You are on page 1of 7

Journal of Perinatology

https://doi.org/10.1038/s41372-019-0436-4

ARTICLE

Amniotic fluid transitioning from clear to meconium stained during


labor—prevalence and association with adverse maternal and
neonatal outcomes
Daniel Tairy1 Ohad Gluck

1 ●
Ori Tal1 Jacob Bar1 Neri Katz2 Zvia Hiaev1 Michal Kovo1 Eran Weiner1
● ● ● ● ●

Received: 15 March 2019 / Revised: 11 May 2019 / Accepted: 28 May 2019


© The Author(s), under exclusive licence to Springer Nature America, Inc. 2019

Abstract
Objective The objective of this study is to compare pregnancy outcomes in deliveries complicated by primary meconium-
stained amniotic fluid (MSAF, present at membrane rupture) and secondary MSAF (transitioned from clear to MSAF during
labor).
Methods The medical records and neonatal charts of all deliveries ≥ 370/7 weeks between October 2008 and July 2018 were
1234567890();,:
1234567890();,:

reviewed. The primary outcome was composite adverse neonatal outcome that included early neonatal complications.
Results Of 30,215 deliveries during the study period, 4302 (14.2 %) were included: 3845 (89.4%) in the primary MSAF
group and 457 (10.6%) in the secondary MSAF group. The rate of the primary outcome was higher in the secondary MSAF
group (p = 0.006). This association remained significant after controlling for background confounders. The secondary
MSAF group had higher rate of cesarean deliveries (CDs) and assisted vaginal deliveries. There was a higher rate of
composite adverse neonatal outcome when secondary MSAF was diagnosed < 3 vs. >3 h before delivery (p = 0.004).
Conclusion Secondary MSAF was associated with higher rates of adverse neonatal outcome, CDs, and assisted vaginal
deliveries, compared with primary MSAF.

Introduction mortality [5–7]. The association has been shown to correlate


with the thickness of the meconium [6].
Meconium-stained amniotic fluid (MSAF) has been repor- Presence of MSAF at the time of membrane rupture
ted to occur in ~9.2–20.4% of deliveries [1, 2]. The fre- (primary MSAF) is a finding that is familiar to every
quency of MSAF increases with gestational age from obstetrician and has traditionally been thought to be a sign
31 weeks to term gestation and the independent predictors of fetal distress. However, large studies portraying the
for MSAF include advanced gestation, advanced maternal association between amniotic fluid transitioning from clear
age, preeclampsia, prolonged labor, labor induction, black to MSAF during labor (secondary MSAF) and maternal and
or South Asian ethnicity, and vaginal breech delivery [3, 4]. neonatal outcomes are lacking.
MSAF is associated with adverse maternal and neonatal Starting October 2008, we have implemented an insti-
outcomes including higher incidence of cesarean deliveries tutional protocol that mandates obstetricians and midwives
(CDs), severe fetal acidemia, low Apgar scores at 1 and to report their subjective impression of the color of amniotic
5 min, meconium aspiration syndrome, and perinatal fluid (clear, meconium stained, bloody) during every
delivery (both vaginal and CDs) and to specifically report
transition from clear to MSAF during labor. Prior to
* Eran Weiner October 2008, the color of amniotic fluid was described
masolbarak@gmail.com occasionally (not routinely), according to the medical
1
team’s judgment.
Department of Obstetrics and Gynecology, the Edith Wolfson
Therefore, 10 years after the implementation of the
Medical Center, Holon, Israel affiliated with Sackler Faculty of
Medicine, Tel Aviv University, Tel Aviv, Israel protocol, we aimed to study the differences between pri-
2 mary and secondary MSAF in correlation with various
Department of Neonatal Intensive Care, the Edith Wolfson
Medical Center, Holon, Israel affiliated with Sackler Faculty of adverse pregnancy and neonatal outcomes in a very large
Medicine, Tel Aviv University, Tel Aviv, Israel cohort from a single university hospital.
D. Tairy et al.

