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Paediatrica IndonesianaVOLUME 53 NUMBER 4 July

Original Article

Paediatr Indones, Vol. 53, No. 4, July 2013187

Obesity as a risk factor for

dengue shock syndrome in children

Maria Mahdalena Tri Widiyati, Ida Safitri Laksanawati, Endy Paryanto Prawirohartono

AbstractBackground Dengue hemorrhagic fever (DHF) leads to high

morbidity and mortality if not be treated properly and promptly.

Obesity may play a role in the progression of DHF to dengue shock

syndrome (DSS) and could be a prognostic factor.

Objective To evaluate childhood obesity as a prognostic factorfor DSS.

Methods We reviewed medical records of patients with DHF

and DSS admitted to Department of Child Health, Dr. Sardjito

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6XEMHFWVZHUHDJHGOHVVWKDQ\HDUVDQGIXOILOOHG:+2FULWHULD

IRU'+)RU'667KHH[FOXVLRQFULWHULDZHUHWKHGHQJXH

fever, a milder form of disease, or other viral infections. Riskfactors for DSS were analyzed by logistic regression analysis.

Results2ISDWLHQWVZKRPHWWKHLQFOXVLRQFULWHULDWKHUHZHUH'66SDWLHQWVDVWKHFDVHJURXSDQG'+)SDWLHQWV

DVWKHFRQWUROJURXS8QLYDULDWHDQDO\VLVUHYHDOHGWKDW

ULVNIDFWRUVIRU'66ZHUHREHVLW\25&,WR

VHFRQGDU\LQIHFWLRQW\SH25&,WRSODVPDOHDNDJHZLWKKHPDWRFULWLQFUHDVH!25&,

WRSODWHOHWFRXQW/25&,WR

DQGLQDGHTXDWHIOXLGPDQDJHPHQWIURPSULRUKRVSLWDOL]DWLRQ

25&,WR %\PXOWLYDULDWH DQDO\VLV

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Conclusion Obesity is not a risk factor for DSS, while plasma

OHDNDJHZLWKKHPDWRFULWLQFUHDVH!LVDVVRFLDWHGZLWK'66

[Paediatr Indones. 2013;53:187-92.].

Keywords: dengue hemorrhagic fever, dengue shock

syndrome, obesity

From the Department of Child Health, Gadjah Mada University Medical6FKRRO'U6DUGMLWR+RVSLWDO<RJ\DNDUWD,QGRQHVLD

Reprint requests to: Maria Mahdalena Tri Widiyati, Department of Child

+HDOWK*DGMDK0DGD8QLYHUVLW\0HGLFDO6FKRRO'U6DUGMLWR+RVSLWDO -DODQ.HVHKDWDQ1R6HNLS<RJ\DNDUWD,QGRQHVLD7HO

)D[(PDLOZLGLQD\D#\DKRRFRP

Dengue infection is a disease endemic to

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of patients.,WLVDYLUDOGLVHDVHZLWKKLJK

morbidity and mortality in children aged less than

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years. The prevalence of morbidity and mortality

of dengue hemorrhagic fever (DHF) varies across

regions, mainly due to differences in age status of the

population, vector density, spread rate of Dengue virus,Dengue viral serotype prevalence, and meteorological

conditions.5

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factors for dengue shock syndrome (DSS), in order to

provide proper and prompt treatment, thus decreas

ing mortality due to DHF. Risk factors predicted to

be associated with DSS were obesity, platelet count

/ plasma leakage with hematocrit in

FUHDVH!secondary infection,DQGLQDGHTXDWH

fluid management from prior hospitalization.

Theoretically, increase production of interleukin

,/,/DQGWXPRUQHFURVLVIDFWRUA71)A)

mediator in obese patients may have an association

7/27/2019 53-4-1


Maria MT. Widiyati et al: Obesity as a risk factor for dengue shock syndrome

188Paediatr Indones, Vol. 53, No. 4, July 2013

with DSS, due to progressive plasma leakage in

DHF. Previous studies have reported that obesity

contributes to the occurrence of DSS. However,

it is still unclear if obese children are at higher risk

RIGHYHORSLQJPRUHVHYHUH'+)LH'66WKDQQRQ

obese children. The aim of this study was to evaluate

obesity as a risk factor for DSS in children.

Methods

We assessed the possibility of obesity as a risk factor

IRUGLVHDVHVHYHULW\ LQ'66DQGQRQ'66SDWLHQWV

6XEMHFWVZHUHDJHGOHVVWKDQ\HDUVIXOILOOHG:+2

FULWHULDIRU'+)RU'66DQGZHUHDGPLWWHG

to the Department of Child Health at Dr. Sardjito+RVSLWDO<RJ\DNDUWDIURP-XQHWR)HEUXDU\

:HH[FOXGHGSDWLHQWVZLWKGLDJQRVHVRIGHQJXHIHYHU

or other viral infections.

