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The Association of Maternal Race and Ethnicity

and the Risk of Postpartum Hemorrhage


Allison Bryant, MD, MPH,* Jill M. Mhyre, MD, Lisa R. Leffert, MD, Rebecca A. Hoban, MD, MPH,
Mohammad Y. Yakoob, MD, MS, and Brian T. Bateman, MD
BACKGROUND: There are profound racial and ethnic disparities in obstetric outcomes in the
United States, but little is known about disparities in risk of postpartum hemorrhage (PPH).
We explored the association of race and ethnicity on the risk of PPH due to uterine atony with
sequential adjustment for possible mediating factors.
METHODS: This analysis was based on the Nationwide Inpatient Sample, from between 2005
and 2008. The frequencies of atonic PPH and atonic PPH resulting in transfusion or hysterectomy
were estimated. We developed multivariable logistic regression models to estimate the odds of
these outcomes in maternal racial/ethnic groups by sequentially adding potential mediators.
RESULTS: Hispanic ethnicity and Asian/Pacific Islander race were associated with a statistically
significant increased odds of atonic PPH in comparison with Caucasians, despite adjustment
for potential mediators (adjusted odds ratio [OR] for Hispanics: 1.21, 99% confidence interval
[1.18, 1.25]; for Asians/Pacific Islanders: 1.31 [1.25, 1.38], with Caucasians as reference).
Similar results were observed for these racial/ethnic groups for atonic PPH resulting in transfusion or hysterectomy.
CONCLUSION: Hispanic ethnicity and Asian/Pacific Islander race are significant risk factors
for atonic PPH independent of measured potential mediators; biological differences may play a
role. (Anesth Analg 2012;115:112736)

acial disparities in obstetric outcomes in the


United States (US) are some of the most profound in medicine. They have been documented
in preterm delivery,13 hypertensive disorders,46 intrauterine growth restriction,7,8 intrauterine fetal demise,9
and maternal mortality.10,11 For many of these complications, African-Americans are disproportionally affected,
with rates in Hispanics and Asians comparable to those
observed in Caucasians.12
Highlighting disparities in these outcomes has been
useful in understanding the social, economic, and quality-
of-care determinants of obstetric health, and the way in
which these vary by racial and ethnic groups in the US.12
For some complications, particularly preterm d
elivery,13,14
it has also helped to expose probable differences in
genetic predisposition. These differences have been examined using modern genetic approaches to increase the
From the *Department of Obstetrics, Gynecology and Reproductive
Biology, Massachusetts General Hospital, Harvard Medical School, Boston,
MA; Department of Anesthesiology, University of Michigan Health
System, Ann Arbor, MI; Department of Anesthesia, Critical Care, and
Pain Medicine, Massachusetts General Hospital, Harvard Medical School,
Boston, MA; Department of Newborn Medicine, Tufts Medical Center and
Department of Global Health, Harvard School of Public Health, Boston,
MA; Department of Epidemiology, Harvard School of Public Health,
Boston, MA.
Accepted for publication June 22, 2012.
Funding: This publication was supported by the Amos Medical Faculty
Development Award of the Robert Wood Johnson Foundation, Grant no.
RWJF-67875 (to A.B.) and T32 Training Grant GM007592 (to B.T.B.).
The authors declare no conflict of interest.
Reprints will not be available from the authors.
Address correspondence to Brian T. Bateman, MD, Department of Anesthesia,
Critical Care, and Pain Medicine, Massachusetts General Hospital, Harvard
Medical School, 55 Fruit Street, Boston, MA 02114. Address e-
mail to
BBateman@partners.org.
Copyright 2012 International Anesthesia Research Society
DOI: 10.1213/ANE.0b013e3182691e62

November 2012 Volume 115 Number 5

understanding of the pathophysiologic basis of preterm


birth.13,1517
Racial/ethnic disparities in postpartum hemorrhage
(PPH) have been less intensively studied. PPH represents
a diverse range of etiologies, each of which has distinct
risk factors.18 Uterine atony is the most common cause of
PPH, accounting for approximately 80% of cases.19 Given
that atony is caused by a deficient response to endogenous
and exogenous signals that promote uterine contraction
after delivery, it is an etiology of PPH likely to be susceptible to genetic factors. The severity of PPH due to atony
may also depend on the quality of the clinical response
and management, features that may differ by maternal
race/ethnicity.
In this study we therefore examined racial/ethnic variation in rates of atonic PPH, including the more severe subgroups of atonic PPH with transfusion or hysterectomy,
and estimated the extent to which it can be explained by
demographic factors, clinical management, comorbidities,
socioeconomic factors, and h
ospital-level factors.