Methods of Obstetricians and Gynecologists criteria [12], which were


fully adopted by our institution for hypertensive disorders
Study population diagnosis and management.
Oligohydramnios was defined as amniotic fluid index
The medical records, delivery charts, and neonatal charts ≤ 5 cm and polyhydramnios as amniotic fluid index
of all singleton vertex deliveries ≥ 37 gestational weeks ≥ 24 cm [13].
between October 2008 (the time at which we began man- Immediately after birth, all neonates were examined by
dating the documentation of amniotic fluid characteristics in pediatricians. Birthweight percentiles for gestational age were
all delivery reports) and July 2018 from a single university assigned using the updated local growth charts [14]. Small for
hospital were reviewed. We excluded all deliveries < gestational age (SGA) was defined as actual birthweight ≤
37 weeks, multiple pregnancies, non-vertex presentation, 10th percentile for gestational age. The following data were
terminations of pregnancy, intra-uterine fetal deaths collected from the neonatal discharge records: cord blood pH,
(IUFDs), pregnancies with a known major fetal malforma- sepsis (positive blood or cerebrospinal fluid culture), need
tion, cases with missing data, and cases with clear/ bloody for blood transfusion, need for phototherapy, respiratory
amniotic fluid. According to our departmental protocol, distress syndrome, meconium aspiration syndrome, need for
early amniotomy is preferred in every labor (if membranes mechanical ventilation or support, necrotizing enterocolitis,
are intact), as part of active management of labor. intraventricular hemorrhage (all grades), hypoxic-ischemic
The study was approved by our institutional ethical encephalopathy, seizures (diagnosed clinically and confirmed
review board (decision number 0232-16-WOMC dated 28 electrographically by a pediatric neurologist), hypoglycemia
November 2017). (Blood glucose < 40 mg/dL), hypothermia,and periventricular
leukomalacia.
Exposure Our NICU protocol mandates routine cranial ultrasound
for every neonate born ≤ 34 weeks. Cranial ultrasound is
Maternal demographics, neonatal outcomes, and pregnancy performed in neonates > 34 weeks based on clinical
complications were compared between deliveries in which suspicion. Further imaging (such as magnetic resonance
MSAF was present from the time of membrane rupture imaging) is performed as needed. All cases with findings
(primary MSAF) and deliveries in which amniotic fluid suspicious for periventricular leukomalacia are routinely
transited from clear to MSAF during labor (secondary confirmed on repeat ultrasound at age 6–7 weeks.
MSAF). In addition, a comparison of the neonatal outcomes The following data regarding pregnancy outcome were
was performed for the cases of secondary MSAF between collected from the chart of each patient: induction of labor,
those in which the transition to meconium occurred < 3 h vs. placental abruption, mode of delivery (vaginal, assisted
>3 h from delivery. vaginal, or cesarean including the indication for CDs),
intrapartum fever, chorioamnionitis, revision of the uterine
Data collection cavity, manual removal of the placenta, postpartum
hemorrhage (that necessitated medical and/or surgical
The following characteristics were collected from the treatment), and postpartum blood transfusion.
medical chart of each patient: maternal age, gravidity, par- Intrapartum fever was defined as elevated temperature
ity, pre-pregnancy weight, and height (from which the body 38.0 °C or greater during labor with no other signs
mass index was calculated), gestational diabetes mellitus of chorioamnionitis. Clinical chorioamnionitis was
(GDM), pre-GDM, chronic hypertension, preeclampsia, diagnosed in the presence of maternal fever (temperature
smoking, gestational age at delivery, pre-pregnancy diag- 38.0 °C or greater) with no evidence of an extra uterine
nosis of thrombophilia (defined as any thrombophilia, cause accompanied by at least two of the following: fetal
inherited or acquired, which necessitated thrombo-prophy- tachycardia, maternal tachycardia, leukocytosis, uterine
laxis) [8, 9], drug abuse, oligohydramnios, polyhydramnios, tenderness, or new onset of foul-smelling vaginal dis-
epidural, and trials of labor after a previous CD. charge [15].
Gestational age was calculated based on the woman’s
first ultrasound examination in the pregnancy and last Primary outcome
menstrual period [10]. A woman was considered to have
diabetes mellitus if she had a diagnosis of type 1/type 2 in The primary outcome was a composite variable of neonatal
the medical record or GDM based on the National Diabetes morbidity, defined as any of the following: umbilical pH ≤ 7.1,
Group criteria [11]. Chronic hypertension and preeclampsia seizures, hypoxic-ischemic encephalopathy, intraventricular
were diagnosed according to the current American College hemorrhage, periventricular leukomalacia, hypoglycemia,
Amniotic fluid transitioning from clear to meconium stained during labor—prevalence and association. . .

