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HIV Diagnoses Among Men Who Have Sex With Men and Women—United States and 6 Dependent Areas, 2008-2011 Sonia Singh, PhD, MHS, Xiaohong Hu, MS, William Wheeler, MPH, and H. Irene Hall, PhD, MPH
Men who have sex with men (MSM) constitute the majority of persons diagnosed with HIV in the United States. In 2011, 61.8% of HIV diagnoses were attributed to male-to-male sexual contact.1 Data from the Center for Disease Control and Prevention’s (CDC) National HIV Surveillance System indicate that MSM are the only risk group with significant increases in HIV incidence in recent years,2 and reducing HIV incidence is one of the 3 primary goals in the National HIV/AIDS Strategy.3 Some MSM also have sex with women (MSMW). Scant information compared to MSM exists on the epidemiology of MSMW, who have the potential to bridge HIV transmission risk from MSM to women. Some studies have reported bisexual compared to heterosexual men are more likely to exchange sex, use substances, experience forced sex, and have more sexual partners.4,5 A meta-analysis estimated that MSMW are more than 5 times as likely to be HIVpositive as men who have sex with women exclusively.6 In a previous analysis of National HIV Surveillance System (NHSS) data derived from AIDS cases reported nationally from June 1981 through June 1990, MSMW constituted 26% of all males diagnosed with AIDS, increasing from 23% in 1983 to 26% in 1989. Racial/ethnic distributions for MSMW included 41% Black/African American, 31% Hispanic/Latino and 21% White.7 Because of the unique attributes and behaviors of MSMW, it is important to characterize this population to guide tailored prevention efforts. We described HIV diagnoses among MSMW using NHSS data from 2008 through 2011. In particular, we estimated numbers, percentages, and trends of HIV diagnoses among MSMW.
METHODS Data from the NHSS were used to estimate numbers and percentages of MSMW and men who have sex with men only (MSMO) aged 13 years and older diagnosed with HIV from
Objectives. We sought to describe HIV diagnoses among men who have sex with men and women (MSMW), who have the potential to bridge HIV transmission risk from men who have sex with men (MSM) to women. Methods. Applying National HIV Surveillance System data for persons aged 13 years and older, we examined estimated numbers and percentages of HIV diagnoses among MSMW and MSM only (MSMO) from 2008 to 2011, and estimated the annual percentage change and 95% confidence intervals, by age and race/ethnicity. Results. In 2011, 26.4% of 30 896 MSM diagnosed with HIV infection also had had sex with women. A larger percentage of MSMW were Black/African American (44.5%) compared with MSMO (36.0%), and fewer MSMW were White (26.4%) compared with MSMO (36.2%); similar percentages were classified as either MWMW or MSMO among other racial/ethnic groups. Among MSMW, HIV diagnoses were relatively stable and MSMO increased more than 6% annually among those aged 13 to 29 years. Conclusions. Many MSM diagnosed with HIV infection had also had sex with women. Intensified interventions are needed to decrease HIV infections overall for MSMW and reverse the increasing trends among young MSMO. (Am J Public Health. 2014;104:1700–1706. doi:10.2105/AJPH.2014.301990)
2008 to 2011. For these analyses, we used data reported to the CDC as of June 30, 2012 from all 50 states, the District of Columbia and 6 US dependent areas with fully implemented confidential name-based HIV infection reporting by April 2008.1 These 6 US dependent areas consist of American Samoa, Guam, the Northern Mariana Islands, Puerto Rico, the Republic of Palau, and the US Virgin Islands. These are newly diagnosed cases that have been reported to the NHSS. They represent all known newly diagnosed cases, although there may be other newly diagnosed cases that have not yet been reported. A diagnosis of HIV infection could occur at any stage of disease. The 50 states, the District of Columbia, and the 6 US dependent areas report to the CDC National HIV Reporting System (NHSS) data. Physicians, other health care providers, and laboratories report persons diagnosed with HIV infection to state and local health departments which in turn report data to the CDC. Data are collected on case report forms additionally by medical record abstraction and notification from partner services interviews.
