Epidemiologic Reviews Vol. 31, No. 1
? The Author 2009.Published by Oxford University Press on behalf of the Johns Hopkins Bloomberg School of Public Health. DOI: 10.1093/epirev/mxp011
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial
License (http://creativecommons.org/licenses/by-nc/2.5/uk/), which permits unrestricted non-commercial use, Advance Access publication October 21, 2009
distribution, and reproduction in any medium, provided the original work is properly cited.
Environmental Contributions to Disparities in Pregnancy Outcomes
Marie Lynn Miranda, Pamela Maxson, and Sharon Edwards
Accepted for publication September 15, 2009.
One of the most persistent disparities in American health status is the pronounced difference in birth outcomes
between non-Hispanic black and non-Hispanic white women. Poor pregnancy outcomes have a substantial impact
on mortality, morbidity, and health care costs. Increasing evidence indicates that environmental exposures are
associated with poor birth outcomes. This paper reviews the latest research on how environmental exposures
affect pregnancy outcomes and then discusses how these exposures may be embedded within a context of
significant social and host factor stress. The analysis suggests that environmental, social, and host factors are
cumulatively stressing non-Hispanic black women and that this cumulative stress may be a cause of the persistent
disparities in pregnancy outcomes.
environment; environmental pollution; health status disparities; infant, low birth weight; pregnancy outcome;
premature birth; public health
INTRODUCTION learning disabilities (14, 15), behavioral disabilities (16),
and motor impairment (17). Of similar importance is the
One of the most persistent disparities in American health impact of lower birth weight on increased risk of diabetes,
status is the pronounced difference in birth outcomes be- obesity, cardiovascular disease, and other health problems in
tween non-Hispanic black and non-Hispanic white women. adulthood (18?20). In 2006, high rates of adverse outcomes
Striking and persistent racial disparities exist in the rates of meant that 454,583 infants were born preterm and that
low birth weight (<2,500 g), very low birth weight 267,218 infants were born low birth weight (4), creating
(<1,500 g), preterm birth (<37 weeks of gestation), very a sizable population starting life with an increased risk
preterm birth (<34 weeks of gestation), and infant mortality of short-term and long-term health and developmental
(livebirth with infant death before 12 months of age) (1?4) complications?a population disproportionately represented
(Table 1). (Please note, to better assess disparities in preg- by children of color. Thus, understanding, and subsequently
nancy outcomes, unless otherwise stated, we restricted our intervening to prevent, these adverse outcomes is of critical
analysis to women carrying singleton pregnancies. Unlike importance to the overall health of the nation.
multifetal gestations, it is reasonable to have a public health In addition to the adverse health impact of poor preg-
expectation that singleton pregnancies can be carried to term nancy outcomes, economic costs are substantial. In 2006,
and delivered at appropriate birth weights.) In 2005, while the Institute of Medicine estimated that the annual cost of
the overall leading cause of infant mortality in the United preterm birth in the United States was approximately $26
States was congenital anomalies, disorders related to short billion, or approximately $51,600 per preterm infant, with
gestation and low birth weight were the leading cause for two-thirds of the costs related to medical care (6). These
non-Hispanic black infants (5). figures underestimate the true costs because minimal data
Poor pregnancy outcomes have a significant impact on exist on the costs of long-term disabilities specifically at-
mortality, morbidity, and health care costs. Preterm birth tributable to preterm birth. Many of these conditions impose
and low birth weight are leading causes of neonatal and significant financial costs on families and on the health care,
infant mortality, as well as short-term and long-term mor- public education, and social welfare systems.
bidity (6, 7). Conditions associated with poor pregnancy Although it is widely agreed that maternal and fetal health
outcomes include respiratory distress syndrome (8), variable and well-being are determined by multiple forces, surpris-
heart rate (9), cerebral ventriculomegaly (10), cerebral palsy ingly little is known about how those forces combine in
(11), mental retardation (12), blindness (13), deafness (12), certain subpopulations. For example, elevated physical
Correspondence to Dr. Marie Lynn Miranda, Nicholas School of the Environment, Duke University, A134-LSRC, Box 90328, Durham, NC 27708
(e-mail: mmiranda@duke.edu).
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68 Miranda et al.
Table 1. Birth Outcomes Among US Singleton Livebirths in 1996
and 2006, by Maternal Race (4)
1996 2006
Outcome
No. % No. %
Total births 3,784,805 4,121,930
Preterm birth 364,356 9.63 454,583 11.03
Non-Hispanic White 183,652 8.02 214,935 9.68
Non-Hispanic Black 90,333 16.11 98,251 16.54
Hispanic 67,319 9.87 112,006 11.03
Very preterm birth 104,550 2.76 121,122 2.94
Non-Hispanic White 46,524 2.03 50,910 2.29
Non-Hispanic Black 33,442 5.96 33,221 5.59
Hispanic 18,442 2.70 29,611 2.92
Figure 1. Forces shaping pregnancy outcomes.