Subjects were divided into two groups. The

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RU,,SRVLWLYHWRXUQLTXHWWHVWGD\VRIIHYHUSODWHOHW

FRXQWPP3, and positive signs of plasma

leakage such as increased hematocrit, or having

pleural effusion, or ascites. The case group included

SDWLHQWVGLDJQRVHGZLWK'+)JUDGH,,,RU,9ZKRPHW

WKHDERYHFULWHULDRI'+)JUDGH,RU,,SOXVVLJQVRIshock, such as weak pulse, narrowing pulse pressure,

poor tissue perfusion, clammy skin, and decreased

urine output.

Sample size was calculated based on the formula

IRUDQ XQSDLUHG FDVHFRQWURO VWXG\ in which the

SURSRUWLRQRIWKHHIIHFWRQWKHFRQWURO3ZDV

FOLQLFDOO\VLJQLILFDQWZKHQRGGVUDWLRV25ZDVAZDV=ADQGBZDV=B

7KHPLQLPXPVXEMHFWVUHTXLUHGZHUHFKLOGUHQ

Data was collected from medical records, clinical

reports containing patients’ data, parents, and disease

KLVWRU\1XWULWLRQDOVWDWXVZDVDVVHVVHGE\%0,NJ

m) for age, according to the WHO Growth Chart

The determinant was obesity, whereas the

outcome was dengue severity (DSS or DHF). Con

founding factors were infection type, platelet count,

fluid management during prior hospitalization, and

plasma leakage. Children were classified as obese if

WKHLU%0,IRUDJHZDV!6'DQGQRQREHVHLI%0,

IRUDJHZDV6'7\SHRILQIHFWLRQZDVFODVVLILHGDV

either primary or secondary infection. Primary infec

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Secondary infection was defined as having positive

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alone. Mild thrombocytopenia was defined as having

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QLDZDVGHILQHGDVKDYLQJSODWHOHWFRXQW

uL. Plasma leakage was defined as increased vascular

permeability characterized by ascites, pleural effusion

and increased hematocrit. Mild plasma leakage was

GHILQHGDVKHPDWRFULWLQFUHDVHZKLOHVHYHUH

plasma leakage was defined as hematocrit increase

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at the previous hospital if the patient received the

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protocol, while otherwise was classified as inappropriate.

2GGVUDWLRVZLWKFRQILGHQFHLQWHUYDOZHUH

calculated to assess an association between obesity

and DHF severity. This study was approved by the

Ethics Committee for Medical Research and Health,

Gadjah Mada University Medical School.

Results

:H LQFOXGHG VXEMHFWV LQ WKLV VWXG\ FRQVLVWLQJRIFKLOGUHQZLWK'66DQG

children without DSS. The basic characteristics of

subjects of both groups are shown in Table 1.

Univariate and multivariate logistic regression

analyses were performed to identify an association

between obesity and DSS. Univariate analysis revealed

that the significant risk factors for DSS were obesity,

VHFRQGDU\LQIHFWLRQW\SHSODWHOHWFRXQW

/ SODVPD OHDNDJH ZLWK KHPDWRFULW LQFUHDVH !

DQGLQDGHTXDWHIOXLGPDQDJHPHQWIURPSULRU

hospitalization. For multivariate analysis, we included

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SODVPD OHDNDJHZLWKKHPDWRFULW LQFUHDVH!

DQGLQDGHTXDWH IOXLGPDQDJHPHQWIURPWKHSULRU

hospitalization. Logistic regression analysis results are

presented in Table 2.

Our results showed that obesity was not a risk

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However, plasma leakage with hematocrit increase

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WR

7/27/2019 53-4-1




Table 1. Basic characteristics of subjects

Characteristics DSS group(n=116)

non-DSS group(n=226)

Total(n=342)

Gender, n (%)

MaleFemale 55 (47.4)61 (52.6) 122 (54.0)104 (46.0) 177 (51.8)165 (48.2)

Age, n (%)

1-4 years5-9 years10-14 years15-18 years

18 (15.5)58 (50.0)35 (30.2)5 (4.3)

39 (17.2)79 (35.0)86 (38.1)22 (9.7)

57 (16.6)137 (40.1)121 (35.4)27 (7.9)

Nutritional status, n (%)

Non-obeseObese

93 (80.2)23 (19.8)

93 (88.2)23 (19.8)

294 (86.0)48 (14.0)