METHODS
Data Source

The cohort was obtained from the Nationwide Inpatient


Sample (NIS), an administrative database that contains
information on approximately one fifth of US hospitalizations. For this study, the NIS was used as a large convenience sample. For each admission recorded in the
dataset, there is information regarding patient demographic characteristics, admission source, disposition,
and up to 15 diagnoses and 15 procedures recorded using
International Classification of Diseases 9th revision codes
(ICD-9 CM). Information on the dataset is available at
http://www.hcup-us.ahrq.gov/nisoverview.jsp. The database is maintained as part of the Healthcare Utilization
www.anesthesia-analgesia.org 1127

Maternal Race/Ethnicity and Postpartum Hemorrhage

Project (HCUP) of the Agency for Healthcare Research and


Quality.

Patients

We selected inpatient delivery hospitalizations from the


years 2005 to 2008 using a modified version of the algorithm previously described by Kuklina et al.20 Delivery
hospitalizations were identified by the presence of a
diagnosis code for delivery, or procedure codes indicating delivery (e.g., forceps, breech extraction, or cesarean
delivery). Hospitalizations with diagnoses indicating
hydatiform mole, ectopic pregnancy, or other abnormal
products of conception, or procedure codes indicating abortion were excluded (Appendix 1). There were 3,531,938
delivery admissions identified in this manner. We then
excluded patients for whom race/ethnicity was missing
(n = 891,597) or coded as a category other than Caucasian,
African-American, Hispanic, or Asian/Pacific Islander (n =
151,367). Race/ethnicity is systematically not reported for
several states contributing data to the NIS, which accounts
for the large number of missing values. The final cohort for
analysis included 2,488,974 admissions.
Race/ethnicity was defined on the basis of its documentation in the hospital discharge abstracts. Some states report
race and ethnicity separately (e.g., African-
American-
Hispanic or Caucasian-Hispanic); in these cases, race and
ethnicity are combined into a single variable in the NIS
dataset, with ethnicity taking precedence over race (e.g.,
African-American-Hispanic is coded Hispanic).

Definition of Outcomes

We considered the association of race/ethnicity on 3 outcomes: (1) PPH from uterine atony, (2) PPH from uterine
atony requiring transfusion of packed red blood cells, and
(3) PPH from uterine atony requiring hysterectomy. These
were defined using appropriate ICD-9 CM diagnosis and
procedure codes (Appendix 2). Validation studies have suggested that the positive predictive value for PPH codes is in
excess of 80%.21,22

Characteristics of the Study Patients


and Hospitals

Five classes of characteristics were extracted for each of the


delivery admissions analyzed: (1) maternal age, (2) delivery type, (3) obstetric conditions and medical comorbidities,
(4) primary expected payer, and (5) hospital characteristics.
Maternal age at the time of delivery was extracted from the
dataset and categorized into 1 of 7 groups (<20, 20 to 24, 25
to 29, 30 to 34, 35 to 39, 40 to 44, or >44 years old).
Delivery type was defined as vaginal, cesarean without labor, and cesarean after labor. The cesarean after labor
group was identified by the presence of an ICD-9 code
indicating cesarean along with an ICD-9 code consistent
with labor before the cesarean delivery.23 Recorded cesarean delivery, in the absence of a code indicating labor, was
defined as cesarean without labor. Relevant obstetric conditions and medical comorbidities were identified using
appropriate ICD-9 CM codes and included induction
of labor, multiple gestations, polyhydramnios, diabetes
(preexisting and gestational), chorioamnionitis, stillbirth,

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grand multiparity, preeclampsia, obesity, fibroids, placental


abruption, p

lacenta previa, previous cesarean delivery,


chronic anemia, PPH with retained placenta, and prolonged labor. Primary expected payer, a potential surrogate
for socioeconomic status, was categorized as Medicaid,
Medicare, private insurance, self-pay, no charge, or other.
Hospital characteristics extracted from the NIS included
ownership (defined as government nonfederal, private
not-for-profit, and private investor-owned), teaching status (teaching hospital or nonteaching), and location (urban
or rural). The annual delivery volume for each hospital
included in the dataset was also determined and categorized into 6 groups (1 to 250, 251 to 500, 501 to 1000, 1001 to
2000, 2001 to 4000, and >4000 deliveries per annum).

Statistical Analysis

The distribution and frequency of maternal age group,


delivery type, obstetric conditions and medical comorbidities, primary expected payer, and hospital characteristics
were compared across the 4 racial/ethnic groups using 2
analysis. We then fit logistic regression models to determine the relation between the racial/ethnic groups of the
3 PPH outcomes of interest (each examined in a separate
set of models). There were 4969 admissions excluded from
the analysis because 1 or more covariates were missing.
The models for each outcome were constructed in a nested
manner so as to ascertain the residual disparity present after the adjustment for each set of covariates. The 2
continuous variables considered, age and annual hospital delivery volume, had nonlinear associations with the
outcomes considered and were included as categorical
variables in the models. Each of the models was compared
with the model that preceded it using the likelihood ratio
test. The Akaike Information Criterion (AIC) was also
calculated for each of the models; this measure assesses
the goodness-of-model fit accounting for the number of
parameters in the model. The potential for multicollinearity affecting the estimates for race/ethnicity was assessed
by calculating a variance inflation factor for race/ethnicity
when considered with all other covariates. Variance inflation factors for the race/ethnicity categories ranged from
1.07 to 1.32, suggesting that collinearity was not an issue
in these analyses. A c-statistic was calculated for the final
model for each of the outcomes to measure the discrimination of the considered covariates.