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All data were collected as part of routine HIV surveillance and as mandated by federal, state or local laws or regulations, ethical review or approval for this analysis is waived.8,9 A MSMW was defined as a person who, at the time of HIV diagnosis, had a history of having sex with at least 1 male as well as a history of having had sex with at least 1 female. A MSMO was defined as a person who, at the time of HIV diagnosis, had a history of having sex with at least 1 male but not sex with a female. MSM comprised both MSMW and MSMO. MSM was defined as a person who, at the time of HIV diagnosis, had a history of either having sex with at least 1 male but not sex with a female or both sex with at least 1 male and sex with at least 1 female. We examined trends in reported HIV diagnoses with estimated numbers and percentages for 2008 and 2011, and estimated annual percentage change (EAPC) and 95% confidence intervals (CIs). Data were stratified by age at diagnosis, race/ethnicity (American Indian/ Alaska Native, Asian, Black/African American, Hispanic/Latino ethnicity [regardless of race], Native Hawaiian or other Pacific Islander,
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White, or multiple races), and year of HIV diagnosis. Data were adjusted for reporting delays and missing risk factor information but not for incomplete reporting.1,10 We determined concurrent diagnosis of HIV infection and stage 3 (AIDS). Concurrent diagnosis is defined as a diagnosis of stage 3 (AIDS) within 3 months of HIV diagnosis. We used a standardized Kaplan---Meier survival method to determine time to an AIDS diagnosis after receiving an HIV diagnosis from 1996 through 2009. Cases were followed through 2010. Estimates of the percentage of persons diagnosed with HIV who later had an AIDS diagnosis after one year and after 3 years were calculated by age at diagnosis, race/ethnicity, and year of diagnosis. For HIV surveillance, there is a presumed hierarchy for risk factor ascertainment that a specific risk factor is most likely responsible for transmission. The hierarchy gives priority to having sex with a male. Persons with more than 1 reported risk factor for HIV infection are classified in the transmission category first
listed in the hierarchy with the exception of MSM and intravenous drug use, which together constitute 1 category. Risk factor information is collected from medical records as well as notification during partner services interviews. It is possible that there is an underreporting of risk factors in the medical records. Furthermore, once a risk factor is identified during chart review, it is possible that no further inquiry is performed for additional risk factors such as sex with a female in addition to having sex with a male. To assess whether the MSMW risk factor is underestimated in HIV surveillance, we conducted an additional analysis applying selfreported risk factor information. Self-reported data from the Supplement to HIV/AIDS Surveillance (SHAS) Project for the years 2000 to 2004 including 9 states were used to adjust for diagnoses among MSMW. We determined the percentage of cases classified in SHAS as MSMW and MSMO that were classified differently in NHSS, regardless of stage of disease at diagnosis, and applied this distribution
to our case counts to explore potential underestimation.11 SHAS was an extension to the National HIV Surveillance System. It was a cross-sectional project to supplement behavioral surveillance data routinely collected in NHSS. Personal interviews were conducted for persons aged 18 years and older newly diagnosed with HIV. Participants were asked questions on sociodemographics, drug and alcohol use, sexual behavior, HIV diagnosis and treatment and use of social services. Details of the study’s recruitment, methods, and questionnaire are reported elsewhere.4,12 Data were collected in 13 states (Arizona, Colorado, Connecticut, Delaware, Florida, Georgia, Kansas, Michigan, Minnesota, New Jersey, New Mexico, South Carolina, and Washington) and Los Angeles County, representing a mixture of moderate and high HIV prevalence areas. Of these 13 states, 9 were conducting confidential, name-based HIV diagnosis reporting (Arizona, Colorado, Kansas, Michigan, Minnesota, New Jersey, New Mexico, and South Carolina) at the time of the project. At that time, from a national perspective, persons
TABLE 1—Estimated HIV Diagnoses and Estimated Annual Percentage Change (EAPC) Among MSMW and MSMO by Selected Characteristics: United States and 6 Dependent Areas, 2008–2011 MSMW Characteristic
Diagnosed in 2008, No. (%)
MSMO
Diagnosed in 2011, No. (%)
EAPC (95% CI)
Diagnosed in 2008, No. (%)
Diagnosed in 2011, No. (%)
EAPC (95% CI)
Age, y 13–19
466 (5.6)
387 (4.7)
