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Racial Disparities in Preterm Birth
Racial Disparities in Preterm Birth Jennifer F. Culhane, PhD, MPH,* and Robert L. Goldenberg, MD† In the United States, there is a pronounced and persistent race/ethnic disparity in the rate of preterm birth. Even after decades of basic science research and public health initiatives this disparity remains relatively unchanged. Factors that underpin this disparity are elusive and likely, at least in part, derived from complex mechanisms originating from social inequities. In this article several promising areas of research are explored. Specifically, social context or neighborhood-level exposures, maternal nativity, infection/inflammation, and preconception health differentials are discussed in the context of increasing risk of preterm birth among race/ethnic minorities. Semin Perinatol 35:234-239 © 2011 Elsevier Inc. All rights reserved. KEYWORDS preterm birth, racial disparity, racism, preconception, nativity
P
reterm birth (PTB) is associated with more than 75% of all perinatal mortality and at least 50% of perinatal and long-term morbidity.1 Data from 2006 indicate that the infant mortality rate per 1000 live births was 6.68 and the preterm-related infant mortality rate was 2.42.2 PTB has been called the leading obstetrical problem in the United States today.1 In addition to the high rate of PTB in the United States, the United States also suffers from a persistent PTB rate disparity across race/ethnic subgroups. Of particular concern is the disparity between non-Hispanic white and non-Hispanic blacks. For example, in 2007 the overall, non-Hispanic white and non-Hispanic black PTB rates were 12.7, 11.5, and 18.3 per 1000 births, respectively.3 The preterm-related infant mortality rate also varies substantially by maternal race/ethnicity with the non-Hispanic white rate at 1.79 and that for non-Hispanic black women at 6.01.2 The PTB rate disparity has been highlighted in the major publication addressing overall public health goals for the United States, Healthy People 2000, and Health People 2010 and perinatal researchers consistently call for increased attention to this issue. That disparity in the rate of PTB exists is not in question. However, the factors that underpin this disparity and thus the appropriate interventions to reduce this disparity are poorly understood, and discussions in this area often spark
*Department of Pediatrics, Children’s Hospital of Philadelphia, Philadelphia, PA. †Drexel University College of Medicine, Department of Obstetrics and Gynecology, Philadelphia, PA. Address reprint requests to Jennifer F. Culhane, PhD, MPH, Department of Pediatrics, Children’s Hospital of Philadelphia, 3535 Market Street, Ste 880, Philadelphia, PA 19104. E-mail: [email protected]
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controversy pitting biomedical and sociologic approaches. Some insight can be gained by examining how “disparity” is defined. The National Institutes of Health defines disparity as, “differences in the incidence, prevalence, mortality and burden of diseases and other adverse health conditions that exist among specific population subgroups in the US.”4 Recently, researchers from the University of North Carolina (UNC) worked to develop a more comprehensive definition of “disparity.” They write that disparities are, “inequities in disease and well-being that come from discrimination and unequal access to society’s benefits, such as quality education, good jobs, decent and affordable housing, safe neighborhoods and environments, nutritious foods, and adequate healthcare. These inequities result in disproportionately higher rates of death, disease, and disability and have adverse consequences on the physical, mental, spiritual, and social well-being of population groups who, historically and currently, do not experience equivalent social advantage.”5 The NIH definition makes no attempt to elucidate where disparities come from, leaving the reader with the feeling that “disparities” are a fact of life or that they exist without a context. The UNC research team does not permit the notion that disparities just are, but rather their definition encapsulates the concept that disparities arise from somewhere, from discrimination and/or unequal access. During the past several decades the public health and biomedical research communities have acknowledged that disparity in PTB exists, yet little of no reduction has been realized. Embracing the more expanded UNC definition, where root cause is clearly brought to the fore, may fuel novel research generating data that may be used to influence policy and program development in areas not traditionally considered “health”-related (such as housing, education, etc). In
Racial disparities in preterm birth this context, real improvements in disparities may be realized. With attention to the expanded definition, specific promising research areas will be discussed followed by a discussion of the challenges the research community faces in trying to explain and reduce race/ethnic disparities. It is important to note that this article does not attempt to review research activities that show promise in reducing PTB rates overall, but rather focuses specifically on areas of research that might help to reduce the disparity in PTB.
Social Context/ Neighborhood Effects The notion that health is, in part, determined by factors above and beyond individual behavior or use of medical care services is not a new concept, nor is the concern over high infant mortality. In 1925, the Children’s Bureau commissioned a study to explore factors associated with infant mortality. The report concluded, “the fathers of 88% of the babies (infant deaths) included in the Bureau’s studies earned less than $1250 a year . . . As the (family) income doubled the mortality rate was more than halved. Which is the more safe and sane conclusion? That 88% of all these fathers were incorrigibly indolent or below normal mentally, or that sound public economy demands irreducible minimum living standards . . . .”6 This comment suggests that the researchers did not attribute all the risk for infant mortality to individual attributes but rather to the living conditions associated with low income. Interestingly, the concept that social conditions figure prominently in shaping health virtually disappeared by 1950 when public health became dominated by a single-minded focus on individualism, conceptual, methodological, and political. As a result, health status was considered a direct reflection of health behaviors and use of medical care services. Public health interventions have largely focused on identifying people at risk (eg, undereducated, smokers, substance abusers, sedentary, overweight) and providing educational interventions aimed at altering the behavioral culprit. With regard to the racial/ethnic disparity in PTB, the emphasis on individual risk factors has not proven fruitful. The discussions below on race-specific associations between education, prenatal care use and smoking with risk of PTB will demonstrate that single-minded foci on these risk factors will not eliminate the race/ethnic disparity in PTB. An education gradient exists within each race/ethnic group such that women with more education demonstrate a lower rate of PTB. However, non-Hispanic black women with 13 or more years of education have significantly greater rates of PTB when compared with non-Hispanic white women with ⬍12 years of education. When the infant mortality rate for infants born to two-college educated parents was assessed, non-Hispanic black infants had 2 times the rate of infant mortality compared with non-Hispanic whites and this difference was almost completely attributable to differences in the rate of PTB.7 Education differentials alone cannot explain the race/ethnic disparity in PTB.