Low birth weight 228,062 6.03 267,218 6.48
Non-Hispanic White 112,099 4.90 119,122 5.36
Non-Hispanic Black 64,656 11.53 70,308 11.84
Hispanic 36,404 5.34 58,725 5.78
Very low birth weight 41,045 1.08 46,961 1.14 psychosocial stressors on the physical health and general
well-being of black women (24?27). The weathering hy-
Non-Hispanic White 17,858 0.78 18,818 0.85
pothesis argues that cumulative insults to the physical and
Non-Hispanic Black 14,516 2.59 15,480 2.61 emotional health of African-American women accelerate
Hispanic 6,408 0.94 9,947 0.98 their biologic aging (as evidenced by earlier onset of chronic
degenerative health problems such as hypertension, diabe-
tes, and heart disease), compromising their ability to carry
environmental exposures often occur in communities facing fetuses to term (23, 24, 28, 29).
multiple social stressors such as deteriorating housing, in- Figure 1 depicts environmental, social, and host factors as
adequate access to health care, poor schools, high un- 3 sides of an integrated triangle. Health disparities arise
employment, high crime rates, and high poverty rates?all when the forces exerted by the triangle?s sides are asymmet-
of which may compound the effects of physical environ- ric for different population groups. In this review, we use the
mental exposures. This phenomenon is especially severe heuristic presented in Figure 1 to consider how environmen-
for low-income and minority pregnant mothers, with signif- tal exposures affect pregnancy outcomes and how these ex-
icant health implications for the fetuses they carry. posures may be embedded within a context of significant
Although some reviews on the relation of environmental social and host factor stress. In this way, we attempt to
factors and pregnancy outcomes exist, none offer a frame- expand Geronimus?s notion of cumulative stress (23) to
work for understanding environmental exposures within the include physical environmental exposures. We conducted
larger context of social and host factors (21, 22). To garner literature searches of both the biomedical and social science
an understanding of the current literature on environmental fields using key terms associated with pregnancy outcomes
factors linked to pregnancy outcomes, we conducted a care- ??low birth weight??, ??very low birth weight??, ??preterm
ful exploratory review using the PubMed/MEDLINE data- birth??, ??very preterm birth??, ??infant mortality??, as well as
base (National Library of Medicine, Bethesda, Maryland). interacting each of those terms with the term ??environmental
A search for articles with the 2 Medical Subject Headings exposures?? for articles through 2008.
(MeSH) terms ??pregnancy?? and ??environmental exposure??
returned 5,960 results (June 2009). We further explored TRENDS IN ADVERSE PREGNANCY OUTCOMES
the database and citations in the articles we found and
then compiled the most relevant and timely articles in key Nationally, the rate of preterm birth among singletons
environmental-emphasis areas: air quality, metals, water rose from 9.59% to 11.03% from 1990 to 2006. At the same
quality, pesticides, environmental tobacco smoke, and time, the respective rates rose from 7.49% to 9.68% for non-
neighborhood environment. Finally, we supplemented the Hispanic whites, increased from 10.10% to 11.03% for
literature with primary data analysis that enabled us to con- Hispanics, and decreased from 17.68% to 16.54% for non-
sider the extent to which those persons subject to elevated Hispanic blacks (4). It is important to note that the rates for
environmental exposures concurrently face significant low birth weight and preterm birth in the entire US popula-
social and host factor stressors. tion, and when separated by race, are all well above the
To understand the complex etiology of black birth out- Healthy People 2010 targets (30). From 1990 to 2000,
comes relative to those for whites, Geronimus proposed the non-Hispanic black women experienced a decrease in the
??weathering hypothesis?? (23), which postulates that poor rates of preterm birth and low birth weight, resulting in
birth outcomes for African Americans are in part due to the a smaller disparity between the race groups (Figure 2A
cumulative and interactive effects of negative material and and 2B). Since 2000, however, rates for non-Hispanic blacks
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Environmental Contributions to Pregnancy Outcomes 69
A) 20
18
16
14
12
10
8
6 All
Non-Hispanic White
4
Non-Hispanic Black
2 Hispanic
0
Year
B) 14
12
10
8
6
4 All
Non-Hispanic White
2 Non-Hispanic Black
Hispanic
0
Year
Figure 2. Rates of A) preterm birth and B) low birth weight among singleton livebirths, United States, 1990?2006 (31).
have increased, as have the rates for both low birth weight comes than non-Hispanic white and Hispanic women.
and preterm birth for non-Hispanic white and Hispanic Whereas documenting the pattern of geographic variation in
women. The disparities have remained similar because of preterm birth may provide important clues to understanding
all groups experiencing an increased risk (31). the etiology and developing effective interventions, the
Even within racial groups, geographic variation in adverse geographic variation itself also illustrates the degree to which
pregnancy outcomes is significant. Figure 3 shows the the burden of disease is unequally distributed across the United
percentages of preterm births in 2006 among all singleton States and across racial/ethnic groups.
pregnancies to women and by major race/ethnicity groups As a further illustration, using North Carolina data (32;
(4). This figure illustrates the dramatic variations in the burden contact the authors for more information about this data set),
of preterm birth across the United States. When analyzing all Figure 4 demonstrates the geographic variability in preterm
preterm births, outcomes in the Southeast are worse than in birth that becomes apparent at increasingly resolved geo-
other areas of the country. When considering outcomes by graphic scales, from county rates to zip code rates and fi-
race, non-Hispanic black women have dramatically worse out- nally to US Census tract rates for one county in the state (in
Epidemiol Rev 2009;31:67?83
Percentage Percentage
1990 1990
1991 1991
1992 1992
1993 1993
1994 1994
1995 1995
1996 1996
1997 1997
1998 1998
1999 1999
2000 2000
2001 2001
2002 2002
2003 2003
2004 2004
2005 2005
2006 2006
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70 Miranda et al.
