.2 Daily dose of insulin [j./kg/d] Dzienna dawka insuliny 0.95±0.32 0.05-1.79 c [%] 8.0±1.5 5.3-13.9 Height [cm] / Wysokość 164.7±12.0 134-195 Weight [kg] / Waga 59.3±15.1 29.4-103.7 Body mass index (BMI) [kg/m 2 ] 21.5±3.8 14.7-33.0 Systolic blood pressure SBP [mmhg] 118±15 86-161 Diastolic blood pressure DBP [mmhg] 70±10 45-98 Body fat [%] %FAT Zawartość tłuszczu w organizmie [%] 21.9±7.1 9.5-43.5 After performing multiple regression analysis with adjusting to sex and age, a positive correlation between mean systolic and diastolic blood pressure values and BMI was found. Similar statistically significant relation occurred between mean SBP and DBP values and percentage of body fat (tab. V). Mean blood pressure values in groups of patients with obesity, overweight and normal body mass were assessed. Mean SBP value was the lowest in patients with normal body mass. There was no statistically significant difference in mean SBP values between patients with obesity and overweight (fig. 1). Mean DBP value was lower in individuals with normal than with excessive body mass. There was no statistically significant difference in mean DBP values between patients with obesity and overweight (fig. 2). Mean SBP values distribution in following %FAT quartiles was analyzed. Mean SBP values increased from the lower to the upper %FAT quartile, however the difference between particular quartiles was not statistically significant (fig. 3). Mean DBP values increased with the increase in %FAT quartile. There was a statistically significant difference between the lower and upper quartile (fig. 4). Discussion Hypertension occurs in diabetic patients 2-3 times more often than in the general population. Higher blood pressure leads to Table II: Comparison of blood pressure in girls and boys Tabela II: Porównanie wartości ciśnienia tętniczego u dziewcząt i chłopców Table IV: Correlation between body mass index (BMI), %FAT and age, duration of disease, c, daily insulin dose Tabela IV: Zależności między BMI (body mass index), %FAT i wiekiem, czasem trwania choroby, c oraz dzienną dawką insuliny Girls Boys p Parameter / Parametr Body mass index Body fat [%] Dziewczęta Chłopcy Systolic blood pressure 114.6±9.5 121±15.1 0.044 Age r=0.47 r=0.09 Wiek p=0.269 Diastolic blood pressure 69.8±9.5 69.6±9.5 0.36 Duration of diabetes* β=0.03 β=0.06 Czas trwania cukrzycy p=0.714 p=0.493 Table III: Correlation between blood pressure and age, duration of disease, c, daily insulin dose Tabela III: Zależności między ciśnieniem krwi i wiekiem, czasem trwania choroby, c oraz dzienną dawką insuliny Daily dose of insulin r=0.05 Dzienna dawka insuliny p=0.535 c r=0.19 p=0.018 * adjusted to age / dostosowane do wieku r=-0.05 p=0.505 r=0.09 p=0,278 Parameter Parametr Age Wiek Systolic blood pressure r=0,40 Diastolic blood pressure r=0.47 Table V: Correlation between systolic blood pressure, diastolic blood pressureand body mass index, %FAT Tabela V: Zależności między ciśnieniem skurczowym, rozkurczowym oraz BMI (body mass index) i %FAT Duration of diabetes * β=0,04 β=0,17 Parameter Systolic blood pressure Diastolic blood pressure Czas trwania cukrzycy p=0,614 p=0,026 Parametr Daily dose of insulin r=0,10 r=0,05 BMI* β=0.37 β=0.28 Dzienna dawka insuliny p=0,212 p=0,505 c r=-0,03 r=-0,05 Body fat [%]* β=0.23 β=0.29 p=0,666 p=0,524 p=0.004 242 * adjusted to age / dostosowane do wieku * adjusted to sex and age / dostosowane do płci i wieku
Pietrzak I., Mianowska B., Gadzicka A. i wsp. Ciśnienie tętnicze u dzieci i młodzieży z cukrzycą typu 1... diabetic macro- and microangiopathy. Type 1 diabetic children and adolescents have higher blood pressure values and they have hypertension or prehypertension more often in comparison with their healthy peers (3, 4). The relation of pathogenesis of diabetes and hypertension is still a subject of many research. Among pressive factors taking part in the pathogenesis of hypertension in diabetic patients, excessive body mass and associated body fat influence are mentioned. Despite more common occurrence of overweight and obesity in type 1 diabetic children and adolescents, not much is known about their relation with hypertension (2, 16, 17). In this study, the relation between BMI and body fat and blood pressure values in type 1 diabetic children and adolescents was shown. According to BMI in the presented study, obesity was found in 4.88% and overweight in 22.56% of subjects. Schwab et al., examined 27 358 type 1 diabetic patients from Austria and Germany at the age of 0.25-26 years, estimated excessive body mass occurrence (BMI >90 pc) as 16.4 to 25% dependent on age group (18). Meanwhile, in general school age population estimated in the Kiel Obesity Prevention Study in Germany, overweight and obesity were found in 7.2-11% of subjects (9). In the USA, 18% of school age children suffer from obesity and other 18% from overweight (19). In the presented study, a positive correlation between age and indexes describing body mass and body fat content was shown. There is also a positive correlation between hypertension, BMI and the patients age. This relation is well known, illustrated by growth charts and proved in many clinical studies (20-23). Body fat measured with bioimpedance is an age function. According to some studies, it is also dependent on sex, puberty phase and ethnicity (13, 14, 21, 24). SBP [mmhg] 140 138 136 134 132 130 128 126 124 122 120 118 116 114 112 110 F(2, 159)=6.2178, p=0.003 0 1 2 0=normal body mass / prawidłowa masa ciała 1=overweight / nadwaga 2=obesity / otyłość SBP systolic blood pressure / skurczowe ciśnienie tętnicze Fig. 1. SBP in children with normal