1. EURO-6277; No of Pages 5
European Journal of Obstetrics & Gynecology and
Reproductive Biology xxx (2008) xxx–xxx
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Factors associated with umbilical artery acidemia in term
infants with low Apgar scores at 5 min
Anna Locatelli a,*, Maddalena Incerti a, Alessandro Ghidini a,
Massimiliano Greco a, Elisabetta Villa b, Giuseppe Paterlini b
a
Department of Obstetrics and Gynecology, San Gerardo Hospital, University of Milano-Bicocca, Via Solferino 16, 20052 Monza (MI), Italy
b
Department of Neonatology, San Gerardo Hospital, University of Milano-Bicocca, Monza, Italy
Received 13 June 2007; received in revised form 3 December 2007; accepted 9 January 2008
Abstract
Objective: To evaluate predictors of umbilical artery acidemia in term neonates with low Apgar score.
Study design: From a cohort of term singleton deliveries over a 13-year period, we selected neonates with 5-min Apgar score <7. Acidemia
was defined as umbilical artery pH < 7.00 or base excess (BE) À12 mmol/L. Three pathogenic processes of neonatal acidemia were
evaluated: (1) intrauterine vascular disease, defined as preeclampsia, clinical diagnosis of placental abruption, birth weight <10th centile, or
histologic evidence of placental infarction or severe vascular pathology, (2) intrauterine infection, defined as clinical chorioamnionitis,
histologic chorioamnionitis, or early neonatal sepsis, and (3) acute intrapartum events, which included cases of cord prolapse, amniotic fluid
embolism, uterine rupture, sudden and sustained fetal bradycardia or absence of FHR variability with a previously normal pattern, shoulder
dystocia or complicated breech extraction. The associations of such processes with umbilical artery evidence of acidemia were tested using
x2, Fisher’s exact test, Student’s t-test, and logistic regression, with P < 0.05 or odds ratio (OR) with 95% confidence interval (CI) not
inclusive of the unity considered significant.
Results: Among the 27,395 neonates in the cohort, an Apgar score at 5 min <7 was recorded in 94 (0.32%) and it was associated with
umbilical artery acidemia in 33 cases. Logistic regression analysis showed that intrauterine vascular disease was independently associated
with umbilical cord acidemia (P = 0.035, OR = 3.2, 95% CI = 1.1–9.7) whereas intrauterine infection (OR = 1.1, 95% CI 0.4–3.4) and acute
intrapartum events (OR = 2.1 95% CI 0.6–7.0) were not.
Conclusions: Umbilical artery evidence of acidemia is present in 38% of term babies with low Apgar score and it is predominantly associated
with chronic antepartum vascular disease. Neither intrauterine infection nor acute intrapartum events are significantly associated with
umbilical artery acidemia.
# 2008 Elsevier Ireland Ltd. All rights reserved.
Keywords: Low Apgar score; Umbilical artery acidemia; Term pregnancy
Because metabolic acidosis signals greater risk of
1. Introduction
subsequent neurologic injury and multiorgan dysfunction
In 1952, Virginia Apgar proposed her score as a means of [4], measurement of umbilical artery pH has been widely
evaluating the physical condition of infants shortly after adopted as an adjunct to the Apgar score for assessing the
delivery and of predicting neonatal survival [1,2]. A low condition of newborn infants. Indeed, results of cord blood
Apgar score at 5 min at term is commonly indicative of a gas analysis provide a more precise assessment of the
neonate at greater risk of death [3]. newborn than Apgar scores alone [5]. Whereas respiratory
acidosis is usually due to intrapartum events and is not
associated with adverse neonatal outcome [6], metabolic
acidosis can portend greater risks of neonatal asphyxia,
* Corresponding author. Tel.: +39 039 233 4720; fax: +39 039 233 3820.
encephalopathy and cerebral palsy [7]. An umbilical artery
E-mail address: anna.locatelli@unimib.it (A. Locatelli).
