Obesity and overweight are increasing, both

Paediatrica Indonesiana March ‡ VOLUME 54 NUMBER 2 Original Article Physical activity, eating patterns, and insulin resistance in obesity Emy...
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Paediatrica Indonesiana March ‡

VOLUME 54

NUMBER 2

Original Article

Physical activity, eating patterns, and insulin resistance in obesity Emy Huriyati1, Perdana Samekto Nugroho1, Rina Susilowaty2, Madarina Julia3

Abstract Background Unhealthy eating patterns and physical inactivity DUHDVVRFLDWHGZLWKREHVLW\,QVXOLQUHVLVWDQFHDQHDUO\VLJQRIW\SH GLDEHWHVPHOOLWXVLVFRPPRQLQREHVHLQGLYLGXDOV Objective To assess for an association between physical activity and HDWLQJSDWWHUQVWRLQVXOLQUHVLVWDQFHLQREHVHIHPDOHDGROHVFHQWV Methods 6XEMHFWVZHUHREHVHIHPDOHDGROHVFHQWVDJHG \HDUV3HULSKHUDOEORRGVSHFLPHQVZHUHREWDLQHGIRUPHDVXUHPHQWV of fasting blood glucose, insulin, and the homeostatic model DVVHVVPHQW +20$ LQGH[6XEMHFWVZHUHFRQVLGHUHGWREHLQD VWDWHRILQVXOLQUHVLVWDQFHIRU+20$LQGH[•3K\VLFDODFWLYLW\ UHFDOOVIRU[KZHUHSHUIRUPHGWRREWDLQLQIRUPDWLRQRQVXEMHFWV· energy expenditure, as well as intensity and duration of physical DFWLYLW\'DWDRQQXWULHQWVLQWDNHZDVDOVRREWDLQHGXVLQJ[K IRRGUHFDOOV)DWLQWDNHZDVFDWHJRUL]HGLQWRVDWXUDWHGIDWW\DFLG (SAFA), unsaturated fatty acid (UNSAFA), monounsaturated fatty DFLG 08)$ DQGSRO\XQVDWXUDWHGIDWW\DFLG 38)$  Results 6XEMHFWVVSHQWPRVWRIWKHLUWLPHRQOLJKWDFWLYLWLHV 6' KRXUVGD\7KRVHZLWKLQVXOLQUHVLVWDQFHVSHQWVOLJKWO\PRUH WLPHGRLQJOLJKWDFWLYLWLHV&RQYHUVHO\WKH\VSHQWOHVVWLPHLQYLJRURXV DFWLYLWLHVDPHDQGLIIHUHQFHRI &,WR PLQXWHV GD\ 3  6XEMHFWVZKRVSHQWOHVVWKDQPLQXWHGD\LQKHDY\ DFWLYLWLHVKDGKLJKHURGGVIRULQVXOLQUHVLVWDQFH 25&, WR3  7KHUHZHUHQRUHODWLRQVKLSVIRXQGEHWZHHQ nutrients intake, such as energy, protein, fats (SAFA, UNSAFA, 08)$DQG38)$ RUFDUERK\GUDWHVDQGLQVXOLQUHVLVWDQFH Conclusion In obese female adolescents, physical inactivity is associated with insulin resistance, while nutrients intake LV QRW DVVRFLDWHG ZLWK LQVXOLQ UHVLVWDQFH [Paediatr Indones. 2014;54:82-7.] Keywords: insulin resistance, obesity, physical activity, energy, protein, fat, carbohydrate, female adolescents

82‡Paediatr Indones, Vol. 54, No. 2, March 2014

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besity and overweight are increasing, both LQ GHYHORSHG DQG GHYHORSLQJ FRXQWULHV The prevalence of overweight children LQ WKH 8QLWHG 6WDWHV LQFUHDVHG IURP  LQWKHHDUO\VWRLQ,QWKH$VLD Pacific region, the prevalence of overweight and obesity UDQJHGIURPOHVVWKDQLQ,QGLDWRLQ$XVWUDOLD 7KHSUHYDOHQFHLQ&KLQDZDVRQO\RQHWKLUGWKDWRI $XVWUDOLD EXW D  LQFUHPHQW RI SUHYDOHQFH KDV EHHQREVHUYHGRYHUWKHSDVW\HDUV2 In Indonesia, WKH1DWLRQDO%DVLF+HDOWK5HVHDUFKUHSRUWHGWKDW WKHQDWLRQDOSUHYDOHQFHRIXQGHUILYHVZDVZLWK ZHLJKWIRUKHLJKWVWDQGDUGGHYLDWLRQVFRUHVDERYH ,QDGXOWV •\HDUV WKHSUHYDOHQFHRI%0,DERYH kg/m2 ZDVZLWKDERXWRIWKHVHKDYLQJ FHQWUDO REHVLW\ ZDLVW FLUFXPIHUHQFH RI ! FP IRU PDOHVDQG!FPIRUIHPDOHV $JUHDWHUSUHYDOHQFH RIFHQWUDOREHVLW\ZDVVHHQLQIHPDOHV  FRPSDUHG WRPDOHV  

