THE RAPID DISSEMINATION OF HIV in the early 1980s throughout the United States resulted in a steadily escalating number of AIDS cases through the early 1990s, but the available epidemiologic data suggested that the epidemic was most concentrated in urban areas among homosexual men and injecting drug users.1–3 Whether HIV was being disseminated to rural districts or to other populations not recognized as being at risk for HIV were questions that were raised during the 1990s in several contexts. First, resources for patient care and treatment were allocated based on the number of AIDS cases by residence at the time of diagnosis such that urban areas received the greatest share of resources. Patient advocates from less urban and rural areas claimed a higher burden of HIV care than their resources supported as a result of the “coming home” to be cared for by family members of patients with AIDS infected elsewhere.4–6 Second, although AIDS incidence rates in the population in rural areas were fairly stable, reports that the number of AIDS cases was growing faster in rural than in urban areas fueled demands for attention to the HIV threat in rural areas already burdened by inadequate health care.7–9 Third, HIV was increasingly recognized as being transmitted heterosexually.10,11 This meant that there was a risk of HIV transmission among heterosexuals who might not perceive themselves as in a high-risk category. Women, in particular, were increasingly viewed as vulnerable to HIV as a consequence of sex with male partners who engaged in multiple high-risk sexual and drug-using (injecting and noninjecting) behaviors.12 Fourth, many southern states reported persistently high rates of sexually transmitted diseases (STDs).13,14 STDs are associated with increased risk for HIV acquisition, both as epidemiologic markers for high-risk sexual behaviors and because some STDs potentiate HIV transmission.15,16
The intersection of these factors led to a need for more research on rural populations, especially in the southeastern United States, among sexually active minority women to: 1) improve understanding of risk factors for HIV transmission, 2) design special programs for populations not targeted by traditional prevention interventions, and 3) improve access to HIV diagnosis, care, and treatment services in poor, rural communities. In response, the Divisions of HIV/AIDS Prevention and Sexually Transmitted Diseases Prevention of the Centers for Disease Control and Prevention (CDC) in Atlanta convened a consultation in early 2002 to shed light on these research and programmatic needs. The conference brought together epidemiologic, social, clinical, and behavioral perspectives to define an HIV prevention research agenda for women in the nonurban South.
This report is based, in part, on the epidemiologic data presented at the conference. We highlight key features of the HIV epidemic in the South, comparing women with men. By synthesizing available data from HIV/AIDS surveillance, STD surveillance, and studies of risk behaviors in selected rural areas in the South, we offer a comprehensive epidemiologic overview of HIV in the southern region that is unavailable elsewhere.
Sources of Data
We reviewed data from multiple sources to characterize the HIV/AIDS epidemic in the southern United States.
All U.S. states and territories require healthcare providers and institutions to report cases of AIDS to the state or local health department. After the development of the serologic antibody test for HIV, some states implemented similar requirements for the reporting of cases of HIV infection in persons who do not meet the clinical or immunologic criteria that define AIDS.17–19 Case reports are forwarded by states and territories to the CDC. Denominators for the calculation of rates of AIDS incidence and prevalence are derived from U.S. Census Bureau data.20 The methods of HIV/AIDS case reporting, rate calculation, adjustments for delays in reporting cases, adjustments for unreported mode of HIV exposure, and results of evaluations of the completeness and representativeness of the data have been previously described.19–22 Figures include data publicly available on the CDC web site (www.cdc.gov/hiv/graphics.htm).23
Sexually Transmitted Disease Surveillance
STD surveillance is conducted by state and local STD control programs, which report cases of nationally notifiable STDs (i.e., gonorrhea, syphilis, chlamydia, chancroid) to the CDC using standardized case definitions.24 Because of incomplete diagnosis and reporting, the number of cases and the population rates underestimate the impact of STDs at the community level.13 Denominators for the calculation of rates are from U.S. Census Bureau machine-readable data files.13 Data presented are publicly available on the CDC web site (www.cdc.gov/std/stats/slides.htm).25
Supplement to HIV/AIDS Surveillance (SHAS)
In selected states, or selected geographic areas or cities within other selected states, interviews were conducted with persons reported to the health department as a case of either HIV infection (without AIDS) or AIDS. This project supplemented HIV/AIDS case reporting data with self-reported race/ethnicity, socioeconomic status, detailed sexual and drug-using behaviors, access to care, and use of services. SHAS methods have been previously described.26–28 In brief, participants were identified in 2 ways: from HIV/AIDS case reports in a participating state or those persons who presented for care or other services in selected clinical facilities. Eligible persons included men and women ≥18 years of age who gave informed consent and were mentally and physically able to complete the interview. The project was approved by state or local Institutional Review Boards. Modest incentives to participate were offered consistent with local practices for such interview studies.