hypothermia, mechanical ventilation, meconium aspiration Results


syndrome, respiratory distress syndrome, necrotizing enter-
ocolitis, phototherapy, sepsis, or transfusion. Characteristics of the study population

Secondary outcomes A total of 30,215 deliveries occurred at our institution


during the study period. After excluding cases of preterm
Secondary outcomes were pregnancy outcomes including deliveries, multiple pregnancies, non-vertex presentation,
the following: induction of labor, placental abruption, IUFD, terminations of pregnancy, known malformations,
mode of delivery (vaginal, assisted vaginal, or cesarean clear/bloody amniotic fluid, and cases with missing data—
including the indication for CDs), intrapartum fever, chor- 4302 (14.2%) deliveries—were analyzed: 3845 (89.4%) in
ioamnionitis, revision of the uterine cavity, manual removal the primary MSAF group and 457 (10.6%) in the secondary
of the placenta, postpartum hemorrhage (that necessitated MSAF group. Among the secondary MSAF group, 308
medical and/or surgical treatment), and postpartum blood (67.4%) transitioned to MSAF >3 h before delivery and 149
transfusion. (32.6%) transitioned to MSAF <3 h before delivery (Fig. 1).
Maternal demographics of the two groups are presented
Data analysis and compared in Table 1. Patients in the secondary MSAF
group were more likely to be older than 35 compared with
Data were analyzed using Epi info 7 (Centers for Disease patients in the primary MSAF group (17.1% vs. 13.7%, p =
Control and Prevention, Atlanta, GA). Data were presented 0.05). Patients in the secondary MSAF group were more
as follows: continuous variables are presented either as likely to be nulliparous and had lower rate of poly-
mean ± SD or as median and range, as appropriate. Cate- hydramnios, compared with patients in the primary MSAF
gorical variables are presented as n (%). Continuous para- group (41.4% vs. 31.9%, p < 0.001 and 0% vs. 2.4%, p <
meters were compared by the Student’s t-test and 0.001, respectively). The two groups did not differ in other
categorical variables by the χ2- with Yates’ correction test or background demographics.
the Fisher’s exact test, as appropriate. A statistically sig-
nificant p-value of < 0.05 was defined. Neonatal outcomes
Multivariate regression analysis models were used to
identify the independent association of secondary MSAF Neonatal outcomes are presented in Table 2. There was a
and the following outcomes: composite adverse neonatal significant difference in the rate of the primary outcome
outcome, CD, CD due to non-reassuring fetal heart rate (composite adverse neonatal outcome) between the sec-
monitoring (NRFHRM), and assisted vaginal deliveries ondary MSAF group, compared with the primary MSAF
(which separately serves as the dependent variables), (5.5% vs. 2.9%, p = 0.006), as well as the rate of neonatal
whereas the group (primary/secondary meconium), mater- hypoglycemia (1.5% vs. 0.6%, p = 0.04). There were no
nal age, gestational age at delivery, nulliparity, neonatal between-group differences in neonatal birthweight or the
birthweight, and induction of labor served as independent rate of SGA neonates. Table 3 presents neonatal outcomes
variables. for the cases of secondary MSAF, comparing those cases in

Fig. 1 Study design


30,215 deliveries during the study period Excluded (n=4741):
2,897 preterm deliveries
1,125 mulple pregnancies
265 IUFDs/terminaons
169 known malformaons
25,474 273 missing data
Deliveries assessed 12 non-vertex presentaon

20,855 Clear amnioc fluid


317 Bloody amnioc fluid
4,302
Deliveries included in the study

3,845 (89.4%) 457(10.6%)


Primary meconium group Secondary meconium group

308(67.4%) 149(32.6%)
Transion >3 hr before delivery Transion <3 hr before delivery
D. Tairy et al.

