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doi: 10.1111/ppe.

12360 1

Apgar Score Components at 5 Minutes:


Risks and Prediction of Neonatal Mortality
Sven Cnattingius,a Mikael Norman,b Fredrik Granath,a Gunnar Petersson,a Olof Stephansson,a,c Thomas Frisella
a
Clinical Epidemiology Unit, Department of Medicine Solna,
b
Division of Pediatrics, Department of Clinical Science, Intervention and Technology, Karolinska Institutet, Stockholm, Sweden
c
Division of Epidemiology, School of Public Health, University of California, Berkeley, CA

Abstract
Background: The Apgar score consists of five components: heart rate, respiratory effort, muscle tone, reflex
irritability, and colour. Although the Apgar score has been used for 60 years, the specific contribution of the
Apgar score components with respect to risks and prediction of neonatal mortality remains unknown. Likewise,
the value of reduced scores (including less than five Apgar score components) has rarely been investigated.
Methods: In a population-based cohort study of 148 765 liveborn singleton infants in Sweden 2008–2013, we
investigated components of Apgar score at 5 min with respect to relative risks and prediction (using ROC curves,
sensitivity, and positive predictive values) of neonatal mortality.
Results: Reduced values (0–1) of heart rate, respiratory effort, and colour were independently associated with
increased relative risks of neonatal mortality. For the full Apgar score, the sensitivity and positive predictive
values of neonatal mortality (cut-off ≤3) were by gestational age: ≤31 weeks: 56.1% and 49.2%; 32–36 weeks: 25.0%
and 18.2%; and ≥37 weeks: 35.2% and 9.3%, respectively. When only heart rate and respiratory effort were
considered (range 0–4; cut-off ≤2), corresponding values were 66.7% and 34.9%; 37.5% and 13.0%; and 46.3% and
7.6%, respectively.
Conclusions: A reduced Apgar score has generally the same predictability of neonatal mortality as the full Apgar
score. The full Apgar score or reduced scores may be better predictors of neonatal mortality in very preterm
infants (≤31 weeks) than in infants with longer gestations.

Keywords: Apgar score, neonatal mortality, prediction, risk.

The Apgar score, developed by the US anaesthesiolo- congenital anomalies.3,4 Still, large and more recent
gist Virginia Apgar in the early 1950’s,1 is universally studies find that low Apgar score at 5 min is associ-
used to assess new-born’s health. Initially, the Apgar ated with substantially increased risks of neonatal
score at 1 min was used to assess the need of immedi- and infant mortality, both in preterm and term
ate resuscitation. Later, Apgar score at 5 min was infants.5–7 Compared with normal Apgar score at
shown to be a better predictor of neonatal survival 5 min (7–10), low Apgar scores (0–3 or 4–6) are associ-
than Apgar score at 1 min.2 ated with substantially higher relative risks of neona-
With the introduction of modern neonatal intensive tal mortality in term than in preterm infants.
care, the value of the Apgar score was questioned, However, as neonatal mortality rates increase with
especially for infants requiring resuscitation at birth. decreasing gestational age, the absolute neonatal mor-
Low Apgar score in preterm infants may reflect physi- tality rate difference between infants with low and
ologic immaturity rather than poor condition at birth, normal Apgar scores increases with decreasing gesta-
and a low Apgar score may also be caused by mater- tional age.6
nal drugs, infections, neurological diseases, and The Apgar score consists of five components: heart
rate, respiratory effort, muscle tone, reflex irritability,
Correspondence:
and colour. Each component is given the same weight,
Sven Cnattingius, Clinical Epidemiology Unit, Department of
Medicine Solna, Karolinska Institutet, Karolinska University
and ranges from 0 to 2; thus, Apgar score ranges from
Hospital Solna, Stockholm, Sweden. 0 to 10. These components may not be of equal impor-
E-mail: sven.cnattingius@ki.se tance,8,9 and heart rate and respiratory effort may be

© 2017 John Wiley & Sons Ltd


Paediatric and Perinatal Epidemiology, 2017, , –
2 S. Cnattingius et al.

