Journal of Perinatology (2012) 32, 163169

r 2012 Nature America, Inc. All rights reserved. 0743-8346/12

www.nature.com/jp

ORIGINAL ARTICLE

The contribution of heart disease to pregnancy-related mortality

according to the pregnancy mortality surveillance system
J Burlingame1, B Horiuchi2, P Ohana3, A Onaka2 and LM Sauvage1
1

University of Hawaii, John A Burns School of Medicine, Department of Obstetrics, Gynecology and Womens Health, Honolulu,
HI, USA; 2State of Hawaii, Department of Health, Honolulu, Hawaii, USA and 3Research Corporation of the University of Hawaii,
Honolulu, HI, USA

Objective: The objective of this study was to demonstrate the increasing

importance of heart disease as a cause of pregnancy-related mortality in
Hawaii and the rest of the United States.

Study Design: Hawaiis Department of Public Health identified all

pregnancy-associated death certificates from 1991 to 2007. Hospital
records and autopsy reports were reviewed to determine whether deaths
were pregnancy-related.
Result: From 1991 to 2007, Hawaii registered 156 deaths occurring
within 1 year of pregnancy, which represented 4.2% of the total number of
women who died in the same 17 to 46 years age group and 9.0% of the
total number of women who died in the same 17 to 34 years age group.
The pregnancy-related mortality ratio was 22.4 and the pregnancyassociated mortality ratio was 50. The leading cause of pregnancyassociated mortality was heart disease (20.5%) followed by cancer (18.6%)
and suicide/homicide (12.2%). Pregnancy-related deaths (n 70) were
attributed to heart disease (45.7%) followed by sepsis (14.2%) and
hemorrhage (12.9%). The new Hawaii death certificate beginning in 2006
increased the detection of both pregnancy-related and -associated deaths.
Conclusion: Heart disease is the most common cause of pregnancyrelated mortality in Hawaii, and with improved ascertainment, may be
determined to be the most common cause of pregnancy-related mortality
in the rest of the United States.
Journal of Perinatology (2012) 32, 163169; doi:10.1038/jp.2011.74;
published online 9 June 2011
Keywords: death certificate; pregnancy-related mortality ratio; Hawaii

Introduction
By most estimates, pregnancy-related mortality is underestimated
and misclassified because of inconsistent reporting and changing
Correspondence: Dr J Burlingame, University of Hawaii, John A. Burns School of Medicine,
Department of Obstetrics, Gynecology and Womens Health, 1319 Punahou Street, Suite 824,
Honolulu, HI 96826, USA.
E-mail: burlinga@hawaii.edu
Received 16 November 2010; revised 16 March 2011; accepted 2 May 2011; published online
9 June 2011

disease classification.15 This is particularly true for pregnancyrelated deaths due to cardiac disease.610 A pregnancy-related
death is defined as a death caused by pregnancy or an illness
directly exacerbated by pregnancy. Frequently, the information is
only as good as the diagnosis or cause of death listed on the death
certificate.1114 Unfortunately, there has not been a consistent
method for defining what is pregnancy-related. International
Classification of Diseases (ICD) codes, ICD-9 codes and more
recently ICD-10 codes, as well as physician determinations have
been used to establish what is directly and indirectly caused by
pregnancy. The term pregnancy-associated mortality has been used
primarily in developing countries to describe deaths temporarily
related to pregnancy (within 365 days) without determination
whether the cause of death was directly caused or exacerbated
by pregnancy.15
The pregnancy mortality surveillance system (PMSS), a project
by the Division of Reproductive Health at the Centers for Disease
Control, was created to improve the identification of pregnancyrelated deaths. The Centers for Disease Control acquires this data
by requesting from each State all the death certificates that can
be matched to a birth or fetal death certificate within 1 year of
the maternal death.2 Unfortunately, States have been collecting
PMSS data using different methodologies, which often lead to
inaccuracies with comparisons. From 1991 to 2005, the Hawaii
Department of Health provided, like most other States, PMSS
information by matching maternal death certificates to birth and
fetal death certificates if they occurred within a 1-year period of
each other. Since 2006, maternal death certificates have also been
recorded electronically and included a question asking whether
the decedent had been pregnant within 1 year of her death.
These modifications to the death certificate were made to increase
reporting accuracy and collect all deaths temporally related
to pregnancy, including those associated with miscarriage,
termination and early stillbirth.
Nationally, heart disease has become the leading cause of
pregnancy-related mortality, and cardiomyopathy is the primary
cause of cardiac deaths (7.7% of total pregnancy-related deaths).6,7
Heart disease can be exacerbated by pregnancy and is most

