Sexually Transmitted Diseases:
The Changing Epidemiology of Syphilis
Peterman, Thomas A. MD, MSc; Heffelfinger, James D. MD, MPH; Swint, Emmett B. MS; Groseclose, Samuel L. DVM, MPH
From the Division of STD Prevention, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta Georgia
Correspondence: Thomas A. Peterman, Mailstop E02, CDC, Atlanta, GA 30333. E-mail: firstname.lastname@example.org.
Received for publication November 4, 2004, and accepted January 11, 2005.
AFTER DECLINING EVERY YEAR since 1990, and less than 2 years after the launching of the National Plan to Eliminate Syphilis in the United States, rates of primary and secondary syphilis increased slightly in 2001.1 New epidemics involving men who have sex with men (MSM) have since been detected in most major US cities.
If we could identify the persons who are most likely to acquire the next syphilis infections and why, we might be able to reach them early and prevent acquisition or reach them soon after they are infected and treat them before they transmit to others. This requires identifying characteristics of persons acquiring infection, how they are meeting partners, and how they are transmitting infection. When this information is known, we can warn the population at risk so they can take precautions to avoid infection or perhaps recognize an infection when they get it. We can also more effectively target screening campaigns and alert health care workers to look for infections among persons at risk.
We also want to know how large the current syphilis epidemic will become because it will help with resource allocation decisions. Interventions early in an epidemic may halt transmission that could otherwise eventually become highly magnified. However, effective interventions can be expensive, even early in an epidemic. It is easier to justify extensive interventions for an epidemic that would otherwise grow to millions of cases (e.g., acquired immunodeficiency syndrome [AIDS]) than it is for an epidemic that would ultimately involve a small number of cases (e.g., hantavirus pulmonary syndrome).
Finally, we want to know what this epidemic is telling us about other sexually transmitted infections, particularly human immunodeficiency virus (HIV). There has been concern that advances in antiretroviral therapy were leading to disinhibition of the sexual behaviors that were changed due to the AIDS epidemic.2,3 A relaxation of safe-sex practices could lead to resurgence of HIV and AIDS; however, increases in HIV transmission can be very difficult to identify because of the long and variable incubation period. Thus, other indicators have been used to try to identify effectiveness of HIV prevention programs.4 Some studies have suggested there have been increases in unprotected anal sex.3,5,6 Other studies suggest gonorrhea rates have increased among MSM.6,7 Is the current syphilis epidemic another indication that HIV transmission is increasing?
We will address these questions by reviewing surveillance data reported to CDC and published epidemiologic research from the United States and elsewhere.
Who Is at Risk?
Evidence From Surveillance.
The incidence of primary and secondary syphilis in the United States fell dramatically with the introduction of penicillin in the 1940s (Fig. 1). After reaching a nadir in the late 1950s, rates began a gradual rise, with peaks occurring about every 10 years.8 Although it is tempting to suggest that the rise and fall reflects a waxing and waning of population-based immunity8a, this seems unlikely because these epidemics have occurred in quite distinct populations. Overall national trends can be quite deceptive because they can hide epidemics that are occurring in different populations. An epidemic in one population can be masked by a similar decline in a similar-size population or by a much smaller decline in a much larger population. This phenomenon has occurred repeatedly with syphilis.
Syphilis surveillance information is collected for every reported case, so the number of variables collected to characterize subgroups is limited to sex, age, race, and county of residence. Gender of sex partners has not been reported to CDC in the past but will be in the future. Some very distinct trends become apparent when we look at trends within broad subgroups.
Men and women have had roughly similar timing of peaks and troughs in syphilis rates between 1963 and the late 1990s (Fig. 2). However, the epidemic that peaked in 1982 involved many more men than women, while the epidemic that peaked in 1990 involved approximately equal numbers of men and women. The current (2003) epidemic, once again, involves many more men than women. The male:female rate ratio (Fig. 2) peaked at 3.6 in 1979 (3 years before the number of cases peaked among men). Following its peak in 1979, the male:female ratio continued to fall during the 1990 epidemic, to a low of 1.2 in 1992–1997. Since 2000, the ratio has increased dramatically, reaching 5.2 in 2003. Congenital syphilis rates, which reflect rates in women, increased substantially during the 1990 epidemic but not in 1982 or 2002.9
The age distribution of syphilis cases has changed dramatically over the past epidemics, particularly for men (Fig. 3). In 1982, rates were highest for 20- to 29-year-old men. By 1990, 30- to 34-year-old men had rates that were nearly the same as the 20- to 24-year-olds. In 2003, rates were highest for 35- to 39-year-old men, and even 40- to 44-year-old men had rates that exceeded 20- to 24-year-olds. The median age group for male cases was 25 to 29 in 1982 and 35 to 39 in 2003.