Figure 3. Rate of preterm birth among singleton livebirths, by maternal race, United States, 2006 (4). The Healthy People 2010 target rate of
preterm birth is 7.6% (30).
this case, Durham County). Note that the values in the boxed Air quality
key for this figure are the same as those for Figure 3, making
the additional insight from more resolved geographic scale Air quality throughout the gestational period, as well as
clearer. A rich area of current investigation revolves around during specific windows of vulnerability, has been shown to
how the geographic pattern of poor birth outcomes may influence the risk of low birth weight, preterm birth, fetal
correlate with environmental exposures (V. Berrocal, Duke growth restriction, and fetal and infant death (33, 77?92).
University, unpublished manuscript) (33?35). Minority populations, who are already at risk of adverse
birth outcomes, are additionally more likely to be exposed
to and experience the effects of poor air quality (2, 77, 93,
CHARACTERIZING DISPARITIES 94). In comparison to white children, a substantially higher
percentage of African-American children aged 0?5 years
The relative differences in adverse birth outcomes have were found to live in poor households located in relatively
remained fairly constant over the past few decades, narrow- close proximity to one or more industrial sources of air
ing only slightly because of the increase in white multifetal pollution (95). Furthermore, certain subpopulations may
gestations (36). Numerous studies have found that socioeco- be even more susceptible to air pollution?those whose
nomic status and income inequality are correlated with birth general health status is compromised or those with social
outcomes (37?40). A variety of other social factors have disadvantages that translate into increased environmental or
been linked to poor birth outcomes, including maternal ed- occupational exposure to toxins, adverse behaviors (poor
ucation (41?45), marital status (46), pregnancy intention diet, alcohol consumption, and smoking), and lack of ade-
(47), and teenage pregnancy (48). In addition, host factors quate access to health care and preventive health measures
such as maternal obesity (49, 50), maternal comorbidities (96).
(M. L. Miranda, Duke University, unpublished manuscript) Several components of air pollution have been associated
(51), and genetic vulnerabilities (52?69) have each been with adverse birth outcomes. Ritz et al. (97), in their South-
linked to poor pregnancy outcomes. Here, we review the ern California sample, found an increased risk of preterm
environmental factors that may contribute to disparities in birth with increasing levels of carbon monoxide and partic-
poor birth outcomes. Given that non-Hispanic black women ulate matter less than 2.5 lm in aerodynamic diameter dur-
tend to be more systematically exposed than non-Hispanic ing pregnancy. Also in California, Huynh et al. (98) found
white women to adverse environmental conditions (70?74), that the top 2 quartiles of exposure to particulate matter less
the physical environment likely interacts with adverse social than 2.5 lm in aerodynamic diameter induced a modest
environments (75, 76), as well as host factors, to contribute effect of preterm birth following adjustment for maternal
to the observed poorer birth outcomes for non-Hispanic age, race/ethnicity, education, marital status, and parity,
black women. with the quartile with the highest measurements of
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Environmental Contributions to Pregnancy Outcomes 71
Figure 4. 2006 preterm birth rates among North Carolina and Durham County singleton livebirths, by county (top), zip code (middle and bottom
left), and US Census tract (bottom right) (32). The Healthy People 2010 target rate of preterm birth is 7.6% (30).
particulate matter less than 2.5 lm in aerodynamic diameter ated with maternal exposure to sulfur dioxide, nitrogen di-
having the most effect on preterm birth. oxide, and carbon monoxide during the first month of
Timing of exposure during pregnancy has been associated pregnancy (87).
with outcomes as well. Increased exposure to sulfur dioxide In addition to ambient air concentrations of pollutants,
and particulate matter less than 10 lm in aerodynamic di- areas of locally poor air quality associated with mobile
ameter during the last 6 weeks of pregnancy has been asso- sources may impact pregnancy outcomes. A Taiwan study
ciated with an increased risk of preterm delivery (99). found that mothers living within 500 m of a freeway were
Conversely, an increased odds ratio was observed for low significantly more likely to deliver preterm than mothers
birth weight with maternal exposure to sulfur dioxide during living 500?1,500 m from the freeway (100). In Los Angeles
the first month of pregnancy and an increased risk of pre- County, California, researchers determined a 10%?20%
term birth with exposure to sulfur dioxide and carbon mon- increase in low birth weight and preterm birth risk for
oxide during the last month of pregnancy. An increased risk women living near high-traffic roads (100, 101). Impor-
of fetal growth restriction has also been shown to be associ- tantly, many more minorities (60% of Hispanics and 50%
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72 Miranda et al.
of non-Hispanic blacks, compared with 33% of non- ularly among those newborns with the highest exposure.