Table 1 Maternal demographics of the study groups Table 2 Neonatal outcomes of the study groups
Secondary Primary MSAF p-value Secondary Primary p-value
MSAF n = 457 n = 3845 MSAF n = 457 MSAF n = 3845

Composite adverse neonatal 25 (5.5) 111 (2.9) 0.006


Maternal age (years) 29.9 ± 5.5 29.5 ± 5.3 0.1 outcome (primary outcome)
Maternal age 78 (17.1) 527 (13.7) 0.05 Birthweight (gr) 3336 ± 397 3345 ± 422 0.6
> 35 years SGA 43 (9.4) 348 (9.1) 0.79
GA at delivery 39.3 ± 0.9 39.3 ± 1.1 1.0 Umbilical pH ≤ 7.1 2 (0.4) 9 (0.2) 0.32
(weeks) Seizures 0 (0) 4 (0.1) 1.0
Gravidity 2.6 ± 1.6 2.7 ± 1.7 0.1 Hypoxic-ischemic 0 (0) 6 (2) 1.0
encephalopathy
Parity 1.1 ± 1.2 1.3 ± 1.3 0.01
Intraventricular hemorrhage 0 (0) 1 (0.03) 1.0
Nulliparity 188 (41.4) 1225 (31.9) <0.001 Periventricular leukomalacia 1 (0.2) 0 (0) 0.10
BMI (kg/m2) 23.5 ± 3.3 23.7 ± 3.5 0.3 Hypoglycemia 7 (1.5) 24 (0.6) 0.04
GDM/PGDM 34 (7.4) 284 (7.4) 0.9 Hypothermia 0 (0) 2 (0.05) 1.0
Chronic hypertension 24 (5.2) 263 (6.8) 0.07 Mechanical ventilation 5 (1.1) 31 (0.8) 0.6
Meconium aspiration 5 (1.1) 39 (1.0) 0.8
Preeclampsia 24 (5.2) 263 (6.8) 0.2 syndrome
Smoking 70 (15.3) 499 (13.0) 0.2 Respiratory distress syndrome 0 (0) 2 (0.05) 1.0
Thrombophilia 9 (2.0) 74 (1.9) 0.9 Necrotizing enterocolitis 0 (0) 0 (0) 1.0
Drug abuse 3 (0.7) 28 (0.7) 1.0 Phototherapy 5 (1.1) 35 (0.9) 0.6
Sepsis 1 (0.2) 0 (0) 0.10
Oligohydramnios 20 (4.4) 143 (3.7) 0.5
Transfusion 2 (0.4) 13 (0.3) 0.7
Polyhydramnios 0 (0) 91 (2.4) <0.001
Epidural 379 (82.69) 3111 (80.9) 0.31 Continuous variables are presented as mean ± SD and categorical
variables as n (%) p-values in bold are statistically significant
TOLAC 31 (6.8) 253 (6.6) 0.8
SGA small for gestational age
Continuous variables are presented as mean ± SD and categorical
variables as n (%) p-values in bold are statistically significant
BMI body mass index, GDM gestational diabetes mellitus, PGDM pre- controlling for maternal age, gestational age at delivery,
gestational diabetes mellitus, TOLAC trial of labor after a previous
nulliparity, neonatal birthweight, and induction of labor.
cesarean
These included composite adverse neonatal outcome
(adjusted odds ratio (aOR) = 1.63, 95% confidence interval
which the transition to MSAF occurred <3 h vs. >3 h before (CI) 1.26–5.63), CD (aOR = 1.2, 95% CI 1.05–3.14), CD
delivery. There was a higher rate of composite adverse due to NRFHRM (aOR = 1.57, 95% CI 1.22–6.23), and
neonatal outcome when the diagnosis of secondary MSAF assisted vaginal deliveries (aOR = 1.12, 95% CI
occurred <3 h from delivery (10.1% vs. 3.2%, p = 0.004) 1.02–5.12).
and mean birthweight was significantly lower (3299 ± 336
vs. 3389 ± 345, p = 0.008).
Discussion
Pregnancy outcomes
Main findings
Table 4 presents pregnancy outcomes of the study groups.
Compared with the primary MSAF group, there were higher The aim of this study was to study the correlation between
rates of both assisted vaginal deliveries (10.1% vs. 6.0%, secondary MSAF and adverse pregnancy outcomes
p = 0.002) and CDs (22.3% vs. 16.6, p = 0.003) in the including maternal and neonatal morbidities, compared with
secondary MSAF group. Moreover, the rate of CDs due to primary MSAF. Our main findings were as follows: (1)
NRFHRM was higher in the secondary MSAF group secondary MSAF was subjectively described in about 1.8%
compared with the primary MSAF group (8.9% vs. 4.0%, of the term singleton deliveries studied; (2) secondary
p < 0.001). There was also a higher rate of inductions of MSAF was associated with our primary outcome of com-
labor in the secondary MSAF group (26.5% vs. 19.8%, p < posite adverse neonatal outcome; (3) within the secondary
0.001) compared with the primary MSAF group. Other MSAF, a transition to MSAF <3 h before delivery was
pregnancy outcomes including placental abruption, intra- associated with higher rate of composite of adverse neonatal
partum fever, chorioamnionitis, and maternal blood trans- outcomes; (4) compared with primary MSAF, secondary
fusions did not differ between the groups. MSAF was associated with higher rates of assisted vaginal
Table 5 presents the independent associations of deliveries and CDs (including CDs for NRFHRM), and
secondary MSAF and adverse pregnancy outcomes after higher rate of induction of labor.
Amniotic fluid transitioning from clear to meconium stained during labor—prevalence and association. . .