Race-specific rates have only been available since 1981 (Fig. 4). In 1981, the black:white ratio was 13.2. The black:white ratio rose to as high as 62:1 in 1993 and has since fallen to 5.2:1 in 2003; during this time rates among blacks fell (from 74.1–8.1 per 100,000), while rates among whites increased (from 1.2–1.5 per 100,000).
Geographic analyses are a bit more complicated because the ideal unit of analysis is not so obvious. One crude analysis dividing the United States into 4 regions is quite revealing (Fig. 5). The 1982 epidemic was predominantly in the South, though lesser increases were seen in the other regions at about the same time. The 1990 epidemic was big in all regions, but the timing varied. The increase started in the West in 1986, then Northeast and South in 1987, and reached the Midwest in 1988. In 2002, the largest number of cases among MSM were reported from the 8 cities studied in this special journal issue: New York, Atlanta, Fort Lauderdale, Miami, Chicago, Houston, Los Angeles, and San Francisco (Fig. 6). This list includes at least 1 city from each region.
Fairly simple analyses of limited surveillance information have shown the epidemics of 1982, 1990, and 2003 had different gender, age, race, and geographic characteristics. Additional information from specific studies has helped characterize who was involved in these epidemics.
The 1982 epidemic appears to be at least partly due to increases among MSM (with a male:female case ratio peaking in 1979 and declining when the AIDS epidemic was identified in the early 1980s). There are relatively few epidemiologic studies in the literature from that era, and there is no information on sexual orientation in the surveillance database. Analysis of CDC data from syphilis case investigations in 1982 found sexual orientation was determined for 59% of white men and 72% of black men; 71% of the white men and 35% of the black men were MSM.10 It is not clear why this epidemic was largest in the South.
The 1990 epidemic was focused largely among black heterosexuals in urban areas and in the rural South.8,10 Several studies associated that epidemic with the exchange of sex for drugs and the use of crack cocaine, but other factors cited included a decreased effectiveness of STD prevention and control programs, increasing poverty, disenfranchisement of minorities, and urban decay.10,11
The current epidemic has largely involved MSM. Although national surveillance data do not include information on sexual orientation, the extreme male:female rate ratio is highly suggestive, and review of partner notification records confirms that many of the cases were MSM and many were HIV infected. In some areas, the magnitude of the epidemic has been masked by concomitant declines among heterosexuals. For example, in Chicago, between 2000 and 2002, female cases decreased from 129 to 43, while male cases increased from 166 to 310, so there was probably a decrease among heterosexual men that partially masked the increase among MSM. In San Francisco, where there was little syphilis among heterosexuals, the increase in MSM over this interval is much clearer; while there were only 5 and 4 female cases, male cases increased from 48 to 311.
The largest numbers of primary and secondary syphilis cases among MSM were reported from the cities highlighted in this journal supplement (Fig. 6). These cities were also among the top in the number of MSM infected with HIV.12 However, major increases in the male:female rate ratio for primary and secondary syphilis have occurred in many large cities in the United States. In 1998, in selected cities with populations >200,000 that reported at least 10 men or 10 women with primary or secondary syphilis, 10 (29%) of 34 had a male:female rate ratio greater than 2.13 In 2002, 30 (77%) of 39 such cities had a male:female rate ratio greater than 2.9 This rapid geographic spread may be partly due to recruitment of sex partners at circuit parties or while traveling for other reasons.14
Evidence From Investigations Into the Current Epidemic.