Hispanic whites) live in areas failing to meet 2 or more of Birth weight was lower among those with the highest com-
the national ambient air quality standards (102). bined cord plasma chlorpyrifos and diazinon exposure
levels. High levels of exposure to polycyclic organic matter
Metals increased the odds of small-for-gestational-age births (131).
Proximity to agricultural areas has also been associated
Exposure to metals increases the risk of adverse birth with adverse birth outcomes. Increases in the risk of neural
outcomes (69, 103, 104). The effects of the heavy metals tube defect have been associated with maternal residence
cadmium and manganese, the exposure routes of which in- within 1,000 m of agricultural applications of benomyl,
clude cigarette smoke and food consumption, have been methyl carbamate or organophosphorus pesticides, or pesti-
poorly studied, but rodent studies indicate the occurrence cides listed as endocrine disruptors, cholinesterase inhibitors,
of birth deformities and fetal growth restriction (103). Sev- or developmental toxins (132). Schreinemachers (133) found
eral human studies have shown a significant correlation be- that in rural, agricultural counties, where wheat acreage
tween cadmium and decreased birth weight (105, 106). occupies a larger percentage of the land and where frequency
Arsenic and lead have been shown to increase incidence of use of chlorophenoxy herbicides is higher, anomalies of
of low birth weight and preterm birth (105, 107?110). Ex- the circulatory/respiratory and musculoskeletal/integumental
posure to high concentrations of arsenic has also been asso- system significantly increased.
ciated with a 6-fold increase in stillbirth after adjusting for
potential confounders (111). Non-Hispanic black women Environmental tobacco smoke
experience greater exposure to environmental lead over
the life course (112?116), which may aggravate their risk Tobacco smoke can contain as many as 4,000 different
of both hypertension and poor birth outcomes (110, 117, chemicals (134). Exposure to environmental tobacco smoke
118). Furthermore, long-term child outcomes for prenatal may begin in utero and continue throughout development.
lead exposure include cognitive effects at 12 and 24 months One in 5 American children less than 7 years of age lives in
of age (119). a home in which someone, usually a parent, smokes regu-
larly (135). Despite lower general exposure to environmen-
Water quality tal tobacco smoke compared with non-Hispanic white
children, non-Hispanic black children have higher rates of
Water quality may be associated with low birth weight, tobacco-related illnesses and levels of cotinine, the major
fetal growth restriction, and risk of spontaneous abortion nicotine metabolite (136). Inner-city children have a greater
and stillbirth. Recent evidence has suggested that chlorina- likelihood of environmental tobacco smoke exposure, with
tion by-products such as trihalomethanes from water disin- 70%?80% of them reported to have levels of cotinine in-
fection may increase the risk of low birth weight and dicative of environmental tobacco smoke exposure (137).
stillbirth (120, 121). Water contamination caused by waste Prenatal and childhood exposure to secondhand tobacco
disposal increases the risk of low birth weight. Rodenbeck smoke is known to increase risk of outcomes such as low
et al. (122) found that the odds ratio for very low birth birth weight (138, 139), birth defects (140), sudden infant
weight compared with normal birth weight was 3.3 for ma- death syndrome (141?143), and asthma and respiratory ill-
ternal exposure to trichloroethylene via contaminated drink- nesses (135). Combined prenatal exposure to environmental
ing water from waste-disposal practices. Proximity to tobacco smoke and polycyclic aromatic hydrocarbons at
landfill sites is associated with a slight statistically signifi- levels currently found in several major US cities has been
cant increased risk of neural tube defects, low birth weight, associated with decreased birth weight and head circumfer-
and very low birth weight, with adjusted risks of 1.05, 1.03, ence (144). In addition, exposure to polycyclic aromatic
and 1.05, respectively (123). Herbicide-contaminated drink- hydrocarbons is likely to contribute to the occurrence of
ing water in Iowa has been associated with fetal growth small-for-gestational-age as well as preterm birth among
restriction for births occurring between 1984 and 1990 African Americans (145). Refer to Figure 5 for rates of
(124). In addition, there are incidents and general evidence tobacco use across the United States (146).
of racial (and class) inequities in exposure to contaminants Smoking during pregnancy may be linked to home-
in water, as well as proximity to potential water contamina- environment conditions (147, 148) or to physical abuse
tion sources (125?127). (138). The combination of physical abuse, smoking, and alco-
hol consumption/illicit drug use is significantly related to birth
Pesticide use weight (138). In the United States in 2006, women reporting
tobacco use during pregnancy delivered preterm at a rate of
The use of pesticides is ubiquitous, and many women 14.0% compared with 11.0% among women not reporting
continue to use pesticides during pregnancy (128). Prenatal tobacco use. Low infant birth weight is also significantly
pesticide exposure has been associated with adverse birth higher among smokers, with rates of 11.0% among those using
outcomes. Increased levels of dichlorodiphenyldichloro- tobacco and 6.1% among those not using tobacco (4).
ethane have been associated with lower birth weight and Rates of self-reported tobacco use during pregnancy de-
smaller head circumference (129). Whyatt et al. (130) found clined in all race groups from 1996 to 2006. There remains
a significant inverse relation between organophosphates in racial disparity in maternal smoking during pregnancy na-
umbilical cord plasma and birth weight and length, partic- tionally, with non-Hispanic white women more likely than
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Environmental Contributions to Pregnancy Outcomes 73
Figure 5. Tobacco use by US state, 1996 and 2006 (146).
