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Impact of Labor on Outcomes in Transient Tachypnea of the Newborn:

Population-Based Study
Erol Tutdibi, Katharina Gries, Monika Bücheler, Bjorn Misselwitz, Rolf L. Schlosser
and Ludwig Gortner
Pediatrics 2010;125;e577-e583; originally published online Feb 15, 2010;
DOI: 10.1542/peds.2009-0314

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Impact of Labor on Outcomes in Transient Tachypnea

of the Newborn: Population-Based Study
AUTHORS: Erol Tutdibi, MD,a Katharina Gries, MD,a WHAT’S KNOWN ON THIS SUBJECT: ECS is known as a main risk
Monika Bücheler, MD,b Bjorn Misselwitz, MD, MPH,c factor for TTN, because of its crucial role in perinatal lung fluid
Rolf L. Schlosser, MD,d and Ludwig Gortner, MDa clearance. Our study emphasizes and outlines the impact of labor
aCenter of Pediatrics and Neonatology, Children’s University
before birth on respiratory outcomes in TTN.
Hospital of Saarland, Homburg, Germany; bInstitute of Quality
Assurance Saarland, Saarbrucken, Germany; cInstitute of Quality
WHAT THIS STUDY ADDS: Our study indicates that TTN is
Assurance Hesse, Eschborn, Germany; and dDepartment of
Neonatology, Children’s University Hospital, Frankfurt, Germany strongly related to ECS and low GA. Furthermore, the absence of
exposure to labor contractions is associated with increased risk
transient tachypnea of the newborn, mode of birth, outcome, and severe course of TTN at term, with longer duration of oxygen
population-based studies supplementation.
TTN—transient tachypnea of the newborn
ECS— elective cesarean section
GA— gestational age
CS— cesarean section
OR— odds ratio
CI— confidence interval OBJECTIVE: Our aim was to assess the effect of labor on the risk and course of transient tachypnea of the newborn (TTN) in term neonates
doi:10.1542/peds.2009-0314 from a contemporary, population-based cohort.
Accepted for publication Oct 5, 2009 METHODS: We analyzed perinatal characteristics of term singleton
Address correspondence to Erol Tutdibi, MD, Children’s newborns (gestational age [GA] of ⱖ37 completed weeks) who were
University Hospital of Saarland, Center of Pediatrics and
born between January 2001 and December 2005 in the federal states of
Neonatology, Kirrberger Strasse, 66421 Homburg/Saar,
Germany. E-mail: Hesse and Saarland (Germany). TTN was diagnosed on the basis of
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). International Classification of Diseases, 10th Revision codes.
Copyright © 2010 by the American Academy of Pediatrics RESULTS: Of a total of 275 459 births, 239 971 fulfilled the inclusion
FINANCIAL DISCLOSURE: The authors have indicated they have criteria of GA of ⱖ37 completed weeks and singleton live birth. Among
no financial relationships relevant to this article to disclose. those, 13 346 term infants were admitted for neonatal care and 1423
were diagnosed as having TTN. The overall incidence of TTN was 5.9
cases per 1000 singleton live births in our study cohort. Elective cesar-
ean section, low GA, male gender, and low birth weight were associated
with TTN. The duration of oxygen supplementation for newborns with
TTN was associated inversely with the duration of labor (r ⫽ ⫺0.151;
P ⫽ .028).
CONCLUSIONS: Our study indicates that TTN is strongly related to elec-
tive cesarean section and low GA. Furthermore, the absence of expo-
sure to labor contractions is associated with increased risk and severe
course of TTN at term, with longer duration of oxygen supplementation.
Pediatrics 2010;125:e577–e583