Early reports describing the syphilis epidemics in MSM were mostly anecdotal. In Houston, the number of MSM with primary and secondary syphilis increased from 9 in 2000 to 68 in 2002.15 Of the MSM with known HIV status, 58% were coinfected with HIV. Many of these patients reported anonymous sexual contacts met through chat rooms, web sites, bath houses, bars, and parks. The use of “party drugs” such as methamphetamines also appeared to be more common than in the past, but the information had not been systematically collected. (This information is now systematically collected in Houston.) A San Francisco STD clinic survey included 1318 MSM (54 diagnosed with early syphilis).16 Multivariate analysis found men who used methamphetamines and Viagra were much more likely to have syphilis than men who did not use methamphetamines (odds ratio 6.1). In southern California, 33 (50%) of 66 MSM with syphilis reported anonymous sex, and 26 (40%) reported using illicit drugs, most often crystal methamphetamine.17 Of the 57 men who knew their HIV serostatus, 34 (60%) were HIV infected.
Oral sex may be an important mode of syphilis transmission in the current epidemic. The Chicago health department began collecting information on oral sex in 2000 after hearing that many MSM were surprised to learn they had syphilis because they had practiced only oral sex, which they assumed was “safe.”18 Data on oral sex were available for 65% of the 962 cases of primary and secondary syphilis cases reported between 2000 and 2002. Of the 325 MSM, oral sex was the only sexual exposure for 18 (22.7%) of 79 with primary syphilis, and 48 (19.5%) of 246 with secondary syphilis. Interestingly, oral sex associated with crack cocaine use was also thought to play a prominent role in the 1990 epidemic.8
Three case-control studies have been conducted in the United States. In early 2000, a study in Los Angeles compared MSM with primary and secondary syphilis to controls from gay medical clinics matched by age group.19 Cases were more likely than controls to report HIV seropositivity (64% vs. 32%), visiting a bathhouse during the interview period (43% vs. 14%), a history of STDs other than syphilis (63% vs. 41%), and crystal methamphetamine use (29% vs. 13%). A small case-control study in Miami in 2001 found no major differences between MSM with syphilis and MSM controls, possibly due to overmatching because the controls were taken from the same clinics.20 A study in New York City in 2001 compared 88 MSM with primary or secondary syphilis to 176 MSM controls matched by age and type of health care provider.21 HIV prevalence was 48% among syphilis cases compared to 15% for controls. The median number of sex partners in the previous 6 months was similar for cases (6) and controls (5). Inability to contact half or more of their sex partners from the past 6 months was reported more often by cases (74%) than controls (57%). Nearly 80% of all participants had visited at least 1 venue for the purpose of meeting a sex partner. Methamphetamine use was more often reported by cases (24%) than controls (12%). Multivariate analysis showed syphilis to be significantly associated with HIV infection (OR 7.3), income greater than $30,000 per year (OR 2.7), unprotected anal intercourse (OR 2.6), and nonwhite race (OR 1.5). Among HIV-infected participants, syphilis cases were more likely than controls to be on antiretroviral therapy (69% vs. 44%) and to report having an undetectable viral load (58% vs. 24%). Half of the HIV-infected persons reported having at least 1 partner who was known to be HIV negative, and 30% had unprotected anal intercourse with a partner of unknown HIV status.
Based on this information, we can deduce that the persons most at risk in this syphilis epidemic are MSM. Among MSM, those at highest risk are known to be HIV-infected, have multiple partners, have anonymous partners, or use illicit drugs such as methamphetamine. The epidemic rapidly spread to involve most cities that had large MSM communities.
How Large Will This Epidemic Get?
This syphilis epidemic appears to be occurring simultaneously in Europe and Canada, as well as in the United States, and seems to be involving similar risk groups.22–26 In Amsterdam, between 1994 and 1999, there was an increase in the number of MSM visiting the STI clinic (1410–2462) and an increase in the percentage infected with rectal gonorrhea (4.0–6.8) and early syphilis (0.4–1.4).24 In the United Kingdom, syphilis increased from 132 cases in 1995 to 326 in 2000, mostly among MSM, some of whom were HIV positive.25 In Paris, during 9 months of 2000, there were 10 MSM with early syphilis diagnosed in a clinic that had seen no cases in MSM for a few years.26 A review of data from Europe found MSM syphilis outbreaks reported in the Netherlands, Ireland, France, and Norway, including HIV-infected MSM.25 Thus, unlike the 1990 epidemic in the United States, the current epidemic among MSM rapidly became widespread in the United States and around the world. Because the epidemic is already widespread geographically, future growth must come from spread within the areas that already have cases rather than from introduction and spread in new geographic areas.
