Paediatrica Indonesiana

March 

VOLUME 54

NUMBER 2

Original Article

Caesarean delivery and risk of developing atopic

diseases in children
Anak Agung Tri Yuliantini1, Mohammad Juffrie2, Ketut Dewi Kumara Wati1

Abstract
Background Caesarean delivery has been suggested to alter
neonatal immune responses and increase the risk of atopic
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ILQGLQJV
Objective To investigate a possible association between caesarean
GHOLYHU\DQGWKHGHYHORSPHQWRIDWRSLFGLVHDVHVLQFKLOGUHQ
Methods 7KLVFDVHFRQWUROVWXG\LQYROYHGFKLOGUHQDJHG
PRQWKV\HDUVLQ6DQJODK+RVSLWDO'HQSDVDU,QGRQHVLD)LIW\
infants and children with a confirmed diagnosis of atopic diseases
DQG  VH[SDLUHG FRQWUROV QRQDWRSLF LQIDQWV DQG FKLOGUHQ
ZHUHHQUROOHG'HPRJUDSKLFGDWDZDVREWDLQHGLQFOXGLQJPRGH
RI GHOLYHU\ DQG UHOHYDQW KLVWRU\ FRQQHFWHG WR DWRSLF GLVHDVHV
Skin prick test to four common aeroallergens was performed in
DOO VXEMHFWV 3RVVLEOH FRQIRXQGLQJ IDFWRUV ZHUH FRQVLGHUHG LQ D
PXOWLYDULDEOHORJLVWLFUHJUHVVLRQPRGHO
Results Caesarean section was not significant as a risk factor for
DWRSLFGLVHDVHVLQDPXOWLYDULDWHDQDO\VLV>25&,WR
 3 @ However, multiple logistic regression analysis
showed that atopic diseases was significantly associated with a
SRVLWLYHIDPLO\KLVWRU\RIDWRS\)XUWKHUPRUHFDHVDUHDQVHFWLRQ
was associated with a higher risk of atopic diseases in a subgroup
DQDO\VLVIRUIDPLO\KLVWRU\RIDWRS\>25 &,WR
3 @
Conclusion Children delivered by caesarean section and have a
IDPLO\KLVWRU\RIDWRS\KDYHDIROGKLJKHUULVNRIDWRSLFGLVHDVHV
[Paediatr Indones. 2014;54:94-100.]
Keywords: atopic diseases, cesarean delivery,
children.

he prevalence of atopic diseases in childhood

KDVLQFUHDVHGLQPDQ\FRXQWULHVAtopic
diseases is typically chronic and may restrict
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The proportion of caesarean sections has increased up
WRRIDOOGHOLYHULHVFRPSDUHGWRWKHVZKHQ
WKLVSURSRUWLRQZDVJHQHUDOO\EHORZ Children
delivered by caesarean section have been shown to
have delayed and altered establishment of gut flora
DQG F\WRNLQH SURGXFWLRQ Decreased exposure
to microorganisms early in life leads to insufficient
VWLPXODWLRQ RI 7K O\PSKRF\WHV DQG WKHUHIRUH D
SUHGRPLQDQFH RI WKH 7K DOOHUJLF UHVSRQVHV 
Some investigators have reported increased risk for
developing asthma and atopic diseases among children
delivered by caesarean section compared to those
delivered vaginally, while others have found no
VXFKUHODWLRQVKLS
Although the relationship between mode of
delivery and the prevalence of allergic diseases has
been investigated in many countries, there have

From the Department of Child Health, Udayana University Medical

School/Sanglah Hospital, Denpasar and Gadjah Mada University Medical
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Reprint requests to$QDN$JXQJ7UL<XOLDQWLQL'HSDUWPHQWRI&KLOG
+HDOWK8GD\DQD8QLYHUVLW\0HGLFDO6FKRRO6DQJODK+RVSLWDO-OPulau
1LDV'HQSDVDU%DOL,QGRQHVLD7HO)D[(PDLO
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94Paediatr Indones, Vol. 54, No. 2, March 2014

Anak Agung Tri Yuliantini et al: Caesarean delivery and risk of atopic diseases

EHHQIHZVXFKUHSRUWVLQ,QGRQHVLD7KHSXUSRVHRI
this study was to assess for a relationship between a
history of caesarean delivery and atopic diseases in
LQIDQWVDQGFKLOGUHQ