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Postnatal respiratory complications ies reported that ECS increased the natal questionnaire includes informa-
among term infants are common. The risk of neonatal respiratory morbidity tion on all diagnoses, on the basis of
most commonly reported cause of and rates of admission to the NICU, International Classification of Diseases,
neonatal respiratory distress is tran- compared with GA-matched newborns 10th Revision codes. We excluded all sets
sient tachypnea of the newborn (TTN), after spontaneous vaginal delivery. of data that did not coincide completely
with an estimated incidence of 1% to The aim of this study was to assess in all of these variables and those that
2% of all newborns.1 The disorder is whether maternal characteristics, were incomplete. Data from infants with
reported to be benign and self-limiting, mode of birth, labor before birth, and congenital malformations affecting the
with resolution usually occurring by 2 perinatal factors were associated with cardiorespiratory system, chromosomal
to 5 days of age. In severe courses of the risk and course of TTN among term aberrations, depression at birth (Ap-
TTN, complications such as pneumo- singleton newborns in a large, repre- gar score at 5 minutes of ⬍7 or umbil-
thorax, need for extracorporeal mem- sentative, cohort study in Germany, ical artery pH of ⬍7.10), fetal hydrops,
brane oxygenation, and death have which has not yet been evaluated. Fur- or mothers with alcohol or drug abuse
been reported.2 Known risk factors for thermore, neonatal outcomes were also were excluded from the study. CS
TTN include lower gestational age (GA) addressed with respect to the progno- was defined as elective when surgery
and birth weight, male gender, and sis of respiratory failure in TTN, de- was performed before the onset of la-
elective cesarean section (ECS).3 pending on labor before birth. To the bor, with all other cases defined as
best of our knowledge, no studies have secondary CS.
In recent decades, the rates of cesar-
ean section (CS), especially those per- investigated the impact of labor on the
Identification of TTN Cases
formed electively at term and partly at severity of TTN courses.
The data sets for all newborns who
maternal request, have shown an in-
METHODS were transferred to a NICU because of
creasing trend.4 In Germany, accord-
respiratory problems were reviewed
ing to data supplied by the Federal Of- Study Population and Data Sources
thoroughly. TTN was defined on the ba-
fice for Quality Assurance, the overall We analyzed perinatal databases re- sis of characteristic clinical signs pre-
CS rate for all singleton deliveries in- corded by the national neonatal audit senting within 24 hours after birth and
creased constantly from 21.6% to program of the federal states of Hesse radiographic findings, in agreement
29.3% between 2001 and 2007.5 The and Saarland in Germany, for single- with most authors.1,6,8 We identified
major clinical reasons for performing tons born at GA of ⱖ37 weeks between newborns with TTN on the basis of re-
a CS have not changed and include January 2001 and December 2005. Re- spiratory distress diagnoses (Interna-
breech presentation, suspected fetal corded GAs were based on maternal tional Classification of Diseases, 10th
distress, failure to progress in labor, last menstrual period or early prena- Revision code P22), as reported to the
and previous CS. The fifth most com- tal ultrasound examination findings. Federal Office for Quality Assurance
mon indication for a CS has changed The register provides detailed infor- register by the responsible neonatolo-
and now is reported to be “maternal mation for ⬎98% of all infants born gist. Cases with suspicion of TTN were
request.” In the literature, the risks alive in Hesse and Saarland. The peri- validated through the absence of other
and benefits of ECS are controversial. natal birth registers include data morbidities affecting respiration, par-
Some authors favor planned CS in at- about the mother, the current preg- ticularly perinatal infection, persistent
tempts to prevent the fear of childbirth nancy and delivery, and the postnatal pulmonary hypertension, and meco-
associated with labor and delivery, uri- course, as documented by the obstetri- nium aspiration syndrome. Finally, we
nary and fecal incontinence, and pelvic cian in charge of the birth by using paired mother-infant data sets of all
prolapse. CS-related maternal morbid- an evaluated standardized question- eligible cases of TTN on the basis of
ity and mortality rates in the German naire.7 We also used neonatal data sets coinciding variables documented on
population have decreased markedly including data for all infants who were the perinatal and neonatal question-
in recent years. However, ECS remains admitted to a neonatal center in Hesse naires, including date and time of
major surgery, with potential impor- or Saarland within the first 10 postna- birth, zip code, gender, and birth
tant surgical complications for the tal days. Neonatal data were docu- weight. Therefore, deliveries were di-
mother that lead to extended hospital mented by the hospital to which the vided into groups without labor (no-
stays.6 The impact of ECS on neonatal infant was transferred and were re- labor group) and with labor (labor
respiratory outcomes was summa- ported to the neonatal audit center group). Outcome variables of interest
rized recently.2 Epidemiological stud- with another questionnaire. The neo- were diagnosis of TTN, oxygen therapy,