Sensitivity Analyses

Given the potential for misclassification of PPH from other


etiologies as atony, we conducted a sensitivity analysis
excluding patients with obstetric trauma, uterine rupture,
PPH from coagulopathy, uterine inversion, and amniotic
fluid embolism, and reassessed the association between
race/ethnicity and each of the 3 outcomes in the final
model. An additional sensitivity analysis was performed
using a generalized estimating equation clustering on the
hospital at which delivery occurred, to account for correlated outcomes at the hospital level. Finally, we examined
the frequency of each of the study outcomes and distribution of covariates separately in the analytic dataset and in
NIS delivery admissions excluded from analysis because

ANESTHESIA & ANALGESIA

Table 1. Study Population, by Maternal Race/Ethnicity, 20052008


Race/ethnicity
White

Asian/Pacific
Islander

Hispanic

104,402
308,126
384,705
341,839
185,727
39,684
2498

7.64
22.54
28.14
25.01
13.59
2.90
0.18

54,968
103,108
80,909
52,653
27,796
7011
447

16.82
31.54
24.75
16.11
8.50
2.15
0.14

92,570
189,004
179,214
127,907
60,335
13,050
647

13.97
28.52
27.04
19.30
9.10
1.97
0.10

3660
14,658
35,370
47,038
25,788
5104
317

2.77
11.11
26.81
35.65
19.55
3.87
0.24

920,572
247,347
199,182
263,519
28,057
10,547
73,675
17,936
6980
6353
48,941
25,357
11,444
14,083
7170
202,126
70,291
3687
11,554

67.34
18.09
14.57
19.28
2.05
0.77
5.39
1.31
0.51
0.47
3.58
1.86
0.84
1.03
0.52
14.79
5.14
0.27
0.85

212,719
62,556
51,686
47,056
6619
2113
18,618
6802
3849
3003
18,978
11,443
7546
4767
1609
52,554
32,335
854
1304

65.06
19.13
15.81
14.39
2.02
0.65
5.69
2.08
1.18
0.92
5.80
3.50
2.31
1.46
0.49
16.07
9.89
0.26
0.40

452,472
120,562
89,810
78,518
7924
3180
46,606
14,862
3860
5676
26,000
13,140
5027
6056
3360
112,724
51,557
1491
3466

68.26
18.19
13.55
11.85
1.20
0.48
7.03
2.24
0.58
0.86
3.92
1.98
0.76
0.91
0.51
17.01
7.78
0.23
0.52

90,775
20,954
20,339
17,608
1966
615
14,004
3841
591
666
3191
937
2151
1228
1231
17,912
6630
332
1299

68.73
15.87
15.40
13.33
1.49
0.47
10.60
2.91
0.45
0.50
2.42
0.71
1.63
0.93
0.93
13.56
5.02
0.25
0.98

774,159
101,687
281,035
146,652
62,614
1,182,134
550,252

56.67
7.44
20.57
10.74
4.58
86.53
40.28

210,952
24,143
48,846
41,576
1433
302,401
187,470

64.52
7.38
14.94
12.72
0.44
92.49
57.34

353,840
44,634
165,243
91,521
7586
635,648
328,511

53.38
6.73
24.93
13.81
1.14
95.90
49.56

74,910
12,398
29,951
13,074
961
128,325
68,230

57.06
9.44
22.81
9.96
0.73
97.74
51.97

44,675
86,764
194,748
356,396
441,780
242,738

3.27
6.35
14.25
26.07
32.32
17.76

3819
9145
32,261
90,743
111,079
79,914

1.17
2.80
9.87
27.75
33.97
24.44

4492
14,813
47,159
140,975
221,543
233,862

0.68
2.24
7.12
21.27
33.42
35.28

1136
2159
7996
27,890
55,355
37,532

0.86
1.64
6.05
21.12
41.91
28.42

9330
408,631
878,472
28,747
1650
38,813

0.68
29.92
64.33
2.11
0.12
2.84

3729
194,333
111,013
9801
1009
6718

1.14
59.50
33.99
3.00
0.31
2.06

3088
416,997
173,650
52,980
5197
10,088

0.47
62.99
26.23
8.00
0.79
1.52

232
31,963
92,324
5231
149
2058

0.18
24.22
69.97
3.96
0.11
1.56

N
Age (years)
<20
2024
2529
3034
3539
4044
>44
Delivery type
Vaginal
Cesarean without labor
Cesarean with labor
Labor induction
Multiple gestation
Polyhydramnios
Diabetes (pre-existing and gestational)
Chorioamnionitis
Stillbirth
Grand multiparity
Preeclampsia
Obesity
Fibroid
Placental abruption
Placenta previa
Previous cesarean
Chronic anemia
PPH with retained placenta
Prolonged labor
Control/ownership of hospital
Government or private (collapsed category)
Government, nonfederal (public)
Private, not-for-profit (voluntary)
Private, investor-owned (proprietary)
Private (collapsed category)
Urban hospital location (vs. rural)
Teaching hospital (vs. nonteaching hospital)
Annual delivery volume of hospital
1250
251500
5011000
10012000
20014000
>4000
Primary expected payer
Medicare
Medicaid
Private Insurance
Self-pay
No charge
Other