Methods
$FDVHFRQWUROVWXG\ZDVSHUIRUPHGLQWKHRXWSDWLHQW
clinic at the Department of Child Health, Sanglah
+RVSLWDO'HQSDVDUIURP'HFHPEHUXQWLO-XO\
 ,QFOXVLRQ FULWHULD IRU WKH FDVH JURXS ZHUH
FKLOGUHQ DJHG  PRQWKV \HDUV ZLWK D GHILQLWH
GLDJQRVLV RI DWRSLF GLVHDVHV $Q DWRSLF GLVHDVH ZDV
defined as the presence of or a history of at least
RQHRIWKHIROORZLQJDVWKPDDOOHUJLFUKLQLWLVDWRSLF
GHUPDWLWLV RU IRRG DOOHUJ\ 7KHVH GLVHDVHVV ZHUH
diagnosed by pediatricians/physicians (pediatric
UHVLGHQWV RI 6DQJODK +RVSLWDO 7KH GLDJQRVLV ZDV
confirmed by fulfillment of the Sanglah Hospital
Guidelines Criteria, with or without the support of a
SRVLWLYHVNLQSULFNWHVW:HH[FOXGHGFKLOGUHQVXIIHULQJ
from severe form of atopic diseases, undergoing
treatment with antihistamines and/or corticosteroids,
who had incomplete data or whose parents refused to
SDUWLFLSDWHLQWKHVWXG\
Inclusion criteria for the control group were
FKLOGUHQ DJHG  PRQWKV \HDUV ZLWKRXW D KLVWRU\
RIDQ\DWRSLFGLVHDVHV7KHVHFKLOGUHQZHUHVHHQLQ
WKH KRVSLWDO IRU RWKHU XQUHODWHG SUREOHPV )RU WKH
control group, we also excluded children suffering
IURP GLVHDVHVV UHTXLULQJ VWHURLG DQGRU ORQJWHUP
antihistamine treatment, and who had incomplete
GDWD 7KH PLQLPXP UHTXLUHG VDPSOH VL]H ZDV
calculated with type I error (A SRZHUB)
25 FOLQLFDOMXGJPHQWDQG3 
WREHDWRWDORIFKLOGUHQ
Demographic data regarding birth weight,
age, number of siblings, exposure to environmental
cigarette smoke (exposure to any smoker at home),
exposure to kitchen smoke (bedroom and kitchen
XQGHU WKH VDPH URRI FRWWRQILOOHG PDWWUHVV XVDJH
carpet usage, pets, duration of breast feeding, the age
DW ZKLFK VHPLVROLG IRRG ZDV ILUVW LQWURGXFHG WKH
age at which formula milk was first introduced, and a
family history of atopic diseases were obtained from a
TXHVWLRQQDLUHFRPSOHWHGE\WKHSDUHQWV
Subjects underwent skin prick tests to common