e578 TUTDIBI et al
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application of continuous positive

airway pressure therapy, mechani-
cal ventilation, antibiotic treatment,
extracorporeal membrane oxygen-
ation therapy, incidence of pulmonary
air leaks, duration of hospitalization,
and death. For qualitative comparison
with national data, the German Neona-
tal and Perinatal Database was used.5

Statistical Analyses
For statistical analyses, we used SPSS
15 (SPSS, Chicago, IL). Continuous vari-
ables were compared by using t tests
when data were distributed normally;
otherwise, the nonparametric Mann-
Whitney U test was used. Categorical
variables were analyzed by using Pear-
son’s ␹2 test or Fisher’s exact test, as
appropriate. Correlation studies were
performed by using Pearson’s correla-
tion coefficient. The statistical signifi-
cance level was set at P ⱕ .05 for all
analyses with 2-tailed comparisons.
Results of multivariate regression FIGURE 1
analyses (including the confounders Cohort design of study, with deliveries from 2001 to 2005 in the federal states of Hesse and Saarland
maternal age, parity, smoking, diabe-
tes mellitus, mode of delivery, GA, birth
weight, and gender) were expressed
as odds ratios (ORs) and 95% confi- with maternal data. Variables within summarized in Table 1. Compared with
dence intervals (CIs). the maternal and neonatal data sets the national German perinatal data for
coincided for 6843 (73.2%) of those term singletons born between 2001
RESULTS 9352 infants. There were no significant and 2005, study infants with TTN were
During the study period, the perinatal differences between all term infants more likely to have an inappropriate
birth registers included data for and those with matched perinatal data birth weight for GA (small for GA: 15.8%
275 459 deliveries, including 259 312 in sets, with respect to basic maternal vs 9.6%; large for GA: 13.5% vs 10.6%;
Hesse between 2001 and 2005 and and neonatal variables (data not P ⬍ .001) and more often were male
16 147 in Saarland between 2004 and shown). Of the 9352 admitted neo- (60.3% vs 51.4%; P ⬍ .001).
2005 (Fig 1). Among these deliveries, nates, postnatal respiratory problems The mode of birth was closely related
239 971 (87%) fulfilled the inclusion were found as leading causes for neo- to GA. Nearly 70% of all ECSs were per-
criteria of GA of ⱖ37 weeks and single- natal admission for a total of 2984 new- formed at GAs of 37 to 38 completed
ton live birth. Of these term newborns, borns (31.9%), including TTN (n ⫽ weeks. The main indications for ECSs
13 346 (5.6%) were transferred to a 1423), meconium aspiration syndrome were as follows: previous CS (31.7%),
neonatal ward. After application of the (n ⫽ 223), persistent pulmonary hy- breech presentation (17.6%), cephalo-
exclusion criteria (congenital anoma- pertension of the newborn (n ⫽ 24), pelvic disproportion (13.8%), and ma-
lies affecting the cardiorespiratory and infection (n ⫽ 1314). The overall ternal disorders (11.7%). For 11.6% of
system or chromosomal aberrations, incidence of TTN was 5.9 cases per ECSs, the indications for surgery in-
n ⫽ 1871; asphyxia, n ⫽ 1603; fetal hy- 1000 singleton live births in our study cluded other malpresentations, pla-
drops, n ⫽ 8; mothers with alcohol or cohort. cental and umbilical cord complica-
drug abuse, n ⫽ 512), data for the re- The main characteristics of the study tions, and pregnancy disorders. In
maining 9352 newborns were matched cohort and newborns with TTN are 13.6% of cases, however, the indication