Infection type, n (%)

PrimarySecondaryMissing data

16 (13.8)73 (62.9)27 (23.3)

27 (11.9)101 (44.7)98 (43.3)

43(12.6)174 (50.9)125 (36.6)

Plasma leakage, n (%)Hct** increase > 25%Hct**KPETGCUGŭ

89 (76.7)27 (23.3)

111 (49.1)115 (50.9)

200 (58.5)142 (41.5)

Pleural effusion, n (%)

YesNoMissing data

112 (96.6)4 (3.4)0(0)

208 (92.1)17 (7.5)1 (0.4)

320 (93.6)18 (5.3)1 (0.3)

Ascites, n (%)

YesNoMissing data

97 (83.6)19 (16.4)0 (0)

86 (38.1)139 (61.5)

1 (0.4)

183 (53.5)158 (46.2)

1(0.3)

Platelet count, n (%)

< 20,000/μLŮz.

44 (37.9)72 (62.1)

54 (23.9)172 (76.1)

98 (28.7)244 (71.3)

2TGXKQWUƀWKFOCPCIGOGPVPAdequateInadequateMissing data

56 (48.3)10 (8.6)50 (43.1)

51 (22.6)1 (0.4)

174 (77.0)

107 (31.3)11 (3.2)

224 (65.5)

Bleeding manifestations, n (%)

YesNoMissing data

30 (25.9)86 (74.1)2 (0.9)

52 (23.0)173 (76.6)

1 (0.4)

82 (24.0)259 (75.7)

1 (0.3)

Complications, n (%)

EncephalopathyDIC*

SepticemiaProlonged shockLung edemaNone

15 (12.9)2 (1.7)4 (3.4)9 (7.8)6 (5.2)

80 (69.0)

1 (0.4)2 (0.9)0 (0)0 (0)1 (0.4)

222 (98.3)

16 (4.7)4 (1.2)4 (1.2)9 (2.6)7 (2.0)

302 (88.3)

*DIC=disseminated intravascular coagulation

**Hct=hematocrit

Table 2. Univariate and multivariate analysis of risk factors for DSS

Risk factorsUnivariate

P valueMultivariate*

OR 95% CI OR 95% CI

Obesity 1.88 1.01 to 3.51 0.07 1.03 0.32 to 3.31Secondary infection type 1.22 0.61 to 2.43 0.69 - -Plasma leakage with hematocrit increase >25% 3.42 2.06 to 5.65 0.00 2.51 1.12 to 5.59Platelet count < 20,000/μL 1.93 1.20 to 3.16 0.01 0.95 0.44 to 2.07+PCFGSWCVGƀWKFOCPCIGOGPVHTQORTKQTJQURKVCNK\CVKQP 9.12 1.13 to 73.66 0.02 8.10 0.98 to 66.70

* logistic regression analysis

7/27/2019 53-4-1




Discussion

Based on our univariate and multivariate analyses,

obesity was not a risk factor for DSS in our subjects

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other studies. However, in contrast to our

results, Chuansumrit et al. showed that children with

!WKSHUFHQWLOHERG\ZHLJKWIRUDJHZHUHPRUHOLNHO\

WRKDYHJUDGH,,,DQG,9'+)WKDQWKRVHZLWKOHVVHU

ERG\ZHLJKW3Mongkalangoon found that

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&,WR

Theoretically, obesity may affect the severity of

dengue infection due to the increased production of

white adipose tissue (WAT) which causes increased

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patients should be measured using skin fold thickness,

theoretically a more direct measure of adipose tissue

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indicator for obesity in our study may be the reason

for the insignificant association between obesity and

'660HGLDWRUV,/,/DQG71)A) have also

been thought to increase capillary permeability and

may underlie the process of progressive and severe

plasma leakage. However, Hung et al., in a study onLQWHUIHURQG DQG71)A levels in the acute phase of

DHF and DSS patients, found that elevated levels did

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3Thus, further studies are needed to clearly

define an association between obesity and DSS.

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ZDVDVVRFLDWHGZLWK'6625&,

WRLQWKLVVWXG\6LPLODUO\&KXDQVXPULW et al.

reported that predictors for DSS were hematocrit

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partial thromboplastin time (APTT) > 44 seconds,SURWKURPELQWLPH377!VHFRQGVDQGWKURPELQ

WLPH77!VHFRQGV Tantracheewathorn et

al. reported that DHF patients with bleeding and

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VKRFNDGMXVWHG25&,WR

Several studies have shown an association

between hematocrit level and DSS, although they

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retrospective study in Jakarta found that hematocrit

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DQGRISDWLHQWVUHVSHFWLYHO\25

&,WR Malavige et al. reported hematocrit

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RISDWLHQWVUHVSHFWLYHO\3 Kan et al.