difficult to assess due to medical interventions. age was based on the following hierarchy: date of
Although the Apgar score has been used for more embryo transfer (3.9%), ultrasound assessment (gen-
than half a century, we are unaware of studies investi- erally before 18 gestational weeks; 94.3%), and the last
gating the specific contribution of the Apgar score menstrual period (1.8%). Infants were stratified into
components with respect to mortality risks. being born very preterm (≤31 completed weeks),
In this population-based study, we investigated moderately preterm (32–36 weeks), and at term
each component of the Apgar score at 5 min individu- (≥37 weeks). Definitions and categorizations of covari-
ally and its incremental contribution as part of the ates considered are provided in Table S1.
Apgar score with respect to risks and prediction of
neonatal mortality in preterm and term infants.
Statistical analysis
Neonatal mortality rates were calculated for Apgar
Methods
score and each component of Apgar score, for all
births and stratified by gestational age. To assess the
Study population
association between separate Apgar score compo-
In Stockholm and Gotland counties, Sweden (includ- nents (using Apgar score as a continuous variable),
ing around 2.1 million inhabitants), a standardized polychoric correlations were calculated, which are
electronic medical record system, covering all antena- interpreted as the correlation in the continuous traits
tal, obstetric, and neonatal care, is available. Starting underlying the ordinal categories of the Apgar score
at the first antenatal visit, data are prospectively components.11 The incremental prediction of neonatal
recorded by midwives and physicians. Original infor- mortality from each component was estimated from
mation from antenatal, obstetric, and neonatal records multivariable regression models, where all compo-
was abstracted to construct the population-based nents were modelled in a joint model. To enable calcu-
Stockholm-Gotland Obstetric Data Base. Using the lation of relative risk (RR) and 95% confidence
infant’s person-unique national registration number,10 interval (CI), we fit Poisson regression models (with
information about neonatal death was retrieved from empirical, robust standard errors) based on the
the nation-wide Swedish Cause of Death Swedish methods of generalized estimating equations.
Register. In supplementary analyses, we extended the multi-
From 2008 to 2013, there were 149 800 live singleton variable model of neonatal mortality to include: (i)
births recorded in the Stockholm-Gotland Obstetric gestational length, birthweight-for-gestational age,
Data base. After excluding infants with no informa- and mode of delivery; and (ii) maternal age, parity,
tion on Apgar score at 5 min (n = 761) or gestational family situation, maternal smoking, body mass index,
age (n = 274), the study population included 148 765 height, mother’s country of birth, infertility problems,
infants. We wanted to investigate the value of Apgar hypertensive diseases, and year of delivery. Due to
score and Apgar score components for overall neona- the low number of neonatal deaths in strata of covari-
tal mortality, and therefore refrained from other ates and the strong association between gestational
exclusions, like excluding infants with congenital age and neonatal mortality, these models were run
anomalies or chromosomal aberrations, which are separately. Categorizations and parameterizations of
generally diagnosed later in the neonatal period. continuous covariates were decided based on good-
Neonatal death was defined as death within the first ness of fit in univariate models (Table S1).
27 completed days of life (0–27 days). This study was To estimate the prediction of neonatal mortality
approved by the Research Ethics Committe at when using all available values (i.e. from 0 to 10) on
Karolinska Institutet, Stockholm (No. 2009/275-31 Apgar score and reduced component scores (after
and No. 2012/365-32). excluding one, two, or three Apgar score compo-
nents), we plotted receiver operating characteristic
(ROC) curves and calculated the area under curve
Exposures
(AUC) from logistic regression models. We decided a
Apgar score at 5 min and its components heart rate, priori to comply with the original score giving each
respiratory effort, muscle tone, reflex irritability, and component the same weight, and to include heart rate
colour were main exposures. Estimation of gestational and respiratory effort in all models. We also

© 2017 John Wiley & Sons Ltd


Paediatric and Perinatal Epidemiology, 2017, , –
Apgar score components and neonatal mortality 3