Four SHAS states in the South participated in a special “Rural SHAS” project during 1995 through 1996. The project was conducted in selected rural areas and small cities with populations of less than 250,000: Delaware, all nonmetropolitan statistical areas in the state; Florida, Ocala County; Georgia, Waycross and Albany Health Districts; and South Carolina, Edisto Health District. Additional questions on presumed duration of infection, migration, and other social, demographic, and behavioral data were asked. Detailed methods and response rates (64%) have been previously reported.29,30 We summarize data previously reported from interviews of 608 persons with HIV (42%) or AIDS (58%) participating in Rural SHAS in Delaware (8%), Florida (15%), Georgia (66%), and South Carolina (11%).
We followed U.S. Census Bureau definitions of geographic regions of the United States. The South includes 16 states* (Alabama, Arkansas, Delaware, Florida, Georgia, Kentucky, Louisiana, Maryland, Mississippi, North Carolina, Oklahoma, South Carolina, Tennessee, Texas, Virginia, and West Virginia) and the District of Columbia. We used U.S. Office of Management and Budget definitions of “urban” (metropolitan statistical areas [MSAs] with >500,000 population), “less urban” (MSAs with 50,000– 500,000 population), and “nonurban” (also referred to as “rural” or “nonmetropolitan” areas with <50,000 population) except where otherwise specified.31
For purposes of categorizing the presumed mode of exposure to HIV among persons diagnosed with HIV or AIDS who reported more than one risk, the CDC uses a hierarchical classification system. Of more than 807,000 persons reported with AIDS through 2001, 14% had multiple exposure modes and were classified hierarchically.20 The hierarchy is male-male sexual contact (MSM); injecting drug use (IDU); both male-male sex and injecting drug use (MSM-IDU); hemophilia/coagulation disorder; heterosexual contact with a partner known to be infected with HIV or to have an AIDS diagnosis, or to be in a recognized HIV risk group, i.e., an injecting drug user, a bisexual male, a hemophiliac, a transfusion recipient with HIV infection; and receipt of blood transfusion, blood components, or tissue. Most case report data on mode of exposure to HIV are abstracted from medical records. Persons with HIV/AIDS who are interviewed specifically to ascertain more complete risk histories (e.g., SHAS interviewees) may be more likely to have complete case report data, including multiple HIV exposure modes, as well as data on risk behaviors that were included in the survey such as history of STDs, noninjecting drug use, and exchange of sex for drugs or money.
Characteristics of Populations with HIV/AIDS and Sexually Transmitted Diseases in the South
Over 60% of the U.S. population resides in urban areas.32 Throughout a period of decreasing AIDS incidence after the introduction of highly active antiretroviral therapy in the mid-1990s, the proportionate distribution of cases by size of population of area of residence stayed relatively stable.23 In 1994, 85% of nearly 76,000 AIDS cases in men and women were reported from urban areas, and in 2001, 81% of over 41,000 cases were from urban areas. The percentage of cases reported from nonurban areas in those same years was 6% and 7%, respectively. The rates of reported AIDS cases per 100,000 population in 2001 were 19.0, 9.5, and 5.8 for urban, less urban and nonurban areas, respectively.
The South constituted 36% of the U.S. population of 281.4 million in 2000.33 In the South and Midwest, a much higher percentage of the population resides in less urban or nonurban areas than in the Northeast or West (South: 22% less urban, 26% nonurban; Midwest: 20%, 27%; Northeast: 11%, 10%; West: 16%, 14%).33 The South is the region currently having the largest proportion of AIDS cases from less urban and nonurban areas (Fig. 1). In contrast, in the Northeast and the West, more than 90% of AIDS cases resided in large (>500,000 population) metropolitan areas at the time of AIDS diagnosis. Table 1 presents AIDS rates comparing urban, less urban, and nonurban areas by region. Although rates in nonurban areas are consistently lower than rates in urban or less urban areas within each region, among nonurban areas, the relatively higher rates in the South are noteworthy.34
The burden of HIV/AIDS care continues to increase in the South. The South accounted for the largest proportion (39%) of the more than 362,000 persons living with AIDS as of December 2001 (Fig. 2). AIDS prevalence has increased steadily because effective treatments prolong survival after an AIDS diagnosis.35 Because the South currently contributes the highest number of prevalent AIDS cases, it is likely that resources needed for patient care and treatment will escalate in this region.