Black

PPH = postpartum hemorrhage.

race was coded or was coded other than Caucasian,


African-American, Hispanic, or Asian/Pacific Islander. This
was to assess the degree of bias that may have been introduced by using complete case analysis.
Data analyses were performed using Stata version
10.0 (Stata, College Station, TX) and SAS version 9.1 (SAS
Institute, Cary, NC).

RESULTS

The final cohort for analysis included 2,488,974 delivery


admissions. The overall distribution of race/ethnicity was

November 2012 Volume 115 Number 5

54.9% Caucasian, 13.1% African-American, 26.6% Hispanic,


and 5.3% Asian/Pacific Islander. Clinical characteristics
of the study cohort are presented in Table 1. There was a
significant difference in the distribution of the patient
characteristics across race/ethnic groups (P < 0.001 for
all variables). A comparison between the analyzed sample and the proportion of NIS delivery admissions that
were excluded is shown in Appendix 3; the characteristics of the patients were generally very similar in these 2
groups. The overall frequency of PPH from atony was
2.14%; PPH from atony resulting in transfusion, 0.24%;

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Maternal Race/Ethnicity and Postpartum Hemorrhage

Table 2. Frequency per 10,000 Deliveries and 99% Confidence Intervals of Postpartum Hemorrhage (PPH)
from Atony, PPH from Atony Resulting in Transfusion, and PPH from Atony Resulting in Hysterectomy by
Race/Ethnicity
PPH from atony resulting
in transfusion

PPH from atony


Race/ethnicity

Per 10,000 (99% CI)

White
African-American
Hispanic
Asian/Pacific Islander
Overall

27,104
6435
16,389
3338
53,266

198.3 (195.2201.3)
196.8 (190.6203.1)
247.3 (242.3252.2)
252.7 (241.6263.9)
214.0 (211.6216.4)

2525
958
2004
412
5899

and PPH with atony associated with hysterectomy, 0.034%.


Unadjusted frequency varied by race/ethnicity, as shown
in Table 2.
Table 3 shows the nested models examining the association between race/ethnicity and PPH from uterine atony.
In the unadjusted, univariate analysis (model 1), in comparison with Caucasians, Hispanics and Asians/Pacific
Islanders had significantly higher odds, while the odds
in African-Americans were not increased. With the addition of covariates in sequential models, African-American
race became increasingly (although only slightly) protective, with the estimates in Hispanics and Asians/Pacific
Islanders remaining relatively unchanged. The likelihood
ratio tests and AIC showed that each sequential model
was significantly better than the one that preceded it. The
c-statistic for the final model was 0.653, indicating that the
model had modest ability to discriminate patients with
atonic PPH from those without.
Table 4 shows the nested models examining the outcome of atonic PPH resulting in blood transfusion. The
unadjusted, univariate odds of this outcome were significantly increased for
African-
Americans, Hispanics, and
Asians/Pacific Islanders. For African-Americans, the odds
of the outcome decreased from approximately 1.6 in model
1 (univariate model) to 1.2 in model 6 (which included all
mediating factors); for Hispanics the odds decreased from
1.6 in model 1 to 1.4 in model 6. For both groups, most of
the decrease in odds was associated with adjustment for
obstetric and medical comorbidities (model 4) and primary
payer type (model 5). The estimated odds associated with
Asian/Pacific Islander race changed little among the models. Again, by both the likelihood ratio test and AIC, each
sequential model improved upon the one that preceded it.
The c-statistic for model 6 was 0.747, indicating moderate
discrimination with the model.
Table 5 shows the nested models examining the outcome of atonic PPH resulting in hysterectomy. The unadjusted, univariate odds of this outcome were significantly
increased for African-Americans, Hispanics, and Asians/
Pacific Islanders; the
age-
adjusted disparities were even
more profound. After adjustment for all variables (model
6),
African-
Americans had an approximately 1.3-fold
higher odds and Hispanics and Asians approximately 1.5fold higher odds than Caucasians. Both the likelihood ratio
test and AIC showed significant improvement of the model
at each step, with the exception of the addition of payer

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Per 10,000 (99% CI)


18.5
29.3
30.2
31.2
23.7

(17.519.4)
(26.931.7)
(28.532)
(27.235.1)
(22.924.5)