DHURDOOHUJHQV KRXVH GXVW PLWH Dermatophagoides

pteronyssinus and Dermatophagoides farinae), cockroach
(Blattela germanica), and Aspergillus sp (Stallergens,
France) on the volar aspect of the forearm or the
EDFN+LVWDPLQHZDVXVHGDVWKHSRVLWLYHFRQWURODQG
VDOLQHDVWKHQHJDWLYHFRQWURO$VNLQSULFNWHVWZDV
FRQVLGHUHGSRVLWLYHIRUDZKHDODQGIODUHVL]HG!
PPDIWHUPLQXWHVWRDWOHDVWRQHRIWKHFRPPRQ
DHURDOOHUJHQV
Descriptive analyses of the characteristics of the
FRQWURODQGFDVHJURXSZHUHSHUIRUPHG8QLYDULDWH
analyses comparing variable differences between the
FRQWURODQGFDVHJURXSVZHUHGRQHXVLQJ&KLVTXDUH
DQG)LVKHUVH[DFWWHVWVZKHUHDSSURSULDWH$3YDOXH
RIZDVFRQVLGHUHGWREHVWDWLVWLFDOO\VLJQLILFDQW
2GGVUDWLRV25VDQG&,VZHUHHVWLPDWHGZLWK
the use of multivariate logistic regression analyses
WKDWDOORZHGIRUSRWHQWLDOFRQIRXQGHUV$VHFRQGDU\
analysis was performed to examine an association
between caesarean delivery and atopic diseases, in the
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Ethical approval for this study was obtained
from Udayana University Medical School Ethics
Committee and informed consent was obtained from
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Results
One hundred two children were recruited into this
VWXG\ EXW RQO\  VXEMHFWV ZHUH DQDO\]HG 7ZR
subjects were excluded due to the presence of severe
atopic dermatitis that the skin prick test could not
EHSHUIRUPHGVXEMHFWDQGGXHWRWUHDWPHQWZLWK
FRUWLFRVWHURLGVVXEMHFW7KHPHDQDJHRIVXEMHFWV
ZDV  6'  \HDUV UDQJH  PRQWKV \HDUV
6L[W\WZR VXEMHFWV  ZHUH GHOLYHUHG YDJLQDOO\
DQGZHUHGHOLYHUHGE\FDHVDUHDQVHFWLRQ
Subjects demographic characteristics are shown
in Table 1. Most of our study subjects in the case
JURXSVXIIHUHGIURPDOOHUJLFUKLQLWLVIROORZHG
E\DVWKPDDWRSLFGHUPDWLWLVDQGIRRG
DOOHUJ\
The relationships between each risk factor and
the occurrence of atopic diseases were analyzed.:H
found a significant association between caesarean
section and atopic diseases in a bivariate analysis,
EXW QRW LQ PXOWLYDULDWH DQDO\VHV 0XOWLSOH ORJLVWLF

Paediatr Indones, Vol. 54, No. 2, March 201495

Anak Agung Tri Yuliantini et al: Caesarean delivery and risk of atopic diseases
Table 1. Characteristics of study subjects
Characteristics
Male gender, n (%)
Median age (SD), years
Median body weight (SD), kg
Median body height (SD), cm
Siblings, n (%)
0

Birth weight, n (%)
<2,500 g
I
'ZENWUKXGN[DTGCUVHGFHQTVJGTUVOQPVJUP

Formula milk < 6 months, n (%)
Age when semi-solid food was introduced, n (%)
<6 months
OQPVJU
Family history of atopic diseases, n (%)
Yes
No
Father has history of atopic diseases, n(%)
Yes
No
Mother has history of atopic diseases, n(%)
Yes
No
Siblings have history of atopic diseases, n(%)
Yes
No
Kitchen smoke exposure, n (%)
Cigarette smoke exposure, n (%)
%QVVQPNNGFOCVVTGUUWUCIGP

Carpet usage, n (%)
Mosquito coil smoke exposure, n (%)
Pets exposure, n (%)
Positive skin prick test, n (%)

regression analysis including significant confounders

revealed that the significant risk factors associated
with atopic diseases were a positive parental history
of atopy, kitchen smoke exposure, and pets exposure
(Table 2).
:H DOVR DVVHVVHG IRU D SRVVLEOH DVVRFLDWLRQ
between caesarean delivery and atopic diseases in a
subgroup of subjects who had a family history with
DWRSLFGLVHDVHVVXEMHFWVKDGDIDPLO\KLVWRU\
of atopic diseases (Table 1).2IWKHVHVXEMHFWV
VXEMHFWVIURPWKHFDVHJURXSDQGVXEMHFWVIURPWKH
FRQWURO JURXS ZHUH GHOLYHUHG E\ FDHVDUHDQ VHFWLRQ
Caesarean section was significantly associated with
a higher risk of atopic diseases in this subgroup of
IDPLO\ KLVWRU\ RI DWRS\ >25  &,  WR 
3 @

96Paediatr Indones, Vol. 54, No. 2, March 2014

Case (atopic)
n = 50
25 (50)
6.0 (3.2)
21.6 (9.4)
111.8 (22.4)

Control (non-atopic)
n = 50
25 (50)
5.7 (3.2)
18.9 (7.2)
105.1 (25.6)

14 (28)
36 (72)

10 (20)
40 (80)

0 (0)
50 (100)
17 (34)
33 (66)

2 (4)
48 (96)
17 (34)
33 (66)

9 (18)
41 (82)

16 (32)
34 (68)

46 (92)
4 (8)