235 With regard to prenatal care, very little advantage in PTB rate reduction exists for women entering care in the first trimester compared with those entering care in the third trimester. With this said, non-Hispanic black women entering care in the first trimester have significantly increased rates of PTB compared with non-Hispanic white women entering care in the third trimester. As with education, focusing on getting all women into care within the first trimester of pregnancy will do little to reduce the race/ethnic disparities in PTB. Finally, a health behavior that is consistently associated with increased risk of PTB is smoking. Women who smoke have about 1.5 times the risk of PTB compared with nonsmokers. Interestingly, non-Hispanic black women have significantly lower rates of antenatal smoking compared with non-Hispanic white women. The 3 examples presented provide evidence that addressing individual attributes have not, and likely will not, lead to reductions in the race/ethnic disparity of PTB. In the tradition of public health from the early 1900s, the public health community has recently called for a “new public health” focusing on the upstream social conditions that pattern and condition health status independent of, or in interaction with, individual characteristics.8 As a result, the research community has turned attention to reexamining the role that social context or “neighborhood” has on the production of risk and the race/ethnic disparity. The association between neighborhood disadvantage, race/ethnicity, and risk of adverse reproductive outcomes is complex. As a first step, it is easy to provide evidence that race/ethnic minorities generally have lower socioeconomic position compared with whites9 –11 and reside in neighborhoods with more economic deprivation and social disorder and differential access to health enhancing resources.12-15 Culhane et al16 assessed the neighborhood characteristics for pregnant black and white women in Philadelphia. Although all women enrolled in this study were Medicaid recipients and thus socioeconomically disadvantaged at the individuallevel, the neighborhood characteristics were markedly different by race. Specifically, disadvantaged non-Hispanic white women lived in block groups with significantly lower rates of properties with 20% or more of their market value in tax arrears, lower rates of homelessness and fewer crimes against persons. Others have also shown that black women are more likely than white women to live in economically deprived neighborhoods with fewer medical and social services, poorer housing quality, and higher rates of crime and violence, factors that have been hypothesized to contribute to poor maternal health and adverse birth outcomes.17-20 When the PTB rate of women residing in disadvantaged neighborhoods are compared with those living in more advantaged areas, without regard to maternal race/ethnicity, a consistent pattern of risk emerges. A small set of studies specifically examining the impact of neighborhood-level socioeconomic status on preterm birth rate21-29 found that, even after adjustment for behavioral and individual-level socioeconomic variables, neighborhood-level unemployment rate was significantly associated with an increased risk of
236 preterm delivery. There is substantial evidence that non-Hispanic black women have more exposure to adverse neighborhood conditions compared with their non-Hispanic white counterparts and that adverse neighborhood conditions are associated with increased risk of PTB. The picture becomes more complex when maternal race is also considered. For example, O’Campo, and others evaluated the association between neighborhood-deprivation and risk of PTB for nonHispanic white and non-Hispanic black women in stratified models in 8 metropolitan areas in the United States. Interestingly, neighborhood deprivation was more strongly associated with PTB for non-Hispanic white women compared with non-Hispanic black women.30 Across the 8 metropolitan areas only 2 (odds ratio 1.23 and 1.26) of 8 regions demonstrated significant associations between neighborhood deprivation and risk of PTB in the non-Hispanic black models. For non-Hispanic white women, 7 of the 8 areas had significant odds ratios for neighborhood deprivation with values ranging from 1.48 to 2.24. Because the analytical strategy was to use race-specific models the contribution of neighborhood deprivation to the racial disparity in PTB rates cannot be evaluated. In sum, non-Hispanic black women live in more disadvantaged neighborhoods and neighborhood disadvantage is associated with increased risk of PTB. What is not established is the contribution of this exposure to the racial/ethnic disparity in PTB. Further research in this area seems warranted.