0301-2115/$ – see front matter # 2008 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.ejogrb.2008.01.003
Please cite this article in press as: Locatelli A, et al., Factors associated with umbilical artery acidemia in term infants with low Apgar
scores at 5 min, Eur. J. Obstet. Gynecol (2008), doi:10.1016/j.ejogrb.2008.01.003

2. EURO-6277; No of Pages 5
2 A. Locatelli et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology xxx (2008) xxx–xxx
pH < 7 and a BE À12 mmol/L have been suggested as Meconium was graded as thin or thick, the latter being
optimal cut-offs to define fetal metabolic acidosis [8]. greenish, opaque and non-watery. Only thick meconium was
Although the Apgar score provides a convenient short- considered for the purpose of the statistical analysis. Blood
hand for the status of the newborn, it is often incorrectly used samples from umbilical arteries were routinely obtained
as a correlate of neonatal acidosis. In fact, only a minority of immediately after delivery on all infants deemed to be
neonates with low Apgar scores at 5 min have cord evidence viable. The samples were placed in ice and blood gas
of metabolic acidosis [9]. We have examined the prenatal analysis, inclusive of pH and base excess (BE), was usually
characteristics of term infants with low Apgar scores at performed within 15 min of delivery (Blood Gas Analyzer
5 min to evaluate predictors of cord blood gas evidence of OMNI 3 e OMNI S Roche, Basel; Switzerland). Small-for-
gestational age was defined as a birth weight <10th centile
metabolic acidosis.
adjusted for gender and gestational age according to Italian
standards [11].
Placentas were collected and examined in high-risk
2. Materials and methods
pregnancies or in the presence of perinatal complications.
We have accessed a prospectively collected database of Histopathologic findings were classified according to
neonates born at 37.0 weeks or greater at our institution from standard published protocols [12]. Acute inflammatory
1/1993 to 12/2005. The computerized obstetric and neonatal lesions in the amnion, umbilical and chorionic vessels, and
databases of S. Gerardo Hospital, Monza, Italy, provide choriodecidua were classified as present or absent indepen-
information on all births occurring at the hospital. Data dently from the severity or extent of the lesions.
concerning labor and delivery are abstracted and recorded Uteroplacental vascular pathology was defined as evidence
within 24 h of delivery. The hospital is a tertiary care facility of absent or incomplete conversion of the basal spiral
and serves as referral center for a vast area north-east of arteries, placental abruption, villous infarcts and fibrosis,
Milan. Strict and consistent diagnostic and clinical manage- fibrinoid necrosis, atherosis, increased syncythial knotting,
ment algorithms were implemented in labor and delivery and X-cell proliferation. Neonatal outcome variables
during the study period for term deliveries. Such algorithms considered were hypoxic–ischemic encephalopathy [13];
differed for pregnancies classified as low risk or high risk. multiorgan dysfunction (defined as involvement of one or
The study fulfilled the exemption criteria from submission to more organ system, lung, kidneys, heart, and intestines); and
the Institutional Review Board because it involved existing neonatal death [14].
Statistical analysis included x2 or Fisher’s exact test for
data and the information was recorded by the investigator in
such a manner that individual subjects could not be categorical variables, Student’s t-test for continuous vari-
ables, and logistic regression with a two-tailed P < 0.05 or
identified, directly or through identifiers linked to the
subjects. an odds ratio (OR) with 95% confidence interval (CI) not
Included in the present study were all singleton, liveborn inclusive of unity considered significant. Perinatal variables
neonates without major congenital anomalies and with a 5- were evaluated in reference to umbilical artery evidence of
acidemia, defined as pH < 7.0 and/or BE À12 mmol/L
min Apgar score <7. The attending obstetric and/or
pediatric personnel were responsible for assignment of [8]. In addition to the information recorded in the database,
the Apgar scores. Gestational age was based on the date of we have computed the following three composite variables
the last menstrual period and prenatal ultrasound examina- to shed light onto the processes underlying cord blood
tion before 22 weeks, which is routinely done at our acidemia: (1) intrauterine vascular disease, defined as
preeclampsia (blood pressure >140/90 mmHg with protei-
institution.
nuria >300 mg/24 h or >100 mg/dl in two specimens
Fetal heart rate (FHR) monitoring pattern on admission or
collected >6 h apart), clinical diagnosis of placental
during labor was interpreted according to the Boylan
abruption, birth weight <10th centile, or histologic evidence
classification [10]. FHR was monitored intermittently
during the first and second stage of labor by certified nurse of placental infarction or severe vascular pathology [15]. (2)
midwives. Continuous electronic monitoring was imple- Intrauterine infection, defined as clinical chorioamnionitis
mented in the presence of obstetric or medical risk factors, or (diagnosed in the presence of two or more of the following:
temperature elevation to at least 38 8C, white blood cell
if the FHR was non-reassuring at intermittent auscultation.