PPH from atony resulting


in hysterectomy
N
380
131
262
69
842

Per 10,000 (99% CI)


2.8
4.0
4.0
5.2
3.4

(2.43.1)
(3.14.9)
(3.34.6)
(3.66.8)
(3.13.7)

type. The c-statistic for model 6 was 0.831, indicating good


discrimination with the model.
In the sensitivity analysis in which we repeated the fitting of model 6 for each of the 3 outcomes after excluding
patients with obstetric trauma, uterine rupture, PPH from
coagulopathy, uterine inversion, and amniotic fluid embolism, we observed little change in the estimates for the race/
ethnic groups (results not shown). The additional sensitivity
analysis, using a generalized estimating equation clustering
on hospital, also did not substantially change the association between race/ethnicity and the outcome (results not
shown).

DISCUSSION

PPH is a leading cause of obstetric morbidity and mortality, both in the US and worldwide.10,18,19 While racial/
ethnic disparities have been extensively studied for other
obstetric outcomes, less detail has been reported regarding disparities in PPH. In this sample of >2 million US
births, Hispanic ethnicity and Asian/Pacific Islander race
were associated with a higher incidence of PPH from
uterine atony than was Caucasian race, consistent with a
few other reports in the literature.2426 We also report an
increased risk among these populations for atonic PPH
requiring transfusion or hysterectomy. African-American
race was also an apparent risk factor for the more severe
forms of atonic PPH.
The approach we used of residual direct effect modeling seeks to determine the extent to which disparities are
explained by patient and systems factors by sequentially
adding groups of variables into a model of an outcome
and observing the impact of adjusting for those variables
on the estimates of the effect of race. While these factors
(including demographics, maternal comorbidities, obstetric management, and hospital characteristics) were able
to explain much of the increased odds for severe atonic
PPH in African-Americans (with the greatest attenuation
occurring with the addition of comorbidities), they did not
significantly account for the increased odds observed in
Hispanics or Asian women in atonic PPH overall, or severe
atonic PPH. The persistence of risk of atonic PPH among
Hispanics and Asians/Pacific Islanders after adjusting for
mediators may reflect underlying biological differences that
contribute to this complication. The molecular mechanisms
by which the uterus contracts in the 3rd stage of labor to
prevent PPH are not well understood, though candidate

ANESTHESIA & ANALGESIA

November 2012 Volume 115 Number 5

www.anesthesia-analgesia.org 1131

0.60
<0.01
<0.01

<0.01

256,509.00
412.38

513,038.0

<0.01
<0.01
<0.01

Referent
0.96 (0.920.99)
1.22 (1.191.25)
1.33 (1.271.39)

Model 2

511,075.2

255525.59
1966.81

Referent
0.97 (0.941.01)
1.23 (1.21.26)
1.30 (1.241.36)

Model 3

<0.01

0.04
<0.01
<0.01

497,325.3

248,634.64
13781.91

Referent
0.90 (0.860.93)
1.21 (1.181.24)
1.30 (1.241.37)

Model 4

<0.01

<0.01
<0.01
<0.01

497,301.2

248617.59
34.09

Referent
0.89 (0.860.92)
1.19 (1.161.23)
1.30 (1.241.37)

Model 5

<0.01

<0.01
<0.01
<0.01

495,685.4

247,798.68
1637.83

Referent
0.88 (0.850.92)
1.21 (1.181.25)
1.31 (1.251.38)

Model 6

<0.01

<0.01
<0.01
<0.01

Model 2
P

Model 3
P

82,510.67

41,245.33
140.32
<0.01

81,659.66

40,817.83
855.01

<0.01

Referent
Referent
<0.01 1.56 (1.411.72) <0.01 1.51 (1.361.66) <0.01
<0.01 1.63 (1.51.76)
<0.01 1.63 (1.51.76)
<0.01
<0.01 1.70 (1.481.95) <0.01 1.73 (1.511.99) <0.01

77,557.9

38,750.95
4133.76

<0.01

Referent
1.28 (1.151.41) <0.01
1.55 (1.441.68) <0.01
1.71 (1.491.96) <0.01

Model 4

77,506.53

38,720.26
61.37

<0.01

Referent
1.22 (1.11.35)
<0.01
1.44 (1.331.57) <0.01
1.71 (1.481.96) <0.01

Model 5

77,317.28

38,614.63
211.25

<0.01

Referent
1.18 (1.071.31) <0.01
1.44 (1.321.58) <0.01
1.69 (1.471.94) <0.01

Model 6

Model 1 = race/ethnicity only; model 2 = race/ethnicity and age group; model 3 = race/ethnicity, age group, and mode of delivery; model 4 = race/ethnicity, age group, mode of delivery, and patient comorbidities; model
5 = race/ethnicity, age group, mode of delivery, patient comorbidities, and primary payer type; model 6 = race/ethnicity, age group, mode of delivery, patient comorbidities, primary payer type, and hospital characteristics;
AIC = Akaike Information Criterion.
Odds ratios and 99% confidence intervals shown.