Heart disease and pregnancy-related mortality

J Burlingame et al

164

commonly associated with maternal death in the postpartum

period. From 1991 to 1997, 50% of maternal cardiac-related deaths
in the United States occurred between 42 and 365 days
postpartum.9 Heart disease occurs in Hawaii 10 years earlier than
the average recorded in the rest of the United States.1618
Therefore, heart disease is of particular concern when evaluating
the causes of pregnancy-related mortality in Hawaii.
It is hypothesized that an electronic death certificate with
a specific pregnancy-related question will increase the detection
of pregnancy-associated deaths and enable us to ascertain
pregnancy-related cardiac mortality more accurately. It is also
hypothesized that heart disease will be the leading cause of
pregnancy-related deaths in Hawaii.
Methods
Institutional review board approval was obtained from the
University of Hawaii at Manoa. The Hawaii Department of
Health identified pregnancy-associated deaths using two
methods. Before 2006, maternal death certificates were identified
non-electronically by matching them to the birth and/or fetal
death certificates generated within 1 year of each other.
Starting in 2006, pregnancy-associated deaths were identified
electronically and included the new question on the death
certificate asking whether the decedent had been pregnant
within the previous year.
Once the decedents were identified, records pertaining to each
death were requested from all listed hospitals and a selected sample
of autopsy reports (20.5%) made available by the Department of the
Medical Examiner of the City and County of Honolulu was also
reviewed. These autopsy reports were chosen for review at the

principal authors discretion because of nonspecific diagnoses

listed on the death certificate.
A pregnancy-associated death was defined as any maternal
death occurring during pregnancy or within 1 year since delivery.
Deaths that occurred during pregnancy or within 1 year of
pregnancy and resulted from complications of pregnancy, or
a chain of events that was initiated by pregnancy or the
aggravation of an unrelated condition by the physiological effects
of pregnancy or its management, were deemed as pregnancyrelated (the common Centers for Disease Control definition of
pregnancy-related deaths).19 Pregnancy-related and -associated
ratios were defined, respectively, as the number of such maternal
deaths per 100 000 live births.
Data extracted from the medical records included age, county
and city of residence, hospital, occupation, level of education,
marital status, date of death, date of live birth and/or fetal death,
parity, method of delivery, causes of maternal death (primary,
secondary, tertiary and other), race and the pregnancy question
(for 2006 and 2007). The duration of preexisting illnesses could
not be determined in most cases from the available records and
was thus not included in the analysis.
The principal author reviewed all the records to ascertain
whether each death was pregnancy-related or -associated using
the relevancy of the primary, secondary, tertiary and other causes
of death to each one of these classifications.
Results
There were a total of 156 pregnancy-associated deaths during the
17-year period spanning from 1991 to 2007, which represented
4.2% of the total number of women who died in the same 17 to
50.0