non-Hispanic black women to smoke, who in turn are more Neighborhood economic conditions can influence pre-
likely than Hispanic women to smoke (4). Refer to Figure 6 term birth through differences in access to health care, qual-
for self-reported tobacco use among pregnant women across ity and type of food available in grocery stores, amount of
the United States. green space, number of safe places for exercise, and amount
of environmental pollutants (161, 162). Neighborhood dis-
Neighborhood environment advantage is often quantified by using neighborhood-level
poverty rate or income level. Areas of concentrated poverty,
Elements of the built environment can also influence ma- typically defined as neighborhoods with poverty rates
ternal health (149) through direct exposure and by limiting higher than 20%, are associated with diminished quality
the effectiveness of traditional medical care and outreach of the neighborhood?s social and physical environment,
strategies (150). Neighborhoods with higher concentrations high rates of neighborhood turnover and mobility, crime,
of non-Hispanic blacks and Hispanics have higher levels of social disorder, and attenuation of both individual socio-
physical environmental contaminants than economically economic attainment and upward mobility (76). Mothers
comparable neighborhoods with higher concentrations of from neighborhoods with lower median household in-
non-Hispanic whites (151). Research has shown that anxi- comes have been found to be at greater risk of adverse
ety, depression, and psychological distress more generally birth outcomes (163).
increase with number of housing problems (152, 153). Living in tracts with high unemployment, low educa-
Higher neighborhood problem scores have been associated tional levels, poor housing, a low proportion of managerial
with poor self-rated health, psychological distress, and im- or professional occupations, and high poverty levels in-
paired physical function, independent of age, sex, neighbor- creases the odds of preterm birth for non-Hispanic whites.
hood socioeconomic status, individual deprivation, and Interestingly, effects were still significant, but smaller, for
social capital (154). The built environment can also restrict non-Hispanic blacks. Tract-level low educational levels,
residents? physical activity (155, 156). Non-Hispanic blacks high unemployment, low-level occupations, and high
disproportionately live in low socioeconomic status neigh- poverty rates increased the odds of preterm birth for
borhoods suffering from problems such as dilapidated build- non-Hispanic blacks (164, 165). Masi et al. (166) found that
ings, lack of space for exercise, and lack of public services, tract economic disadvantage was associated with signifi-
which in turn negatively affect health (157?160). cantly lower birth weight for all maternal racial/ethnic
groups.
In a recent study, women who lived in more disadvantaged
neighborhoods had greater stress levels, reported less inter-
nal locus-of-control and emotional support, and were more
likely to smoke, drink alcohol, use hard drugs, and have later
or no prenatal care and inadequate weight gain. Strongest
associations with neighborhood risk were observed for
smoking, hard-drug use, and net weight gain during preg-
nancy (167). Conversely, neighborhoods with high levels
of residential stability may be conducive to strong ties
among residents, lower levels of perceived stress, and more
positive health outcomes. Residential stability, then, may be
protective of mental and physical health (151) and has been
associated with an increase in birth weight (168).
Neighborhood racial composition has been related to birth
Figure 6. Self-reported tobacco use by pregnant women with US outcomes. The risk of low birth weight increases with degree
singleton livebirths, by state, 2004 (31). of residential segregation at the census tract level after
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74 Miranda et al.
adjusting for individual-level risk factors and census tract neighborhoods that have high crime or unemployment rates
poverty (169). Birth weight is lower and preterm birth rates or are violent, are overcrowded, or have high median rents is
are higher in metropolitan statistical areas with moderate to associated with low birth weight and very low birth weight
high levels of isolation (170). Small-for-gestational-age births (42, 177, 178). In 2007, dramatic disparity existed in pov-
were most likely in neighborhoods with the lowest and high- erty rates by race group: 24.5% of non-Hispanic blacks and
est immigrant populations, representing isolation and segre- 21.5% of Hispanics were living in poverty compared with
gation, respectively (171). 8.2% of non-Hispanic whites. There is also geographic dis-
parity in poverty rates. The poverty rate in 2007 was 14.2%
in the South, 11.4% in the Northeast, 11.1% in the Midwest,
DISCUSSION and 12% in the West (179).
We argue that psychosocial stressors shape the effects of
Health disparities arise through differences in levels of environmental exposures. Recent animal studies indicate
exposure, combinations of exposures, and response to expo- that enriched environments may reverse some of the long-
sures originating from all 3 sides of the triangle shown in term deficits in learning associated with lead exposure. In
Figure 1. Considering how all 3 sides operate simulta- this study, lead-exposed rats were randomly assigned to
neously is critical to disentangling the complex etiology ??isolation?? cages or ??environmental enrichment?? cages
of poor pregnancy outcomes. Social stressors that have been after exposure. Results indicate that lead-induced spatial
linked to poor maternal health may co-occur with, or even learning deficits may be reversed by stimulating postexpo-
cause, disparities in environmental exposures. For example, sure environments?with obvious implications for treat-
the effects of institutionalized racism can segregate African ment of childhood lead intoxication (180). In addition,
Americans into neighborhoods that are more polluted, have a feedback loop may exist in that the psychosocial stress
higher rates of unemployment and crime, and have lower induced by symptomatic and asymptomatic behaviors and
levels of resources (172). At the same time, host factors, participation in a treatment regime may affect the attributes
such as presence of maternal complications and personality of the child?s environment that might otherwise serve a pro-
traits related to the stress response, may amplify or mitigate tective role. For example, children exposed to lead place heavy
the effect of the environmental exposure in some individuals burdens on caretakers and may overwhelm the personal, pro-
within the community. fessional, and financial resources available to parents, signif-
Within the framework of Figure 1, the area within the icantly affecting their ability to provide a supportive home
triangle represents the ??space?? that has been carved out environment (K. Joyner, United Parents Against Lead,
for any particular maternal-child pair to prosper. The area personal communication, 1999).