Effect estimates
White
Referent
AfricanAmerican
1.59 (1.441.75)
Hispanic
1.64 (1.521.77)
Asian/Pacific Islander
1.70 (1.481.95)
Model characteristics
Log likelihood
41,315.49
Likelihood ratio test (vs.
previous model): Chi square
AIC
82,638.99

Model 1

Table 4. Models Showing the Relationship Between Race/Ethnicity and Postpartum Hemorrhage (PPH) from Uterine Atony Resulting in Transfusion

Model 1 = race/ethnicity only; model 2 = race/ethnicity and age group; model 3 = race/ethnicity, age group, and mode of delivery; model 4 = race/ethnicity, age group, mode of delivery, and patient comorbidities; model
5 = race/ethnicity, age group, mode of delivery, patient comorbidities, and primary payer type; model 6 = race/ethnicity, age group, mode of delivery, patient comorbidities, primary payer type, and hospital characteristics;
AIC = Akaike Information Criterion.
Odds ratios and 99% confidence intervals shown.

Effect estimates
White
Referent
AfricanAmerican
0.99 (0.961.03)
Hispanic
1.25 (1.221.29)
Asian/Pacific Islander 1.28 (1.221.34)
Model characteristics
Log likelihood
256,715.19
Likelihood ratio
test (vs. previous
model): Chi square
AIC
513,438.4

Model 1

Table 3. Models Showing the Relationship Between Race/Ethnicity and Postpartum Hemorrhage (PPH) from Uterine Atony

13,587.67
13,579.92
14,255.69
14,775.28
15,062.21

Model 1 = race/ethnicity only; model 2 = race/ethnicity and age group; model 3 = race/ethnicity, age group, and mode of delivery; model 4 = race/ethnicity, age group, mode of delivery, and patient comorbidities; model
5 = race/ethnicity, age group, mode of delivery, patient comorbidities, and primary payer type; model 6 = race/ethnicity, age group, mode of delivery, patient comorbidities, primary payer type, and hospital characteristic;
PPH = postpartum hemorrhage; AIC = Akaike Information Criterion.
Odds ratios and 99% confidence intervals shown.

13,572.02

<0.01
6742.00
37.65
0.81
6760.83
2.25
<0.01
6761.95
707.78
<0.01
7115.84
523.58
<0.01
7377.63
298.94
7527.10

Referent
Referent
1.40 (1.061.84) <0.01 1.33 (1.011.75)
0.01
1.57 (1.251.97) <0.01 1.54 (1.221.94) <0.01
1.64 (1.162.32) <0.01 1.58 (1.122.23) <0.01
Referent
Referent
Referent
Referent
1.44 (1.111.88) <0.01 1.77 (1.362.3) <0.01 1.62 (1.252.11) <0.01 1.42 (1.091.86) <0.01
1.42 (1.151.75) <0.01 1.66 (1.352.05) <0.01 1.62 (1.322)
<0.01
1.6 (1.31.98)
<0.01
1.87 (1.332.62) <0.01 1.58 (1.122.21) <0.01 1.67 (1.192.35) <0.01 1.65 (1.172.32) <0.01

Model 6
P
Model 5
P
Model 4
P
Model 3
P
Model 2
P
Model 1

Table 5. Models Showing the Relationship Between Race/Ethnicity and PPH from Uterine Atony Resulting in Hysterectomy

Effect estimates
White
AfricanAmerican
Hispanic
Asian/Pacific Islander
Model characteristics
Log likelihood
Likelihood ratio test (vs.
previous model): chi square
AIC

Maternal Race/Ethnicity and Postpartum Hemorrhage

1132
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genes and molecular mechanisms are currently being