A tracing was considered non-reassuring if it presented any count at least 15,000 cells/mm, uterine tenderness and foul-
of the following characteristics: persistent tachycardia smelling amniotic fluid); histologic chorioamnionitis; or
>180 beats/min, reduced or absent variability (<5 bpm); early neonatal sepsis (diagnosed in the presence of positive
bradycardia <100 beats/min lasting longer than 10 min; blood cultures within 72 h of birth). (3) Acute intrapartum
repetitive late decelerations or severe variable decelerations. events, defined as cases of cord prolapse, amniotic fluid
All tracings within 1 h of birth were reviewed to confirm embolism, uterine rupture, sudden and sustained fetal
appropriate classification. Amniotic fluid characteristics bradycardia or absence of FHR variability with pattern
(including subjective assessment of amniotic fluid volume at previously normal, shoulder dystocia, or complicated breech
membrane rupture and fluid color) were also recorded. extraction [4,8,16].
Please cite this article in press as: Locatelli A, et al., Factors associated with umbilical artery acidemia in term infants with low Apgar
scores at 5 min, Eur. J. Obstet. Gynecol (2008), doi:10.1016/j.ejogrb.2008.01.003

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Table 1
Demographic and antepartum characteristic of gestations resulting in neonates with 5-min Apgar score <7
À12, N = 33 pH ! 7 and/or BE > À12, N = 53
pH < 7 and/or BE
Variable P-value
32.6 Æ 4.2 32.7 Æ 4.7
Maternal age (years) 0.91
Caucasian ethnicity 30 (90.9%) 47 (88.6%) 1
Nulliparity 25 (75.7%) 35 (66.0%) 0.47
39.7 Æ 1.4 40 Æ 1.1
Gestational age at delivery (weeks) 0.60
Premature rupture of membranes 11 (33.3%) 16 (30.1%) 0.94
Diabetes 0 (0%) 5 (9.4%) 0.17
Preeclampsia 3 (9.0%) 0 (0%) 0.053
Data are expressed as no. (%), or mean Æ S.D. BE: base excess, expressed in mmol/L.
Placental information was available in 56/86 (65%)
3. Results
cases. No significant differences were observed in the rates
A cohort of 29,395 consecutive pregnancies fulfilled the of placental diagnoses of inflammatory or vascular lesions
study inclusion criteria. A 5-min Apgar score <7 was (Table 2).
reported in 94 cases (0.32%) and a score <3 in 9 cases We then evaluated two composite variables that reflect
(0.03%). Cord gas analysis was obtained in 86/94 cases with intrauterine processes antedating labor and which are often
5-min Apgar score <7 (in 8 cases gas analysis was not implicated in the causation of low Apgar scores and fetal
performed), which constitute the study population. Umbi- acidemia: intrauterine infection and vascular disease.