Maternal Nativity The “Hispanic-birth paradox” is a widely acknowledged phenomenon in the United States. The “paradox” is that Mexican immigrants as a group demonstrate elevated risk at the individual –level (limited use of prenatal care, socioeconomic disadvantage, low educational attainment) but have birth outcomes that rival those of non-Hispanic white women.31 Interestingly, additional research in this area suggests that this advantage diminishes over time or as Hispanic women “acculturate” or integrate into the wider U.S. culture.32 Specifically, Mexican women with longer durations of residence in the United States, who were born in this county, who self-identify as American as opposed to Mexican, or who speak English as opposed to Spanish in the home, have birth outcomes that more closely resemble those of non-Hispanic black women.32 Evidently, something about acculturating is deleterious to reproductive health. Although very little work has been done to assess if an “African/Caribbean birth paradox” exists, or if “acculturation” confers a health disadvantage in this group, recent studies do suggest that black immigrants have better birth outcomes compared with US-born black women. Howard et al33 used 5 years of New York City vital record data to categorize all births to black women into 8 groups. Examples of the groups include African black, non-Hispanic American black, Cuban black, and West Indian/Brazilian black. The risk of PTB was compared across all groups with the use of nonHispanic American black as the reference. When maternal ancestry alone was assessed, 4 groups, including African
J.F. Culhane and R.L. Goldenberg black, demonstrated significantly reduced risk of PTB compared with non-Hispanic American black. After the introduction of nativity into the model, African black and South and Central American black women showed significantly reduced rates of PTB compared with non-Hispanic American black women. These data indicate that black women with an identified non-U.S. family ancestry and/or foreign-born maternal nativity have significantly lower risk of PTB compared with American black women. Another recent study examined the health behaviors, perceived health status, sociodemographic and psychosocial characteristics of pregnant foreign born and U.S.-born black women in Philadelphia.34 This investigation concluded that foreign-born black women were significantly less likely to engage in adverse health behaviors and rated their physical and mental health better than U.S.-born black women. These differences remained after adjustment of socioeconomic and psychosocial attributes. Why these differences exist was not explained. In addition, whether these behavioral and psychosocial characteristics were associated with differential birth outcomes was not reported. Importantly, the health behavioral differentials and differences in self-rated health were not explained by adjustment for traditional measures of socioeconomic status. Why foreign-born black women have lower rates of PTB than U.S.-born black women remains a mystery. One theory posits that selective migration underpins this observation. Simply stated, immigrant women may potentially represent a select group on both observed (health behaviors, etc) and unobserved (organization, motivation) characteristics and thus may have different patterns of health risk. The extent to which selectivity accounts for the protective effect of foreignborn status needs further study. It is also possible that foreign-born black women do not experience or perceive discrimination and social marginalization in the same way as their native born counterparts. For example, what exactly does it mean to be categorized as “nonHispanic American black?” A very significant proportion of these women are likely descendents of generations raised in slavery or subjected to virtual serfdom. Is the U.S.-born disadvantage a legacy of the historical exposure to extreme discrimination and the ongoing effect of marginalization with the associated limitations in access to opportunities? Research to assess why foreign-born black women have better birth outcomes compared with their U.S.-born counterparts may also shed light on factors that underpin the black/white disparity in PTB observed in this country.
Other Potential Explanations Although we have focused primarily on social explanations for disparities in PTB, some evidence suggests that other factors, such as variation in some of the genes controlling aspects of the inflammatory pathway, may also play a role. So too might differences in diet and body size found between various racial/ethnic groups. For example, it is clear that thinner women, defined as those with lower body mass indices, have lower rates of spontaneous PTB, whereas those women
Racial disparities in preterm birth with greater body mass indices tend to have more indicated PTB, often because of higher incidents of hypertension and diabetes.35 Differences in diet and body size between race/ ethnic groups and how these differences might contribute to PTB differentials needs further study. The biomedical exposure most studied with respect to the disparity in PTB between black and white women is infection. Also, although a detailed presentation of genetic, nutritional and infection related contribution to disparities in PTB is beyond the scope of this work, some more detailed attention to the role of infections is in order.
Infection/Inflammation Infection has long been considered a major contributor to PTB with the proportion of PTBs attributable to infection increasing as gestational age decreases.36 What is also clear is that non-Hispanic back women have much higher rates of urogenital tract infections compared with their non-Hispanic white counterparts. For example, data from the Vaginal Infections in Pregnancy Study showed the prevalence of 6 urogenital infections in black women were substantially greater than in any other racial group, and each of these infections has been associated with PTB.37 Bacterial vaginosis (BV) has been associated with PTB in nearly all studies evaluating this relationship with BV⫹ women demonstrating about a 2-fold increase in PTB compared with BV negative women. In virtually every study conducted in the United States, black women have a 2– to 4-fold increase in the prevalence of BV compared with their white counterparts. Not only do nonHispanic black women have significantly greater rates of BV, data do exist indicating that differences in bacterial morphotypes associated with BV positivity vary by race/ethnic group.38 Culhane and Cauci have shown that among BV⫹ women (Nugent score 7-10) non-Hispanic black women have significantly higher rates of mobilluncus compared with white women.38 Researchers have also shown that high perceived stress is associated with an increased likelihood of BV.39,40 The association between stress and BV may shed light on why black women have such elevated rates of BV. Mechanistically, BV may lead to PTB through ascending infection of BV-related organisms into the fetal membranes, often manifesting as histologic chorioamnionitis.41 black women have significantly more histologic chorioamnionitis than do white women. It is beyond the scope of this article to review the vast literature detailing the race/ethnic distribution of urogenital tract infections, the mechanisms through which infection can lead to PTB, and the results of intervention trials treating infection in pregnancy. However, it is estimated that as much as 50% of the disparity in PTB rates between black and white women may be explained by differences in urogenital infections between the 2 groups.42 Interestingly, in several studies that have examined this issue, factors, such as age at first intercourse and number of sexual partners have not explained the difference in the rate of urogenital infections between black and white women. Why non-Hispanic black women have elevated rates of BV and if the organisms asso-
237 ciated with BV differ by race/ethnic group deserves further research attention. Possibly, women with a certain constellation of bacteria comprising their BV are more at risk for PTB than those with a different set of organisms. Additionally, “type” of BV may systematically vary by race/ethnicity.