explored.2729 Recently, polymorphisms in -2 adrenoreceptors were found to correlate with progress of active labor.30
We speculate that differential expression of genes, or genetic
polymorphisms that vary by race/ethnicity, might contribute to the disparities noted.
Interestingly,
African-
American race was associated
with slightly lower odds of atonic PPH in comparison with
Caucasian race, but increased odds of atonic PPH resulting
in transfusion and hysterectomy. The odds of these severe
forms of atonic PPH shifted substantially towards the null
with the inclusion of patient comorbidities into the explanatory models. This suggests that African-American women
hemorrhage from atony less often than do Caucasian
women, but when they do, the hemorrhage tends to
be more severe, and this increase in severity is largely
explained by the higher prevalence of comorbid conditions
that confer risk of atonic hemorrhage requiring transfusion
or hysterectomy (e.g., fibroids, preeclampsia, and preexisting anemia).
Disparities in outcomes may also arise from variation
in the quality of obstetrical care provided. The relationship between hospital or provider volume and quality of
care has been explored in surgical fields31,32 and in obstetrics.33,34 In general, data from previous studies suggest
that greater provider and hospital obstetrical volume is
associated with better clinical outcomes; low obstetric volume has been associated with increased risk of PPH.19 It
does not appear that hospital-level characteristics played
a significant role in mediating the observed disparities in
atonic PPH in our study; inclusion of hospital delivery
volume, teaching status, and location in our sequential
models resulted in only a small shift in point estimates
for atonic PPH.
The large number of births in the NIS allowed us to
robustly examine the role of a large number of potential
mediators of the association of race/ethnicity and atonic
PPH, even for the relatively rare outcomes of atonic PPH
resulting in transfusion or hysterectomy. We were also able
to include sufficient numbers of Hispanics and Asians/
Pacific Islanders to make valid conclusions about these
understudied groups. The analyses, however, are not without limitations. Outcomes and exposures were determined
from data collected for administrative purposes, and
while a study such as this can only be conducted using the
large number of subjects that administrative data afford,
certain conditions and outcomes may be miscoded.3537
Assuming that such misclassification is not systematically
different among the racial/ethnic groups, any misclassification should attenuate the estimates of the effect of race/
ethnicity towards the null. Despite our efforts to adjust
for a full range of potentially explanatory patient and hospital characteristics, there may be important unmeasured
or undermeasured variables in our dataset that might
mediate some of the effect of race/ethnicity or confound
the association of mediators with the outcomes. These
unmeasured/unreported variables may bias the estimates
of the direct effect of race.38 In particular, maternal body
mass index, length of labor, and neonatal birth weight are
factors that vary by race/ethnicity, are associated with

ANESTHESIA & ANALGESIA

PPH incidence or severity, and are not captured in our


analyses.3946 Inability to adjust for these factors, in particular newborn birth weight, could also explain the slight
protective association of African-American race on atonic
PPH. Furthermore, we base our definition of PPH on
administrative coding rather than estimated blood loss.
The threshold for diagnosing PPH may vary by institution
or individual practitioner, although we assume that this
is nondifferential among the racial/ethnic groups. Finally,
race/ethnicity is not recorded in approximately one quarter of the hospitalizations for delivery represented in
the NIS. Despite the fact that the NIS includes sampling
weights to facilitate extrapolation to the entire US population, this kind of inference is not appropriate for analyses of race/ethnicity in which a large portion of the study
population was excluded from analysis due to missing
data. Rather, we use those delivery admissions from the
NIS in which race/ethnicity is coded as a large convenience sample to study the effects of interest; this results
in a sample that is less representative of the entire delivering population in the US than the NIS dataset in its complete form. Of note, however, there was generally good
balance in risk of the study outcomes and key covariates
between the analyzed and excluded samples (Appendix
3). The race/ethnicity categories are defined in the NIS,
with Hispanic ethnicity taking precedence over race. Thus
the Hispanic category in our analysis includes patients
identified as Caucasian-Hispanic and African-American/
Hispanic, which introduces substantial heterogeneity in
ancestry in this group. The assignment of patient race and
ethnicity takes place at the hospital level, and while common practice is to ask the patient to self-identify these
variables, actual practice likely varies among states and
hospitals.
Our data demonstrate that racial/ethnic disparities persist in atonic PPH and severe atonic PPH despite
adjustment for numerous potential explanatory variables, particularly among Hispanics and Asians/Pacific
Islanders. The disparity may point to variation in the
genetic predisposition to atonic PPH. Further investigation into the contributions of biological and health service mediators should be undertaken, with an eye toward
interventions to mitigate the current disparities. In the
meantime, clinicians should be aware of these differences
in risk and take adequate measures (e.g., active management of the 3rd stage of labor, having uterotonics readily
available) to reduce the incidence and consequences of
PPH in all women. E

November 2012 Volume 115 Number 5

Appendix 1. Definition of Delivery-Related


Admission
Diagnosis/procedure
codes
Inclusion criteria
ICD-9 CM diagnosis codes
Outcome of delivery
Normal delivery
ICD-9 CM procedure codes
Forceps, vacuum, and breech
extraction
Internal and combined version
and extraction
Other manually assisted
deliveries
Episiotomy
Cesarean delivery
Exclusion criteria
ICD-9 CM diagnosis codes
Ectopic or molar pregnancy
Pregnancy with abortive outcome
ICD-9 CM procedure codes
Abortion

V27.x
650.x
72.x
73.22
73.59
73.6
74.074.2, 74.4, 74.9

630.x633.x
634.x639.x
69.01, 69.51, 75.0

Appendix 2. Definitions of Obstetric Conditions


Postpartum hemorrhage
from uterine atony
Blood transfusion
Hysterectomy
Cesarean delivery
Labor
Labor induction
Multiple gestation
Polyhydramnios
Diabetes (pre-existing
and gestational)
Chorioamnionitis
Stillbirth
Grand multiparity
Preeclampsia
Obesity
Fibroid
Placental abruption
Placenta previa
Previous cesarean
Chronic anemia
Postpartum hemorrhage
with retained placenta
Prolonged labor