Table 3 Neonatal outcome in


Transition to MSAF <3 h Transition to MSAF >3 h p-value
the secondary MSAF group
before delivery n = 149 before delivery n = 308
stratified according to the time
of transition from clear to MSAF Composite adverse neonatal 15 (10.1) 10 (3.2) 0.004
outcome (primary outcome)
Birthweight (gr) 3299 ± 336 3389 ± 345 0.008
SGA 14 (9.3) 29 (9.4) 1.0
Umbilical pH ≤ 7.1 1 (0.6) 1 (0.3) 0.6
Seizures 0 (0) 0 (0) 1.0
Hypoxic-ischemic encephalopathy 0 (0) 0 (0) 1.0
Intraventricular hemorrhage 0 (0) 0 (0) 1.0
Periventricular leukomalacia 1 (0.6) 0 (0) 0.3
Hypoglycemia 4 (2.6) 3 (0.9) 0.16
Hypothermia 0 (0) 0 (0) 1.0
Mechanical ventilation 2 (1.3) 3 (0.9) 0.7
Meconium aspiration syndrome 3 (2.0) 2 (0.6) 0.18
Respiratory distress syndrome 0 (0) 0 (0) 1.0
Necrotizing enterocolitis 0 (0) 0 (0) 1.0
Phototherapy 3 (2.0) 2 (0.6) 0.18
Sepsis 1 (0.6) 0 (0) 0.32
Transfusion 1 (0.6) 1 (0.3) 0.6
Continuous variables are presented as mean ± SD and categorical variables as n (%) p-values in bold are
statistically significant
SGA small for gestational age

Table 4 Selected pregnancy outcomes in the study groups Table 5 Multivariable regression analysis for independent associations
with secondary MSAF
Secondary Primary MSAF p-value
MSAF n = 457 n = 3845 aOR* 95% CI