of the triangle is larger for women with few social and In another example, one of the key contaminants of con-
environmental stressors and more protective host factors cern in tobacco smoke is cadmium (181). Even after control-
and, of course, is smaller for those who experience social ling for potential confounders, cadmium has been negatively
or environmental stress or who have host factor vulnerabil- correlated with children?s psychometric test scores. Cadmium
ities. Imagine a new environmental exposure that affects has an even greater negative effect than lead on verbal IQ
a particular individual or group of individuals (Figure 7, scores (182). Importantly, diets often associated with those in
left). The force of that exposure will reduce the space/area lower socioeconomic brackets?namely, those high in fat or
of the triangle available to that individual/group (Figure 7, low in calcium, protein, or iron?promote absorption of cad-
top right). If, however, the individual or group has protective mium in the body (183). Although these examples relate
social factors in place, then the resiliency created by the more to child development, it is plausible that similar phe-
positive social factors may mitigate in whole or in part nomena may be playing out with respect to pregnancy
against the adverse environmental exposures. This resil- outcomes.
iency essentially increases the space available, although Maternal stress?defined by any physical or psychologi-
not necessarily equal to the area that was available prior cal challenge that threatens normal homeostasis?plays an
to the exposure (note the bowing out of the social-factors important role in the maternal and fetal immune or inflam-
side of the triangle (Figure 7, bottom right)). matory response. (So a stressor on the social-factors side of
Poverty status can act as an indicator of a whole suite of the triangle can induce or coengage a stress on the host-
risk factors for poor pregnancy outcomes, as well as a mea- factor side of the triangle, in the form of an immune or
sure of potential resiliency to other stressors, especially so inflammatory response.) For example, bacterial vaginosis,
on the social-factors side of the triangle in Figure 1. Mothers a microbial genital tract infection, is a known risk factor for
living in poverty have higher rates of clinical depression, are adverse birth outcomes and is clearly associated with, and
more likely to suffer from chronic stress, and experience possibly the cause of, a heightened maternal and fetal in-
more negative life events than do nonpoor mothers (173, flammatory response. High levels of chronic stress have
174). They are nearly 3 times as likely to suffer from do- been associated with bacterial vaginosis in pregnant women
mestic violence and have more negative health behaviors, (162, 184, 185). Low socioeconomic status, young, or un-
such as smoking and inactivity (148, 175). They are also married women are more likely to develop bacterial vagi-
more likely to be unmarried and solely responsible for rais- nosis, after controlling for known risk factors such as
ing their children (176). Furthermore, they may lack ade- income, education, and history of sexually transmitted dis-
quate social networks, which can act as a buffer to the ease (186). Ten percent of women with bacterial vaginosis
detrimental effects of stress and depression (46). Living in experience adverse pregnancy outcomes such as
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Environmental Contributions to Pregnancy Outcomes 75
Figure 7. Conceptual representation of social/environmental interactions.
spontaneous preterm delivery, premature rupture of mem- (172, 202?204) as well as encourage unhealthy behaviors
branes, and amniotic fluid infection (186). as a coping mechanism for stress (148, 205, 206).
Inflammation in gestational tissues more generally is To explore the extent to which non-Hispanic black
a major risk factor for adverse birth outcomes. Proinflam- women tend to cluster more on the higher-risk end of envi-
matory cytokines stimulate the synthesis and release of ronmental, social, and host factor stressors, we constructed
1) maternal prostaglandins and metalloproteases; 2) fetal Table 2. For each category of stressor (environmental, so-
inflammatory cytokines, cortisol, and dehydroepiandroster- cial, and host), we include a series of risk factors and show
one sulfate; and 3) placental corticotrophin-releasing hor- how non-Hispanic blacks and non-Hispanic whites are dis-
mone (187?190). These effects may be one of the pathways tributed across the risk spectrum for each factor.