From the Center for Health and Nutrition, Department of Histology and Cell Biology2, Department of Child Health, Gadjah Mada University 0HGLFDO6FKRRO25 &,WR  3  @ There were no significant differences in energy intake between the two groups, including protein LQWDNH HLWKHU LQ JUDPV RU  HQHUJ\ RU LQ W\SHV RI fats consumed (Table 3  &RUUHODWLRQ DQDO\VLV GLG not reveal associations between intake of calories, protein, fats, or carbohydrates to the HOMA index (Table 4 

Table 1. Clinical and demographic characteristics of subjects Characteristics Mean age (SD), years Mean BMI (SD), kg/m2 Mean HOMA index (SD) Mean fasting insulin (SD), mU/mL Mean fasting glucose (SD), mg/dL

Insulin resistance (n=44) 13.82 (0.85) 30.18 (2.63) 5.25 (3.82) 22.86 (12.10) 91.14 (21.69)

Non-insulin resistance (n=33) 13.56 (0.96) 29.09 (2.40) 2.30 (0.68) 11.13 (3.39) 84.73 (11.02)

Table 2. Pattern of physical activities in subjects with and without insulin resistance

Mean energy expenditure (SD), Mets-min/day Mean duration of heavy activities (SD), min/day Mean duration of medium activities (SD), min/day Mean duration of light activities (SD), hrs/day * Independent sample T-test

84‡Paediatr Indones, Vol. 54, No. 2, March 2014

Insulin resistance Non-insulin resistance Mean difference (95%CI) (n = 44) (n = 33) 1,915.26 (123.87) 1,938.98 (116.15) 27.78 (-31.76 to 79.07) 2.63 (7.34) 7.59 (11.76) 4.96 (0.61 to 9.31) 23.172 (9.40) 30.51 (29.32) 7.34 (-6.13 to 20.81) 23.57 (0.49) 23.38 (0.50) 0.19 (-0.42 to 0.03)

P value* 0.40 0.03 0.28 0.09

Emy Huriyati et al: Physical activity, eating patterns, and insulin resistance in obesity Table 3. Pattern of food intake in subjects with and without insulin resistance

Energy, kcal Fat Total amount intake, g % energy Carbohydrates Total amount intake, g % energy Total protein Total amount intake, g % energy Saturated fatty acids Total amount intake, g % energy Unsaturated fatty acids Total amount intake, g % energy Monounsaturated fatty acids Total amount intake, g % energy Polyunsaturated fatty acids Total amount intake, g % energy

Insulin resistance (n = 44) mean (SD) 1,115.48 (284.36)

Non-insulin resistance (n = 33) mean (SD) 1,179.19 (337.97)

P value

-63.72 (-205.18 to 77.75)

0.37

39.82 (12.45) 32.01 (5.79)

45.10 (15.39) 34.13 (4.64)

-5.28 (-11.60 to 1.05) -2.12 (-4.57 to 0.32)

0.10 0.09

150.25 (43.01) 53.85 (6.48)

152.46 (44.13) 51.96 (5.33)

-10.02 (-22.16 to 17.74) 1.89 (-0.79 to 4.57)

0.83 0.18

39.10 (10.17) 14.20 (2.43)

41.21 (13.41) 13.96 (2.10)

-2.11 (-7.46 to 3.24) 0.24 (-0.81 to 1.30)

0.44 0.65

17.65 (7.88) 13.80 (3.50)

18.79 (6.77) 14.63 (3.57)

-1.14 (-4.55 to 2.27) -0.83 (-2.45 to 0.80)

0.51 0.31

17.42 (5.98) 13.81 (3.05)

17.95 (5.33) 14.23 (3.33)

-0.54 (-3.16 to 2.08) -0.42 (-1.88 to 1.03)

0.68 0.56

10.17 (3.63) 8.06 (1.97)

10.73 (2.97) 8.50 (1.66)

-0.56 (-2.10 to 0.98) -0.43 (-1.28 to 0.41)

0.47 0.31

7.25 (3.11) 5.75 (1.91)

7.23 (2.90) 5.74 (2.11)

0.02 (-1.37 to 1.41) 0.01 (-0.90 to 0.93)

0.98 0.98

Table 4. Pearson’s correlation of energy intake vs. HOMA index Pattern of energy intake Energy intake, kcal % energy from protein % energy from fat % energy from unsaturated fat % energy from saturated fat % energy from carbohydrates