Understanding why the epidemics are occurring may also help predict how far they will spread. The current syphilis epidemic, involving MSM who are disproportionately HIV infected, may be partly due to the emergence of effective HIV therapy in the mid-1990s.2,3 In San Francisco, a case-control study found MSM who took antiretrovirals were more likely than untreated MSM to acquire an STD after a diagnosis of AIDS.27 Optimism about treatment may have also led to changes in behavior among persons who were not infected. A study in Sydney found increases in reported unprotected anal intercourse with a casual partner (in the previous 6 months) for both HIV-infected men (35% in 1996 to 46% in 2000) and HIV-uninfected men (16% in 1996 to 27% in 2000).28 Other studies, including a meta-analysis, have found no evidence for changes in sexual activity after starting protease inhibitors.29,30 However, even if there were no changes in behavior of individuals, decreasing mortality from AIDS could have a large effect on syphilis and other STDs by increasing the survival (and thus the prevalence) of the most sexually active MSM.31,32
Changes in the approach to HIV-risk reduction among MSM may also be contributing to increases in syphilis. Early in the AIDS epidemic, MSM decreased their number of partners and increased condom use.5 These are strategies that reduced their risk for all STDs. However, now, increasingly, MSM are choosing other prevention strategies. Some choose partners who have the same HIV-infection status.5 This sorting based on serologic test results (sero-sorting) can reduce HIV risk while increasing the risk of other STDs. Others have switched from anal to oral sex, which may protect from HIV more than syphilis.18 Methamphetamine and Viagra use may also increase risk for some MSM.16 Thus, increases in syphilis may be caused by a combination of factors occurring in the community, including increases in sero-sorting, oral sex, drug use, disinhibition related to therapeutic advances, and longer lifespan of highly sexually active HIV-infected MSM. Rapid geographic dissemination of infection was probably facilitated by frequent travel and increasing use of the Internet to recruit sex partners.33 The ultimate size of the syphilis epidemic will depend on the number of MSM making these changes, and the extent of spread into other groups not currently at risk.
What Is the Syphilis Epidemic Telling Us About Other STDs and HIV?
There is some evidence that other STDs are also increasing among MSM. While gonorrhea rates fell among MSM soon after the onset of the AIDS epidemic, several areas noted increases in gonorrhea among MSM as the number of AIDS deaths declined in the late 1990s. Increases in gonorrhea among MSM have been reported from several areas. For example, cases of gonorrhea among MSM in the Denver Metro Health Clinic dropped from 1809 (in 1982) to 90 (in 1988) and 34 (in 1995).6 There has since been a slow increase up to 136 (in 2001). There was also an increase in visits by MSM in the time after HAART became available from 555 (7.2% of male visits in 1995) to 1088 (13.0% of male visits in 2001). Similar increases were noted using a variety of approaches in other areas.34,35
Nationally, gonorrhea surveillance is unable to track trends among MSM because sexual orientation is not reported. However, a system designed to track antimicrobial resistance in gonorrhea, the Gonococcal Isolate Surveillance Project (GISP) has obtained sexual orientation information from a sample of men with urethral gonorrhea in 29 clinics since 1992. Of 34,942 cases identified by GISP between 1992 and 1999, the proportion that were MSM increased from 4.5% in 1992 to 13.2% in 1999.7 Compared with heterosexuals, MSM were about 5 years older, were more often white, and more often had gonorrhea previously. Despite these disturbing trends identified in some studies, national surveillance shows relatively little impact of the increases in gonorrhea among MSM. Nationally, the decline in reported gonorrhea rates that began in the 1970s stopped in 1998.9 However, increases have occurred in women as well as men in many areas, and the male:female ratio has remained relatively stable at 1.0.