Preconception Maternal Health Virtually all interventions aimed at reducing PTB, including those that target infection/inflammation, have been conducted during pregnancy. These include interventions to improve access to high-quality prenatal care, bed rest, nutrition counseling, caloric or vitamin/mineral supplementation, smoking, drug- or alcohol-cessation programs, and treatment for pelvic infections. The initiation of the interventions during pregnancy may explain why most of the interventions have failed to reduce PTB possibly because the underlying pathophysiology, such as inflammation/infection may have already been initiated and thus it was too late to interrupt the processes. Furthermore, it may take weeks or months after the behavioral risk factor is modified to see consequent improvements in pathophysiologic conditions leading to the PTB. The strategy of intervening to lower risk for subsequent disease has been demonstrated in relation to cardiovascular disease, in which predisease markers have been targeted with some success. For these reasons altering the timing of interventions to either before the first pregnancy or between pregnancies may prove more successful. As an example, periodontal disease is a risk factor for PTB more common in black women. The trials aimed at treating periodontal disease during pregnancy have generally failed to reduce PTB.43 It is hypothesized that the treatment during pregnancy may be too late to reduce the inflammatory pathway leading to PTB already initiated and/or the treatment itself enhances the inflammatory state. Treatment of periodontal disease before pregnancy appears to be a more logical approach in women with this risk factor. Thus, optimizing women’s health before gestation to reduce rates of preterm birth holds promise for reducing disparity. We know that non-Hispanic black women of childbearing age have significantly worse health profiles compared with their non-Hispanic white counterparts. For example, black women have greater rates of obesity, greater rates of type II diabetes, greater rates of high blood pressure, consume a greater fat diet, and as mentioned previously, have elevated rates of urogenital tract infections and periodontal disease.44 Although “treating” these adverse health conditions before pregnancy may help “even the reproductive playing field,” losing site of what places minority women at risk of risk in the first place45 would seem irresponsible. In other words, reducing the approach to race/ethnic disparities in PTB to targeting only biomedical risk factors— even if done so before pregnancy—would likely be an incomplete and less effective response. Ideally, interventions addressing issues more akin to social inequalities should not be pitted against those targeting biomedical risk factors. However, historically, our emphasis has been heavily weighted to biomed-
238 ical approaches. The lack of improvement in health disparities in general and in PTB specifically using this approach indicates that the time to elevate social justice approaches to the fore has come.
Summary and Challenges In the United States, there is a pronounced and persistent race/ethnic disparity in the rate of PTB. After decades of public health initiatives aimed at identifying and ameliorating individual-level risk factors (behavioral, biomedical) associated with increased risk of PTB very little reduction in the disparity, or for that matter the overall PTB rate, in the United States has been realized. Recently, there seems to be increasing interest in the social factors that may contribute to this disparity. Even against the backdrop of increasing interest in social factors, researchers and public health practitioners face significant challenges. First, our knowledge base regarding what social exposures or experiences lead to increased risk is limited largely because of limited grant funding in this area. Studies aimed at unraveling the complex social conditions leading to increased risk and the mechanisms through which these exposures operate will likely call for research methodology not traditionally funded by mainstream agencies. The role of social exposures, such as income inequality or discrimination, cannot be merely an afterthought or an add-on to clinic research. If reducing disparity is really a primary objective, innovative, nontraditional research will need to be cultivated and the knowledge base in this area developed. In addition, if necessary, within the context of limited funding, it is possible that novel approaches will need to be prioritized over research initiatives aimed at more traditional, individual-based risk. It is also very important to keep in mind that reducing the overall rate of condition is not the same thing as reducing the disparity. In fact, interventions that may reduce overall prevalence may not reduce disparity in the same condition. Finally, it is likely that interventions within the social realm will take years to implement and even longer to evaluate. It took a long time to establish the race/ethnic disparity in the United States and it seems unrealistic that real improvements will be realized with the traditional 3- to 5-year funding cycles.
References 1. Goldenberg RL, Culhane JF, Iams JD, et al: Epidemiology and causes of preterm birth. Lancet 371:75-84, 2008 2. MacDorman MF: Disparities in perinatal medicine: Focus on infant mortality, stillbirth and preterm birth. Data Sources NCHS Linked Infant Birth/Infant Death Data Set. Paper presented at the Eunice Kennedy Shriver NICHD workshop, August 5, 2011 3. NCHS data brief no. 39. Available at: http://www.cdc.gov/nchs/data/ databriefs/db39.pdf. Accessed March 18, 2011 4. Olivia C-P, Baquet C: What is a health disparity? Public Health Rep 117:426-434, 2002 5. Satia J, Hogan V, the Health Disparities Strategic Planning Work Group: Health disparities strategic plan. Paper presented at the University of North Carolina at Chapel Hill, Gillings School of Global Public Health, December 2007 6. Yankauer A: A classic study of infant mortality 1911-1915. Pediatrics 94:874-877, 1994
J.F. Culhane and R.L. Goldenberg 7. Schoendorf KC, Hogue CJ, Kleinman JC, et al: Mortality among infants of black as compared with white college-educated parents. N Engl J Med 326:1522-1526, 1992 8. Krieger N: Epidemiology and the web of causation: Has anyone seen the spider? Soc Sci Med 39:887-903, 1994 9. Oliver M, Shapiro T, Wealth B, et al: A New Perspective on Racial Inequality New York, Routledge, 1997 10. Mishel L, Bernstein J, Allegrotto S: State of Working America 2004/05 Ithaca, Cornell University Press, 2005 11. Conley D, Black B: Living in the Red. Berkeley, University of California Press, 1999 12. Krieger N, Chen JT, Waterman PD, et al: Painting a truer picture of US socioeconomic and racial/ethnic health inequalities: The Public Health Disparities Geocoding Project. Am J Public Health 95:312323, 2005 13. Subramanian SV, Chen JT, Rehkopf DH, et al: Racial disparities in context: A multilevel analysis of neighborhood variations in poverty and excess mortality among black populations in Massachusetts. Am J Public Health 95:260-265, 2005 14. Massey D, Denton N: American Apartheid. Cambridge, Harvard University Press, 1993 15. Zenk S, Schulz AJ, Israel BA, et al: Fruit and vegetable access differs by community racial composition and socieconomic position in Detroit, Michigan. Ethn Dis 16:275-280, 2006 16. Culhane JF, Rauh VA, Elo IT, et al: Exposure to chronic stress and ethnic differences in rates of bacterial vaginosis among pregnant women. Am J Obstet Gynecol 187:1272-1276, 2002 17. LeClere FB, Rogers RG, Peters KD: Neighborhood social context and racial differences in women’s heart disease mortality. J Health Soc Behav 39:91-107, 1998 18. Robert SA: Community-level socioeconomic status effects on adult health. J Health Soc Behav 39:18-37, 1998 19. Morenoff JD: Neighborhood mechanisms and the spatial dynamics of birth weight. Am J Sociol 108:976-1017, 2003 20. Messer LC, Kaufman JS, Dole N, et al: Neighborhood crime, deprivation, and preterm birth. Ann Epidemiol 16:455-462, 2006 21. Zhong-Cheng L, Wilkins R, Kramer MS: Effect of neighborhood income and maternal education on birth outcomes: A population-based study. CMAJ 10:1415-1420, 2006 22. Pickett KE, Collins JW Jr, Masi CM, et al: The effects of racial density and income incongruity on pregnancy outcomes. Soc Sci Med 60: 2229-2238, 2005 23. Luo ZC, Kierans WJ, Wilkins R, et al: Disparities in birth outcomes by neighborhood income: Temporal trends in rural and urban areas, British Columbia. Epidemiology 15:679-686, 2004 24. Kaufman JS, Dole N, Savitz DA, et al: Modeling community-level effects on preterm birth. Ann Epidemiol 13:377-384, 2003 25. Ahern J, Pickett KE, Selvin S, et al: Preterm birth among African American and white women: A multilevel analysis of socioeconomic characteristics and cigarette smoking. J Epidemiol Community Health 57: 606-611, 2003 26. Pickett KE, Ahern JE, Selvin S, et al: Neighborhood socioeconomic status, maternal race and preterm delivery: A case-control study. Ann Epidemiol 12:410-418, 2002 27. Farley TA, Mason K, Rice J, et al: The relationship between the neighbourhood environment and adverse birth outcomes. Paediatr Perinat Epidemiol 20:188-200, 2006 28. Messer L, Laraia BA, Kaufman JS, et al: The development of a standardized neighborhood deprivation index. J Urban Health 83:1041-1062, 2006 29. Ponce NA, Hoggatt KJ, Wilhelm M, et al: Preterm birth: The interaction of traffic-related air pollution with economic hardship in Los Angeles neighborhoods. Am J Epidemiol 162:140-148, 2005 30. O’Campo P, Burke JG, Culhane JF, et al: Neighborhood deprivation and preterm birth among non-Hispanic black and white women in eight geographic areas in the United States. Am J Epidemiol 167:155163, 2008 31. Hummer RA, Biegler M, Deturk PB: Race ethnicity, nativity, and infant mortality in the United States. Soc Forces 77:1083-1118, 1999
Racial disparities in preterm birth 32. Franzini L, Ribble JC, Keddie AM: Understanding the Hispanic paradox. Ethn Dis 11:496-518, 2001 33. Howard DL, Marshall SS, Kaufman JS, et al: Variation in low birth weight and preterm delivery among Blacks in relation to ancestry and nativity: New York City 1998-2002. Pediatrics 11:e1399-e1405, 2006 34. Elo IT, Culhane JF: Variation in health behaviors by nativity among pregnant Black women in Philadelphia, American. J Public Health 100: 2185-2192, 2010 35. Baron CM, Girling LG, Mathieson AL, et al: Obstetrical and neonatal outcomes in obese parturients J Matern Fetal Neonatal Med 23:906913, 2010 36. Mueller-Heubach E, Rubinstein DN, Schwarz SS: Histologic chorioamnionitis and preterm delivery in different patient populations Obstet Gynecol 75:622-626, 1990 37. Goldenberg RL, Klebanoff MA, Nugent R, et al: Bacterial colonization of the vagina during pregnancy in four ethnic groups. Vaginal Infections and Prematurity Study Group Am J Obstet Gynecol 174:1618-1621, 1996 38. Culhane JF, Nyirjesy P, McCollum K, et al: Variation in vaginal immune parameters and microbial hydrolytic enzymes in bacterial vaginosis
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P
reterm birth (PTB) is associated with more than 75% of all perinatal mortality and at least 50% of perinatal and long-term morbidity.1 Data from 2006 indicate that the infant mortality rate per 1000 live births was 6.68 and the preterm-related infant mortality rate was 2.42.2 PTB has been called the leading obstetrical problem in the United States today.1 In addition to the high rate of PTB in the United States, the United States also suffers from a persistent PTB rate disparity across race/ethnic subgroups. Of particular concern is the disparity between non-Hispanic white and non-Hispanic blacks. For example, in 2007 the overall, non-Hispanic white and non-Hispanic black PTB rates were 12.7, 11.5, and 18.3 per 1000 births, respectively.3 The preterm-related infant mortality rate also varies substantially by maternal race/ethnicity with the non-Hispanic white rate at 1.79 and that for non-Hispanic black women at 6.01.2 The PTB rate disparity has been highlighted in the major publication addressing overall public health goals for the United States, Healthy People 2000, and Health People 2010 and perinatal researchers consistently call for increased attention to this issue. That disparity in the rate of PTB exists is not in question. However, the factors that underpin this disparity and thus the appropriate interventions to reduce this disparity are poorly understood, and discussions in this area often spark
*Department of Pediatrics, Children’s Hospital of Philadelphia, Philadelphia, PA. †Drexel University College of Medicine, Department of Obstetrics and Gynecology, Philadelphia, PA. Address reprint requests to Jennifer F. Culhane, PhD, MPH, Department of Pediatrics, Children’s Hospital of Philadelphia, 3535 Market Street, Ste 880, Philadelphia, PA 19104. E-mail: [email protected]
234
0146-0005/11/$-see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1053/j.semperi.2011.02.020
controversy pitting biomedical and sociologic approaches. Some insight can be gained by examining how “disparity” is defined. The National Institutes of Health defines disparity as, “differences in the incidence, prevalence, mortality and burden of diseases and other adverse health conditions that exist among specific population subgroups in the US.”4 Recently, researchers from the University of North Carolina (UNC) worked to develop a more comprehensive definition of “disparity.” They write that disparities are, “inequities in disease and well-being that come from discrimination and unequal access to society’s benefits, such as quality education, good jobs, decent and affordable housing, safe neighborhoods and environments, nutritious foods, and adequate healthcare. These inequities result in disproportionately higher rates of death, disease, and disability and have adverse consequences on the physical, mental, spiritual, and social well-being of population groups who, historically and currently, do not experience equivalent social advantage.”5 The NIH definition makes no attempt to elucidate where disparities come from, leaving the reader with the feeling that “disparities” are a fact of life or that they exist without a context. The UNC research team does not permit the notion that disparities just are, but rather their definition encapsulates the concept that disparities arise from somewhere, from discrimination and/or unequal access. During the past several decades the public health and biomedical research communities have acknowledged that disparity in PTB exists, yet little of no reduction has been realized. Embracing the more expanded UNC definition, where root cause is clearly brought to the fore, may fuel novel research generating data that may be used to influence policy and program development in areas not traditionally considered “health”-related (such as housing, education, etc). In
Racial disparities in preterm birth this context, real improvements in disparities may be realized. With attention to the expanded definition, specific promising research areas will be discussed followed by a discussion of the challenges the research community faces in trying to explain and reduce race/ethnic disparities. It is important to note that this article does not attempt to review research activities that show promise in reducing PTB rates overall, but rather focuses specifically on areas of research that might help to reduce the disparity in PTB.