14 (28)
36 (72)

31 (62)
19 (28)

9 (18)
41 (82)

27 (54)
23 (46)

7 (14)
43 (86)

18 (36)
32 (64)
31 (62)
24 (48)
3 (6)
13 (26)
6 (12)
25 (50)
48 (96)

2 (4)
48 (96)
20 (40)
30 (60)
9 (18)
14 (28)
11 (22)
15 (30)
18 (36)

Discussion
The relatively high rate of caesarean sections in
Denpasar   warrants an investigation for an
association between mode of delivery and the
SUHYDOHQFHRIDWRSLFGLVHDVHV:HIRXQGWKDWFDHVDUHDQ
delivery was significant as a risk factor for atopic
diseases by bivariate analysis, but not by multivariate
DQDO\VHV ,Q D VXEJURXS DQDO\VLV RI VXEMHFWV ZLWK D
family history of atopic diseases, we found that there
was an association between caesarean section and
DWRSLFGLVHDVHV
Caesarean section is associated with delayed
intestinal colonization, which could deprive newborns
of immunostimulatory impulses at a critical period
in life when the immune system and the gut barrier

Anak Agung Tri Yuliantini et al: Caesarean delivery and risk of atopic diseases
Table 2. Relationships between each risk factor and atopic diseases
Risk factors
Family history of atopic diseases
- Mother
- Father
- Siblings
Male gender
Siblings < 1
Caesarean delivery
Birth weight < 2,500 g
Exclusively breastfed
Formula milk < 6 months
Semi-solid food introduction at < 6 months of age
Kitchen smoke exposure
Cigarette smoke exposure
%QVVQPNNGFOCVVTGUUWUCIG
Carpet usage
Mosquito coil smoke exposure
Pets exposure

Atopic
diseases
n
Yes
No
27
31
18
25
14
25
0
17
28
9
31
24
3
13
6
25

7
9
2
25
10
13
2
17
28
16
20
30
9
14
11
15

OR (95%CI)

P value

Unadjusted
7.2 (2.7 to 19.1)
7.4 (2.9 to 18.6)
13.5 (2.9 to 62.2)
1.0 (0.5 to 2.2)
1.6 (0.6 to 3.9)
2.8 (1.2 to 6.6)
0.5g(0.4 to 0.6)
1.0 (0.4 to 2.3)
1.2 (0.5 to 2.6)
2.1 (0.8 to 5.5)
2.4 (1.1 to 5.5)
0.6 (0.3 to 1.4)
0.3 (0.1 to 1.1)
0.9 (0.4 to 2.2)
0.5 (0.2 to 1.4)
2.3 (1.0 to 5.3)

OR (95%CI)

P value

Adjusted*
< 0.0001
< 0.0001
< 0.0001
1.000
0.349
0.013
0.495
1.000
0.712
0.106
0.028
0.229
0.065
0.822
0.183
0.041

14.8 (4.0 to 54.7)

14.5 (4.0 to 51.8)
3.5 (0.6 to 19.6)

< 0.0001
< 0.0001
0.155

2.4 (0.7 to 8.4)

0.164

4.9 (0.9 to 25.1)

4.2 (1.3 to 13.9)
0.6 (0.16 to 1.9)

0.054
0.019
0.362

0.3 (0.06 to 1.8)

6.1 (1.7 to 21.9)

0.203
0.005

g Fischers exact test (2 cells (50,0%) have expected count less than 5. The minimum expected count is 1,00.)
* Adjusted by multivariate analysis (family history of atopic diseases, semi-solid food introduction at < 6 months of age, kitchen smoke exposure, cigarette
smoke exposure, mosquito coil smoke exposure, and pets)