–5.6 (–11.3, 0.6)
1050 (5.2)
1277 (5.6)
6.3 (2.2, 10.6)
20–24
1348 (16.2)
1421 (17.4)
1.5 (–2.2, 5.4)
3514 (17.5)
4933 (21.7)
12.3 (10.0, 14.7)
25–29 30–39
1229 (14.8) 2029 (24.4)
1263 (15.5) 1872 (23.0)
–0.3 (–4.5, 4.1) –3 (–6.5, 0.6)
3317 (16.6) 5239 (26.2)
4175 (18.4) 5241 (23.0)
7.0 (4.5, 9.5) –0.6 (–2.6, 1.4)
40–49
2020 (24.3)
1872 (23.0)
–3.4 (–7.2, 0.5)
4775 (23.8)
4594 (20.2)
–2.7 (–4.9, –0.5)
50–59
913 (11.0)
993 (12.2)
1.9 (–4.0, 8.1)
1652 (8.2)
1993 (8.8)
5.6 (1.7, 9.8)
‡ 60
304 (3.7)
341 (4.2)
3.9 (–6.8, 15.8)
484 (2.4)
535 (2.4)
2.8 (–5.1, 11.4) –1.5 (–14.4, 13.4)
Race/ethnicity American Indian/Alaska Native Asian Black/African American Hispanic/Latinoa Native Hawaiian/Other Pacific Islander White Multiple races Total
35 (0.4)
23 (0.3)
–8 (–25.9, 14.4)
96 (0.5)
96 (0.4)
154 (1.9)
194 (2.4)
5 (–6.7, 18.1)
427 (2.1)
511 (2.2)
3811 (45.9) 1956 (23.5)
3625 (44.5) 2004 (24.6)
–2.4 (–5.1, 0.4) 0.3 (–3.3, 4.1)
6816 (34.0) 4271 (21.3)
8185 (36.0) 5262 (23.1)
16 (0.2)
12 (0.1)
–11.5 (–33.6, 18.0)
42 (0.2)
49 (0.2)
2150 (25.9)
2149 (26.4)
–0.7 (–3.7, 2.4)
8057 (40.2)
8226 (36.2)
186 (2.2)
140 (1.7)
–8.2 (–18.4, 3.3)
8308 (100)
8148 (100)
–1.3 (–3.1, 0.5)
321 (1.6)
418 (1.8)
20 029 (100)
22 748 (100)
5.1 (–1.9, 12.6) 5.9 (4.0, 7.8) 6.2 (4.0, 8.5) 2.7 (–14.1, 22.8) 0.0 (–1.5, 1.5) 8.8 (1.0, 17.1) 3.6 (2.6, 4.7)
Note. CI = confidence interval; MSMO = men who have sex with men only; MSMW = men who have sex with men and women. The number of diagnoses was adjusted for reporting delays and missing risk factor information but not for incomplete reporting. Because column totals were calculated independently of the values for the subpopulations, the values in each column might not sum to the column total. The 6 US dependent areas were American Samoa, Guam, the Northern Mariana Islands, Puerto Rico, the Republic of Palau, and the US Virgin Islands. a Hispanic/Latino might be of any race.
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a
with AIDS from participating sites had a demographic profile that approximated the national profile of persons reported with AIDS. All analyses were conducted using SAS version 9.3 (SAS Institute, Cary, NC).
1400 -2.4 (-6.2, 1.5)
1200 1000 800 600 3.3 (-4.4, 11.6)
400 200
4.5 (-3.6, 13.4)
0
2008
2009
2010
2011
Year Black/African American Hispanic/Latino White
b 4000 3500
Number of Diagnoses
Of an estimated 50 007 persons aged 13 years and older diagnosed with HIV during 2011, 8148 (16.3%) were MSMW and 22 748 (45.5%) were MSMO. In 2011, among MSMW diagnosed with HIV, 4.7% were aged 13 to 19 years, 32.9% aged 20 to 29 years, 23.0% aged 30 to 39 years, 23.0% aged 40 to 49 years, 12.2% aged 50 to 59 years, and 4.2% aged 60 years and older (Table 1). A similar distribution of age at diagnosis was observed for MSMO. A larger percentage of MSMW were Black/African American (44.5%) compared with MSMO (36.0%), and fewer MSMW were White (26.4%) compared with MSMO (36.2%). By race, the proportion of new diagnoses among MSMW were as follows: 10.8% for American Indian/Alaska Native, 19.9% for Asian, 15.7% for Black/African American, 18.2% for Hispanic/Latino, 15.0% for Native Hawaiian/Other Pacific Islander, 15.6% for White, and 17.0% for multiple races. The most common facilities of diagnosis for MSMW were inpatient hospital (18.2%) and private physician’s office (17.0%). The most common facilities of diagnosis for MSMO were private physician’s office (22.8%) and inpatient hospital (13.5%). From 2008 to 2011, the number of diagnoses among MSMW was relatively stable over time, although for MSMO there was an increase (EAPC = 3.6; 95% CI = 2.6, 4.7; Table 1). For MSMO, increases were observed for those younger than 29 years and for those aged 50 to 59 years (EAPC = 5.6; 95% CI = 1.7, 9.8) while a decrease was observed for ages 40 to 49 years (EAPC = –2.7; 95% CI = –4.9, –0.5). Overall, for MSMW, there were no significant changes over time by race/ ethnicity, while for MSMO, there were increases for Blacks/African Americans (EAPC = 5.9; 95% CI = 4.0, 7.8), Hispanics/Latinos (EAPC = 6.2; 95% CI = 4.0, 8.5) and multiple races (EAPC = 8.8; 95% = 1.0, 17.1). From 2008 to 2011, among MSMW aged 13 to 24 years, the number of HIV diagnoses for all
Number of Diagnoses
RESULTS
3000 11.4 (8.7, 14.2)
2500 2000 1500 8.8 (4.6, 13.1)
1000 500 0
10.4 (5.9, 15.1)
2008
2010
2009
2011
Year Note. MSMO = men who have sex with men only; MSMW = men who have sex with men and women. The number of diagnoses was adjusted for reporting delays and missing risk factor information but not for incomplete reporting. Numbers in parentheses indicate 95% confidence intervals. The 6 US dependent areas were American Samoa, Guam, the Northern Mariana Islands, Puerto Rico, the Republic of Palau, and the US Virgin Islands. Hispanic/Latino might be of any race.
