Sexually Transmitted Diseases:
Within the Hidden Epidemic: Sexually Transmitted Diseases and HIV/AIDS Among American Indians and Alaska Natives
Kaufman, Carol E. PhD*; Shelby, Laura MScPH†; Mosure, Debra J. PhD†; Marrazzo, Jeanne MD, MPH‡; Wong, David MD§; de Ravello, Lori MPH¶; Rushing, Stephanie Craig MPH∥; Warren-Mears, Victoria PhD, RD, LD∥; Neel, Lisa MPH**; Eagle, Sara Jumping MD*; Tulloch, Scott BS¶; Romero, Francine PhD††; Patrick, Sarah PhD, MPH‡‡; Cheek, James E. MD, MPH§§; for the Task force on STD Prevention and Control Among American Indians and Alaska Natives
From the *American Indian and Alaska Native Programs, University of Colorado at Denver and Health Sciences Center, Aurora, Colorado; †Division of STD Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia; ‡Department of Medicine, University of Washington, Seattle, Washington; §Division of Epidemiology, Centers for Disease Control and Prevention, Atlanta, Georgia; ¶Assignee to the Indian Health Service Division of Epidemiology and Disease Prevention, Centers for Disease Control and Prevention, Albuquerque, New Mexico; ∥Northwest Portland Area Indian Health Board, Portland, Oregon; **Native American Management Services, Inc., Reston, Virginia; ††Albuquerque Area Southwest Tribal Epidemiology Center, Albuquerque Area Indian Health Board, Albuquerque, New Mexico; ‡‡Center for Rural Health Improvement, National Center of Excellence in Women's Health, Sanford School of Medicine, University of South Dakota, Sioux Falls, South Dakota; §§Division of Epidemiology and Disease Prevention, Indian Health Service, Albuquerque, New Mexico.
Support for this project came from the National Institute of Mental Health grants R01 MH59017 and R01 MH69086, and the Centers for Disease Control and Prevention.
Correspondence: Carol Kaufman, PhD, American Indian and Alaska Native Programs, University of Colorado at Denver and Health Sciences Center, MS F800, P.O. Box 6508, Aurora, CO 80045. E-mail: firstname.lastname@example.org.
Received for publication December 8, 2005, and accepted February 3, 2007.
Objectives: To review the epidemiology, research, and prevention programs for sexually transmitted diseases in American Indians and Alaska Natives (AI/ANs).
Study Design: We reviewed the current national and regional trends in sexually transmitted diseases (STDs) for AI/ANs from 1998–2004, peer-reviewed studies from January 1996, through May 2006, and reports, unpublished documents, and electronic resources addressing AI/AN STD prevention and control.
Results: STD prevalence among AI/ANs remains high. For example, the case rate of C. trachomatis in the North Central Plains AI/AN populations is 6 times the overall US rate. Trends for C. trachomatis also show sustained increases. Little research exists on STDs for this population, and most is focused on HIV/AIDS. Fear of compromised confidentiality, cultural taboos, and complex financial and service relationships inhibit effective surveillance, prevention, and management.
Conclusions: Recommendations for STD control in this population include improved local surveillance and incorporation of existing frameworks of health and healing into prevention and intervention efforts. Research defining the parameters of cultural context and social epidemiology of STDs is necessary.
SEXUALLY TRANSMITTED DISEASES (STD) in American Indians and Alaska Natives (AI/ANs) are an important public health concern, with reported case rates for chlamydia, gonorrhea, and syphilis that are 2 to 6 times higher than rates in non-Hispanic whites (in keeping with the 1977 National Congress of American Indians and the National Tribal Chairmen's Association resolution, we use the term American Indians and Alaska Natives, abbreviated to AI/AN. We also use the term Native to refer to both American Indians and Alaska Native peoples).1 Recent data suggest that the gap in prevalence of most reportable STDs between AI/AN and other racial/ethnic groups may be widening.1,2 Women infected with chlamydia and gonorrhea often experience significant sequelae including pelvic inflammatory disease, ectopic pregnancy, and tubal infertility.3 Untreated syphilis may cause congenital syphilis in newborns, blindness, stroke, heart disease, and death.3,4 In addition, these STDs have been shown to facilitate the acquisition and transmission of HIV.3,5,6 The annual direct cost of STDs, including HIV, is estimated to be between $9.3 and $15.5 billion dollars.3,7 For facilities that care for AI/ANs, the costs associated with a higher STD burden may strain already scarce resources.