PDWXUH &KLOGUHQ GHOLYHUHG E\ FDHVDUHDQ VHFWLRQ

have been shown to have a delayed and altered
development in the establishment of gut flora, as well
DVDOWHUHGF\WRNLQHVSURGXFWLRQ'HFUHDVHGH[SRVXUH
to microorganisms early in life leads to insufficient
VWLPXODWLRQ RI 7K O\PSKRF\WHV DQG WKHUHIRUH D
SUHGRPLQDQFHRIWKH7KDOOHUJLFUHVSRQVHV:KHQ
combining subjects with and without an atopic family
history, we found that caesarean delivery was not
DVVRFLDWHGZLWKWKHULVNRIDWRSLFGLVHDVHV7KLVILQGLQJ
may have been due to major differences between the
SRSXODWLRQVDQGWKHYDULDEOHVREVHUYHG:HGLGQRW
examine gut flora colonization or cytokines production
LQRXUVWXG\
Previous studies on caesarean delivery and
the development of allergic diseases has produced
FRQIOLFWLQJUHVXOWV Our study, consistent with data
IURP DQ (QJOLVK ELUWK FRKRUW RI  FKLOGUHQ
found no convincing evidence that infants delivered
by caesarean section had an increased risk of
developing allergic diseases (asthma, hay fever, and
HF]HPD 'HOLYHU\ E\ FDHVDUHDQ VHFWLRQ ZDV DOVR
not associated with the subsequent development of
asthma, wheezing, or atopy in later childhood in a
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Outcome variables examined in the Bristol study were

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PRQWKVRIDJH\HDUVROGVLPLODUWRPRVWFKLOGUHQ
LQRXUVDVWKH\ZHUHDJHGRYHU\HDUV7KHVHODVWWZR
VWXGLHVXVHGVXEMHFWVZLWKDWRSLFDQGQRQDWRSLFIDPLO\
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The Finnish Health Register reported that the
FXPXODWLYHLQFLGHQFHRIDVWKPDDWWKHDJHRI\HDUV
was significantly higher in children delivered by
caesarean section than in those delivered vaginally,
but no associations were observed between caesarean
section and other allergic diseasess (hay fever and
DWRSLF HF]HPD ,Q D IROORZLQJ VWXG\ RQ WKLV ELUWK
FRKRUW RI  FKLOGUHQ WKH\ IRXQG D WUHQG WRZDUG
PRUH SRVLWLYH VNLQ SULFN UHDFWLRQV DW WKDW DJH A
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adults revealed a strong effect of caesarean section
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showed no associations with atopy, allergic rhino
FRQMXQFWLYLWLVDQGDWRSLFGHUPDWLWLV0HWDDQDO\VHV
LQ  FRQFOXGHG WKDW FDHVDUHDQ GHOLYHU\ ZDV
associated with a moderately increased risk of allergic
rhinitis, asthma, hospitalization for asthma, and
perhaps food allergy/food atopy, but not with inhalant
DWRS\ DQG HF]HPDDWRSLF GHUPDWLWLV Factors such

Paediatr Indones, Vol. 54, No. 2, March 201497

Anak Agung Tri Yuliantini et al: Caesarean delivery and risk of atopic diseases

DVWKHGXUDWLRQRIIROORZXSLQYHVWLJDWHGYDULDEOHV
and the definition of allergic diseases also may have
SURGXFHGFRQIOLFWLQJUHVXOWV2XUVWXG\GLIIHUHGIURP
previous studies in terms of outcomes, as we used the
term atopic diseases, a collection of various atopic
GLVHDVHVVLQVWHDGRIVLQJOHDWRSLFGLVHDVHVHQWLW\
Therefore, although caesarean section is
considered to be a risk factor for allergic diseasess, a
GHILQLWHDVVRFLDWLRQKDVQRW\HWEHHQGHWHUPLQHG7KH
lack of association in our subjects might due to the fact
that most children in our study were already over 2
\HDUVRIDJH6LQFHFDHVDUHDQGHOLYHU\H[SRVXUHRFFXUV
only once at the beginning of life, while other risk
factors such as parental history of atopy, and exposure
to household pets and kitchen smoke, affect subjects
for longer durations in life, the role of caesarean
GHOLYHU\ DV D ULVN IDFWRU PD\ EH OHVV LQIOXHQWLDO $
SUHYLRXV+RQJ.RQJVWXG\UHSRUWHGDVLJQLILFDQWGRVH
response association between household gas cooking
and the prevalence of respiratory illnesses (allergic
rhinitis, asthma, bronchitis, sinusitis, and pneumonia)
in preschool children in a residential estate with low
outdoor air pollution, after controlling for potential
FRQIRXQGLQJIDFWRUV7KLVVWXG\SURYLGHVDGGLWLRQDO
evidence that household gas cooking increases the risk
RI UHVSLUDWRU\ LOOQHVVHV DPRQJ SUHVFKRRO FKLOGUHQ22
An earlier US report indicated that exposure or
allergic reactions to pets were the predominant risk
IDFWRUIRUDVWKPDDPRQJFKLOGUHQDQGDGROHVFHQWV
$ VLJQLILFDQW GRVHUHVSRQVH DVVRFLDWLRQ EHWZHHQ
exposure to cats and the prevalence of asthma in
FKLOGUHQZDVDOVRUHSRUWHGLQ'HQSDVDU24
Caesarean section was associated with allergic
rhinitis and atopy in children with a parental history
RI DVWKPD RU DOOHUJLHV25 Also, caesarean delivery
ZDV DVVRFLDWHG ZLWK D IROG LQFUHDVH LQ WKH RGGV
of parental reporting of food allergies (to egg, fish,
RU QXWV LQ  1RUZHJLDQ FKLOGUHQ IROORZHG WR
WKHDJHRI\HDUV&,IRU25WR7KH
observed association between caesarean delivery and
food allergy among Norwegian infants was stronger
after the analysis was stratified by maternal history
RIDOOHUJ\1RUZHJLDQFKLOGUHQZKRZHUHGHOLYHUHGE\
caesarean section and had a maternal history of allergy
KDGDIROGKLJKHURGGVRIIRRGDOOHUJ\WKDQWKRVH
who were delivered vaginally and had no maternal
KLVWRU\RIDOOHUJ\&,IRU25WR26 :HDOVR
examined whether the association between caesarean