Trends in HIV infection are more difficult to track due to the long and variable incubation period. There is little doubt that some of these MSM with syphilis and HIV are transmitting HIV, and some previously HIV-uninfected men are acquiring syphilis and HIV at the same time. However, at the present time, their net contribution to HIV incidence in a community is not large. Estimates of the number of new infections have remained unchanged at about 40,000 per year over the last several years. There are a few reports of possible increases in some areas,36 while other areas have documented no change.37
The incidence of syphilis is lower than most other STD, so a small group of people could have a big effect on syphilis trends without having a noticeable impact on trends of other STDs even if everyone with syphilis also acquired gonorrhea and HIV. In 2002, in the United States there were reports of less than 7000 cases of primary and secondary syphilis,9 356,000 cases of gonorrhea,9 and an estimated 900,000 persons living with HIV.38 In New York City, there were 435 cases of primary and secondary syphilis,9 12,727 cases of gonorrhea,9 and an estimated 75,000 living with HIV.39 An additional 220 incident cases of each STD in New York City would produce a 50% increase in primary and secondary syphilis, a 1.7% increase in gonorrhea, and a 0.3% increase in the number of persons living with HIV.
Many poorly understood factors influence disease trends. Trends in syphilis, gonorrhea, and HIV infection have rarely moved in concert, even when monitored in fairly small and discrete groups.40,41 Certainly there were declines in the incidence of syphilis, gonorrhea, and HIV among MSM in the late 1980s and early 1990s, but this was a time marked by behavior changes that were extraordinary in scope, and by the deaths of the most sexually active persons in the community.31
At present, the epidemic appears to be concentrated in a small proportion of MSM who are likely to be HIV infected and report unprotected sex with many anonymous partners. If behavioral risk increases among other MSM, infection would likely follow. A key role for surveillance will be to detect any extension of this epidemic into these other groups. Detecting extension into “less risky” MSM will be difficult. An increase in cases among women would be easier to detect, so trends among women should be monitored.
We do not exactly know what is responsible for the continued decline in syphilis in the heterosexual populations targeted by the syphilis elimination campaign,42 but major decreases in syphilis have taken place, and rates continue to fall among women. Our challenge now is to have similar success with MSM. Many interventions appear to be working. They are described in the following papers.
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6.Rietmeijer CA, Patnaik JL, Judson FN, Douglas JM Jr. Increases in gonorrhea and sexual risk behaviors among men who have sex with men: a 12-year trend analysis at the Denver Metro Health Clinic. Sex Transm Dis 2003; 30:562–567.
7.Fox KK, del Rio C, Holmes KK, et al. Gonorrhea in the HIV era: a reversal in trends among men who have sex with men. Am J Public Health 2001; 91:959–964.
8.Nakashima AK, Rolfs RT, Flock ML, Kilmarx P, Greenspan JR. Epidemiology of syphilis in the United States, 1941–1993. Sex Transm Dis 1996; 23:16–23.
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9.Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance, 2002. Atlanta, GA: US Department of Health and Human Services, 2003.
10.Rolfs RT, Nakashima AK. Epidemiology of primary and secondary syphilis in the United States, 1981 through 1989. JAMA 1990; 264:1432–1437.
11.Rolfs RT, Goldberg M, Sharrar RG. Risk factors for syphilis: cocaine use and prostitution. Am J Public Health 1990; 80:853–857.
12.Holmberg SD. The estimated prevalence and incidence of HIV in 96 large US metropolitan areas. Am J Public Health 1996; 86:642–654.
13.Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance, 1998. Atlanta, GA: US Department of Health and Human Services, 1999.
14.Mansergh G, Colfax GN, Marks G, Rader M, Guzman R, Buchbinder S. The circuit party men’s health survey: findings and implications for gay and bisexual men. Am J Public Health 2001; 91:953–958.
15.D’Souza G, Lee JH, Paffel JM. Outbreak of syphilis among men who have sex with men in Houston, Texas. Sex Transm Dis 2003; 30:872–873.
16.Wong W, Chaw J, Kent C, Alpers L, Klausner J. Risk factors for early syphilis among men who have sex with men seen in an STD clinic, San Francisco 2002–2003. National STD Prevention Conference, Philadelphia, March 10, 2004. Abstract C02B.
17.Centers for Disease Control and Prevention. Outbreak of syphilis among men who have sex with men: Southern California, 2000. MMWR Morb Mortal Wkly Rep 2001; 50:117–120.
18.Centers for Disease Control and Prevention. Transmission of primary and secondary syphilis by oral sex: Chicago, IL. MMWR Morb Mortal Wkly Rep 2004; 53:966–968.