Induction of labor 121 (26.5) 760 (19.8) <0.001 Composite adverse neonatal outcome (primary 1.63 1.26–5.63
Placental abruption 6 (1.3) 73 (1.9) 0.5 outcome)
Cesarean delivery 102 (22.3) 639 (16.6) 0.003 Cesarean delivery 1.20 1.05–3.14
Cesarean delivery due 41 (8.9) 154 (4.0) <0.001 Cesarean delivery due to NRFHRM 1.57 1.22–6.23
to NRFHRM Assisted vaginal delivery 1.12 1.02–5.12
Assisted vaginal 46 (10.1) 231 (6.0) 0.002 *
Adjusted for: maternal age, gestational age at delivery, nulliparity,
delivery neonatal birthweight, and induction of labor
Intrapartum fever 5 (1.1) 22 (0.6) 0.2
Chorioamnionitis 2 (0.4) 20 (0.5) 1.0
9.2–20.4% of all deliveries [1, 2]. Previous studies have
Revision of the 19 (4.2) 153 (4.0) 0.8
uterine cavity suggested that the presence of MSAF may reflect fetal
Manual removal of the 7 (1.5) 100 (2.6) 0.2 maturity and not necessarily be a marker for fetal distress
placenta [2, 3, 16], although distinction between primary and sec-
Postpartum hemorrhage 28 (6.1) 302 (7.8) 0.2 ondary MSAF was not made in most previous studies.
Maternal blood 27 (5.9) 301 (7.8) 0.2 A few studies have investigated the difference between
transfusion primary and secondary MSAF. Meis et al. [17] in a land-
Continuous variables are presented as mean ± SD and categorical mark paper from 1978 described that “early heavy MSAF”
variables as n (%) p-values in bold are statistically significant was associated with increased fetal and neonatal morbidity
NRFHRM non-reassuring fetal heart rate monitoring and death, whereas “late passage of MSAF” encountered no
perinatal losses, but was associated with increased neonatal
Interpretation of the results in the context of morbidity occurring late in labor. They also described that
previous observations “early light MSAF (constituting over half of all meconium
cases) was not associated with any increased intrapartum or
The presence of MSAF during labor is a finding that is neonatal morbidity or death. Hiersch et al. [18] found that
familiar to every obstetrician, with a prevalence of the latter is associated with higher rate of both adverse
D. Tairy et al.