98Paediatr Indones, Vol. 54, No. 2, March 2014

delivery and atopic diseases differed by family history

RI DWRSLF GLVHDVHVV :H IRXQG WKDW VXEMHFWV ZLWK D
family history of atopy and delivered by caesarean
VHFWLRQKDGDKLJKHUULVNRIDWRSLFGLVHDVHV
Early life exposure to allergens may vary by mode
of delivery, and absence or avoidance of these factors
PD\ UHGXFH WKH ULVN IRU DWRSLF GLVHDVHV :H ZHUH
unable to collect data on other variables, including
maternal smoking, gestational age, intrauterine
infection, NICU admission, antibiotic administration
DIWHUELUWKRUSHULSDUWXPFRPSOLFDWLRQV,QIRUPDWLRQ
on the type of milk formula given to our subjects
(cows milk formula, hydrolyzed cows milk formula, or
VR\PLONIRUPXODZDVDOVRQRWFROOHFWHGLQWKLVVWXG\
Nor was data regarding the use of probiotics collected
in our study, so the factors mentioned above were not
FRQWUROOHGIRU$OWKRXJKZHGLGQRWKDYHLQIRUPDWLRQ
about dust mites, we did collect data on the presence
RIFDUSHWDQGFRWWRQILOOHGPDWWUHVVHVDWKRPH
A limitation of our study was the wide age range
of subjects, as the effect of caesarean delivery may
have been different among older subjects, in terms of
the interval between caesarean delivery and the event
RIDWRSLFGLVHDVHV7KLVLVDFDVHFRQWUROVWXG\LQZKLFK
WKH FRQWURO ZDV KRVSLWDOEDVHG KHQFH WKH FRQWURO
group may not represent the general population of
QRUPDOFKLOGUHQ5HFDOOELDVPD\KDYHDOVRDIIHFWHG
WKHTXHVWLRQQDLUHGDWDFROOHFWHG$OLPLWHGVWDWLVWLFDO
power on the subgroup analysis differed by family
history of atopic diseasess in our study, probably due
WRDOLPLWHGVDPSOH
In conclusion, children who have a family history
of atopy and are delivered by caesarean section have a
IROGKLJKHUULVNRIDWRSLFGLVHDVHV&DHVDUHDQVHFWLRQ
as a delivery option should be carefully considered in
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Acknowledgments
Our sincere gratitude to physicians and nurses in charge at the
Outpatient Clinic, Department of Child Health of Sanglah
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FRQVWUXFWLQJPHWKRGRORJ\DQGVWDWLVWLFDODQDO\VLVLQWKLVVWXG\

Conflict of interest
None declared

Anak Agung Tri Yuliantini et al: Caesarean delivery and risk of atopic diseases

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