calculated the sensitivity and positive predictive val- (Table 1). Within these groups, an Apgar score of 0 or
ues of cut-off values for the full Apgar score and 1 was more common in very preterm infants (n = 31;
reduced component scores with respect to neonatal 48%) than in moderately preterm (n = 11; 33%) or
mortality. term infants (n = 45; 22%). In infants with absent
heart rate (value = 0), 97% (31 of 32 infants) had
Apgar score ≤3, whereas the corresponding rate for
Results
infants with 0 values in other Apgar score compo-
nents ranged from 68% (respiratory effort) to 43%
Apgar score and components of Apgar score and
(muscle tone) (data not shown in table).
mortality risks
Of 148 765 singleton infants, 135 (0.91 per 1000)
Overall, reduced values of Apgar score components died during the neonatal period (Table 2). In very pre-
(0–1) at 5 min ranged from 0.2% (heart rate) to 9.1% term infants, neonatal mortality rates were 492.3 per
(colour) (Table 1). The prevalence of reduced values 1000 in infants with Apgar score 0–3 and 17.9 per 1000
of Apgar score components increased with decreasing in infants with Apgar score 7–10 (absolute rate differ-
gestational age. In very preterm infants, reduced com- ence in neonatal mortality was 474.4 per 1000). In term
ponent values ranged from 11.2% (reduced heart rate) infants, corresponding neonatal mortality rates were
to 57.7% (reduced muscle tone). 93.1 and 0.17 per 1000, providing a substantially lower
Sixty-five very preterm infants (≤31 weeks), 33 absolute rate difference (92.9 per 1000). However,
moderately preterm infants (32–36 weeks), and 204 compared with infants with Apgar score 7–10, a very
term infants (≥37 weeks) had a 5 min Apgar score ≤3 low (0–3) Apgar score was associated with a

Table 1. Prevalence of Apgar Score and its components at 5 min

All ≤31 weeks 32–36 weeks ≥37 weeks

(n = 148 765) (n = 828) (n = 5518) (n = 142 419)

No. (%) No. (%) No. (%) No. (%)

Apgar score at 5 min


0–3 302 (0.2) 65 (7.9) 33 (0.6) 204 (0.1)
4–6 958 (0.6) 147 (17.8) 124 (2.2) 687 (0.5)
7–10 147 505 (99.2) 616 (74.4) 5361 (97.2) 141 528 (99.4)
Heart rate
0 32 (0.02) 11 (1.3) 4 (0.1) 17 (0.01)
1 311 (0.2) 82 (9.9) 49 (0.9) 180 (0.1)
2 148 422 (99.8) 735 (88.8) 5465 (99.0) 142 222 (99.9)
Respiratory effort
0 384 (0.3) 77 (9.3) 45 (0.8) 262 (0.2)
1 2264 (1.5) 232 (28.0) 278 (5.0) 1754 (1.2)
2 146 117 (98.2) 519 (62.7) 5195 (94.1) 140 403 (98.6)
Muscle tone
0 642 (0.4) 94 (11.4) 63 (1.1) 485 (0.3)
1 6307 (4.2) 383 (46.3) 651 (11.8) 5273 (3.7)
2 141 816 (95.3) 351 (42.4) 4804 (87.1) 136 661 (96.0)
Reflex irritability
0 617 (0.4) 94 (11.4) 64 (1.2) 459 (0.3)
1 3101 (2.1) 284 (34.3) 339 (6.1) 2478 (1.7)
2 145 047 (97.5) 450 (54.3) 5115 (92.7) 139 482 (97.9)
Colour
0 240 (0.2) 47 (5.7) 27 (0.5) 166 (0.1)
1 13 230 (8.9) 371 (44.8) 1064 (19.3) 11 795 (8.3)
2 135 295 (90.9) 410 (49.5) 4427 (80.2) 130 458 (91.6)

Percentages may not sum up to 100% because of rounding.

© 2017 John Wiley & Sons Ltd


Paediatric and Perinatal Epidemiology, 2017, , –
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Table 2. Apgar score and its components at 5 min and risks of neonatal mortality

All ≤31 weeks 32–36 weeks ≥37 weeks


S. Cnattingius et al.

No.a (Rate)b RR (95% CI)c No.a (Rate)b RR (95% CI)c No.a (Rate)b RR (95% CI)c No.a (Rate)b RR (95% CI)c