neonatal outcome and assisted vaginal delivery; Locatelli study. Second, we are aware of the possibility of mis-
et al. [19] found that secondary MSAF was associated with diagnosis of secondary MSAF as primary and vise versa
poorer neonatal outcomes including NICU admission, (fe.g., late amniotomy/“posterior” MSAF, which may not be
increased risk for low 5 min Apgar score and umbilical visible due to fetal position). Third, we have only collected
artery pH < 7.1 compared with controls with clear AF; Meis short-term neonatal outcomes. Lastly, we are aware that the
et al. [20] found, in another paper, that the combination of use of a composite outcome may be viewed as a limitation of
late passage of meconium in labor with NRFHRM may this study. However, we believe its utilization was neces-
indicate a fetus at risk for asphyxia. sary, because the individual components of the composite
However, all of these were of relatively small sample. are rare complications. We have described and validated the
Our study included a substantially larger cohort of women, same composite neonatal outcomes in our previous pub-
as well as a wider and more detailed spectrum of maternal lications with other pregnancy complications [21–23].
and neonatal outcomes. In addition, the very large cohort
allowed us to control for various confounders to validate
our results. These aspects provided the current study the Conclusion
power to discover further correlations between secondary
MSAF and adverse maternal and neonatal outcomes. In In conclusion, secondary MSAF observed in labor was
addition, the large cohort allowed us to specifically study associated with composite adverse neonatal outcome,
the correlation between secondary MSAF and adverse especially when diagnosed within the last 3 h of labor.
neonatal outcomes in relation to the transition time to Secondary MSAF was also associated with higher rates of
meconium during labor. assisted vaginal deliveries and CDs, particularly in the
In the current study we have found an association setting of NRFHRM. These findings highlight the impor-
between secondary MSAF and the primary outcome of tance of reporting intrapartum transition of amniotic fluid
composite adverse neonatal outcome (which was defined a from clear to MSAF, which should raise the alert of
priori). This result may not be surprising, as changing of AF obstetricians and neonatologists during labor.
from clear to MSAF during labor (secondary MSAF) may
indicate a new insult of fetal distress during labor. Further Acknowledgements We thank Meir Azran, Computing and Informa-
tion Systems, E. Wolfson Medical Center, Holon, Israel, and Ela
support of this hypothesis is the finding that neonates with
Smirin, archive, E. Wolfson Medical Center, Holon, Israel.
poorer outcome were those in which transition to MSAF
occurred <3 h before delivery. The direct correlation
Compliance with ethical standards
between secondary MSAF during labor and adverse neo-
natal outcomes emphasizes the concept of MSAF (and Conflict of interest The authors declare that they have no conflict of
specifically a transition to MSAF during labor) as a strong interest.
marker for inadequate fetal wellbeing. Moreover, secondary
MSAF was associated with a higher rate of both assisted Publisher’s note: Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional affiliations.
vaginal deliveries and CDs compared with primary MSAF.
Specifically, the rate of CDs due to NRFHRM was higher in
the secondary MSAF, which strengthens the hypothesis of
secondary MSAF as an indicator of fetal distress.
References
1. Whitfield JM, Charsha DS, Chiruvolu A. Prevention of meconium
Strengths and limitations aspiration syndrome: an update and the Baylor experience. Proc
(Bayl Univ Med Cent). 2009;22:128–31. https://doi.org/10.1080/
There are a few strengths of the current study: first, as 08998280.2009.11928491
2. David AN, Njokanma OF, Iroha E. Incidence of and factors asso-
far as we know, this is the largest study to be performed, ciated with meconium staining of the amniotic fluid in a Nigerian
in this topic, of over 30,000 deliveries from a single University Teaching Hospital. J Obstet Gynaecol (Lahore).
center. Second, we were able to study both neonatal 2006;26:518–20. https://doi.org/10.1080/01443610600797426
and maternal outcomes. Third, we specifically studied 3. Balchin I, Whittaker JC, Lamont RF, Steer PJ. Maternal and fetal
characteristics associated with meconium-stained amniotic fluid.
the correlation between secondary MSAF and adverse Obstet Gynecol. 2011;117:828–35. https://doi.org/10.1097/AOG.
neonatal outcomes in relation to the transition time to 0b013e3182117a26
meconium during labor. 4. Addisu D, Asres A, Gedefaw G, Asmer S. Prevalence of meco-
Our study is not without limitations. First, we are aware nium stained amniotic fluid and its associated factors among
women who gave birth at term in Felege Hiwot comprehensive
that the diagnosis of primary and secondary MSAF was a specialized referral hospital, North West Ethiopia: a facility based
subjective impression of the obstetrician or midwife during cross-sectional study. BMC Pregnancy Childbirth. 2018;18:429.
labor, which was not defined or standardized prior to the https://doi.org/10.1186/s12884-018-2056-y
Amniotic fluid transitioning from clear to meconium stained during labor—prevalence and association. . .

