Open access Original research

Association between uterine

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contractions before elective caesarean
section and transient tachypnoea of the
newborn: a retrospective cohort study
Satoshi Shinohara ‍ ‍, Atsuhito Amemiya, Motoi Takizawa

To cite: Shinohara S, Abstract

Amemiya A, Takizawa M. Strengths and limitations of this study
Objective We evaluated the association between the
Association between uterine presence of predelivery uterine contractions and transient
contractions before elective ►► We used the findings of an objective test to evalu-
tachypnoea of the newborn (TTN) in women undergoing an
caesarean section and ate the risk of transient tachypnoea of the newborn,
elective caesarean section.
transient tachypnoea of the thus avoiding complicated or subjective patient
newborn: a retrospective Design A retrospective cohort study.
examinations.
cohort study. BMJ Open Setting National Hospital Organization Kofu National
►► Our study population was limited to women under-
2020;10:e033154. doi:10.1136/ Hospital, which is a community hospital, between January
going an elective caesarean section, and our anal-
bmjopen-2019-033154 2011 and May 2019.
ysis was adjusted for many known risk factors of
Participants The study included 464 women who
►► Prepublication history for transient tachypnoea of the newborn.
underwent elective caesarean section. The exclusion
this paper is available online. ►► Our study was a retrospective, single-­centre study.
To view these files, please visit criteria were missing data, twin pregnancy, neonatal
►► Our analysis did not control for maternal asthma,
the journal online (http://​dx.​doi.​ asphyxia, general anaesthesia and elective caesarean
which is a known risk factor of transient tachypnoea
org/​10.​1136/​bmjopen-​2019-​ section before term.
of the newborn.
033154). Primary and secondary outcome measures Patients
were grouped according to the presence or absence of
Received 23 July 2019 uterine contractions on a 40-­min cardiotocogram (CTG)
Revised 23 October 2019 performed within 6 hours before caesarean delivery. We birth and require invasive or non-­ invasive
Accepted 24 February 2020
performed a multivariable logistic regression analysis respiratory support.7 8
to examine the association between predelivery uterine Several studies have demonstrated that
contractions and TTN. catecholamines play an important role in
Results The incidence of TTN was 9.9% (46/464), and
fetal alveolar fluid clearance,9–11 a process
38.4% (178/464) of patients had no uterine contraction.
that begins before term birth and continues
The absence of uterine contractions was significantly
associated with an increased risk of TTN (adjusted OR through labour and after delivery.1 The spon-
2.04; 95% CI 1.09 to 3.82) after controlling for gestational taneous surge in catecholamine secretion
diabetes mellitus, small for gestational age, male sex and caused by uterine contractions is particularly
caesarean section at 37 weeks. important for fetal alveolar fluid clearance,12
Conclusions Accurate risk stratification using a CTG and previous studies found that elective
could assist in the management of infants who are at risk caesarean section before the onset of labour
of developing TTN. is a significant risk factor for TTN.3 13 14 The
number of elective caesarean sections has
increased in Japan over the last decades, and
Introduction the caesarean section rate reached 11.5% in
Transient tachypnoea of the newborn (TTN) 2013.15 The elective caesarean section rate
is a parenchymal lung disorder character- is expected to continue to increase due to
© Author(s) (or their ised by pulmonary oedema resulting from increased maternal age,16 multiple gesta-
employer(s)) 2020. Re-­use
delayed resorption and clearance of fetal tions after fertility treatment17 and maternal
permitted under CC BY-­NC. No
commercial re-­use. See rights alveolar fluid.1 Clinical characteristics appear request.18 Inevitably, the number of newborns
and permissions. Published by shortly after delivery and include tachy- with TTN will also increase. Therefore, it is
BMJ. pnoea, nasal flaring and grunting.1–3 TTN is important to completely understand the risk
Obstetrics and Gynecology, Kofu a common cause of respiratory distress in late factors of TTN.
National Hospital, Kofu, Japan preterm and term infants and is generally a Many reports indicate that caesarean
Correspondence to benign disease treated with a brief course of section before the onset of labour is a risk
Dr Satoshi Shinohara; oxygen.4–6 However, some patients develop factor for TTN.3 13 14 However, another study
​shinohara617@​gmail.​com severe respiratory distress immediately after found conflicting results.3 The problem