Despite the high morbidity and economic costs of STDs for this population, current practices of screening, treatment, and follow-up in AI/AN communities appear to be suboptimal.8,9 Improvements in STD control and prevention are clearly needed, yet little is known about which components of STD programs or prevention activities may be most effective for controlling the spread of STDs in this population.
The challenges of addressing STDs in the AI/AN community reach beyond resource allocation or clinical models of treatment. The epidemiologic profile of STDs among AI/ANs manifests from myriad factors, including complex social and sexual networks, varying cultural proscriptions regarding sexual activity, health, and help-seeking, availability of appropriate treatment and partner management strategies, and coordination of tribal, state, and federal programs. In this article, we will review the current epidemiologic evidence, research, and programmatic activities related to STDs, including HIV/AIDS, among AI/ANs. Thus, this effort represents the first comprehensive synthesis of an often obscure and elusive literature on STDs in AI/AN communities.
Demographic and Health Context of AI/ANs
Health disparities are often highly correlated with economic and social disparities. A review of the conditions in which many AI/ANs live may provide important context to the rates and trends of STDs in this population. According to the 2000 US Census, AI/ANs comprise less than 2% of the total US population.10 They may belong to one or more of 560 federally recognized tribes or Alaska Native Villages,11 all immensely diverse in cultural traditions, ways of living, and epidemiologic profiles. About 60% do not live on a reservation or tribal area, yet frequently travel between urban areas and tribal lands for ceremonies, education, or employment opportunities. About 28% of all AI/ANs live in poverty, compared with 12% of the total population.10 Unemployment rates are above 10% for most tribes (likely underestimated since they exclude persons no longer looking for work); households are crowded; and educational achievement lags behind other Americans, with only 10% of all AI/ANs living on tribal lands holding a bachelor's degree or higher, compared with 24% in the US general population.10 AI/ANs also endure elevated levels of mortality and morbidity. For example, age-adjusted mortality rates show that AI/ANs are over 7 times more likely to die from alcoholism when compared with the US general population, one and a half times as likely to die from firearm wounds, and over 3 times as likely to die in a motor vehicle-related injury.12 Although we know little about how this environment may shape AI/AN sexual risk-taking and the subsequent patterns of STDs, evidence suggests that trauma and ongoing stress may be deleterious to sexual health.13–15
Materials and Methods
For the purposes of this article, “STDs” refer to chlamydia, gonorrhea, syphilis, and HIV/AIDS. HIV/AIDS can be nonsexually transmitted, but we include the disease in this review because of its close association with sexual activity. We used published reports from Centers for Disease Control and Prevention (CDC) surveillance systems of nationally notifiable diseases to calculate rates of chlamydia, gonorrhea, and syphilis and HIV/AIDS among AI/ANs.16–19 Cases are defined according to CDC's Sexually Transmitted Diseases Treatment Guidelines.20 Laboratories or physicians are required to send reports of positive cases of chlamydia, gonorrhea, syphilis, and AIDS to local or state health departments, which are subsequently forwarded to CDC for compilation.20 The case rate is then calculated using the relevant estimated census population base (county, state, etc.), corrected for projected increases (or declines).
Compulsory reporting of AIDS is required in all 50 states and the District of Columbia. However, not all states have implemented CDC standards for name-based HIV reporting, and some have large AI/AN populations such as California, Illinois, and Washington. Oregon and Connecticut have name-based HIV reporting only for children under the age of 13.18 For this reason, surveillance-based estimates of HIV prevalence are likely to characterize the HIV-related profile inaccurately for the AI/AN population. Here, we present only national AIDS rates.
For local AI/AN rates, we used data provided by the CDC and Indian Health Service (IHS) for IHS service areas to demonstrate the increased differentials in areas of relative AI/AN concentration.21 The IHS divides its responsibilities into 12 regions, comprising 621 service counties (usually on or near tribal lands), with an estimated service population of some 1.7 million AI/ANs, (about 61% of all AI/ANs in the United States). Case rates were compiled using AI/AN population data from these counties, in combination with AI/AN case-reporting geographically linked to these counties (summarized to the regional level). No IHS regional estimates of AIDS cases are available.