Mean difference (95%CI)

r -0.17 0.04 -0.14 -0.03 -0.12 0.09

HOMA P value 0.15 0.74 0.23 0.78 0.29 0.39

Discussion :H IRXQG D KLJKHU SUHYDOHQFH   RI LQVXOLQ resistance in obese adolescents than that observed  LQ)UHQFKDGROHVFHQWV Although daily energy expenditure did not VLJQLILFDQWO\GLIIHUEHWZHHQWKHLQVXOLQDQGQRQLQVXOLQ resistant groups, we observed that subjects with insulin resistance had, on average, a shorter duration of heavy intensity activities compared to those without LQVXOLQ UHVLVWDQFH $Q $PHULFDQ VWXG\ VKRZHG D significant, positive correlation between daily energy expenditure and insulin sensitivity, as assessed by a euglycemic insulin clamp, a more accurate method

WRDVVHVVLQVXOLQVHQVLWLYLW\WKDQWKH+20$LQGH[ However, that method is impractical for use in an HSLGHPLRORJLFDOVWXG\ Physical exercise lowers fasting insulin levels and increases insulin sensitivity through increased glucose transport into muscle cells and increased glycogen deposits in muscles to replace the glycogen ORVWLQH[HUFLVH$QRWKHUEHQHILFLDOHIIHFWRISK\VLFDO H[HUFLVHLVWKHLQFUHDVHLQIDWIUHHPDVVWKDWLQFUHDVHV PXVFOH YROXPH DQG JOXFRVH WUDQVIHU WR PXVFOHV :HLJKWORVVGXHWRSK\VLFDODFWLYLW\GHFUHDVHVLQVXOLQ UHVLVWDQFHLQREHVHDGROHVFHQWV As a result, physical LQDFWLYLW\ ZDV DVVRFLDWHG ZLWK LQVXOLQ UHVLVWDQFH Although not statistically significant, we observed that subjects with insulin resistance had longer GXUDWLRQVRIVHGHQWDU\DFWLYLWLHV A study reported the association between energy intake and insulin resistance, suggesting that that a negative energy balance would increase insulin VHQVLWLYLW\ However, we found no significance difference in energy intake between the insulin UHVLVWDQWDQGQRQLQVXOLQUHVLVWDQWJURXSV Protein intake, in this case, high protein intake, can GHFUHDVHJOXFRVHUHVSRQVH$VWXG\RQK\SHULQVXOLQHPLF obese men and women showed a significant glucose

Paediatr Indones, Vol. 54, No. 2, March 2014‡85

Emy Huriyati et al: Physical activity, eating patterns, and insulin resistance in obesity

UHVSRQVHZLWKDKLJKSURWHLQGLHW SURWHLQ IDWDQGFDUERK\GUDWH FRPSDUHGWRDVWDQGDUG GLHW SURWHLQIDWDQGFDUERK\GUDWH ,Q our study, protein intake did not correlate with insulin UHVLVWDQFH3URWHLQFRQWDLQLQJIRRGVVWLPXODWHLQVXOLQ E\GLIIHUHQWPHDQV/DYLJQHet alIRXQGDFRUUHODWLRQ EHWZHHQ SURWHLQ LQWDNH DQG LQVXOLQ VHQVLWLYLW\ &RG protein prevented insulin resistance in muscles of obese rats, as cod protein has a higher glucose disposal rate FRPSDUHG WR WKDW RI FDVHLQ DQG VR\ SURWHLQ Milk and whey have an ability to rapidly increase insulin secretion, despite causing a low glucose response JO\FHPLFLQGH[ LQVXOLQHPLFLQGH[   :HGLGQRWREVHUYHDQ\DVVRFLDWLRQEHWZHHQIDWRU carbohydrate intake and insulin resistance, neither in absolute amounts nor in percentage of energy derived IURPIDWRUFDUERK\GUDWHV9HVVE\et al compared a saturated fatty acid diet to a monounsaturated fatty DFLGGLHW 6$)$GLHWHQHUJ\08)$GLHW HQHUJ\38)$HQHUJ\  08)$GLHWVDWXUDWHG IDWW\DFLGHQHUJ\PRQRXQVDWXUDWHGIDWW\DFLG HQHUJ\SRO\XQVDWXUDWHGIDWW\DFLG 7KH6$)$GLHW caused a decrease in the insulin sensitivity index (Si) RI 3 EXWWKH6LUHPDLQHGWKHVDPHIRU WKRVHRQWKH08)$GLHWPrevious studies have shown that type of fat consumed daily affected serum lipid FRQFHQWUDWLRQ3DWLHQWVZLWKW\SHGLDEHWHVPHOOLWXV had a larger proportion of saturated fatty acid and lower OLQROHLFDFLGFRPSDUHGWRQRUPDOLQGLYLGXDOV'LHWDOVR affected the composition of fatty acid in muscles, which is also influenced by physical activity and muscle fiber FRPSRVLWLRQ Insulin sensitivity is determined by fat oxidative FDSDFLW\$FFXPXODWLRQRIIDWW\DFLGPHWDEROLWHVLQWKH cytosol, such as diacylglycerol and ceramide, disturbs WKH ILUVW VWHS LQ LQVXOLQ VLJQDOLQJ 'LDF\OJO\FHURO inhibits early signaling events through promoting serin phosphorylation from Insulin receptor substrate  ,56 ZKLOHFHUDPLGHLVNQRZQWRLQKLELWLQVXOLQ VWLPXODWLRQ WR $NW SURWHLQ NLQDVH %  ,Q DFWLYH individuals, an increase in the ability to oxidize muscle fat and fatty acid metabolites while exercising, is recognized as an important factor in the association between muscular fat oxidative capacity and insulin VHQVLWLYLW\22 In conclusion, we observe that longer duration of heavy intensity physical activity is associated with EHWWHULQVXOLQVHQVLWLYLW\,QREHVHIHPDOHDGROHVFHQWV