Shinohara S, et al. BMJ Open 2020;10:e033154. doi:10.1136/bmjopen-2019-033154 1

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appears to be the lack of consensus on the definition contraction, is typically used to assess fetal well-­being. In

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of labour onset between these studies and worldwide.19 this study, CTG data were recorded using an actocardio-
Furthermore, the different definitions of labour onset are graph (Toitu MT-­516GE; Tofa Medical, Malvern, Penn-
based on various features, including cervical dilatation, sylvania). The prepregnancy body mass index (BMI) was
cervical effacement and uterine contractions.19 There- calculated according to the WHO standard (body weight/
fore, these studies are still open for further consideration. height squared (kg/m2)). Maternal weight gain during
Given the ambiguity surrounding the onset of labour, pregnancy was calculated by subtracting the patient’s
we examined the relationship between the presence of prepregnancy body weight from her body weight at the
uterine contractions before caesarean section alone and last prenatal visit before delivery. We defined SGA as a
TTN rather than considering all features of the onset of weight below the 10th percentile in each gestational
labour. Furthermore, no study to date has used the pres- week.22 The diagnosis of GDM was made if there was at
ence of uterine contractions to identify newborns at risk least one abnormal plasma glucose value (≥92, 180 and
of developing TTN. Therefore, we aimed to examine the 153 mg/dL for fasting, 1-­hour and 2-­hour plasma glucose
association between the presence of uterine contractions concentration, respectively) after a 75 g oral glucose toler-
before an elective caesarean section and TTN. ance test.23
Neonatal asphyxia was defined as an Apgar score
remaining less than 7 at 5 min after birth or as an arterial
Methods blood pH of less than 7.00.24 A diagnosis of TTN, which
Study design was the outcome of interest in this study, required each of
We performed a retrospective observational cohort study the following: respiratory rate >60 breaths/min, constant
of women who underwent an elective caesarean section tachypnoea for ≥12 hours, prominent central pulmonary
with spinal and epidural anaesthesia between January vessels or thickened interlobar fissures on a chest X-­ray
2011 and May 2019 at the National Hospital Organi- and exclusion of other causes of respiratory distress, such
zation Kofu National Hospital, which is a community as surfactant deficiency, pneumonia, meconium aspira-
hospital. We excluded women with multiple pregnan- tion, congenital heart disease or metabolic disorder.25 A
cies, missing data and those who underwent an elective neonatologist diagnosed TTN based on the above diag-
caesarean section before a term delivery. In addition, nostic criteria in the first few hours after a baby was born.
we excluded cases in which the infant had neonatal Moreover, when the neonatologist diagnosed TTN, all
asphyxia. The Human Subjects Review Committee of the infants were treated in the neonatal intensive care unit.
National Hospital Organization Kofu National Hospital
reviewed and approved the study protocol and waived Statistical analyses
the need for informed consent because of the retrospec- The Mann-­Whitney U test and χ2 test (or Fisher’s exact test
tive study design. However, patients were provided the when the expected frequency was <5) were used to eval-
opportunity to refuse the usage of their data through uate the effects of potential confounding factors of TTN.
the hospital’s website. All procedures were performed in The Mann-­Whitney U test was used to analyse continuous
accordance with the 1964 Helsinki Declaration and its variables such as maternal age, and the χ2 test (or Fisher’s
later amendments. exact test when the expected frequency was <5) was used
for categorical variables such as incidence of obstetric
Data collection complications. A multiple logistic regression model was
We collected obstetric data from medical and operative used to identify the variables significantly associated with
records. We recorded maternal age, parity, gestational TTN. The logistic regression models were adjusted by
age at delivery, prepregnancy weight status and maternal uterine contraction, GDM, SGA infants, infant sex and
weight gain. Additionally, we assessed the presence of gestational age at delivery. All analyses were performed
gestational diabetes mellitus (GDM), small for gesta- using the Bell Curve for Excel (Social Survey Research
tional age (SGA), infant sex and neonatal asphyxia. Information, Tokyo, Japan) and IBM SPSS Statistics for
These potential confounding factors have been previ- Windows V.25. The significance level was set at p<0.05.
ously described as TTN risk factors.13 20 21 During the
study period, 523 women underwent elective caesarean Patient and public involvement
section. A total of 59 (missing data, n=12; twin pregnancy, Patients were not invited to comment on the study design
n=38; neonatal asphyxia, n=2; general anaesthesia, n=1; and were not consulted to develop patient-­ relevant
elective caesarean section before term delivery, n=6) outcomes or interpret the results.
were excluded. Cases of neonatal asphyxia were excluded
because this diagnosis was statistically underrepresented
in our study sample. Results
The women were grouped according to the presence A total of 464 women were considered eligible for inclu-
or absence of uterine contractions on a 40 min cardioto- sion in this study. The mean maternal age was 32.8±5.1
cogram (CTG) obtained within 6 hours before caesarean years, and the mean maternal prepregnancy BMI was
section. CTG, which records fetal heart rate and uterine 21.7±3.9 kg/m2, with 124 (26.7%) nulliparous women,