The IHS estimates used here were calculated in a similar manner as national CDC STD rates, using AI/AN cases and AI/AN-specific county populations. However, local variability in adherence to those specifications is possible,21 and may be a particular problem at tribally-operated facilities (distinct from IHS-, privately-, or publicly-operated facilities). Because of tribal sovereignty, these facilities are not tied to the same reporting requirements that are mandated by states; tribally-operated facilities may choose not to report STD cases to the state or county surveillance system.22 The extent of this problem and its affect on overall or regional rates is not possible to determine. One study indicated that of those responding to a survey, 85% of tribally-operated and urban Indian health care facilities report HIV/AIDS cases to state or county authorities, and only 71% report chlamydia and gonorrhea (however, only 55% of facilities participated in the survey).23
Literature Search Strategy
We performed a Medline and PsycInfo search of articles appearing in peer-reviewed journals on STDs among AI/ANs from January 1996 through May 2006. We constructed two lists of terms for our search strategy: one for STDs, which included “sexually transmitted diseases,” “STDs,” and each of 4 STDs (chlamydia, gonorrhea, syphilis, and HIV/AIDS). The second list was comprised of population terms, including “American Indian,” “Alaska Native,” “Native American,” and “Aboriginal.” We selected those articles that focused on AI/AN populations and STDs, including studies based on Canadian populations. We included studies on human papillomavirus (HPV) that appeared as a result of these search terms. HPV is not a reportable STD, but is a significant area of morbidity for AI/AN populations and thus merits mention. We excluded quantitative studies that mentioned AI/AN groups with small sample sizes. Finally, because research challenges, programs, and services in these communities often do not appear in peer-reviewed journals or program proceedings, we conducted internet and manual searches to identify available reports delineating sexual risk factors and STD prevention and control efforts occurring in AI/AN communities. Additionally, each member of the Taskforce (coauthors) has worked with diverse AI/AN communities in different capacities; each contributed relevant unpublished literature to this review.
Epidemiology of STDs Among AI/ANs
Trends in AI/AN chlamydia case rates from 1998–2004 show a slightly lower rate of annual average increase (4%) when compared with the overall US case rate (6%); however, the AI/AN rates are over twice as high as the overall US rates (Fig. 1). Figure 2 shows specific IHS regional patterns of chlamydia case rates for 2004. All IHS regions except the California region have higher case rates when compared with the overall US rate; the Aberdeen area (North-Central Plains) chlamydia rate was 6 times higher than the overall US rate.
In contrast to the pattern for chlamydia, the AI/AN gonorrhea case rate was similar to the US rate. However, the AI/AN trend over this time period reflects a 3% average annual increase, whereas that for the United States overall reveals a 2% average annual decrease for the same period (Fig. 1). Figure 3 shows IHS regional trends for gonorrhea. All but 3 regions (Aberdeen, AK, and Phoenix) show lower rates than the US rate; however, both Aberdeen and Alaska regions are twice the level of the overall US rate, and all but 3 regions (Billings, Nashville, and Oklahoma City) have shown increases over the prior 6 years, counter to the overall United States trend (data not shown).
The national case rates for primary and secondary syphilis among AI/ANs have increased from 2.2 to 3.2 per 100,000 from 2000 through 2004, paralleling the overall US case rate increase (2.1–2.7 per 100,000).17 For the IHS service population, the estimated increase is from 1.3 to 3.5 per 100,000.21 Syphilis often occurs in association with discrete outbreaks, and thus national statistics may mask such events occurring in specific AI/AN communities.9 In one Southwest US American Indian community, for example, over 93 cases of syphilis were reported between 2000 and 2003, with 3 associated cases of congenital syphilis.9,24 In a 2004 outbreak in Maricopa County, AZ, the AI/AN rate was 18.6 per 100,000.25 In the Southeast United States, the AI/AN rate for one community reached levels of 112.4 cases per 100,000 persons in 2001, a 78% increase over a 5-year period.9
The number of AIDS cases among AI/ANs has increased during the years from 1990 (223 cases) to 2003 (3,026 cases).18 The CDC-estimated rate of AIDS for this population is slightly less than would be expected given the AI/AN representation in the population. However, several dimensions of the AIDS epidemic for this group are especially concerning. AI/ANs experience a faster time course from initial diagnosis of HIV infection to AIDS-defining illness than any other racial group in the United States. In 2001, 48% of AI/ANs diagnosed with HIV were subsequently diagnosed with AIDS within 12 months, compared with 40% for the general population.19 They also experience one of the lowest survival rates after an AIDS diagnosis is made.19 Available data do not provide information on whether the rapid progression (and low survival) is due to a late diagnosis of HIV, or an accelerated viral pathogenesis. Among those diagnosed with AIDS, AI/AN youth ages 13 to 24 make up 6% of all AI/AN cases, cumulatively, compared with 4% of those same ages in the general population.18 Finally, in 2004, 33% of AI/ANs diagnosed with AIDS were women or girls, a level second only to blacks (35%).26
Research, Reports, and Programs on STDs and HIV/AIDS Among AI/ANs
A total of 71 peered-reviewed journal articles were published from January, 1996, through May, 2006, on STDs among AI/ANs. Fifty-eight articles had an exclusive or primary HIV/AIDS focus and 14 had a primary focus on STDs other than (or in addition to) HIV/AIDS. (Table 1). Three articles focused on trends and patterns. McNaghten and colleagues looked specifically at national AI/AN patterns of STDs,27 although Miller et al.,8 Patrick et al.,31 and Shields et al.,29 examined patterns of specific STDs in community samples among which AI/ANs comprised a substantial proportion. Thoroughman and colleagues,30 provided an important footnote to these efforts by showing substantial racial misclassification of AI/AN women in Oklahoma in STD case reporting.