Social Context/ Neighborhood Effects The notion that health is, in part, determined by factors above and beyond individual behavior or use of medical care services is not a new concept, nor is the concern over high infant mortality. In 1925, the Children’s Bureau commissioned a study to explore factors associated with infant mortality. The report concluded, “the fathers of 88% of the babies (infant deaths) included in the Bureau’s studies earned less than $1250 a year . . . As the (family) income doubled the mortality rate was more than halved. Which is the more safe and sane conclusion? That 88% of all these fathers were incorrigibly indolent or below normal mentally, or that sound public economy demands irreducible minimum living standards . . . .”6 This comment suggests that the researchers did not attribute all the risk for infant mortality to individual attributes but rather to the living conditions associated with low income. Interestingly, the concept that social conditions figure prominently in shaping health virtually disappeared by 1950 when public health became dominated by a single-minded focus on individualism, conceptual, methodological, and political. As a result, health status was considered a direct reflection of health behaviors and use of medical care services. Public health interventions have largely focused on identifying people at risk (eg, undereducated, smokers, substance abusers, sedentary, overweight) and providing educational interventions aimed at altering the behavioral culprit. With regard to the racial/ethnic disparity in PTB, the emphasis on individual risk factors has not proven fruitful. The discussions below on race-specific associations between education, prenatal care use and smoking with risk of PTB will demonstrate that single-minded foci on these risk factors will not eliminate the race/ethnic disparity in PTB. An education gradient exists within each race/ethnic group such that women with more education demonstrate a lower rate of PTB. However, non-Hispanic black women with 13 or more years of education have significantly greater rates of PTB when compared with non-Hispanic white women with ⬍12 years of education. When the infant mortality rate for infants born to two-college educated parents was assessed, non-Hispanic black infants had 2 times the rate of infant mortality compared with non-Hispanic whites and this difference was almost completely attributable to differences in the rate of PTB.7 Education differentials alone cannot explain the race/ethnic disparity in PTB.
235 With regard to prenatal care, very little advantage in PTB rate reduction exists for women entering care in the first trimester compared with those entering care in the third trimester. With this said, non-Hispanic black women entering care in the first trimester have significantly increased rates of PTB compared with non-Hispanic white women entering care in the third trimester. As with education, focusing on getting all women into care within the first trimester of pregnancy will do little to reduce the race/ethnic disparities in PTB. Finally, a health behavior that is consistently associated with increased risk of PTB is smoking. Women who smoke have about 1.5 times the risk of PTB compared with nonsmokers. Interestingly, non-Hispanic black women have significantly lower rates of antenatal smoking compared with non-Hispanic white women. The 3 examples presented provide evidence that addressing individual attributes have not, and likely will not, lead to reductions in the race/ethnic disparity of PTB. In the tradition of public health from the early 1900s, the public health community has recently called for a “new public health” focusing on the upstream social conditions that pattern and condition health status independent of, or in interaction with, individual characteristics.8 As a result, the research community has turned attention to reexamining the role that social context or “neighborhood” has on the production of risk and the race/ethnic disparity. The association between neighborhood disadvantage, race/ethnicity, and risk of adverse reproductive outcomes is complex. As a first step, it is easy to provide evidence that race/ethnic minorities generally have lower socioeconomic position compared with whites9 –11 and reside in neighborhoods with more economic deprivation and social disorder and differential access to health enhancing resources.12-15 Culhane et al16 assessed the neighborhood characteristics for pregnant black and white women in Philadelphia. Although all women enrolled in this study were Medicaid recipients and thus socioeconomically disadvantaged at the individuallevel, the neighborhood characteristics were markedly different by race. Specifically, disadvantaged non-Hispanic white women lived in block groups with significantly lower rates of properties with 20% or more of their market value in tax arrears, lower rates of homelessness and fewer crimes against persons. Others have also shown that black women are more likely than white women to live in economically deprived neighborhoods with fewer medical and social services, poorer housing quality, and higher rates of crime and violence, factors that have been hypothesized to contribute to poor maternal health and adverse birth outcomes.17-20 When the PTB rate of women residing in disadvantaged neighborhoods are compared with those living in more advantaged areas, without regard to maternal race/ethnicity, a consistent pattern of risk emerges. A small set of studies specifically examining the impact of neighborhood-level socioeconomic status on preterm birth rate21-29 found that, even after adjustment for behavioral and individual-level socioeconomic variables, neighborhood-level unemployment rate was significantly associated with an increased risk of
236 preterm delivery. There is substantial evidence that non-Hispanic black women have more exposure to adverse neighborhood conditions compared with their non-Hispanic white counterparts and that adverse neighborhood conditions are associated with increased risk of PTB. The picture becomes more complex when maternal race is also considered. For example, O’Campo, and others evaluated the association between neighborhood-deprivation and risk of PTB for nonHispanic white and non-Hispanic black women in stratified models in 8 metropolitan areas in the United States. Interestingly, neighborhood deprivation was more strongly associated with PTB for non-Hispanic white women compared with non-Hispanic black women.30 Across the 8 metropolitan areas only 2 (odds ratio 1.23 and 1.26) of 8 regions demonstrated significant associations between neighborhood deprivation and risk of PTB in the non-Hispanic black models. For non-Hispanic white women, 7 of the 8 areas had significant odds ratios for neighborhood deprivation with values ranging from 1.48 to 2.24. Because the analytical strategy was to use race-specific models the contribution of neighborhood deprivation to the racial disparity in PTB rates cannot be evaluated. In sum, non-Hispanic black women live in more disadvantaged neighborhoods and neighborhood disadvantage is associated with increased risk of PTB. What is not established is the contribution of this exposure to the racial/ethnic disparity in PTB. Further research in this area seems warranted.