Apgar score at 5 min


0–3 57 (188.7) 580.0 (401.8, 837.2) 32 (492.3) 27.6 (14.6, 52.1) 6 (181.8) 75.0 (30.3, 185.3) 19 (93.1) 549.2 (305.7, 986.8)
4–6 30 (31.3) 96.2 (61.3, 151.2) 14 (95.2) 5.3 (2.5, 11.5) 5 (40.3) 16.6 (6.0, 45.9) 11 (16.0) 94.4 (46.4, 192.0)
7–10 48 (0.33) 1.0 (Reference) 11 (17.9) 1.0 (Reference) 13 (2.4) 1.0 (Reference) 24 (0.17) 1.0 (Reference)
Heart rate
0 20 (625.0) 7.0 (4.1, 12.1) 10 (909.1) 3.0 (1.3, 6.7) 2 (500.0) 6.3 (2.0, 19.7) 8 (470.6) 8.1 (3.0, 22.2)
1 38 (122.2) 2.9 (1.8, 4.6) 23 (280.5) 1.9 (0.9, 3.8) 5 (102.0) 2.4 (0.8, 7.3) 10 (55.6) 2.2 (0.9, 5.7)
2 77 (0.52) 1.0 (Reference) 24 (32.7) 1.0 (Reference) 17 (3.1) 1.0 (Reference) 36 (0.25) 1.0 (Reference)
Respiratory effort
0 59 (153.6) 9.0 (3.7, 22.2) 30 (389.6) 3.7 (1.1, 13.1) 8 (177.8) 6.5 (0.7, 56.5) 21 (80.2) 11.1 (3.0, 40.8)
1 36 (15.9) 5.8 (2.9, 11.6) 20 (86.2) 3.1 (1.2, 8.3) 4 (14.4) 1.7 (0.4, 7.0) 12 (6.8) 6.1 (2.5, 14.6)
2 40 (0.27) 1.0 (Reference) 7 (13.5) 1.0 (Reference) 12 (2.3) 1.0 (Reference) 21 (0.15) 1.0 (Reference)
Muscle tone
0 64 (99.7) 4.1 (0.9, 17.9) 34 (361.7) 2.2 (0.5, 9.8) 8 (127.0) 8.6 (0.6, 121.1) 22 (45.4) 0.9 (0.1, 9.4)
1 38 (6.0) 2.5 (0.7, 8.5) 18 (47.0) 1.1 (0.3, 3.4) 8 (12.3) 3.9 (0.9, 17.6) 12 (2.3) 0.7 (0.1, 4.4)
2 33 (0.23) 1.0 (Reference) 5 (14.2) 1.0 (Reference) 8 (1.7) 1.0 (Reference) 20 (0.15) 1.0 (Reference)
Reflex irritability
0 63 (102.1) 3.7 (0.9, 15.3) 32 (340.4) 1.8 (0.4, 7.6) 8 (125.0) 1.2 (0.0, 33.2) 23 (50.1) 12.0 (1.2, 122.5)
1 36 (11.6) 4.5 (1.4, 14.8) 19 (66.9) 2.3 (0.9, 6.3) 5 (14.7) 1.4 (0.2, 8.5) 12 (4.8) 10.0 (1.6, 63.1)
2 36 (0.25) 1.0 (Reference) 6 (13.3) 1.0 (Reference) 11 (2.2) 1.0 (Reference) 19 (0.14) 1.0 (Reference)
Colour
0 45 (187.5) 3.5 (1.4, 8.7) 26 (553.2) 2.4 (0.7, 8.6) 3 (111.1) 0.8 (0.1, 5.5) 16 (96.4) 4.4 (1.1, 17.7)
1 55 (4.2) 2.2 (1.1, 4.5) 23 (62.0) 1.2 (0.5, 3.1) 12 (11.3) 1.6 (0.4, 5.9) 20 (1.7) 2.5 (0.9, 6.9)
2 35 (0.26) 1.0 (Reference) 8 (19.5) 1.0 (Reference) 9 (2.0) 1.0 (Reference) 18 (0.14) 1.0 (Reference)

RR denotes relative risk; CI denotes confidence interval.


a
Number of neonatal deaths.
b
Rate per 1000 births.
c
Relative risks of each component are adjusted for effects of the other components.

© 2017 John Wiley & Sons Ltd


Paediatric and Perinatal Epidemiology, 2017, , –
Apgar score components and neonatal mortality 5