Diagnosis/procedure codes
666.1x
99.04
68.368.9
74.074.2, 74.4, 74.9
652.1x, 653.x, 656.3x, 659.0659.3x,
660663.x, 665.1x, 73.073.1, 73.4
73.4
V27.2V27.8, 651.x
657.x
250.x, 648.0x, 648.8x
658.4x
V27.1, V27.3, V27.4, V27.6, V27.7,
656.4x
659.4x, V23.3x
642.4x642.7x
278.0x
654.1x, 218.x
641.2x
641.0x641.1x
654.2x
280.x281.x, 285.2x285.9x
666.0x
662.x

www.anesthesia-analgesia.org 1133

Maternal Race/Ethnicity and Postpartum Hemorrhage

Appendix 3. Comparison of Analyzed Admissions and Those Excluded Because of Missing Race/Ethnicity or
Race/Ethnicity Other than Caucasian, A
frican-American, Hispanic, and Asian/Pacific Islander
Excluded admissions
Outcomes
Atony
Atony with transfusion
Atony with hysterectomy
Age (years)
<20
2024
2529
3034
3539
4044
>44
Delivery type
Vaginal
Cesarean without labor
Cesarean with labor
Labor induction
Multiple gestation
Polyhydramnios
Diabetes (pre-existing and gestational)
Chorioamnionitis
Stillbirth
Grand multiparity
Preeclampsia
Obesity
Fibroid
Placental abruption
Placenta previa
Previous cesarean
Chronic anemia
Postpartum hemorrhage with retained placenta
Prolonged labor
Control/ownership of hospital
Government or private (collapsed category)
Government, nonfederal (public)
Private, not-for-profit (voluntary)
Private, investor-owned (proprietary)
Private (collapsed category)
Urban hospital location (vs. rural)
Teaching hospital (vs. nonteaching hospital)
Annual delivery volume of hospitala
1250
251500
5011000
10012000
20014000
>4000
Primary expected payer
Medicare
Medicaid
Private Insurance
Self-pay
No charge
Other
a

Analyzed admissions

24,493
2150
260

2.35
0.21
0.02

53,266
5899
842

2.14
0.24
0.03

107,699
257,577
297,048
235,802
116,410
23,921
1913

10.35
24.76
28.55
22.67
11.19
2.30
0.18

255,600
614,896
680,198
569,437
299,646
64,849
3909

10.27
24.71
27.33
22.88
12.04
2.61
0.16

722,107
175,191
145,666
186,734
18,304
7592
63,005
16,854
6682
5620
40,644
18,928
10,324
11,706
5157
150,016
67,754
2992
8725

69.24
16.80
13.97
17.90
1.75
0.73
6.04
1.62
0.64
0.54
3.90
1.81
0.99
1.12
0.49
14.38
6.50
0.29
0.84

1,676,538
451,419
361,017
406,701
44,566
16,455
152,903
43,441
15,280
15,698
97,110
50,877
26,168
26,134
13,370
385,316
160,813
6364
17,623

67.36
18.14
14.50
16.34
1.79
0.66
6.14
1.75
0.61
0.63
3.90
2.04
1.05
1.05
0.54
15.48
6.46
0.26
0.71

623,917
73,935
207,422
72,431
62,482
886,084
487,539

59.98
7.11
19.94
6.96
6.01
85.19
46.87

1,413,861
182,862
525,075
292,823
72,594
2,248,508
1,134,463

56.85
7.35
21.11
11.77
2.92
90.40
45.61

30,135
57,431
140,153
226,510
368,898
219,837

2.89
5.51
13.44
21.72
35.37
21.08

43,372
101,450
265,306
558,289
844,564
675,993

1.74
4.08
10.66
22.43
33.93
27.16

5861
419,402
546,939
34,046
615
33,106

0.56
40.33
52.59
3.27
0.06
3.18

16,379
1,051,924
1,255,459
96,759
8005
57,677

0.66
42.31
50.50
3.89
0.32
2.32

Calculated using all admissions, not just those in which race was coded.

DISCLOSURES

Name: Allison Bryant, MD, MPH.


Contribution: This author helped design the study, conduct
the study, and prepare the manuscript.
Name: Jill M. Mhyre, MD.
Contribution: This author helped design the study, conduct
the study, and prepare the manuscript.
Name: Lisa R. Leffert, MD.
Contribution: This author helped design the study and prepare
the manuscript.

1134
www.anesthesia-analgesia.org

Name: Rebecca A. Hoban, MD, MPH.


Contribution: This author helped design the study, conduct
the study, analyze the data, and prepare the manuscript.
Name: Mohammad Y. Yakoob, MD, MS.
Contribution: This author helped design the study, conduct
the study, analyze the data, and prepare the manuscript.
Name: Brian T. Bateman, MD.
Contribution: This author helped design the study, conduct
the study, analyze the data, and prepare the manuscript.
This manuscript was handled by: Cynthia A. Wong, MD.

ANESTHESIA & ANALGESIA

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