Annual rates of reported cases of AIDS in 200123 and of gonorrhea in 200225 by state highlight the impact of HIV and STDs in the southern region. Areas with the highest rates of gonorrhea per 100,000 population in 2002 include many of the same southern states with the highest rates of AIDS per 100,000 population (e.g., Delaware: 201.1 gonorrhea, 31.1 AIDS; Maryland: 176.6, 34.6; South Carolina: 228.1, 17.9; Georgia: 224.6, 20.8; Florida: 133.6, 31.3; Mississippi: 241.7, 14.6; Louisiana: 254.8, 19.3). Similarly, rates of syphilis tend to be higher in the southern states than in other geographic regions.13 Reflecting high-risk sexual behaviors, high rates of STDs call attention to risks for HIV spread or for resurgence of HIV in communities as new cohorts of young men, and women, come of age.36,37 Although studies of HIV incidence have been focused on high-risk populations in some large cities where STDs have experienced a resurgence and current rates of HIV incidence are presumed to be highest,38,39 there have been periodic reports of clusters of new HIV infections associated with high STD rates that have highlighted risks for rapid heterosexual HIV spread within rural communities both in the South and elsewhere.40,41
AIDS rates per 100,000 non-Hispanic black population in rural areas in the South (45) are lower than in blacks in rural areas in the Northeast (222) Midwest, (77) or West (60).33 However, the South is the only region in which more than half of reported AIDS cases are in black persons. Blacks constituted 54%, 51%, and 56% of AIDS cases in urban, less urban, and rural areas of the South, respectively. Given the increasing prevalence of HIV/AIDS in the South, the high number of black men and women with AIDS in this region supports a focus on HIV/STD prevention among minority populations in the South.
Thus, several characteristics differentiate the HIV epidemic in men and women in the South as compared with other regions of the United States: a disproportionate concentration in less urban and rural regions and among blacks, the highest proportion of prevalent HIV/AIDS cases, and high rates of AIDS and STDs.
Demographic and Behavioral Risk Characteristics of Women With HIV/AIDS in the United States and in the South
The population of U.S. women with HIV/AIDS is less heterogeneous than that of men in terms of race/ethnicity and risk exposure category. In 2001, a higher proportion of women reported with AIDS were black (63%) or Hispanic (17%) compared with men with AIDS (44% and 20%, respectively).20 The proportionate distribution of AIDS cases by risk exposure categories differs for nonurban areas compared with urban areas. Because screening of the blood supply has virtually eliminated transmission by blood or blood products, and barring rare or unusual transmission circumstances, women acquire HIV either through sharing drug-injecting paraphernalia or through sexual contact with an HIV-infected male. Among women diagnosed with AIDS through 2001 from urban and less urban areas, the largest proportion acquired HIV as a result of injecting drug use. Smaller proportions were exposed to HIV through heterosexual contact with a male injecting drug user or with other males in a recognized HIV risk category or known to be HIV-positive. However, in rural areas, the risk profile is remarkably different, because heterosexual transmission from male partners not known to be injecting drug users predominates (Fig. 3). In contrast, among men, the proportionate distribution of AIDS cases by risk categories (MSM, IDU, MSM-IDU, and heterosexual contact) are nearly identical regardless of size of metropolitan area of residence (data not shown).23 Many women in rural areas reportedly are unaware of any primary risk behaviors of their male sexual contacts (i.e., injecting drug use, sex with other men) and may only know that a heterosexual partner was diagnosed with HIV.29,42 Secondary heterosexual spread of HIV, i.e., heterosexual transmission from a person who was infected through heterosexual contact, as well as primary heterosexual spread from men who do not acknowledge bisexuality or injecting drug use, combine to challenge understanding of precisely which risk behaviors account for the predominance of heterosexual exposure among women in rural areas.11,29,42 Further research is needed to identify other behavioral characteristics that may be instructive in designing appropriate and effective prevention interventions.43
Because AIDS represents the end stage of HIV disease, examining new diagnoses of HIV infection sheds light on more recent transmission patterns, especially among young adults who are necessarily more recently infected as a result of their recent entry into the age group in which high-risk sexual and drug-using behaviors are initiated. Among the cohort of young women ages 15 to 19 years in 1994 who acquired HIV through heterosexual contact, annual rates of new HIV diagnoses were highest in the South where they increased gradually as the cohort aged (Fig. 4).44 In contrast, among such women infected through injection drug use, rates were highest in the Northeast (data not shown).44 Recent reports suggest that blacks account for 74% of all heterosexually acquired infections reported from 29 HIV-reporting states and that females account for 89% of heterosexually acquired infections in 13 to 19 year olds.45 Given the relative homogeneity of case reports of women with HIV/AIDS, the characteristics of urban versus nonurban HIV-infected women do not differ markedly, except for the predominance of heterosexual transmission among women in the rural South.