substantially larger relative risk of neonatal death in Apgar score, was 0.90 (Table 4, ROC curves in Fig-
term infants than in very preterm infants (Table 2). ure S1). This can be interpreted as, when using infor-
Regardless of gestational age, reduced heart rate mation on all Apgar score values, a randomly selected
was associated with the highest neonatal mortality case of neonatal mortality has a lower Apgar score
rates. However, compared with a component value of than a randomly selected non-case 90% of the time.
2, reduced values of all Apgar score components (0 or When we excluded two of the components muscle
1) were associated with substantially increased neona- tone, reflex irritability, or colour, there were minor,
tal mortality rates (Table 2). However, the Apgar although statistically significant reductions in AUC.
score components were highly correlated (poly- In analyses stratified by gestational age, the 5 min
choric correlations ranged from 0.65 (colour – reflex Apgar score was, if anything, a stronger predictor of
irritability) to 0.94 (reflex irritability – muscle tone), neonatal mortality in very preterm infants than in
Table 3). When Apgar score components were mutu- moderately preterm and term infants (Table 4).
ally adjusted for each other, reduced heart rate, respi- Excluding one or two components did not change the
ratory effort, and colour were associated with prediction of neonatal mortality in any gestational age
increased neonatal mortality risks. Absent heart rate group. When only including heart rate and respira-
and absent respiratory effort (values = 0) provided tory effort, the prediction was significantly reduced
the highest relative risks (Table 2). compared to the full Apgar score in moderately pre-
In very preterm infants (57 neonatal deaths) and in term and term infants. Still, the AUC was highest in
term infants (54 neonatal deaths), absent heart rate very preterm infants.
and reduced respiratory effort (value 0–1) were asso- Of all neonatal deaths, 42.2% had an Apgar score ≤3
ciated with increased neonatal mortality risks. In term (sensitivity), and almost one-fifth of all infants with an
infants, reduced reflex irritability was also associated Apgar score ≤3 died neonatally (positive predictive
with increased neonatal mortality risk. In moderately value [PPV] 18.9%; Table 5). For neonatal mortality,
preterm infants (24 neonatal deaths), only absent heart the sensitivity and the positive predictive value of an
rate conferred an increased risk of neonatal mortality Apgar score ≤3 was substantially higher in very pre-
(Table 2). term infants than in infants with longer gestations.
Apgar score is often assessed in a stressful situation, When we excluded 41 infants born at the border of
when it is difficult to account for other factors. We viability, i.e. at 22–23 completed weeks (24 neonatal
therefore adjusted for birth or maternal characteristics deaths), the sensitivity and positive predictive value
in supplementary analyses only. Overall neonatal of a low Apgar score in very preterm infants
mortality risk patterns remained, although point esti- decreased (sensitivity 42.4%; positive predictive value
mates were changed (Table S2). 31.8%, not shown in table), but were still higher than
corresponding values of neonatal mortality in moder-
ately preterm and term infants (Table 5).
Prediction of neonatal mortality using two to five
For the reduced component scores (including four
components
to two Apgar score components), the cut-off values
The AUC of the full Apgar score, reflecting the pre- were chosen to have the number of infants below the
dictability of neonatal mortality using all values of threshold closest to the number of infants below the

Table 3. Polychoric correlations between Apgar score components at 5 min

All births

Heart rate Respiratory effort Muscle tone Reflex irritability Colour

Heart rate 1.00 0.87 0.81 0.84 0.78


Respiratory effort 1.00 0.80 0.84 0.67
Muscle tone 1.00 0.94 0.67
Reflex irritability 1.00 0.65
Colour 1.00

© 2017 John Wiley & Sons Ltd


Paediatric and Perinatal Epidemiology, 2017, , –
6 S. Cnattingius et al.

Table 4. Sums of Apgar score components as predictors of neonatal mortality

All births ≤31 weeks 32–36 weeks ≥37 weeks


AUC (95% CI) AUC (95% CI) AUC (95% CI) AUC (95% CI)

Full Apgar score (range 0–10) 0.90 (0.87, 0.94) 0.87 (0.82, 0.93) 0.83 (0.73, 0.93) 0.85 (0.78, 0.91)
Excluding one of the following components (range 0–8)
Muscle tone 0.90 (0.87, 0.94) 0.87 (0.82, 0.92) 0.81 (0.71, 0.91) 0.85 (0.79, 0.91)
Reflex irritability 0.90 (0.87, 0.93) 0.87 (0.82, 0.92) 0.82 (0.72, 0.92) 0.84 (0.77, 0.91)
Colour 0.89 (0.85, 0.92) 0.87 (0.81, 0.92) 0.81 (0.71, 0.91) 0.83 (0.77, 0.90)
Excluding two of the following components (range 0–6)
Muscle tone & Irritability 0.89 (0.85, 0.92)a 0.86 (0.81, 0.92) 0.79 (0.68, 0.90) 0.84 (0.78, 0.91)
Muscle tone & Colour 0.87 (0.83, 0.91)a 0.86 (0.80, 0.92) 0.78 (0.68, 0.88) 0.82 (0.75, 0.88)
Reflex irritability & Colour 0.88 (0.85, 0.92)a 0.87 (0.81, 0.92) 0.79 (0.68, 0.89) 0.82 (0.76, 0.89)
Excluding the three following components (range 0–4)
Muscle tone, Reflex irritability, & Colour 0.85 (0.81, 0.89)a 0.85 (0.80, 0.91) 0.73 (0.62, 0.84)a 0.80 (0.74, 0.87)a