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Table 1 Clinical characteristics of the groups with and without uterine contractions
Variable* Uterine contraction (−) (n=178) Uterine contraction (+) (n=286) P value
Maternal age, years 33.0±5.2 32.7±5.0 0.49
Nulliparity 45 (25.3) 79 (27.6) 0.58
Repeat caesarean section 119 (66.9) 189 (65.0) 0.86
2
Prepregnancy BMI, kg/m 22.1±3.5 21.4±4.1 0.005
Birth weight, g 2839±320 2868±345 0.41
GDM 11 (6.2) 19 (6.6) 0.84
SGA 14 (7.9) 20 (7.0) 0.73
Male infant 90 (50.5) 144 (50.3) 0.96
TTN 25 (14.0) 21 (7.3) 0.02
Values are presented as the mean±SD or number (%).
*The Mann-­Whitney U test was used to analyse continuous variables such as maternal age, and the χ2 test (or Fisher’s exact test when the
expected frequency was <5) was used for categorical variables such as incidence of obstetric complications.
BMI, body mass index; GDM, gestational diabetes mellitus; SGA, small for gestational age; TTN, transient tachypnoea of the newborn.

234 male infants (50.4%), 30 GDM women (6.5%) and 34 Discussion

(7.3%) SGA infants. The indications for elective caesarean In this study of women undergoing an elective caesarean
sections were previous caesarean section (n=308, 66.4%), section, a lack of preprocedure uterine contractions
breech presentation (n=79), placenta praevia or low lying was significantly associated with TTN after adjusting for
placenta (n=23), prior myomectomy (n=17), maternal potential confounding factors. To our knowledge, this
disorders (n=7), cephalopelvic disproportion (n=5) and investigation is the first detailed examination of the
other causes (n=25). association between uterine contractions before elective
The overall incidence of TTN was 46 (9.9%). The caesarean section and the incidence of TTN.
prepregnancy BMI was significantly higher in patients Uterine contractions during labour cause an increase in
without uterine contractions, and no other significant stress hormones, such as cortisol and catecholamines.9–11
difference was noted between the groups (table 1). During late gestation, the number of functional sodium
TTN occurred more frequently in women without channels in the fetal lungs increases in response to
uterine contractions (table 2), and the prevalence of increased concentrations of stress hormones.9–12 Conse-
TTN was significantly higher in patients without uterine quently, the mature lung epithelium switches from actively
contractions than in those with uterine contractions secreting chloride and liquid into the air spaces to actively
(14.0% vs 7.3%, p=0.02) (table 1). reabsorbing sodium and liquid.11 However, sodium chan-