Pregnancy-associated

50.0

47.1
42.3
37.8

40.0
28.5

30.0

25.6
Pregnancy-related

20.0
13.1
10.0
2.9

4.5

6.1 7.0

22.4
19.6 21.1

16.6
15.4 16.3

10.2
9.0 9.3

th

PP
C
M
er (9)
C
Ar
rh M
(
yt
hm 5)
i
Va a (
5)
lv
u
At lar
(3
h.
/M )
I(
PH 6)
U
ns TN
p.
C (1
H
em ar )
or d. (
3)
rh
Em age
(
H boli 9)
TN sm
D
is (7)
or
d.
AF (3)
L
In
fe P (
ct
io 1)
C n (1
er
0)
e
Au bro.
to
(
im 4)
Su m.
(
ic
id 4)
e
H
om (1
ic 0)
i
C de
an
(9
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r(
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er MV 9)
A
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)
B
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nk (1
no 5)
w
n
(9
)

0.0

PPCM: peripartum cardiomyopathy, CM: cardiomyopathy, Ath. / MI: atherosclerotic / myocardial infarction, PHTN:
pulmonary hypertension, Unsp. Card.: unspecified cardiac, HTN Disord.: hypertensive disorder, AFLP: acute fatty
liver of pregnancy, Cerebro.: cerebrovasclar, Autoimm.: autoimmune disease, MVA: motor vehicle accident,
OB: obstetric

Figure 1 Cumulative pregnancy-related mortality ratio according to pregnancy-related and -associated causes of death in Hawaii from 1991 to 2007.
Journal of Perinatology

Heart disease and pregnancy-related mortality

J Burlingame et al

165

46 years age group during the period. However, the 17 to 34 years

age group subset represented 9.0% of the total number
of women who died in this age group, whereas the 35 to 46 years
age group subset represented 1.7% of the total number of
women who died in this age group (w2 100.8, P<0.001).
The leading cause of pregnancy-associated death was heart
disease (n 32, 20.5%), followed by cancer (n 29, 18.6%)
and suicide/homicide (n 19, 12.2%). The total number of
pregnancy-associated deaths resulted in a pregnancy-associated
mortality ratio of 50. Of these 156 pregnancy-associated deaths,
70 were pregnancy-related (heart disease, hemorrhage, embolism,
hypertensive disorders, acute fatty liver of pregnancy, infection,
cerebrovascular accidents and autoimmune disease), which
resulted in a pregnancy-related mortality ratio (PMR) of 22.4.
See Figure 1 for more details.
The medical examiner or the pronouncing physician attributed
14 of the 32 cardiac-related deaths (43.8%) to cardiomyopathy,
which represents 9.0% of the total pregnancy-associated
deaths. Nine of these 14 (64.3%) were attributed to peripartum
cardiomyopathy. Atherosclerotic/myocardial infarction accounted
for six of the cardiac-related deaths (18.8%), whereas arrhythmia
accounted for five (15.6%). See Table 1 for more details.
The majority of the cardiac-related deaths occurred within
42 days of delivery (n 21, 65.6%). The mean period for death
from cardiac disease after birth was 72 days (n 26). When death
occurred within 42 days, the mean period was 8 days (n 18).
When death occurred from 43 days to 1 year, the mean period
was 155 days (n 11). Three women died from heart disease
(cardiac failure, cardiac arrest, rheumatic heart disease) while
pregnant.
The mean age (at death) was 30 years (N 156, s.d. 6.4
years), the median interval between maternal date of death and
date of live birth (n 115) was 89 days and the median interval
between maternal date of death and date of fetal death (n 24)
was 2 days. The date of live birth and/or fetal death was missing
in 17 certificates. During the same period, Hawaii recorded
311 785 live births.
The 70 pregnancy-related deaths represented 1.9% of the
total number of women who died in the same 17 to 46 years age
group during the period. However, the 17 to 34 years age group
subset represented 3.6% of the total number of women who died
in this age group, whereas the 35 to 46 years age group subset
represented 1.0% of the total number of women who died in
this age group (w2 31.3, P<0.001).
Of the 156 women, 45 (28.8%) were part Hawaiian, 37 (23.7%)
were Caucasian, 24 (15.4%) were other Pacific Islander,
20 (12.8%) were Filipino, 19 (12.2%) were Japanese, 5 (3.2%)
were other Asian, 4 (2.6%) were Hawaiian and 2 (1.3%) were
African American. See Table 2 for more details.
The number of deaths appeared relatively constant through
most of the 17-year period, except for the significant spike in

2006 following the introduction of the new death certificate.