AUC denotes area under the receiver operating characteristic curve.


a
Significantly reduced AUC compared to full Apgar score (P < 0.05).

cut-off of the full Apgar score (≤3). When one or two very preterm infants than in infants with longer
Apgar score components were excluded, there were gestations.
negligible changes in sensitivity and positive predic-
tive values of neonatal mortality regardless of gesta-
Comparison with other studies
tional age (Table 5). For these reduced component
scores, the sensitivity and positive predictive values The value of Apgar score components may differ
were also consistently higher in very preterm infants whether the focus is neonatal mortality, short-, or
than in infants with longer gestations. When only long-term morbidity. For neonatal mortality, heart
heart rate and respiratory effort were considered rate and respiratory effort are most important. We
(range 0–4), more infants had a score below the cut-off found that almost all infants with absent heart rate
(≤2). This probably contributed to increased sensitiv- (value = 0) had an Apgar score ≤3. Heart rate is also
ity values and reduced positive predictive values: for the component which is most associated with lower
very preterm infants 66.7% and 34.9%, respectively; Apgar scores in preterm infants12 and severe neonatal
for moderately preterm infants 37.5% and 13.0%, morbidity in term infants.13 Muscle tone and reflex
respectively; and for term infants 46.3% and 7.6%, irritability are highly correlated,12,14 and may be more
respectively. relevant for neurological outcomes like cerebral
palsy.15 Colour is generally considered to be least
important; removing colour from the Apgar score has
Comment
reported to improve16 or not influence12 the correla-
tion between the total Apgar score and umbilical
Principal findings
artery pH. Still, we found that reduced colour was
To our knowledge, this is the first study linking the associated with increased neonatal mortality risk after
Apgar score components at 5 min to risks of neonatal adjusting for effects of the other components.
mortality. Reduced values of heart rate and respira- Our results challenge some of the views expressed
tory effort were associated with the highest risks, but by the American Academy of Pediatrics Committee
reduced colour was also independently associated on Fetus and Newborn and American College of
with increased mortality risk. A component score, Obstetricians and Gynecologists Committee on
including three or four Apgar score components, pre- Obstetrical Practice.3 The first recommendation in this
dicted neonatal mortality as well as the full Apgar document reads: “The Apgar score does not predict
score. Both the full Apgar score and reduced scores individual neonatal mortality or neurologic outcome
(including two to four Apgar score components) were, and should not be used for that purpose”. We found
if anything, better predictors of neonatal mortality in that every second very preterm infant (≤31 weeks)

© 2017 John Wiley & Sons Ltd


Paediatric and Perinatal Epidemiology, 2017, , –
© 2017 John Wiley & Sons Ltd
Table 5. Sensitivity and positive predictive values (PPV) of Apgar score and reduced scores at 5 min for neonatal mortality

All births <31 weeks 32–36 weeks ≥37 weeks

Cut-off level No.a Sensitivityb PPVc No.a Sensitivityb PPVc No.a Sensitivityb PPVc No.a Sensitivityb PPVc

Full Apgar score (range 0–10) ≤3 302 42.2 18.9 65 56.1 49.2 33 25.0 18.2 204 35.2 9.3

Paediatric and Perinatal Epidemiology, 2017, , –


Excluding one component (range 0–8)
Muscle tone ≤3 356 48.1 18.3 75 59.6 45.3 41 29.2 17.1 240 44.4 10.0
Reflex irritability ≤3 346 46.7 18.2 74 57.9 44.6 37 29.2 18.9 235 42.6 9.8
Colour ≤2 297 42.2 19.2 62 54.4 50.0 31 25.0 19.4 204 37.0 9.8
Excluding two components (range 0–6)
Muscle tone and Reflex irritability ≤2 228 38.5 22.8 58 50.9 50.0 27 29.2 25.9 143 29.6 11.2
Muscle tone and Colour ≤2 353 47.4 18.1 73 57.9 45.2 38 29.2 18.4 242 44.4 9.9
Reflex irritability and Colour ≤2 334 45.9 18.6 71 56.1 45.1 34 29.2 20.6 229 42.6 10.0
Excluding three components (range 0–4)
Muscle tone, Reflex irritability, and Colour ≤2 508 53.3 14.2 109 66.7 34.9 69 37.5 13.0 330 46.3 7.6