Maternal Nativity The “Hispanic-birth paradox” is a widely acknowledged phenomenon in the United States. The “paradox” is that Mexican immigrants as a group demonstrate elevated risk at the individual –level (limited use of prenatal care, socioeconomic disadvantage, low educational attainment) but have birth outcomes that rival those of non-Hispanic white women.31 Interestingly, additional research in this area suggests that this advantage diminishes over time or as Hispanic women “acculturate” or integrate into the wider U.S. culture.32 Specifically, Mexican women with longer durations of residence in the United States, who were born in this county, who self-identify as American as opposed to Mexican, or who speak English as opposed to Spanish in the home, have birth outcomes that more closely resemble those of non-Hispanic black women.32 Evidently, something about acculturating is deleterious to reproductive health. Although very little work has been done to assess if an “African/Caribbean birth paradox” exists, or if “acculturation” confers a health disadvantage in this group, recent studies do suggest that black immigrants have better birth outcomes compared with US-born black women. Howard et al33 used 5 years of New York City vital record data to categorize all births to black women into 8 groups. Examples of the groups include African black, non-Hispanic American black, Cuban black, and West Indian/Brazilian black. The risk of PTB was compared across all groups with the use of nonHispanic American black as the reference. When maternal ancestry alone was assessed, 4 groups, including African
J.F. Culhane and R.L. Goldenberg black, demonstrated significantly reduced risk of PTB compared with non-Hispanic American black. After the introduction of nativity into the model, African black and South and Central American black women showed significantly reduced rates of PTB compared with non-Hispanic American black women. These data indicate that black women with an identified non-U.S. family ancestry and/or foreign-born maternal nativity have significantly lower risk of PTB compared with American black women. Another recent study examined the health behaviors, perceived health status, sociodemographic and psychosocial characteristics of pregnant foreign born and U.S.-born black women in Philadelphia.34 This investigation concluded that foreign-born black women were significantly less likely to engage in adverse health behaviors and rated their physical and mental health better than U.S.-born black women. These differences remained after adjustment of socioeconomic and psychosocial attributes. Why these differences exist was not explained. In addition, whether these behavioral and psychosocial characteristics were associated with differential birth outcomes was not reported. Importantly, the health behavioral differentials and differences in self-rated health were not explained by adjustment for traditional measures of socioeconomic status. Why foreign-born black women have lower rates of PTB than U.S.-born black women remains a mystery. One theory posits that selective migration underpins this observation. Simply stated, immigrant women may potentially represent a select group on both observed (health behaviors, etc) and unobserved (organization, motivation) characteristics and thus may have different patterns of health risk. The extent to which selectivity accounts for the protective effect of foreignborn status needs further study. It is also possible that foreign-born black women do not experience or perceive discrimination and social marginalization in the same way as their native born counterparts. For example, what exactly does it mean to be categorized as “nonHispanic American black?” A very significant proportion of these women are likely descendents of generations raised in slavery or subjected to virtual serfdom. Is the U.S.-born disadvantage a legacy of the historical exposure to extreme discrimination and the ongoing effect of marginalization with the associated limitations in access to opportunities? Research to assess why foreign-born black women have better birth outcomes compared with their U.S.-born counterparts may also shed light on factors that underpin the black/white disparity in PTB observed in this country.
Other Potential Explanations Although we have focused primarily on social explanations for disparities in PTB, some evidence suggests that other factors, such as variation in some of the genes controlling aspects of the inflammatory pathway, may also play a role. So too might differences in diet and body size found between various racial/ethnic groups. For example, it is clear that thinner women, defined as those with lower body mass indices, have lower rates of spontaneous PTB, whereas those women
Racial disparities in preterm birth with greater body mass indices tend to have more indicated PTB, often because of higher incidents of hypertension and diabetes.35 Differences in diet and body size between race/ ethnic groups and how these differences might contribute to PTB differentials needs further study. The biomedical exposure most studied with respect to the disparity in PTB between black and white women is infection. Also, although a detailed presentation of genetic, nutritional and infection related contribution to disparities in PTB is beyond the scope of this work, some more detailed attention to the role of infections is in order.