lical artery evidence of acidemia was present in 33/86 Neonates with low Apgar score and umbilical artery
(38%). The range of umbilical artery BE of cases with acidemia had higher rates of intrauterine vascular disease
umbilical artery acidemia was À25; À11, while in cases (preeclampsia, abruptio placentae, birth weight <10th
without acidemia was À11.5; À0.1. When we compared centile and placental vascular pathology) than those non-
prenatal variables in cases of low Apgar scores with acidemic (12/33 or 36% vs. 7/53 or 13%, P = 0.012;
umbilical artery acidemia and those without, only maternal OR = 3.7, 95% CI 1.3–10.6), whereas rates of intrauterine
preeclampsia approached statistical significance (Table 1). infection (clinical chorioamnionitis, histologic chorioam-
Table 2 displays the obstetric characteristics of the two nionitis and early neonatal sepsis) were similarly repre-
groups; abruptio placentae was the only event more frequent sented in the two groups (8/33 or 24% vs. 12/53 or 23%,
in acidemic babies. A non-reassuring FHR tracing obtained P = 0.9; OR = 1.1, 95% CI 0.4–2.9). Of interest the
antepartum or intrapartum was observed in 27/33 or 82% of significant association between non-reassuring FHR tracing
cases with umbilical artery acidemia and in 30/53 or 57% of and umbilical artery acidemia observed at univariate
those without acidemia (P = 0.04; OR 2.8, 95% CI 1.1, 7.5). analysis lost significance after taking into account intrau-
In all cases in which FHR tracing was the main indication for terine vascular disease using logistic regression analysis
operative delivery, the baby was born within 30 min of the (P = 0.1, OR = 2.4, 95% CI = 0.8–6.6), suggesting that non-
decision to intervene. In 2 cases of acidemic babies (6%) reassuring FHR tracings reflect in part an underlying
FHR was monitored during labor with intermittent intrauterine vascular disease. In 6 cases (4 in acidemic and 2
auscultation rather than continuously. in non-acidemic neonates) a sudden and sustained fetal
Table 2
Obstetric and histologic characteristics of gestations resulting in neonates with 5-min Apgar score <7
À12, N = 33 pH ! 7 and/or BE > À12, N = 53
pH < 7 and/or BE
Variable P-value
Induction of labor 9/22 (57.9%) 17/42 (43.2%) 0.97
Clinical chorioamnionitis 3 (9.0%) 8 (15.1%) 0.51
Cord prolapse 1 (3.0%) 0 (0%) 0.38
Abruptio placentae 4 (12.1%) 1 (1.8%) 0.07
Oxytocin use 11/22 (50%) 22/42 (52.3%) 0.85
Thick meconium-stained amniotic fluid 13 (39.3%) 24 (45.2%) 0.59
Amniotic fluid embolism 1 (3.0%) 0 (0%) 0.38
Oligohydramnios 2 (6.0%) 8 (15.1%) 0.30
Polyhydramnios 2 (6.0%) 4 (7.5%) 1
Cesarean delivery 20 (60.6%) 30 (56.6%) 0.71
Operative vaginal delivery 4 (12.1%) 2 (3.7%) 0.19
Shoulder dystocia 1 (3.0%) 3 (5.6%) 1
Breech extraction 0 (0%) 1 (1.8%) 1
Uterine rupture 0 (0%) 0 (0%) 1
Acute placental inflammatory lesions 5/21 (23.8%) 9/35 (25.7%) 1
Uteroplacental vascular lesion 6/21 (28.5%) 4/35 (11.4%) 0.20
Data are expressed as no. (%), or mean Æ S.D. BE: base excess, expressed in mmol/L.
Please cite this article in press as: Locatelli A, et al., Factors associated with umbilical artery acidemia in term infants with low Apgar
scores at 5 min, Eur. J. Obstet. Gynecol (2008), doi:10.1016/j.ejogrb.2008.01.003

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Table 3
Logistic regression analysis of predictors of neonatal acidosis
P-value Odds ratio 95% confidence interval
Intrauterine vascular disease 0.01 4.10 1.37–12.2
Intrauterine infection 0.84 1.10 0.37–3.37
Acute intrapartum events 0.24 2.07 0.61–7.01
Table 4
Characteristics and outcome of neonates with 5-min Apgar score <7 according to umbilical artery evidence of acidosis
À12, N = 33 pH ! 7 and/or BE > À12, N = 53
pH < 7 and/or BE
Variable P-value
Apgar score 3 at 5 min 6 (18.1%) 3 (5.6%) 0.08
Female sex 12 (36.3%) 22 (41.5%) 0.63
3284 Æ 591 3312 Æ 453
Birth weight (g) 0.79
47.6 Æ 32.3 46.8 Æ 30.9
Birth weight centile 0.91
Birth weight 10th centile 5 (15.1%) 3 (5.6%) 0.25
Early neonatal sepsis 0 (0%) 0 (0%) 1
Data are expressed as no. (%), or mean Æ S.D. BE: base excess, expressed in mmol/L.
bradycardia or absence of FHR variability was recorded, neonatal muscular, neurologic or cardiovascular diseases
with a previously normal pattern. FHR monitoring was [4]. Conversely, we have observed that intrapartum events
continued until delivery in 5/6 cases, in the remaining one leading to low Apgar scores can be severe enough to cause
the tracing was discontinued 10 min before delivery. Rates permanent neurologic damage without causing acidemia
of acute intrapartum events (cord prolapse, amniotic fluid (for example, trauma at delivery from shoulder dystocia).