86‡Paediatr Indones, Vol. 54, No. 2, March 2014

physical inactivity is associated with insulin resistance, while no association is found between nutrients intake ZLWKLQVXOLQUHVLVWDQFH

References  /HGHUPDQ6$$NDEDV650RRUH%-(GLWRUV·RYHUYLHZRI WKHFRQIHUHQFHRQSUHYHQWLQJFKLOGKRRGREHVLW\3HGLDWULFV   $VLD3DFLILF&RKRUW6WXGLHV&ROODERUDWLRQ7KHEXUGHQRI RYHUZHLJKWDQGREHVLW\LQWKH$VLD3DFLILFUHJLRQ2EHV5HY   5HSRUWRQQDWLRQDOEDVLFKHDOWKUHVHDUFK 5LVNHVGDV -DNDUWD Institute of Research and Development (Badan Penelitian dan Pengembangan Kesehatan), Ministry of Health, Republic RI,QGRQHVLDS  6KDUPD$0&KHWW\972EHVLW\K\SHUWHQVLRQDQGLQVXOLQ UHVLVWDQFH$FWD'LDEHWROV  +XDQJ 3/ $ FRPSUHKHQVLYH GHILQLWLRQ IRU PHWDEROLF V\QGURPH'LV0RGHO0HFK  0F.HRZQ 10 0HLJV -% /LX 6 6DOW]PDQ ( :LOVRQ 3: -DFTXHV3)&DUERK\GUDWHQXWULWLRQLQVXOLQUHVLVWDQFHDQG the prevalence of the metabolic syndrome in the Framingham 2IIVSULQJ&RKRUW'LDEHWHV&DUH  9HVVE\%8XVLWXSD0+HUPDQVHQ.5LFFDUGL*5LYHOOHVH AA, Tapsell LC, et al 6XEVWLWXWLQJ GLHWDU\ VDWXUDWHG IRU monounsaturated fat impairs insulin sensitivity in healthy PHQ DQG ZRPHQ WKH .$1:8 VWXG\ 'LDEHWRORJLD   -DQVVHQ , /HEODQF $* 6\VWHPDWLF UHYLHZ RI WKH KHDOWK EHQHILWV RI SK\VLFDO DFWLYLW\ DQG ILWQHVV LQ VFKRRODJHG FKLOGUHQ DQG \RXWK ,QW - %HKDY 1XWU 3K\V $FW    )HUJXVRQ 0$ *XWLQ % /H 1$ .DUS : /LWDNHU 0 Humphries M, et al (IIHFWV RI H[HUFLVH WUDLQLQJ DQG its cessation on components of the insulin resistance V\QGURPHLQREHVHFKLOGUHQ,QW-2EHV5HODW0HWDE'LVRUG   %HOO/0:DWWV.6LDIDULNDV$7KRPSVRQ$5DWQDP1 Bulsara M, et al([HUFLVHDORQHUHGXFHVLQVXOLQUHVLVWDQFH in obese children independently of changes in body FRPSRVLWLRQ-&OLQ(QGRFULQRO0HWDE  .XF]PDUVNL5-2JGHQ&/*XR66*UXPPHU6WUDZQ/0 Flegal KM, Mei Z, et al&'&JURZWKFKDUWVIRUWKH 8QLWHG6WDWHVPHWKRGVDQGGHYHORSPHQW1DWLRQDO&HQWHU IRU +HDOWK 6WDWLVWLFV 9LWDO +HDOWK 6WDW  ² 

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