FIGURE 1—Estimated HIV diagnoses and estimated annual percentage change (EAPC) by race/ethnicity and year of diagnosis among 13- to 24-year-old (a) MSMW and (B) MSMO: United States and 6 dependent areas, 2008–2011
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races/ethnicities were relatively stable (Figure 1a). The number of diagnoses in 2011 in this age group was higher among Black/African American MSMW (1143) and Hispanic/Latino MSMW (348) than among White MSMW (251). For MSMO aged 13 to 24 years, increases were observed in Blacks/African Americans, Hispanics/Latinos, and Whites
(Figure 1b). The number of diagnoses in 2011 among Black/African American MSMO (3476) was higher than among Hispanic/Latino MSMO (1244) and White MSMO (1228). In 2010, 33.1% of MSMW and 24.4% of MSMO had a concurrent diagnosis of HIV infection and stage 3 (AIDS). Overall, MSMW had higher percentages of AIDS diagnosis after
HIV diagnosis within 1 year (40.6% vs 35.0%) and within 3 years (47.9% vs 41.1%) compared to MSMO (Table 2). At all age groups, MSMW had higher percentages of AIDS diagnosis after HIV diagnosis, both within 1 year and 3 years than MSMO. Black/African American, Hispanic/Latino, White, and multiple-race MSMW had higher percentages
TABLE 2—Percentages of MSMW and MSMO Who Receive a Diagnosis of AIDS 1 Year and 3 Years After Receiving Their Initial Diagnosis of HIV Infection by Selected Characteristics: United States and 6 Dependent Areas, 1996–2009 MSMW
Characteristic Age, y 13–19
MSMO
HIV Diagnosis, No. (%)
AIDS Diagnosis 1 Year After HIV Diagnosis, % (95% CI)
AIDS Diagnosis 3 Years After HIV Diagnosis, % (95% CI)
HIV Diagnosis, No. (%)
AIDS Diagnosis 1 Year After HIV Diagnosis, % (95% CI)
AIDS Diagnosis 3 Years After HIV Diagnosis, % (95% CI)
3020 (4.5)
18.1 (16.2, 20.1)
26.6 (24.4, 28.9)
5456 (3.4)
14.5 (13.0, 15.9)
21.4 (19.8, 23.0)
20–29
18 571 (27.5)
26.5 (25.9, 27.2)
34.5 (33.8, 35.2)
44 941 (27.9)
23.3 (22.9, 23.7)
30.3 (29.8, 30.7)
30–39
21 997 (32.6)
41.9 (41.2, 42.6)
49.2 (48.5, 50.0)
57 383 (35.6)
36.5 (36.1, 36.9)
42.5 (42.1, 42.9)
40–49
15 840 (23.5)
49.7 (48.9, 50.5)
56.5 (55.7, 57.3)
38 884 (24.1)
43.8 (43.3, 44.3)
49.1 (48.6, 49.6)
50–59
6005 (8.9)
56.9 (55.6, 58.2)
63.0 (61.7, 64.3)
11 724 (7.3)
47.9 (47.0, 48.9)
53.0 (52.0, 54.0)
‡ 60
2000 (3.0)
62.0 (59.8, 64.2)
67.1 (64.9, 69.3)
2842 (1.8)
53.1 (51.3, 55.0)
58.8 (56.9, 60.6)
343 (0.5) 642 (1.0)
39.3 (35.1, 43.5) 40.8 (37.5, 44.1)
51.5 (47.2, 55.8) 44.2 (40.9, 47.5)
659 (0.4) 2316 (1.4)
36.3 (33.0, 39.6) 33.7 (31.6, 35.8)
42.7 (39.4, 46.0) 40.2 (38.0, 42.4) 45.2 (44.7, 45.7)