Three articles assessed sexual partner networks.33,35,37 Each of these suggested that the circulation of infected AI/AN persons, coupled with partnering patterns, are likely to provide disease transmission bridges to even remote rural areas. The findings from 2 related articles34,38 indicated that condom use among drug users varies by race of partner, and that male drug users were less likely to use condoms with AI/AN women when compared with partners of other races. Schiff and colleagues presented results of a clinic-based control trial on cervical neoplasia among Southwest AI women.36 They showed the importance of HPV and other STDs to this condition for this population. A multiethnic study on HPV found that the factors associated with the acquisition of HPV for AI women included young age at sex, multiple sexual partners, and women whose partners who reported very high numbers of other partners (average of 29 partners).39 One article offered a guide on holistic approaches to STD prevention among AI/AN youth.28 Finally, Speier32 provides the results of a qualitative study on AN community perceptions on infectious diseases, including STDs. Her results indicate that community members were reasonably knowledgeable about prevalent infectious diseases, but wanted holistic prevention and treatment approaches which incorporated community values and concerns.
Table 2 provides a summation of 64 articles with an HIV/AIDS focus (5 of which also appear in Table 1). We classified each of the 64 articles by its main topic and subtopic (when appropriate). Overall, for studies with AI/AN populations or subgroups, prevention or intervention was the HIV/AIDS topic with the most articles (15), followed by reviews, overviews, or trends (14), and substance use and care or treatment for HIV-positives (13 each).
The categorization of articles in the table demonstrates a growing research effort on many dimensions of HIV/AIDS about AI/AN populations; even so, the number of articles is small, and randomized control studies are all but absent. Nonetheless, many of these articles provide information that may be applicable to the prevention and control of other STDs in this population, for example, sexual risk factors among AI/ANs, or community approaches to intervention.
Epidemiology of Sexual Risk-Taking Behaviors Among AI/ANs
As in the national population, the majority of STDs among AI/ANs occur among young people. Among AI/ANs, 68% of all chlamydia cases, and 60% of all gonorrhea cases occur among those aged 15 to 24.17 In our review, we found one large study on sexual risk-taking among AI/AN youth. In 2000–2001, the Bureau of Indian Affairs (BIA) conducted a survey on risk-taking behavior with over 5600 high school students enrolled in BIA schools.100 This study, using comparable questions to the national Youth Risk Behavior Study (YRBS),101 found that 59% of high-school students reported having had sex, compared with 46% of the national sample, that 24% reported having 4 or more partners during their lifetime versus 14% of the national sample, and that 56% of those sexually active used a condom at last intercourse versus 58% nationally. (Note that important methodological differences between the two studies precluded significance testing of differences.) Of those who had already had sex, 11% of AI/AN youth reported initiating sex before the age of 13, compared with 7% nationally.100,101 The results indicate that sexual risk-taking is comparatively high among AI/AN youth, even though condom use appears to be roughly equivalent. An earlier study (1992), also based on a survey with BIA high school students, found similar patterns.102 Unfortunately, very little ethnographic data exists on the context of decision-making that produces such numbers. One report found that youth indicate that an environment of risk, including level of exposure to substance use, perceived sexual activity of peers, and role models in families or communities, were key to their sexual decision-making context.103
STD Prevention and Control Efforts in AI/AN Communities
STD prevention and control activities are sparse in AI/AN communities, and, as in peer-reviewed articles, HIV/AIDS appears to have received greater attention than other STDs. We have summarized the results of our search for reports and guides, descriptions of model programs or activities, and electronic resources in Table 3.