body mass, overweight and obesity Ryc. 1. Wartości SBP u dzieci z prawidłową masą ciała, nadwaga i otyłością DBP [mmhg] 82 80 78 76 74 72 70 68 66 64 F(2, 159)=2.4305, p=0.091 0 1 2 0=normal body mass / prawidłowa masa ciała 1=overweight / nadwaga 2=obesity / otyłość DBP diastolic blood pressure / rozkurczowe ciśnienie tętnicze Fig. 2. DBP in children with normal body mass, overweight and obesity Ryc. 2. Wartości DBP u dzieci z prawidłową masą ciała, nadwaga i otyłością SBP [mmhg] 130 128 126 124 122 120 118 116 114 112 110 108 106 F(3, 158)=3.2950, p=0.022 1 2 3 4 %FAT - quartiles / kwartyle SBP systolic blood pressure / skurczowe ciśnienie tętnicze Fig. 3. SBP in children in %FAT quartiles Ryc. 3. Porównanie SBP pomiędzy kwartylami %FAT DBP [mmhg] 80 78 76 74 72 70 68 66 64 62 60 F(3, 158)=4.5846, p=.00417 1 2 3 4 FAT% - quartiles / kwartyle DBP diastolic blood pressure / rozkurczowe ciśnienie tętnicze Fig. 4. DBP in children in %FAT quartiles Ryc. 4. Porównanie DBP między kwartylami %FAT 243
Szadkowska A., Pietrzak I., Szlawska J. et al. Blood pressure in children and adolescents with type 1 diabetes mellitus... Pediatric Endocrinology, Diabetes and Metabolism 2009, 15, 4 244 The results of our own investigations are compatible with other authors observations, which proved BMI influence on blood pressure values. Overweight and obese children and adolescents had higher blood pressure values and, as proved in the literature, hypertension and prehypertension occurred among them more often in comparison with subjects with normal weight (8, 22, 23, 25). According to Guimaraes and al., SBP and DBP were increased (>90 percentile) respectively in 46.5% and 42% obese boys and 39.3% and 44% obese girls. The increase in BMI for 1 unit caused 1.198 mmhg increase in SBP. McCarthy et al. showed that more than a half of adolescents (11-14 years old) with hypertension or prehypertension is overweight (25). In diabetic children and adolescent population, it was shown that hypertension occurs almost twice more often in type 2 than in type 1 diabetic patients, depicting more common obesity occurrence in the first patient group (11). BMI is a commonly accepted as easily available indicator of overweight and obesity. It is used as a relative body fat marker because the increase in body fat is accompanied by the increase in BMI. It should be remembered that BMI depends directly on body mass that consists of not only fat but also muscle mass. In children and adolescents proportion in fat and fat free mass depends on sex and is changing with age and puberty phase (13, 21). In boys, there is an increase in percentage of body fat up to about 11 year of age and then a slow decrease, however, in girls relative body fat increases constantly and growth rate decreases after 10 year of age (13). There is a risk of diagnosing overweight or obesity according to BMI in individuals with a lot of muscle mass (14). Recently a bioimpedance method has been used successfully to estimate body fat. This easy, non-invasive and relatively cheap method allows measuring fat mass (FM) and its distribution, total body water (TBW) and lean mass (LM). Results received with the bioimpedance analysis are comparable to these from more technically advanced radiological method (dual-energy X-ray absorptiometry DXA) (14). In this study a positive correlation between fat mass and blood pressure values in type 1 diabetic children and adolescents was proved. Drożdż et al., in the group of 193 healthy children at the age of 8-16 years found that the increase in fat mass measured with the use of bioimpedance is accompanied by the increase in SBP and DBP values (10). There was a statistically significant difference in fat mass in groups with blood pressure values: <50 pc, >50 pc and <95 pc, >95 pc (respectively SBP 14 vs. 16.8 vs. 30.2%; p<0.01; DBP 13 vs. 15.3 vs. 23.2%; p<0.01). Similar observation was found with fat mass radiological estimation. SDP and DBP values correlated positively with body fat in 152 patients at the age of 3-12 years (26). In the group of more than 7300 children it was noticed that in slim boys at the age of 9-11 years increased fat mass was accompanied by more common hypertension occurrence. In adolescents with normal BMI the increase in fat mass was accompanied by SBP increase (9). Authors pointed out the need of simultaneous measurement of a few anthropometric parameters and use of other than BMI fat mass estimation. The citied studies prove our own observation showing coexistence of higher blood pressure values and excessive body mass, especially increased fat mass. More common overweight and hypertension occurrence in type 1 diabetic children and adolescents and adverse influence of fat mass and higher blood pressure on chronic diabetes complications should stimulate to perform studies concerning the pathogenetic relation between blood pressure and fat mass. The acquired results in this topic could help to create some advice concerning complex diabetes treatment and its chronic complications prophylaxis. Conclusion In type 1 diabetic children and adolescents, blood pressure values depend on BMI and fat mass. This is a preliminary study. It is necessary to continue the research study to establish the influence of not only amount but also the distribution of fat tissue and its biological activity on blood pressure in type 1 diabetic children and adolescents. Supported by research grant of Ministry of Science and Higher Education No. NN 407 187836 and NN 402 279134. References 1. Wingard D.L., Barrett-Connor E.: Heart disease and diabetes. 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