5. Hiersch L, Krispin E, Aviram A, Wiznitzer A, Yogev Y, Ashwal 14. Dollberg S, Haklai Z, Mimouni FB, Gorfein I, Gordon ES.
E. Effect of meconium-stained amniotic fluid on perinatal com- Birthweight standards in the live-born population in Israel. Isr
plications in low-risk pregnancies at term. Am J Perinatol. Med Assoc J. 2005;7:311–4. https://doi.org/10.3389/fped.2015.
2016;33:378–84. https://doi.org/10.1055/s-0035-1565989 00063
6. Ziadeh SM, Sunna E. Obstetric and perinatal outcome of preg- 15. Tita ATN, Andrews WW. Diagnosis and management of clinical
nancies with term labour and meconium-stained amniotic fluid. chorioamnionitis. Clin Perinatol. 2010;37:339–54. https://doi.org/
Arch Gynecol Obstet. 2000;264:84–7. https://doi.org/10.1007/ 10.1016/j.clp.2010.02.003
s004040000088 16. Ciftci AO, Tanyel FC, Ercan MT, Karnak I, Büyükpamukçu N,
7. Maymon E, Chaim W, Furman B, Ghezzi F, Shoham Vardi I, Hiçsönmez A. In utero defecation by the normal fetus: a radio-
Mazor M. Meconium stained amniotic fluid in very low risk nuclide study in the rabbit. J Pediatr Surg. 1996;31:1409–12.
pregnancies at term gestation. Eur J Obstet Gynecol Reprod Biol https://doi.org/10.1016/S0022-3468(96)90841-6
1998. https://doi.org/10.1016/S0301-2115(98)00122-5 17. Meis PJ, Hall M, Marshall JR, Hobel CJ. Meconium passage: A
8. American College of Obstetricians and Gynecologists Women’s new classification for risk assessment during labor. Am J Obstet
Health Care Physicians (ACOG). ACOG Practice Bulletin No. Gynecol. 1978;131:509–13. https://doi.org/10.1016/0002-9378
138. Inherited thrombophilias in pregnancy. Obstet Gynecol. (78)90111-4
2013;122:706–17. https://doi.org/10.1097/01.AOG.0000433981. 18. Hiersch L, Melamed N, Rosen H, Peled Y, Wiznitzer A, Yogev Y.
36184.4e New onset of meconium during labor versus primary meconium-
9. Committee on Practice Bulletins—Obstetrics, American College stained amniotic fluid - Is there a difference in pregnancy out-
of Obstetricians and Gynecologists. Practice Bulletin No. 132: come? J Matern Neonatal Med. 2014;27:1361–7. https://doi.org/
Antiphospholipid syndrome. Obstet Gynecol. 2012;120:1514–21. 10.3109/14767058.2013.858320
https://doi.org/10.1097/01.AOG.0000423816.39542.0f 19. Locatelli A, Regalia AL, Patregnani C, Ratti M, Toso L, Ghidini
10. American College of Obstetricians and Gynecologists. ACOG A. Prognostic value of change in amniotic fluid color during labor.
Practice Bulletin No. 101: Ultrasonography in pregnancy. Fetal Diagn Ther. 2005:20:5–9. https://doi.org/10.1159/
Obstet Gynecol. 2009;113:451–61. https://doi.org/10.1097/AOG. 000081359
0b013e31819930b0 20. Meis PJ, Hobel CJ, Ureda JR. Late meconium passage in labor - A
11. Expert Committee on the Diagnosis and Classification of Diabetes sign of fetal distress? Obstet Gynecol. 1982;59:332–5.
Mellitus. Report of the expert committee on the diagnosis and 21. Gluck O, Kovo M, Tairy D, Barda G, Bar J, Weiner E. Bloody
classificatin of diabetes mellitus. Diabetes Care. 2002;26:S5–20. amniotic fluid during labor – prevalence, and association with
https://doi.org/10.2337/diacare.25.2007.S5 placental abruption, neonatal morbidity, and adverse pregnancy
12. American College of Obstetricians and Gynecologists, Task Force outcomes. Eur J Obstet Gynecol Reprod Biol 2019;234(October
on Hypertension in Pregnancy. Hypertension in pregnancy. 2008):103–7. https://doi.org/10.1016/j.ejogrb.2019.01.011
Report of the American College of Obstetricians and Gynecolo- 22. Weiner E, Schreiber L, Grinstein E, Feldstein O, Rymer-Haskel N,
gists’ Task Force on Hypertension in Pregnancy. Obstet Gynecol. Bar J, et al. The placental component and obstetric outcome in
2013;122:1122–31. https://doi.org/10.1097/01.AOG.0000437382. severe preeclampsia with and without HELLP syndrome. Pla-
03963.88 centa. 2016;47:99–104. https://doi.org/10.1016/j.placenta.2016.
13. Kehl S, Schelkle A, Thomas A, Puhl A, Meqdad K, Tuschy B, 09.012
et al. Single deepest vertical pocket or amniotic fluid index as 23. Weiner E, Miremberg H, Grinstein E, Mizrachi Y, Schreiber L,
evaluation test for predicting adverse pregnancy outcome (SAFE Bar J, et al. The effect of placenta previa on fetal growth and
trial): a multicenter, open-label, randomized controlled trial. pregnancy outcome, in correlation with placental pathology. J
Ultrasound Obstet Gynecol. 2016;47:674–9. https://doi.org/10. Perinatol. 2016;36:1073–78. https://doi.org/10.1038/jp.2016.140
1002/uog.14924

You might also like