See Figure 2 for more details.
The new reporting system identified six of nine women
who died of heart disease in 2006 or 2007 that would
not have otherwise been identified based on the live birth
and/or fetal death certificates. With the new Hawaii system,
36 deaths were reported within a year of pregnancy in 2006
and 2007. On the other hand, two pregnancy-associated deaths
were excluded from the study after hospital chart reviews
confirmed the patients had not been pregnant within a
year previous their death. Hence, medical records need
to be reviewed to determine whether a given death is
pregnancy-related.
Table 1 Causes of pregnancy-related deaths per 100 000 live births in Hawaii
from 1991 to 2007
Cause

Ratio

Cardiac (total)
Peripartum cardiomyopathy
Other cardiomyopathy
Arrhythmia
Valvular
Atherosclerotic/myocardial infarction
Pulmonary hypertension
Unspecified

10.3
2.9
1.6
1.6
1.0
1.9
0.3
1.0

Hemorrhage (total)
Ectopic rupture
Placenta abruption
Placenta previa
Placenta accreta
Disseminated intravascular coagulation

2.9
0.6
0.3
0.3
0.3
1.3

Embolism (total)
Amniotic fluid embolism
Thrombosis

2.2
1.9
0.3

Hypertensive disorders (total)

Central nervous system complications

1.0
1.0

Acute fatty liver of pregnancy

0.3

Infection (total)
Genital tract
General septicemia
Unspecified

3.2
0.6
1.9
0.6

Cerebrovascular accidents

1.3

Autoimmune disease (total)

Systemic lupus erythematosus
Mixed connective tissue disease

1.3
1.0
0.3

Total

22.4
Journal of Perinatology

Heart disease and pregnancy-related mortality

J Burlingame et al

166
Table 2 Pregnancy-related mortality ratios by year, race, maternal age, parity, method of delivery, education, location and marital status in Hawaii from 1991 to 2007
All races

Hawaiian

Part Hawaiian

Other Pacific Islander

Caucasian

Filipino

Japanese

Other/unknown

22.4

0.3

6.1

4.2

5.1

2.9

2.2

1.6

Maternal age (n 69) (in years)

17 to 34
14.8
35 to 46
7.4

0.3
0.0

3.5
2.6

2.6
1.6

4.2
1.0

2.6
0.3

1.3
1.0

0.3
1.0

Parity (n 63)
Nulliparous
Multiparous

5.1
15.1

0.0
0.3

1.9
3.2

0.3
3.5

1.6
3.2

0.6
2.2

0.6
1.6

0.0
0.3

7.4
9.3
0.0
1.0
2.6

0.3
0.0
0.0
0.0
0.0

1.3
3.2
0.0
0.3
0.6

1.3
1.0
0.0
0.3
1.3

1.9
2.2
0.0
0.0
0.6

1.9
0.6
0.0
0.3
0.0

0.3
1.6
0.0
0.0
0.0

0.3
0.6
0.0
0.0
0.0

Education (n 69)
<12 years
12 years
Some college
College graduate
Postgraduate

2.9
11.5
5.1
1.9
0.6

0.0
0.0
0.3
0.0
0.0

0.6
3.5
1.3
0.6
0.0

1.0
1.9
1.3
0.0
0.0

0.3
2.6
1.3
0.6
0.3

0.0
2.6
0.3
0.0
0.0

0.6
1.0
0.3
0.3
0.0

0.3
0.0
0.3
0.3
0.3

Location (n 69)
Oahu
Big Island
Maui
Kauai

17.3
2.2
2.2
0.3

0.0
0.0
0.3
0.0

4.5
1.3
0.3
0.0

3.5
0.0
0.6
0.0

4.2
0.6
0.3
0.0

2.2
0.3
0.0
0.3

1.6
0.0
0.6
0.0

1.3
0.0
0.0
0.0

Marital Status (n 69)