a
No. denotes number of infants below the cut-off value.
b Number of neonatal deaths with Apgar score below the cut-off  100
Sensitivity: .
All neonatal deaths
c Number of neonatal deaths with Apgar score below the cut-off  100
Positive predictive value: .
All infants below the cut-off
Calculation of sensitivity and positive predictive values are based on the following numbers of births and neonatal deaths: all births: n = 148 765; neonatal deaths n = 135; ≤31 weeks:
n = 828; neonatal deaths n = 57; 32–36 weeks: n = 5518; neonatal deaths n = 24; ≥37 weeks: n = 142 419; neonatal deaths n = 54.
Apgar score components and neonatal mortality
7
8 S. Cnattingius et al.

with an Apgar score ≤3 died neonatally, whereas less obstetric, and neonatal records. Information on Apgar
than 2% of those with Apgar score ≥7 died. In term score components and gestational age was almost
infants (≥37 weeks), corresponding rates were close to complete, and follow-up was complete. Apgar score is
10% and less than 0.2%, respectively. We think that more important for early than for late neonatal mor-
these and other results in our study will provide the tality (deaths during the first week of life and deaths
clinician with valuable prognostic information for during the second to fourth weeks of life, respec-
both preterm and term infants. tively), and least important for post-neonatal
Our finding that Apgar score at 5 min may be a bet- mortality (infant death after the fourth week of life).6
ter predictor of neonatal mortality in very preterm As neonatal mortality is a rare event, our possibilities
infants than in infants with longer gestations is to study associations between Apgar score compo-
intriguing and several aspects have to be kept in nents and early or late neonatal mortality were lim-
mind. First, we confirmed previous finding that ited, especially in moderately preterm infants (24
Apgar score ≤3 is associated with a substantially neonatal deaths). Analyses of neonatal mortality were
higher relative risk of neonatal mortality in term than only stratified by gestational age into three groups
in preterm infants.5,6 This clearly indicates that a low (≤31 weeks, 32–36 weeks, and ≥37 weeks), but we
Apgar score is a severe warning sign in term infants. adjusted for gestational age in completed weeks in
However, we also found that the absolute neonatal supplementary analyses. Because of power concerns,
mortality rate difference between very preterm infants we also refrained from studying associations between
with Apgar scores 0–3 and 7–10 was substantially lar- Apgar score components and causes of neonatal
ger than corresponding rate differences in moderately death.
preterm and term infants. Second, low Apgar score Compared with the conventional Apgar score,
and reduced values of the Apgar score components information about Apgar score combined with infor-
are more common in very preterm infants than in mation about neonatal interventions was recently
infants with longer gestations. This may to a large reported to be a better predictor of birth asphyxia and
extent reflect physiologic immaturity in response to severe asphyxia-related neonatal morbidity.19–21
the stress of being born.4,12 However, a large number However, our aim was to study the risks and prog-
of very preterm infants have experienced deviation nostic value of Apgar score components at 5 min
from normal physiology prior to or during labour. For regardless of preceding interventions. In preterm
example, the proportions of pregnancies complicated infants born at the border of viability (22–23 com-
by fetal growth restriction and/or early-onset pleted weeks), the prevailing recommendation during
preeclampsia are higher in very preterm births than in the study period in our region was to withhold resus-
moderately preterm or term births.17,18 In infants with citation. When these infants were excluded, an Apgar
Apgar score ≤3, we found that very preterm infants score ≤3 was still a better predictor of neonatal mortal-
more often had Apgar scores 0 or 1. Thus, low Apgar ity in very preterm infants than in infants with longer
score in very preterm infants may, in addition to gestations. In an emergency situation, more com-
physiologic immaturity, also reflect a high proportion monly occurring in very preterm infants, it may be
of severely depressed infants. It is therefore conceiv- difficult to correctly estimate Apgar score compo-
able that pre-existing pathophysiology in very pre- nents, including heart rate and respiratory effort,
term infants explains that a score only including which often is mechanically assisted.22,23 The interob-
information on heart rate and respiratory effort had server variability in Apgar score has generally been
almost the same prediction of neonatal mortality as assessed as poor, especially in very preterm
the full Apgar score. Our findings support that regu- infants.24,25 Still, we found that the full Apgar score or
lar breathing combined with normal heart rate at a reduced score may be better predictors of neonatal
5 min can be used as a marker of “good condition at mortality in very preterm infants than in infants with
birth” in very preterm infants. longer gestations.