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TABLE 1 Basic Perinatal Characteristics of Study Cohort and Newborns with TTN from week 42 to week 37; in the no-
Total TTN Germany Pb labor group, there was a significant in-
(N ⫽ 13 346) (N ⫽ 1423) (N ⫽ 2 675 841)a
crease in the incidence of TTN with de-
GA, mean ⫾ SD, wk 39.1 ⫾ 1.4 38.8 ⫾ 1.4
Birth weight
creasing GA from 40 to 37 weeks (P for
Mean ⫾ SD, g 3340 ⫾ 598 3351 ⫾ 556 trend ⬍ .01). ECSs at GAs of ⬍40 weeks
⬍10th percentile, % 19.6 15.8 9.2 ⬍.001 showed significantly greater risk for
⬎90th percentile, % 12.5 13.5 10.6 ⬍.001
Apgar score at 5 min, median (range) 9 (7–10) 9 (7–10)
TTN, compared with those at GAs of
Umbilical artery pH, mean ⫾ SD 7.28 ⫾ 0.07 7.27 ⫾ 0.07 ⬎41 weeks (37 weeks of gestation: OR:
Male, % 56.4 60.3 51.4 ⬍.001 4.8 [95% CI: 3.7– 6.3]; 38 weeks of ges-
ECS, % 20.7 42.2 9.2 ⬍.001
tation: OR: 3.7 [95% CI: 2.9 – 4.8]; 39
Data on term singletons obtained from Federal Office for Quality Assurance reports from 2001 to 2005.
b ␹2 test between TTN group and German population. weeks of gestation: OR: 3.4 [95% CI:
2.3– 4.7]; 40 weeks of gestation: OR: 2.0
[95% CI: 1.3–3.0]). Infants born vagi-
for ECS was not defined, and we might the German population (P ⬍ .001) (Ta- nally or through secondary CS showed
have evidence to suggest that CS at ble 1). When data were analyzed ac- no increased risk for TTN.
maternal request may account for this cording to the presence or absence of Data on clinical outcomes of new-
figure. labor and GA separately, the rate of
borns with TTN were compared be-
The TTN rate was linked inversely to GA TTN was greatly increased at each GA
tween the labor and no-labor groups,
and decreased with advancing GA from from 37 to 40 weeks for the no-labor
as summarized in Table 2. Nearly one
37 completed weeks onward (Fig 2). group, compared with the labor group
half of the infants with TTN needed
The overall frequency of ECS was 42.2% (Fig 2). In the labor group, the preva-
supplemental oxygen, irrespective of
among newborns with TTN, compared lence of TTN remained nearly un-
the mode of delivery. However, the
with 9.2% among term singletons in changed between 10.6% and 13.0%
absence of labor before birth was
significantly associated with longer
duration of oxygen supplementation
(P ⬍ .02) and higher rates of contin-
uous positive airway pressure ther-
apy (P ⬍ .05) and mechanical venti-
lation (P ⬍ .002). Infants with TTN
after ECS were more likely to develop
pulmonary air leaks, compared with
newborns after previous labor (2.8%
vs 1.0%; P ⬍ .05). No cases of extra-
corporeal membrane oxygenation
therapy and no neonatal deaths were
The duration of oxygen supplementa-
tion also was correlated inversely with
the duration of labor before birth (r ⫽
⫺0.151; P ⫽ .028). This correlation
remained significant with controlling
for GA, birth weight, and gender of
the newborn (P ⫽ .046). Multivariate
regression analysis of outcome vari-
ables, controlled for perinatal con-
FIGURE 2 founders, confirmed a significant im-
Relative risk of TTN from 37 to 42 weeks of gestation for newborns delivered vaginally or through pact on duration of oxygen therapy for
secondary CS (labor group) or ECS (no-labor group). *Crude relative risk of TTN in newborns delivered
through ECS (no-labor group), compared with GA-matched newborns after spontaneous vaginal de- ECS (OR: 2.2 [95% CI: 1.1–17.9]; P ⬍
livery and secondary CS (labor group). .05). Other outcome variables were