Social, Demographic, and Behavioral Characteristics of Men and Women With HIV/AIDS in Southern Rural Areas
The data presented thus far suggest that HIV-infected women in the South are disproportionately of black race, living in less urban or nonurban areas, and exposed to HIV by an HIV-infected male sex partner without recognized primary risk factors. We were interested in exploring data on possible explanatory factors for the predominance of heterosexual transmission among HIV-infected southern women. Various scenarios could account for this: a self-sustaining heterosexual HIV epidemic fueled by high-risk sexual behaviors in a population with high background rates of STDs known to potentiate HIV spread; immigration of men infected through injecting drug use or male-male sexual contact in larger urban areas who transmit HIV to women in rural areas through sexual contact; and immigration of women who were infected elsewhere, e.g., in larger urban areas, through heterosexual contact with male injecting drug users or bisexual men. The predominance of heterosexually acquired HIV among women in this setting highlights the importance of examining factors associated with HIV transmission for both women and men. In the areas where Rural SHAS was conducted, sexual transmission accounts for the majority of cases in women (66%) and in men (27% heterosexual contact and 40% homosexual contact). Women with HIV/AIDS were less likely than men to have completed high school (50% and 64%, respectively); less likely to be employed (13% and 25%, respectively); and more likely to have an annual income <$10,000 (80% and 58%, respectively) (Fig. 5). A high proportion of women and men reported a history of an STD (55% and 51%, respectively). Noninjecting drug use, especially the use of crack cocaine, has reportedly been associated with increased risk of heterosexual HIV transmission.27,46 In the Rural SHAS project, crack use was reported by 42% of women and 37% of men. Consistent use of latex condoms can protect against HIV transmission; however, the results of the Rural SHAS study highlighted the formidable challenge in promoting condom use given that 98% of women and 69% of men reported unprotected heterosexual contact and that 24% of women and 36% of men practiced risky sex after they knew they were HIV-infected.
Migration after a diagnosis of HIV/AIDS may contribute to further geographic HIV spread.47 In Rural SHAS, 36% of those interviewed migrated to their rural area of residence after they knew they were HIV-infected, 34% migrated to their rural area of residence before testing HIV-positive, with the remaining 30% reporting they had not lived outside of their current rural area of residence. Immigration of persons infected elsewhere (e.g., in urban areas) may account for a substantial proportion of infections among rural residents.30 However, other reports have shown that, once HIV is introduced, rapid spread of HIV within rural sex networks can occur against a background of high STD rates.40
HIV Care and Treatment Issues in Rural Areas
Residents of rural areas, by definition, face challenges in accessing medical care and treatment as a result of greater geographic distances to medical facilities, the relative lack of accessible tertiary care facilities, or fewer highly specialized physicians, who tend to be located in more urbanized settings. Several prior reports have highlighted these challenges. In a study of a cluster of HIV-infected adolescents and young adults in rural Mississippi, a survey of local internists and family practitioners indicated that they treated few HIV-infected patients and lacked knowledge of specialty HIV care practices.40 Setting up a network of social, mental health, and case management services by linking the local health department and local physicians to a remote medical consultant enabled improvements in the quality and accessibility of care in this rural area. A nationally representative sample of HIV-infected persons in the United States found disparities in access to HIV care and treatment for residents of rural areas compared with urban areas.48 Specifically, rural patients were less likely to have received recommended antiretroviral treatment regimens or to have received standard prophylaxis for opportunistic infections. In addition, rural residents were cared for by providers seeing few HIV-infected patients.48 Previous studies have shown that patients whose physicians have greater experience with HIV care have fewer hospitalizations and better survival, including in rural areas.49–51 Lack of insurance among HIV-infected persons in the nonurban South may contribute to poor-quality HIV care and treatment. In the Rural SHAS project, 35% of those interviewed had no insurance and, of these, one third had never received antiretroviral therapy (CDC, unpublished data).