Married
Unmarried

14.4
7.7

0.3
0.0

3.2
2.9

2.6
1.6

4.2
1.0

2.2
0.6

1.3
1.0

0.6
0.6

Period
1991 to 2007 (N 70)

Method of delivery (n 63)

Vaginal
C-section
Forceps
Vacuum
None

Note: total number of live births from 1991 to 2007 311 785.

Discussion
The high maternal mortality rate, cardiac-related mortality rate
and cardiomyopathy cause-specific mortality rate in Hawaii are
striking. The overall PMR for the United States is typically 11.8,
but has been reported as high as 23.0 for certain Black
Americans.1,2,16,19,20 In Hawaii, the overall PMR is 22.4, and the
cardiac-related mortality rate and cardiomyopathy cause-specific
mortality rate may be the highest in the nation. Cardiac disease
has become the leading cause of maternal mortality surpassing
hemorrhage and embolism.5,12,13,21
The cardiac-specific pregnancy-related mortality reported
here exceeds any other rate reported in the United States.
The rate of peripartum cardiomyopathy alone is 2.9 per
100 000 live births. For example, although that North Carolina
Journal of Perinatology

has found cardiomyopathy to be its number one cause of

pregnancy-related death,22 its overall cardiomyopathy (peripartum
cardiomyopathy and cardiomyopathy due to other causes)
cause-specific PMR was 0.88 versus 4.48 in Hawaii. Moreover,
70% of North Carolinas cardiomyopathy-related deaths were
classified as peripartum with an overall cause-specific PMR of
0.4 (0.3 for Whites and 2.1 for Blacks), whereas Hawaiis
peripartum cardiomyopathy cause-specific PMR was 2.9.
A possible cause of the high number of cardiac-specific
pregnancy-related deaths in Hawaii is the high prevalence of
heart disease in Pacific Islanders over other ethnic groups. Racial
disparities in maternal mortality have previously been reported
with African Americans exceeding that of Caucasians and other
minorities.16,21,23,24 Racial disparities also extend to the

Heart disease and pregnancy-related mortality

J Burlingame et al

167
140.0

132.1

120.0

100.0

76.8

80.0
66.9

65.5

58.7

60.0

57.5

53.9
50.3
45.3
41.1

40.0

34.2

30.7

28.7 27.7

27.2
23.1

22.8

20.0

0.0
1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007

Figure 2 Number of pregnancy-associated deaths within 1 year of pregnancy per 100 000 live births in Hawaii.

cardiomyopathy cause-specific PMR. (Perhaps the highest

cardiomyopathy cause-specific PMR reported has been in Haiti
at 32.3 deaths per 10 000 live births.8) This hypothesis is supported
by the finding that 15.6% of the cardiac-related deaths occurred
in the Pacific-Islander population (56.3% if part Pacific Islanders
are included), despite the fact that the 2000 census data for
the State of Hawaii tabulated this ethnicity at only 9.4%.25
In comparison, only 12.5 and 18.8% of the cardiac-related deaths
occurred in the Asian and Caucasian populations, respectively,
compared with the 2000 census data of 41.6 and 24.3%,
respectively. Those with at least two races had their cardiac-related
deaths at 53.1% compared with the 2000 census data of 21.4%
owing certainly in part to the Pacific-Islander component. Pacific
Islanders develop heart disease at 5 to 10 years before Caucasians
and Asians. This propensity toward heart disease may be related
to many factors. For one, methamphetamine abuse is all too
common in Hawaii, and methamphetamine-induced heart failure
occurs at young ages. Methamphetamines increase heart rate
and blood pressure and cause inflammation and artery spasms
that limit blood flow to the heart muscle. Half of those seeking
treatment for methamphetamine abuse in Hawaii are of
Pacific-Islander ancestry.26,27 Pacific Islanders are also plagued
by a constellation of other health problems associated with
heart failure including diabetes, hypertension and obesity,
which may accelerate the course of heart failure.1618,28
Although the number of pregnancy-associated deaths recorded
in Hawaii between 1991 and 2007 represents 4.2% of the total
number of women who died in the same 17 to 46 years age group