19.McLean C, Kaur A, Kerndt P, et al. Case-control study of risk factors for acquiring infectious syphilis among men who have sex with men: Presented at the International Congress of Sexually Transmitted Infections, ISSTDR/IUSTI, Berlin, June 24–27, 2001. J STD AIDS 2001; 12(suppl 2).
20.Bronzan R, Echavarria L, Hermida J, Trepka M, Burns T, Fox K. Syphilis among men who have sex with men in Miami-Dade County Florida. 2002 National STD Prevention Conference, March 4–7, San Diego CA. Abstract P135.
21.Paz-Bailey G, Meyers A, Blank S, et al. A case-control study of syphilis among men who have sex with men in New York City: association with HIV infection. Sex Transm Dis 2004; 31:581–587.
22.Communicable Disease Surveillance Centre. Sexually transmitted diseases quarterly report: syphilis in England and Wales. Commun Dis Rep CDR Wkly 1996; 7:192–194.
24.Stolte IG, Dukers NHTM, deWit JBF, Fennema JSA, Coutinho RA. Increase in sexually transmitted infections among homosexual men in Amsterdam in relation to HAART. Sex Transm Infect 2001; 77:184–186.
25.Nicoll A, Hamers F. Are trends in HIV, gonorrhoea, and syphilis worsening in Western Europe? BMJ 2002; 324:1324–1327.
26.Dupin N, Jdid R, N′Guyen Y-T, Gorin I, Franck N, Escande J-P. Syphilis and gonorrhoea in Paris: the return. AIDS 2001; 15:814–815.
27.Scheer S, Chu PL, Klausner JD, Katz MH, Schwarcz SK. Effect of highly active antiretroviral therapy on diagnoses of sexually transmitted diseases in people with AIDS. Lancet 2001; 357:432–435.
28.Van de Ven P, Prestage G, Crawford J, Grulich A, Kippax S. Sexual risk behavior increases and is associated with HIV optimism among HIV-negative and HIV-positive gay men in Sydney over the 4 year period to February 2000. AIDS 2000; 14:2951–2953.
29.Miller M, Meyer L, Boufassa F, et al, and the SEROCO Study Group. Sexual behavior changes and protease inhibitor therapy. AIDS 2000; 14:F33–F39.
30.Crepaz N, Hart TA, Marks G. Highly active antiretroviral therapy and sexual risk behavior: a meta-analytic review. JAMA 2004; 292:224–236.
31.Chesson HW, Dee TS, Aral SO. AIDS mortality may have contributed to the decline in syphilis rates in the United States in the 1990’s. Sex Transm Dis 2003; 30:419–424.
32.Boily M-C, Bastos FI, Desai K, Masse B. Changes in the transmission dynamics of the HIV epidemic after the wide-scale use of antiretroviral therapy could explain increases in sexually transmitted infections: results from mathematical models. Sex Transm Dis 2004; 31:100–113.
33.McFarlane M, Kachur R, Klausner JD, Roland E, Cohen M. Internet based health promotion and disease control in the 8 cities: successes, barriers, and future plans. Sex Transm Dis 2005; 32 (10) supplement:S60–S64.
34.Centers for Disease Control and Prevention. Increases in unsafe sex and rectal gonorrhea among men who have sex with men: San Francisco, CA 1994–1997. MMWR Morb Mortal Wkly Rep 1999; 48:45–48.
35.Centers for Disease Control and Prevention. Resurgent bacterial sexually transmitted diseases among men who have sex with men: King County, Washington 1997–1999. MMWR Morb Mortal Wkly Rep 1999; 48:773–777.
36.Centers for Disease Control and Prevention. Increases in HIV diagnoses in 29 states, 1999–2002. MMWR Morb Mortal Wkly Rep 2003; 52:1145–1148.
37.Centers for Disease Control and Prevention. Trends in primary and secondary syphilis and HIV infections in men who have sex with men: San Francisco and Los Angeles, California, 1998–2002. MMWR Morb Mortal Wkly Rep 2004; 53:575–578.
38.Fleming PL, Byers RH, Sweeney PA, Daniels D, Karon JM, Janssen RS. HIV prevalence in the United States, 2000. 9th
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