Our review of the available data and literature suggests that research focused on the unique needs of minority, less urban, and nonurban men and women in the southern United States will enhance effectiveness of HIV prevention and care in this region. We have illustrated key features of the HIV epidemic among women compared with men in the nonurban South: the predominance of heterosexual transmission; the disproportionate impact on black women; the complex dynamics of predisposing risk behaviors in men as well as in women; and multiple challenges in access to quality diagnosis, care, and treatment. The southern region has the highest proportion of prevalent AIDS cases, high AIDS and STD rates, and the highest rates of new HIV diagnoses in women. It has the highest proportion, and highest rates, of AIDS in nonmetropolitan areas, although the majority of cases are still reported from urban areas. HIV-infected women in the rural South are characterized by low socioeconomic status. The high proportion of sexually acquired HIV infection reflects numerous factors that facilitate sexual transmission directly (multiple sex partners, lack of condom use, practicing risky sex even after knowledge of HIV infection) and indirectly (drug and alcohol use, STDs). After knowledge of infection, it may be particularly difficult to ensure equity in access to quality HIV care for patients who face logistic or economic barriers.
The population-based surveillance data reported in this article have limitations. Both STD and HIV/AIDS surveillance case reports collect only limited behavioral and clinical data and are most useful to describe the epidemiology in the affected population of men and women in a given area. They are less useful in exploring the underlying social and behavioral factors that determine why some persons or populations are disproportionately at risk for sexually transmitted infections. The SHAS interview data remedy some of the deficiencies of surveillance data but are themselves limited in being less representative of the general population of persons with HIV/AIDS and are subject to other methodological limitations such as recall bias. We only had detailed behavioral data from 4 southern states, which may not be representative of the entire region. Our presentation of supporting data from the relevant literature is necessarily selective and the complex dynamics involved in HIV and STD transmission among rural residents requires more in-depth analysis than we can achieve in this article. Despite the limitations of each of the data sources and supporting evidence presented here, the consistency of findings across multiple sources emphasizes why concerns about the spread of HIV into nonurban areas have been raised persistently for more than 10 years.52,53
Female, minority, nonurban women face a multitude of HIV prevention and care issues. Although we have presented epidemiologic data from multiple sources that document these challenges, structuring an integrated plan to address them remains an elusive goal. The compilation of papers in this special issue provides a framework for prioritizing the effort to fill gaps in research and knowledge. Public health efforts must be mobilized in a more concerted way to prevent the establishment of an endemic HIV presence among these vulnerable women. Migration of high-risk and infected persons from rural to urban and back to rural areas is unlikely to abate. Therefore, the importation into rural populations of HIV knowledge and strategies for prevention, care, and treatment that have proven effective in urban areas would be desirable. Yet, adapting interventions effective in urban settings to rural settings requires further research. We argue that HIV prevention strategies for rural women must also focus on men or they risk having little impact. Research is needed on determinants of partner selection, barriers to condom use, and strategies to reduce social drug and alcohol use. Underlying social factors such as low education and income may prove tougher obstacles to prevention and care in rural regions. Nevertheless, we feel that research that examines the complex interplay of social and behavioral risk factors prevalent in the nonurban South can lead to more effective intervention programs and reduce the HIV burden among women. It is critical to help HIV-infected persons prevent transmission of their infection by reducing barriers to early detection and providing HIV-infected persons with state-of-the-art medical and preventive services.54 Ultimately, preventing heterosexual transmission of HIV and STDs in women may require research that recognizes the interdependence of men and women in practicing safer sex. Ensuring equity in access to HIV education, prevention programs, and treatment in nonurban areas remains a compelling challenge.
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*Northeast: Connecticut, Maine, Massachusetts, New Hampshire, New Jersey, New York, Pennsylvania, Rhode Island, Vermont; Midwest (also referred to as “Central”): Illinois, Indiana, Iowa, Kansas, Michigan, Minnesota, Missouri, Nebraska, North Dakota, Ohio, South Dakota, Wisconsin; West: Alaska, Arizona, California, Colorado, Hawaii, Idaho, Montana, Nevada, New Mexico, Oregon, Utah, Washington, Wyoming.© Copyright 2006 American Sexually Transmitted Diseases Association