The strengths of our study include a rate of Apgar score <7
embolism, uterine rupture, sudden occurrence of non-
reassuring FHR tracing, shoulder dystocia, and complicated in our population (0.3%) consistent with that reported in the
breech extraction) were not significantly associated with recent literature (0.4%) [3]; umbilical artery gas analysis
umbilical artery acidemia (7/33 or 21% vs. 7/53 or 13%, performed in 90% of cases; data collected prospectively, and
P = 0.33; OR = 1.8, 95% CI 0.6–5.4), even after controlling management of labor and delivery following specific and
for the other two composite variables using logistic consistent protocols. Thus we feel that our analysis is based on
regression (P = 0.24) (Table 3). data largely free from selection biases. A limitation of our
As shown in Table 4, there were no significant differences study is that data were not always available in every case; in
in the characteristics of neonates with 5-min Apgar score <7 particular, placental information was missing in 35% of cases.
according to umbilical artery acidemia. Babies with low A pathologic antepartum or intrapartum FHR tracing in
Apgar score and cord acidemia had a neonatal course more neonates with low Apgar scores is associated with a higher
frequently complicated by hypoxic–ischemic encephalopathy probability of metabolic acidosis. As previously reported,
(19/33 or 57.6% vs. 8/53 or 15.1%, P < 0.01; OR = 7.9, 95% however, abnormal FHR tracings have a high false positive
CI 2.4–26.1) or multiorgan dysfunction (9/31 or 29.0% vs. 4/ rate in the prediction of acidosis (in our series of neonates with
48 or 8.3%, P = 0.03; OR = 7.6, 95% CI 2.6–24.3). In the low 5-min Apgar scores it was 57%). Predictive fetal heart rate
acidemic group there were 2 (7%) neonatal deaths, while none patterns demonstrate good sensitivity but poor specificity with
occurred among non-acidemic babies (P = 0.14). Three of the many false positives for intrapartum fetal asphyxia [17]. On
surviving infants developed cerebral palsy, two in the the other hand, in nearly 1 out of 5 (21%) neonates with low
acidemic group and one in the non-acidemic group. Apgar scores at 5 min and acidemia the FHR tracing did not
provide clues of the impending outcome.
In an attempt to understand whether events leading to
umbilical cord acidosis are acute or chronic in nature, we
4. Discussion
grouped together acute intrapartum hypoxic events accord-
ing to an established classification [4,8,16]. No significant
Although low Apgar scores are often considered as
correlates of neonatal acidosis, in our series umbilical artery difference was present in rates of acute events between cases
evidence of acidemia is present only in 38% of babies with with vs. without acidemia. This finding is in line with what
Apgar scores <7 at 5 min. This finding underscores the has been reported in two series evaluating predictors of
importance of obtaining umbilical artery gas analysis in the hypoxic–ischemic encephalopathy [4,18]. We have explored
presence of any depressed neonate, and of not equating low chronic processes which are prevalent in the pregnant
Apgar scores to intrapartum asphyxia. Indeed, factors other population and may lead to acidemia: intrauterine vascular
than acidosis are at play in the majority of neonates with low pathology and intrauterine infection. We integrated placen-
tal pathology findings, which were available in 63% of cases,
Apgar scores, such as maternal sedation, infection, or
Please cite this article in press as: Locatelli A, et al., Factors associated with umbilical artery acidemia in term infants with low Apgar
scores at 5 min, Eur. J. Obstet. Gynecol (2008), doi:10.1016/j.ejogrb.2008.01.003

5. EURO-6277; No of Pages 5
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[4] American College of Obstetricians and Gynecologists, American
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Please cite this article in press as: Locatelli A, et al., Factors associated with umbilical artery acidemia in term infants with low Apgar
scores at 5 min, Eur. J. Obstet. Gynecol (2008), doi:10.1016/j.ejogrb.2008.01.003