On multivariate analyses, no uterine contraction nels remain inactive during elective caesarean sections
(adjusted OR 2.04; 95% CI 1.09 to 3.82) and caesarean because the stress hormone level is low. Thus, compared
section at 37 weeks (adjusted OR 2.47; 95% CI 1.30 to with vaginal birth, elective caesarean section more
4.69) were associated with TTN (table 3). frequently results in TTN.11
A previous population-­ based case-­ controlled study
reported that precaesarean section labour is not protec-
Table 2 Prevalence of TTN according to number of uterine tive against TTN.3 In that study, labour was defined as
contractions before caesarean section any indication of labour, including precipitous labour,
No of uterine contraction(s) Prevalence of TTN* prolonged labour, induction of labour, stimulated labour
and dysfunctional labour. As in our study, the researchers
0 25/178 (14.0)
grouped women based on the presence or absence of
1 4/59 (6.8) uterine contractions and examined the relationship
2 8/79 (10.1) between TTN and caesarean section. However, their study
3 1/48 (2.1) had limitations that ours did not, including its inability
4 1/28 (3.6) to distinguish between elective and emergency caesarean
sections. As several other investigators have concluded,
5 2/18 (11.1)
there is a well-­described physiological mechanism that
6≥ 5/54 (9.1)
explains why uterine contractions could reduce the inci-
*Values are presented as the number of TTN per number of dence of TTN.13 14 26
women stratified according to the number of uterine contractions The time before the onset of labour can be further
(percentage). subdivided to clarify fetal alveolar fluid clearance. For
TTN, transient tachypnoea of the newborn.
example, in Japan, the diagnosis of labour onset was

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Table 3 Crude and adjusted odds ratios of risk factors for TTN
Crude Adjusted
Variable TTN (n) Non-­TTN (n) OR 95% CI OR 95% CI
Uterine contraction
 Present 21 265 1.0 Reference 1.0 Reference
 Absent 25 153 2.06 1.12 to 3.81 2.04 1.09 to 3.82
GDM    
 No 45 389 1.0 Reference 1.0 Reference
 Yes 1 29 0.29 0.04 to 2.24 0.31 0.04 to 2.39
SGA
 No 39 391 1.0 Reference 1.0 Reference
 Yes 7 27 2.59 1.06 to 6.36 2.49 0.99 to 6.32
Male infant    
 No 18 212 1.0 Reference 1.0 Reference
 Yes 28 206 1.60 0.86 to 2.98 1.55 0.82 to 2.93
Caesarean section
 ≥38 weeks 17 250 1.0 Reference 1.0 Reference
 37 weeks 29 168 2.53 1.35 to 4.77 2.47 1.30 to 4.69
GDM, gestational diabetes mellitus; SGA, small for gestational age; TTN, transient tachypnoea of the newborn.