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TABLE 2 Therapy and Outcomes of Infants With TTN and Role of Labor et al18 (5.7 cases per 1000 infants) and
All Infants With TTN Labor Group No-Labor Group P Riskin et al19 (7.2 cases per 1000 in-
(N ⫽ 1423) (N ⫽ 625) (N ⫽ 456)
fants). The inclusion of neonates with
Oxygen supplementation, n (%) 580 (40.7) 258 (41.1) 208 (45.7) .141a
Duration of oxygen supplementation, 1.3 ⫾ 0.9 1.1 ⫾ 0.6 1.3 ⫾ 1.1 ⬍.02b
TTN with GAs of ⱖ35 weeks might ex-
mean ⫾ SD, d plain the higher incidence of TTN in the
Mechanical ventilation, n (%) 60 (4.2) 22 (3.5) 36 (7.9) ⬍.01a study by Riskin et al.19
Continuous positive airway pressure 58 (4.1) 17 (2.7) 26 (5.7) ⬍.05a
therapy, n (%) We found that TTN risk was associ-
Pulmonary air leaks, n (%) 22 (1.5) 6 (1.0) 13 (2.8) ⬍.05a ated strongly with the mode of deliv-
Antibiotic therapy, n (%) 307 (21.6) 177 (28.3) 112 (24.5) NSa
Duration of hospital stay, median 5 (1–15) 5 (1–11) 5 (1–14) NSb
ery and GA. The overall rate of ECS
(5th to 95th percentile range), d was substantially higher in new-
Obstetric data were available for 76% of newborns with TTN (1081 of 1423 newborns) after maternal-neonatal data borns with TTN, compared with term
matching. NS indicates not significant.
a Pearson ␹2 test.
singletons in the German population
b Nonparametric Mann-Whitney U test. (42.2% vs 9.2%; P ⬍ .001). Other risk
factors for TTN were male gender
and inappropriate birth weight for
found not to be influenced by con- factor in TTN.8,9 Defects in active pulmo- GA. Our results agree with previously
founders and mode of birth. nary epithelial sodium transport,10 reported studies that demonstrated
mild pulmonary immaturity and tran- the association of ECS with higher
DISCUSSION sient surfactant deficiency,11 and myo- risk for neonatal respiratory mor-
The present study indicates the posi- cardial left-heart failure attributable bidity and the importance of timing
tive impact of labor on respiratory out- to asphyxia have been discussed as the of ECS to GA of ⱖ39 weeks, to de-
comes among infants with TTN, in main potential pathogenic factors op- crease the TTN risk.18,20–25 In line with
agreement with previous studies; the erative in dysfunction of postnatal lung the report by Richardson et al,26 how-
absence of labor in infants with TTN liquid clearance and TTN pathophysio- ever, ECS performed even at a GA of
was associated with higher rates of logical processes.12 Studies on genetic 40 completed weeks was associated
continuous positive airway pressure risk factors for TTN demonstrated that with a significant increase in the TTN
therapy, mechanical ventilation, and certain functional polymorphisms in rate in our study, which demon-
complications from pulmonary air the ␤-adrenergic receptor– encoding strates the beneficial effects of labor
leaks and longer duration of oxygen genes are associated with higher TTN in the mechanisms mediating post-
supplementation, in comparison with risk.13–15 Rapid clearance of fetal lung natal lung liquid clearance.
infants with TTN who were delivered fluid during postnatal lung adaptation
after having been exposed to uterine Our study has several limitations.
is largely correlated with the onset of
contractions. Multivariate regression The main limitation is that the peri-
labor before birth.16 Labor enhances
analyses, with correction for perinatal natal registers used for this study
the release of catecholamines in ma-
confounders, established that the ab- may contain coding inaccuracies and
ternal and fetal circulation, resulting
sence of labor increased the duration in ␤-adrenergic receptor–mediated data entry errors, which are inher-
of oxygen supplementation by a factor upregulation of surfactant synthesis ent in all population-based analyses.
of 2. The duration of labor was linked and transepithelial sodium ion trans- In our study, 26.8% of all data sets for
significantly to the duration of oxygen port, with subsequent fluid reabsorp- infants who were admitted to the
supplementation (r ⫽ ⫺0.151; P ⫽ tion, in the neonatal lung. Infants deliv- neonatal ward could not be con-
.028). The length of hospital stay for ered through ECS often are deprived of nected with maternal data (for new-
infants presenting with TTN did not dif- this labor-related physiological stress borns with TTN, the matching rate
fer on the basis of labor. response pattern at birth and conse- was 76%). We are aware of the pos-
We suggest that both the incidence and quently experience failure of postnatal sibility that the results might be bi-
severity of TTN are affected by labor respiratory transition.17 According ased by the high loss rate. However,
before birth. TTN is the most common to our study results from a large, basic validation analyses of the main
cause of neonatal respiratory distress population-based, birth cohort, the maternal and neonatal characteris-
in term neonates. Delayed resorption rate of TTN was 0.59% (1423 cases per tics and outcome variables for all
of fetal lung fluid after delivery is con- 239 971 infants), which is comparable 9352 neonates and the 6843 matched
sidered the main pathophysiological to the previous reports by Morrison newborns demonstrated no signifi-