Several potentially effective models do exist, but systematic evaluations of the effectiveness are rare. Screening for STDs at clinics and hospitals appears to occur more regularly for women than for men, but may also inappropriately target older age groups.9 Although a number of clinic-based HIV training programs specifically designed for AI/AN communities exist,121–124 clinical HIV services may not always be offered because of the expense or lack of expertise.125 Comprehensive program assessments, grounded in the particular context of each AI/AN community, are urgently needed.105,126
A number of programs and data-collection initiatives exist that are not documented in peer-reviewed publications, but contribute to the base of our knowledge of STD prevention and control among AI/ANs.104 Tribal epidemiology centers represent multi-institutional cooperative efforts to coordinate monitoring and prevention activities at local levels.127 Several of these centers have identified STDs as a major focus of program and surveillance activities. The Northwest Tribal Epidemiology Center initiative entitled Project Red Talon is designed to provide member tribes with education, training, and technical assistance for the prevention and treatment of STDs.107 The project includes a regional STD profile and needs assessment; technical assistance to tribal health care advocates; and a rolling implementation of new screening and treatment strategies.126 The Inter-Tribal Council of Arizona has developed an HIV/AIDS-focused strategy that is now in the process of national scale-up.109 Tribal and pan-Native urban programs are also increasingly active, both in targeted programmatic activities117 and in efforts to increase coordination and cooperation with state and federal agencies.111,116 In recognition of the potential synergy of such collaborative efforts, the CDC has undertaken initiatives which provide funding directly to tribes, instead of to states in which tribes are located.127 Such steps are vitally important in channeling resources so that they may be most efficiently used in areas with the greatest need. Unfortunately, the continuation of this type of funding is not assured.128
Discussion and Recommendations
The epidemiologic evidence suggests that AI/ANs have elevated case rates of chlamydia, gonorrhea, and syphilis when compared with the national population, and that in areas of relative AI/AN concentrations, the burden is even greater.21 The prevalence of AIDS was not found to be elevated among AI/ANs. However, the association of chlamydia, gonorrhea, and syphilis with HIV transmission places them at risk for progression to this condition. Indeed, extant literature on STDs among AI/ANs is dominated by a focus on HIV/AIDS. Reports, guides, and resources show a similar orientation. The distribution of articles (and resources) is perhaps not surprising given the consequences and visibility of HIV/AIDS relative to other STDs, and the availability of funding to support research in this area.
Clearly, substantial overlap exists for risk factors related to HIV/AIDS and other STDs. However, research on non-HIV/AIDS STDs continues to be particularly valuable for at least 3 reasons: (1) it provides specific information on parameters of these diseases (e.g., community perception of STD risk and consequences) not revealed in HIV/AIDS-focused work; (2) it addresses a major risk factor for HIV/AIDS in a vulnerable population; and (3) chlamydia, gonorrhea, and syphilis require clinical and epidemiologic management distinct from that for HIV/AIDS, and the successful implementation of these protocols for this population is paramount.
Our review indicates that little is known about the application and efficacy of STD screening, treatment, and partner management programs specific to AI/AN communities. Factors that contribute to disparities that affect these communities and need to be considered in assessing these parameters include geographic isolation, poor access to health services, insufficient screening and partner management services, and unique social norms, stigma, and gender dynamics. Youth comprise a substantial proportion of AI/ANs contracting STDs, which poses specific challenges to local prevention activities. Tribal and state laws vary widely (and are frequently contradictory) regarding STD screening or treatment services for minors; definitions for, and enforcement of, mandatory statutory rape reporting; and, increasingly, STD educational activities.
Improvements in STD systems of care for AI/AN populations will occur only if they reflect the local cultural framework of health, healing, and understanding of sexual relationships. Toward this end, we identify 6 areas of future research and programmatic focus: (1) behavioral and disease surveillance systems appropriate for effective localized monitoring and response; (2) AI/AN youth access and treatment policies and procedures; (3) culture- and context-specific partner management systems; (4) existing traditions of sexual health; (5) scientifically rigorous investigation of culturally appropriate prevention and control strategies; and (6) adaptation and evaluation of proven interventions.
The daunting epidemiologic profile of STDs among AI/ANs and the high cost associated with these conditions and their sequelae emphasize the profound need for successful models of intervention. STDs are preventable and many are curable; effective programs could eliminate or narrow extant disparities and substantially reduce health care costs. The cultural context of the STD epidemiology of the AI/AN population poses the challenge to the health community—public and private—for urgent, meaningful, and systematic attention.
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