defined as six regular uterine contractions per hour.23 Previous reports indicate that a caesarean section at
Although the period without uterine contractions and 37 weeks is a major TTN risk factor,29 30 and our findings
that with five regular contractions per hour both occur support this conclusion. In our study, 16 (21.1%) of 76
before the onset of labour, it seems that the effect of each women with no uterine contractions who underwent a
period on stress hormone secretion is not the same. Our caesarean section at 37 weeks delivered an infant who
results demonstrate that the frequency of TTN is higher developed TTN (data not shown).
in patients with no uterine contractions than in patients Our study has limitations. First, this was a single-­centre
with contractions. Although several studies evaluated the study, and it might be difficult to extrapolate our results
association between TTN and events occurring before to the general population. Therefore, a large-­scale, multi-
labour and elective caesarean section,3 13 14 there is no centre, prospective cohort study is needed to confirm our
consensus on the definition of the onset of labour. For results in the general population. Second, we did not eval-
example, the onset of labour was described by Senturk et uate some potential TTN risk factors, including maternal
al26 as the onset of uterine contractions with labour pain asthma31 and low infant thyroid hormone level,32 and
and by Derbent et al27 as regular uterine contractions and there is the possibility that unmeasured confounders may
cervix effacement with dilatation of 2 cm or more. Mean- be associated with TTN in this study. Third, the generalis-
while, Tutdibi et al13 did not define the onset of labour in ability of our findings may be limited by the homogeneity
detail in their study. The diagnosis of labour onset may of this cohort, which only included Japanese women.
depend on the subjective opinion of the obstetrician or In conclusion, although studies with larger sample size
midwife. Objective indicators that can easily be deter- are required, we found that a lack of uterine contractions
mined are needed to identify TTN risk factors. This is before an elective caesarean section was significantly asso-
important because recently, in Japan, relatively few insti- ciated with TTN. Accurate risk stratification using a CTG
tutions allow vaginal birth after caesarean section, as they could assist in the management of infants who are at risk
are concerned about uterine rupture, with only approxi- of developing TTN.
mately 30% of institutions allowing planned vaginal birth
as an option after caesarean section.28 Antepartum CTG Acknowledgements We thank the study subjects for the use of their personal
can be routinely performed before elective caesarean data.
section without additional cost to easily and objectively Contributors SS and MT: data collection. SS: conception or design of the work. SS,
determine the presence or absence of uterine contrac- AA and MT: data analysis and interpretation; critical revision of the article. SS, AA
tions. As TTN is difficult to prevent, obstetricians, paedi- and MT: drafting of the article and final approval of the version to be published.
atricians and other medical professionals involved in an Funding The authors have not declared a specific grant for this research from any
elective caesarean section should be aware of the risk funding agency in the public, commercial or not-­for-­profit sectors.
factors of this complication and prepared to administer Competing interests None declared.
treatment. Patient consent for publication Not required.

4 Shinohara S, et al. BMJ Open 2020;10:e033154. doi:10.1136/bmjopen-2019-033154

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Provenance and peer review Not commissioned; externally peer reviewed. 14 Levine EM, Ghai V, Barton JJ, et al. Mode of delivery and risk of

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respiratory diseases in newborns. Obstet Gynecol 2001;97:439–42.
Data availability statement All data relevant to the study are included in the 15 Maeda E, Ishihara O, Tomio J, et al. Cesarean section rates and local
article. resources for perinatal care in Japan: a nationwide ecological study
Open access This is an open access article distributed in accordance with the using the National database of health insurance claims. J Obstet
Gynaecol Res 2018;44:208–16.
Creative Commons Attribution Non Commercial (CC BY-­NC 4.0) license, which
16 Vaughan DA, Cleary BJ, Murphy DJ. Delivery outcomes for
permits others to distribute, remix, adapt, build upon this work non-­commercially, nulliparous women at the extremes of maternal age - a cohort study.
and license their derivative works on different terms, provided the original work is BJOG 2014;121:261–8.
properly cited, appropriate credit is given, any changes made indicated, and the use 17 Oberg AS, VanderWeele TJ, Almqvist C, et al. Pregnancy
is non-­commercial. See: http://​creativecommons.​org/​licenses/​by-​nc/​4.​0/. complications following fertility treatment-­disentangling the role of
multiple gestation. Int J Epidemiol 2018;47:1333–42.
ORCID iD 18 Mazzoni A, Althabe F, Liu NH, et al. Women's preference for
Satoshi Shinohara http://o​ rcid.​org/​0000-​0003-​3124-​1141 caesarean section: a systematic review and meta-­analysis of
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