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cant differences, which indicated sence of labor are strongly related to According to the analyses of our data
that the findings are robust. the development of TTN in newborns, and previously reported data, it seems
Despite these limitations, the strengths irrespective of GA, even at term. Our that awaiting the onset of labor before
of our study are the large number analyses are in good accordance delivery reduces significantly the risk of
of term newborns from a 5-year, with previous data indicating ECS, postnatal development of TTN and im-
population-based cohort, the maternal low GA, male gender, and inappropri- proves the clinical course of respira-
and obstetric variables available for ate birth weight as main risk factors tory failure. Every pregnant woman
analysis, and the fact that infants with for TTN. Furthermore, the presence of justifiably wishes a short labor
TTN were selected accurately after exclu- labor before birth was shown to improve and an uneventful delivery without
sion of other predetermined causes of respiratory outcomes for infants with complications. Therefore, a growing
respiratory distress, such as perinatal TTN. To the best of our knowledge, this is number of mothers tend toward ECS.
infection, meconium aspiration syn- the first study to demonstrate that not During the decision-making process,
drome, asphyxia, and congenital anoma- only the presence or absence but also women should be given reliable in-
lies. Our main concern was the compara- the duration of labor before birth posi- formation about the risks and bene-
bility of a large number of newborns with tively influences the course of TTN, with a fits associated with CS. When no
validated TTN differentiated according to shorter need for supplemental oxygen clear medical indication or benefit to
the mode of delivery. therapy. No correlations with other out- the mother or fetus is given and ECS
come variables were found. Our results is planned, we suggest, on the basis
CONCLUSIONS clearly indicate ECS as the main risk fac- of our findings, that CS be postponed
The main finding of the present study tor for TTN and the crucial role of labor in until a GA of 39 completed weeks
is that the mode of birth and the ab- respiratory outcomes in TTN. whenever possible.
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PEDIATRICS Volume 125, Number 3, March 2010 e583

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Impact of Labor on Outcomes in Transient Tachypnea of the Newborn:
Population-Based Study
Erol Tutdibi, Katharina Gries, Monika Bücheler, Bjorn Misselwitz, Rolf L. Schlosser
and Ludwig Gortner
Pediatrics 2010;125;e577-e583; originally published online Feb 15, 2010;
DOI: 10.1542/peds.2009-0314
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