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associated with shock in DHF.

Change in hematocrit value is a marker of

plasma leakage and the bleeding process. As such, it

may be used as a simple monitoring tool. However,

hematocrit level cannot be used as an indicator of

shock in DHF, since it is influenced by bleeding and

fluid administration. Bleeding may cause decreased

hematocrit, while dehydration and plasma leakage

may lead to increased hematocrit, tissue perfusion

GLVWXUEDQFHVDQGVXEVHTXHQWO\VKRFN

6DUZDQWRUHSRUWHGWKDWDGHTXDWHIOXLGPDQDJHment at the beginning of the disease may reduce

the risk of death in patients with DHF. Tantrache

ewathorn et al. also mentioned that prompt and proper

fluid management may stabilize the intravascular

fluid and maintain stable hemodynamics, preventing

the progression to shock. However, we found that

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VHYHULW\RI'+)25&,WR

Low platelet count may cause bleeding in DHF,

accelerating the occurrence of shock. We found that

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Dewi et al. found that patients with DSS often had

SODWHOHWFRXQW/FRPSDUHGWRWKDWRIQRQ

'66SDWLHQWV25&,WR Also,

Kan et alUHSRUWHGWKDWSODWHOHWFRXQW/

was associated with the occurrence of DSS. Sutaryo

found that most shock cases had platelet count

/ Our different results were probably

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VXEMHFWVRQO\KDGWKHEOHHGLQJYROXPHUHFRUGHG

Hence, our analysis of the relationship between

severity of bleeding and DHF severity was not valid.

Type of infection was not a risk factor for DSS in

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it is believed that antibodies produced during dengue

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in monocytes, namely, enhancing antibodies and

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produced during primary infection may result in

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infection, stimulating viral replication. Therefore,

7/27/2019 53-4-1




secondary infection by different serotypes tends

to develop into more severe DHF manifestations

(DSS).5

A limitation of this study was incomplete data

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using medical records. Missing data included lack of

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infection diagnoses, and incomplete records on fluid

management from prior hospitalizations. These

problems may have led to bias and affected the results

of this study. Another limitation of our study was the

ODFNRI,/,/DQG71)A measurements, as risk

factors for severe DHF (DSS).

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not a risk factor for DSS, while plasma leakage with

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Acknowledgments

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&RQVXOWDQW3URIGU+0RFK$QZDU00HG6F2EVWHWULFV

&RQVXOWDQWDQGGU1XUQDQLQJVLK3HGLDWULFV&RQVXOWDQWIRUWKHLU

comments. We also thank Mrs. Ndari and Mrs. Haryati from the

Medical Record Unit for their assistance.

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-$P&ROO&DUGLRO

0DGL\RQR%0RHVOLFKDQ606DVWURDVPRUR6%XGLPDQ,

3XUZDQWR6+3HUNLUDDQEHVDUVDPSHO,Q6DVWURDVPRUR6

,VPDHO6HGLWRUV'DVDUGDVDUPHWRGRORJLSHQHOLWLDQNOLQLV

-DNDUWD6DJXQJ6HWRS

:RUOG+HDOWK2UJDQL]DWLRQ:+2DQG8QLWHG1DWLRQVRI

&KLOGUHQ·V)XQGV81,&():+2FKLOGJURZWKVWDQGDUGV

and the identification of severe acute malnutrition in infants

DQGFKLOGUHQ*HQHYD:+2

$QWR66HERGR76XWDU\R6XPLQWD,VPDQJRHQ1XWULWLRQDO

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S, Karunatilaka DH, Aaskov J, et al. Patterns of disease in Sri

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$VVRFLDWLRQEHWZHHQVH[QXWULWLRQDOVWDWXVVHYHULW\RIGHQJXH

hemorrhagic fever, and immune status in infants with dengue

hemorrhagic fever. Am J Trop Med Hyg.²

'HZL5 7XPEHODND$5 6\DULI'5&OLQLFDOIHDWXUHV RI

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3DHGLDWU,QGRQHV

.DQ()5DPSHQJDQ7+)DFWRUVDVVRFLDWHGZLWKVKRFNLQ

FKLOGUHQZLWKGHQJXHKHPRUUKDJLFIHYHU3DHGLDWU,QGRQHV

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pelatihan bagi pelatih dokter spesialis anak dan dokter

spesialis penyakit dalam dalam tatalaksana kasus DBD.

Jakarta)DNXOWDV.HGRNWHUDQ8,p. 45.

53-4-1

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