during the period, it is more than twice higher (9.0%) for the
17 to 34 years age group and more than twice lower (1.7%) for the
35 to 46 years age group, demonstrating the ultimate risk that
pregnancy holds for younger women.
Limitations of this study include that only limited data from
outer island hospitals was available for review. Moreover, most
of the data were abstracted from death certificates and medical
records, and was thus limited to data entered into those records.
In addition, Hawaiis adoption of the National Center for
Health Statistics coding standards for recording ethnicity uses
self-reporting of race/ethnicity and many patients in Hawaii
come from a mixed background.
The extension of the reporting period to 1 year will improve
data ascertainment. It has previously been demonstrated that by
increasing the inclusion and reporting period to 1 year, the
incidence of detected pregnancy-related cardiac-specific deaths
increased by about 57%.1,4 The additional question on the death
certificate regarding pregnancy within 1 year of death increased
the identification (and prevalence) of cardiac-related death in
2006 and 2007 by 200%. Underreporting of pregnancy-related
mortality has been a consistent problem worldwide.20 The utilized
method and the definition of pregnancy mortality clearly affects the
accuracy of the data reflecting the mortality risk. It is important
to collect data consistently between (and among) populations to
make accurate comparisons possible.1,3,16,21,22 24,29 35 Both
pregnancy-associated and -related mortalities should include
all deaths within 1 year of pregnancy in order to identify as
many pregnancy-related deaths as possible. Utilized methods
Journal of Perinatology

Heart disease and pregnancy-related mortality

J Burlingame et al

168

should include the pairing of birth and death certificates, direct

physician reporting and the use of a question regarding recent
pregnancy at the time of completion of the death certificate.
The addition of this question to the death certificate allowed the
identification of deaths not only associated with live births but
also those that ended in miscarriage, termination or fetal death.
Previously, this subset of maternal deaths had been very difficult
to identify. This is a significant step toward the development
of an accurate pregnancy-related mortality rate for Hawaii and
the rest of the United States. It is recommended that such a
question be included on all death certificates across the country.
Another potential improvement to optimize detection of
pregnancy-related deaths would be to review all medical
examiner and police records. Other authors have proposed
this recommendation, but no systematic way has existed to
include this in the PMSS.10,13,14 As all State and Federal
reporting systems move to electronic formats, cross-referencing
of databases should also be considered.
Finally, standardized criteria to determine whether or not
a maternal death is pregnancy-related must be established to
allow data to be easily monitored over time and across States.
ICD-9 and ICD-10 codes remain inadequate. For example, it is
possible that some of the suicides and/or homicides seen in
our review were in fact caused or exacerbated by pregnancy.
Postpartum depression and the increase of partner violence
have previously been reported to be higher during and after
pregnancy thereby providing a direct link to pregnancy as
a cause or reason for exacerbation.34,3640
Our study and others have shown that cardiac-specific
pregnancy-related mortality has surfaced and is the leading
cause of pregnancy-associated mortality. Immediate attention
is needed to optimally screen for and manage parturients with
heart disease not only in Hawaii and the rest of the United States
but also worldwide. With dedicated energies, research and
technologies such as echocardiography and pregnancy-specific
biomarkers, we may have the necessary tools for predicting
heart disease and preventing mortality in high-risk maternal
populations around the world.
Conflict of interest
The authors declare no conflict of interest.
Acknowledgments
This work was supported by the National Institutes of Health (U54 RR014607).

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