Strengths and limitations of the study Conclusions


Study strengths include the population-based design, We are unaware of any single measure that is ideal
including original information from antenatal, for predicting severe asphyxia-related neonatal or

© 2017 John Wiley & Sons Ltd


Paediatric and Perinatal Epidemiology, 2017, , –
Apgar score components and neonatal mortality 9

neurodevelopmental outcomes.26 This study provides 8 Apgar V, James LS. Further observations on the newborn
strong support that a reduced score, including less scoring system. American Journal of Diseases in Children 1962;
104:419–428.
than five Apgar score components, is as valuable as
9 Crawford JS, Davies P, Pearson JF. Significance of the
the full Apgar score to predict neonatal mortality. Our individual components of the Apgar score. British Journal of
results also confirm previous assumptions that the Anaesthesia 1973; 45:148–158.
heart rate and respiratory effort components at 5 min 10 Ludvigsson JF, Otterblad-Olausson P, Pettersson BU,
are central for neonatal mortality. Still, our study was Ekbom A. The Swedish personal identity number:
focused on neonatal mortality, and for a general clini- possibilities and pitfalls in healthcare and medical research.
European Journal of Epidemiology 2009; 24:659–667.
cal assessment of the immediate needs and the prog-
11 Olsson U. Maximum likelihood estimation of the polychloric
nosis of the new-born infant, we see no need to revise correlation-coefficient. Psychometrika 1979; 44:443–460.
the well-established Apgar score. A low Apgar score 12 Hegyi T, Carbone T, Anwar M, Ostfeld B, Hiatt M, Koons A,
can be caused by many other factors than asphyxia,3 et al. The apgar score and its components in the preterm
and we welcome studies of associations between infant. Pediatrics 1998; 101:77–81.
13 Portman RJ, Carter BS, Gaylord MS, Murphy MG, Thieme RE,
Apgar score components and reduced scores with
Merenstein GB. Predicting neonatal morbidity after perinatal
respect to other outcomes, including neonatal asphyxia: a scoring system. American Journal of Obstetrics and
asphyxia-related morbidity and long-term neurologi- Gynecology 1990; 162:174–182.
cal outcomes.27,28 Our finding that the prognostic 14 Minami K, Furuhashi M, Miyazaki K, Yoshida K, Kuno N,
value of Apgar score and reduced scores with respect Ishikawa K. Would omitting the assessment of heart rate be
to neonatal mortality may be larger in very preterm harmful to initial neonatal care? Journal of Maternal-Fetal &
Neonatal Medicine 2007; 20:477–480.
infants than in moderately preterm and term infants
15 Walstab JE, Bell RJ, Reddihough DS, Brennecke SP, Bessell CK,
challenges current view, and may be of clinical Beischer NA. Factors identified during the neonatal period
importance. associated with risk of cerebral palsy. The Australian & New
Zealand Journal of Obstetrics & Gynaecology 2004; 44:342–346.
16 Marx GF, Mahajan S, Miclat MN. Correlation of biochemical
Acknowledgements data with Apgar scores at birth and at one minute. British
Journal of Anaesthesia 1977; 49:831–833.
Financial support was provided by an unrestricted 17 Gilbert WM, Danielsen B. Pregnancy outcomes associated
grant from Karolinska Institutet (Distinguished Profes- with intrauterine growth restriction. American Journal of
sor Award to Cnattingius) and by Stockholm County Obstetrics and Gynecology 2003; 188:1596–1599.
Council (ALF projects 20130156, 20140105, and 18 Pettit F, Mangos G, Davis G, Henry A, Brown MA. Pre-
eclampsia causes adverse maternal outcomes across the
20150118). The authors report no conflicts of interest.
gestational spectrum. Pregnancy Hypertension 2015; 5:198–204.
19 Dalili H, Nili F, Sheikh M, Hardani AK, Shariat M, Nayeri F.
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Supporting Information
Additional Supporting Information may be found in
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