Infection/Inflammation Infection has long been considered a major contributor to PTB with the proportion of PTBs attributable to infection increasing as gestational age decreases.36 What is also clear is that non-Hispanic back women have much higher rates of urogenital tract infections compared with their non-Hispanic white counterparts. For example, data from the Vaginal Infections in Pregnancy Study showed the prevalence of 6 urogenital infections in black women were substantially greater than in any other racial group, and each of these infections has been associated with PTB.37 Bacterial vaginosis (BV) has been associated with PTB in nearly all studies evaluating this relationship with BV⫹ women demonstrating about a 2-fold increase in PTB compared with BV negative women. In virtually every study conducted in the United States, black women have a 2– to 4-fold increase in the prevalence of BV compared with their white counterparts. Not only do nonHispanic black women have significantly greater rates of BV, data do exist indicating that differences in bacterial morphotypes associated with BV positivity vary by race/ethnic group.38 Culhane and Cauci have shown that among BV⫹ women (Nugent score 7-10) non-Hispanic black women have significantly higher rates of mobilluncus compared with white women.38 Researchers have also shown that high perceived stress is associated with an increased likelihood of BV.39,40 The association between stress and BV may shed light on why black women have such elevated rates of BV. Mechanistically, BV may lead to PTB through ascending infection of BV-related organisms into the fetal membranes, often manifesting as histologic chorioamnionitis.41 black women have significantly more histologic chorioamnionitis than do white women. It is beyond the scope of this article to review the vast literature detailing the race/ethnic distribution of urogenital tract infections, the mechanisms through which infection can lead to PTB, and the results of intervention trials treating infection in pregnancy. However, it is estimated that as much as 50% of the disparity in PTB rates between black and white women may be explained by differences in urogenital infections between the 2 groups.42 Interestingly, in several studies that have examined this issue, factors, such as age at first intercourse and number of sexual partners have not explained the difference in the rate of urogenital infections between black and white women. Why non-Hispanic black women have elevated rates of BV and if the organisms asso-
237 ciated with BV differ by race/ethnic group deserves further research attention. Possibly, women with a certain constellation of bacteria comprising their BV are more at risk for PTB than those with a different set of organisms. Additionally, “type” of BV may systematically vary by race/ethnicity.
Preconception Maternal Health Virtually all interventions aimed at reducing PTB, including those that target infection/inflammation, have been conducted during pregnancy. These include interventions to improve access to high-quality prenatal care, bed rest, nutrition counseling, caloric or vitamin/mineral supplementation, smoking, drug- or alcohol-cessation programs, and treatment for pelvic infections. The initiation of the interventions during pregnancy may explain why most of the interventions have failed to reduce PTB possibly because the underlying pathophysiology, such as inflammation/infection may have already been initiated and thus it was too late to interrupt the processes. Furthermore, it may take weeks or months after the behavioral risk factor is modified to see consequent improvements in pathophysiologic conditions leading to the PTB. The strategy of intervening to lower risk for subsequent disease has been demonstrated in relation to cardiovascular disease, in which predisease markers have been targeted with some success. For these reasons altering the timing of interventions to either before the first pregnancy or between pregnancies may prove more successful. As an example, periodontal disease is a risk factor for PTB more common in black women. The trials aimed at treating periodontal disease during pregnancy have generally failed to reduce PTB.43 It is hypothesized that the treatment during pregnancy may be too late to reduce the inflammatory pathway leading to PTB already initiated and/or the treatment itself enhances the inflammatory state. Treatment of periodontal disease before pregnancy appears to be a more logical approach in women with this risk factor. Thus, optimizing women’s health before gestation to reduce rates of preterm birth holds promise for reducing disparity. We know that non-Hispanic black women of childbearing age have significantly worse health profiles compared with their non-Hispanic white counterparts. For example, black women have greater rates of obesity, greater rates of type II diabetes, greater rates of high blood pressure, consume a greater fat diet, and as mentioned previously, have elevated rates of urogenital tract infections and periodontal disease.44 Although “treating” these adverse health conditions before pregnancy may help “even the reproductive playing field,” losing site of what places minority women at risk of risk in the first place45 would seem irresponsible. In other words, reducing the approach to race/ethnic disparities in PTB to targeting only biomedical risk factors— even if done so before pregnancy—would likely be an incomplete and less effective response. Ideally, interventions addressing issues more akin to social inequalities should not be pitted against those targeting biomedical risk factors. However, historically, our emphasis has been heavily weighted to biomed-
238 ical approaches. The lack of improvement in health disparities in general and in PTB specifically using this approach indicates that the time to elevate social justice approaches to the fore has come.
Summary and Challenges In the United States, there is a pronounced and persistent race/ethnic disparity in the rate of PTB. After decades of public health initiatives aimed at identifying and ameliorating individual-level risk factors (behavioral, biomedical) associated with increased risk of PTB very little reduction in the disparity, or for that matter the overall PTB rate, in the United States has been realized. Recently, there seems to be increasing interest in the social factors that may contribute to this disparity. Even against the backdrop of increasing interest in social factors, researchers and public health practitioners face significant challenges. First, our knowledge base regarding what social exposures or experiences lead to increased risk is limited largely because of limited grant funding in this area. Studies aimed at unraveling the complex social conditions leading to increased risk and the mechanisms through which these exposures operate will likely call for research methodology not traditionally funded by mainstream agencies. The role of social exposures, such as income inequality or discrimination, cannot be merely an afterthought or an add-on to clinic research. If reducing disparity is really a primary objective, innovative, nontraditional research will need to be cultivated and the knowledge base in this area developed. In addition, if necessary, within the context of limited funding, it is possible that novel approaches will need to be prioritized over research initiatives aimed at more traditional, individual-based risk. It is also very important to keep in mind that reducing the overall rate of condition is not the same thing as reducing the disparity. In fact, interventions that may reduce overall prevalence may not reduce disparity in the same condition. Finally, it is likely that interventions within the social realm will take years to implement and even longer to evaluate. It took a long time to establish the race/ethnic disparity in the United States and it seems unrealistic that real improvements will be realized with the traditional 3- to 5-year funding cycles.
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