whereby stress can lead to adverse birth outcomes (191). In terms of environmental stressors, we begin with air
A major contribution of maternal ??immune stress?? to ad- quality, including both ozone and particulate matter. These
verse fetal outcomes is likely stimulation of production and air quality grades are taken from the American Lung Asso-
secretion of corticotrophin-releasing hormone, which then ciation?s State of the Air 2009 report (207). A greater pro-
has multiple effects that promote preterm birth and retard portion of non-Hispanic black women living within the
fetal growth. American Lung Association study area were exposed to
Evidence from both animal models and human epidemi- high ozone levels (89.5% compared with 82.9% for non-
ologic research underscores the important role that prenatal Hispanic whites) (207, 208). This differential is not espe-
stress plays in a broad range of fetal developmental out- cially great, likely resulting from the fact that, according to
comes (192). Environmental exposures may be some of the guidelines developed by the American Lung Associa-
the ??physical challenges?? that contribute to maternal im- tion, most American communities that are part of the air
mune stress given that several environmental contaminants quality monitoring network are exposed to unhealthy levels
including heavy metals, air pollution, and environmental of ozone. The contrast for particulate matter is much more
tobacco smoke have been linked to alterations in the host dramatic. Of non-Hispanic blacks in the study area, 52.7%
inflammatory response (193?201). In addition, the stressors lived in communities receiving a grade of ??F?? from the
faced by African-American women as a marginalized group American Lung Association, compared with 38.3% of
may directly compromise their physiologic functioning non-Hispanic whites (207, 208).
Epidemiol Rev 2009;31:67?83
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76 Miranda et al.
Table 2. Distribution (%) of Select Risk Factors for Disparities in Pregnancy Outcomes, by Maternal Race and Housing Status
Data Source
Risk Factor High Risk Low Risk
(Reference No.)
Environmental Factors
Air quality grade?ozone F D C B A County grades from the
American Lung
Non-Hispanic White 82.9 3.1 8.4 3.1 2.6 Association?s State of
Non-Hispanic Black 89.5 3.3 5.1 1.2 0.9 the Air 2009 (207);
2000 US Census (208)
Air quality grade?daily F D C B A County grades from the
PM2.5 exposure American Lung
Association?s State of
Non-Hispanic White 38.3 13.3 27.3 13.1 7.9 the Air 2009 (207);
Non-Hispanic Black 52.7 14.3 21.5 9.3 2.2 2000 US Census (208)
Tenure status Renter Owner American Housing
Survey 2007 (209)
Non-Hispanic White 24.4 75.6
Non-Hispanic Black 52.9 47.1
Primary source of water No Yes American Housing
safe to drink Survey 2007 (209)
Owner-occupied 6.5 93.5
Renter-occupied 11.6 88.4
Opinion of the Worst Best American Housing
neighborhood Survey 2007 (209)
Owner-occupied 0.9 1.7 9.5 41.0 46.9
Renter-occupied 2.4 4.3 16.9 42.0 34.5
Serious crime in the Yes No American Housing
neighborhood in Survey 2007 (209)
the last 12 months
Owner-occupied 13.2 86.8
Renter-occupied 21.6 78.4
Bars on windows of Yes No American Housing
buildings within Survey 2007 (209)
300 feeta
Owner-occupied 6.8 93.2
Renter-occupied 16.9 83.1
Street in need of repair Yes No American Housing
Survey 2007 (209)
Owner-occupied 36.7 63.3
Renter-occupied 44.5 55.5
Table continues
Unlike for air quality, especially good national data are port that a serious crime has occurred in the neighborhood in
not available on quality of drinking water or the built envi- the last 12 months (21.6% compared with 13.2% for owner-
ronment that are broken out by race subgroups. We can occupied units). Renter-occupied housing units are also
indirectly assess these measures, however, by noting that more likely to have bars on the windows of buildings within
non-Hispanic blacks are much more likely to be renter- 300 feet (90 m) (16.9% vs. 6.8%); be on a street in need of
occupants (52.9%) as opposed to owner-occupants, com- repair (44.5% vs. 36.7%); or have trash, litter, or junk on the
pared with non-Hispanic whites (24.4%). In turn, in terms street or properties within 300 feet (14.5% vs. 6.5%) (209).
of water quality, 11.6% of renter-occupants do not have a safe Again, because non-Hispanic blacks are much more likely
primary source of drinking water compared with 6.5% of to live in renter-occupied housing, we can reasonably con-
owner-occupants (209). Because non-Hispanic blacks are clude that non-Hispanic blacks are also more likely to be
much more likely to be renter-occupants, we can reasonably dealing with a depauperate built environment.
conclude that non-Hispanic blacks are also much less likely In addition to documenting differences in environmental
to have a safe primary source of water to drink. exposures, Table 2 also provides data on racial differences in
Table 2 shows similar patterns regarding measures of the host factors. Non-Hispanic black women aged 20?44 years
built environment. Those living in renter-occupied housing are more likely to rate their overall health status as poor or
units are more likely to rate their neighborhoods as being on fair (10.4% compared with 6.5% for non-Hispanic white
the bottom end of the scale (6.7% compared with 2.6% for women) and are more likely to have hypertension (15.3%
owner-occupied units). Renters are also more likely to re- compared with 5.5% for non-Hispanic white women) (210).
Epidemiol Rev 2009;31:67?83
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Environmental Contributions to Pregnancy Outcomes 77
Table 2. Continued
Data Source
Risk Factor High Risk Low Risk
(Reference No.)
Trash, litter, or junk on Yes No American Housing
the street or Survey 2007 (209)
properties
within 300 feet
Owner-occupied 6.5 93.5
Renter-occupied 14.5 85.5
Host Factors
Overall health status Poor Fair Good Very good Excellent Females aged 20?44
years in the Current
Non-Hispanic White 1.6 4.9 18.8 36.8 37.9 Population Survey
Non-Hispanic Black 2.5 7.9 27.1 35.5 27.0 2007 (210)
Hypertension Yes No Females aged 20?44
years in NHANES
Non-Hispanic White 5.5 94.5 2003?2006 (211)
Non-Hispanic Black 15.3 84.7
Overweight/obesity Obese Overweight Healthy Females aged 
20
years in NHANES
Non-Hispanic White 32.2 27.2 38.2 2003?2006 (211)
Non-Hispanic Black 53.2 26.5 19.2
Social Factors
Marital status Not married Married National Vital Statistics,
2006 (CDC) (4)
Non-Hispanic White 26.6 73.4
Non-Hispanic Black 70.7 29.3
Educational attainment No high Some high High school Some college College National Vital Statistics,
school school 2006 (CDC) (4)
Non-Hispanic White 1.5 10.0 26.4 26.8 35.3
Non-Hispanic Black 2.2 21.5 36.4 26.9 13.0
Income-to-poverty ratio <50% 50%?<75% 75%?<100% 100%?<125% 125%?<150% 150%?<175% 
175% Females aged 20?44
years in the Current
Non-Hispanic White 5 3 3 3 4 4 78.7 Population Survey
Non-Hispanic Black 12.8 7.2 6.0 6.1 5.1 5.2 57.5 2007 (210)
Abbreviations: CDC, Centers for Disease Control and Prevention; NHANES, National Health and Nutrition Examination Survey; PM2.5,
particulate matter <2.5 lm in aerodynamic diameter.
a One foot ? 0.3 m.
Non-Hispanic black women aged 20 years or older are also posures are likely embedded within a setting in which both
more likely to be overweight/obese (53.2%/26.5% vs. 32.2%/ social and host factors are less likely to serve as mitigating
27.2% for non-Hispanic white women) (211). In the social- forces. So, the resiliency to environmental exposures that
factors category, non-Hispanic black women giving birth are can be created by positive social and host factors is more
more likely to be unmarried (70.7% vs. 26.6% for non- likely to be absent for non-Hispanic blacks compared with
Hispanic white women) and are more likely to have less than non-Hispanic whites.
a high school education (23.7% vs. 11.5% for non-Hispanic Despite extensive public policy efforts to maximize ac-
white women) (31). Although data on pregnant women spe- cess to prenatal care, significant racial disparities in preg-
cifically are not available, non-Hispanic black women gener- nancy outcomes persist. The systematic and consistent
ally are more likely to have a low income-to-poverty ratio disproportionate exposure of non-Hispanic blacks to both
(12.8% at <50% of the poverty line vs. 5.0% for non- environmental and social stressors, especially within the
Hispanic white women) (210). context of greater presentation of overweight/obesity and
Table 2 demonstrates that, for the multiple factors that comorbidities on the host-factor side, may account for the
affect pregnancy outcomes, non-Hispanic blacks cluster on persistent race-based disparities. We argue that research that
the high-risk end of the spectrum. This finding is consistent carefully examines the joint effects of social and environmen-
with Geronimus?s notion of cumulative stress (23) as de- tal stressors?conducted at the individual level so that we
scribed in the weathering hypothesis, where cumulative truly know who is experiencing multiple stressors?holds
stress is now defined to include physical environmental ex- potential for revealing the complex etiology that likely drives
posures. In terms of the rubric presented in Figure 1, envi- disparities in pregnancy outcomes. Such understanding is
ronmental exposures/stressors are compressing the ??space?? critical to the development of successful intervention
available for maternal-child pairs to prosper?and these ex- programs aimed at narrowing the health disparities in
Epidemiol Rev 2009;31:67?83
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78 Miranda et al.
pregnancy outcomes, which will need to jointly address the 15. Resnick MB, Gueorguieva RV, Carter RL, et al. The impact
multiple components shaping the lives of women during the of low birth weight, perinatal conditions, and sociodemo-
preconception, prenatal, and postnatal periods. graphic factors on educational outcome in kindergarten
[electronic article]. Pediatrics. 1999;104(6):e74.
16. Ross G, Lipper EG, Auld PA. Social competence and be-
havior problems in premature children at school age. Pedi-
ACKNOWLEDGMENTS atrics. 1990;86(3):391?397.
17. Avchen RN, Scott KG, Mason CA. Birth weight and school-
Authors affiliation: Nicholas School of the Environment, age disabilities: a population-based study. Am J Epidemiol.
Duke University, Durham, North Carolina. 2001;154(10):895?901.
This research was supported by funding from the US 18. Osmond C, Barker DJ, Winter PD, et al. Early growth and
death from cardiovascular disease in women. BMJ. 1993;
Environmental Protection Agency (RD-83329301-0).
307(6918):1519?1524.
Conflict of interest: none declared. 19. Barker DJ, Martyn CN, Osmond C, et al. Growth in utero and
serum cholesterol concentrations in adult life [comment].
BMJ. 1993;307(6918):1524?1527.
20. Weiss JL, Malone FD, Emig D, et al. Obesity, obstetric
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