Race/ethnicity American Indian/Alaska Native Asian Black/African American
30 045 (44.6)
40.0 (39.4, 40.5)
48.3 (47.7, 48.9)
43 689 (27.1)
38.4 (37.9, 38.9)
Hispanic/Latinoa
14 168 (21.0)
47.0 (46.2, 47.9)
53.8 (52.9, 54.6)
31 039 (19.3)
38.5 (37.9, 39.1)
44.7 (44.2, 45.3)
42.6 (38.8, 46.5)
56.7 (52.9, 60.4)
37.4 (33.3, 41.4)
44.1 (40.0, 48.1)
Native Hawaiian/Other Pacific Islander White
79 (0.1)
265 (0.2)
20 821 (30.9)
36.6 (35.9, 37.3)
42.7 (42.0, 43.4)
80 613 (50.0)
31.9 (31.6, 32.2)
37.5 (37.2, 37.9)
1325 (2.0)
40.6 (38.1, 43.1)
50.4 (47.8, 53.0)
2621 (1.6)
35.8 (34.0, 37.6)
43.3 (41.4, 45.1)
1996 1997
2413 (3.6) 2278 (3.4)
49.1 (47.0, 51.1) 46.6 (44.4, 48.7)
54.9 (52.8, 57.0) 51.9 (49.8, 54.1)
5269 (3.3) 4891 (3.0)
50.1 (48.6, 51.6) 46.1 (44.6, 47.7)
55.0 (53.5, 56.5) 50.7 (49.1, 52.3)
1998
3226 (4.8)
44.4 (42.6, 46.1)
49.9 (48.2, 51.7)
6232 (3.9)
43.4 (42.1, 44.6)
48.3 (47.0, 49.6)
1999
4167 (6.2)
43.5 (42.0, 44.9)
50.5 (49.0, 52.0)
7175 (4.5)
41.8 (40.6, 42.9)
47.1 (46.0, 48.3)
2000
4563 (6.8)
42.9 (41.5, 44.4)
50.2 (48.8, 51.7)
8350 (5.2)
39.9 (38.8, 40.9)
45.4 (44.4, 46.5)
2001
4999 (7.4)
40.9 (39.6, 42.3)
49.2 (47.8, 50.6)
10 682 (6.6)
35.9 (35.0, 36.8)
42.4 (41.5, 43.3)
2002
5133 (7.6)
40.1 (38.8, 41.4)
48.5 (47.2, 49.8)
11 140 (6.9)
34.8 (33.9, 35.6)
42.2 (41.3, 43.1)
2003
5586 (8.3)
42.2 (40.9, 43.4)
50.4 (49.1, 51.7)
13 527 (8.4)
37.0 (36.2, 37.8)
43.9 (43.1, 44.8)
2004 2005
5928 (8.8) 6022 (8.9)
41.1 (39.9, 42.3) 40.5 (39.3, 41.7)
48.0 (46.8, 49.3) 47.3 (46.1, 48.6)
14 726 (9.1) 15 175 (9.4)
35.1 (34.4, 35.9) 33.4 (32.6, 34.1)
41.8 (41.0, 42.6) 40.0 (39.2, 40.8)
2006
5946 (8.8)
38.7 (37.5, 39.9)
46.4 (45.1, 47.6)
15 637 (9.7)
31.8 (31.1, 32.5)
37.7 (37.0, 38.5)
2007
6003 (8.9)
36.8 (35.5, 38.0)
44.0 (42.7, 45.2)
16 241 (10.1)
29.3 (28.6, 30.0)
35.3 (34.6, 36.1)
2008
5672 (8.4)
37.0 (35.7, 38.3)
NA
16 305 (10.1)
29.6 (28.9, 30.3)
NA
2009
5497 (8.2)
35.1 (33.8, 36.4)
NA
15 880 (9.8)
30.3 (29.5, 31.0)
NA
Totalb
67 433 (100.0)
40.6 (40.2, 40.9)
47.9 (47.5, 48.3)
161 230 (100.0)
35.0 (34.8, 35.2)
41.1 (40.9, 41.4)
Multiple races Year of HIV diagnosis
Note. CI = confidence interval; MSMO = men who have sex with men only; MSMW = men who have sex with men and women; NA = not available. Data were not adjusted for reporting delays and reflect estimates of the probability that persons will have AIDS 1 year and 3 years after their initial HIV diagnosis, as determined by the standardized Kaplan–Meier method. The 6 US dependent areas were American Samoa, Guam, the Northern Mariana Islands, Puerto Rico, the Republic of Palau, and the US Virgin Islands. a Hispanic/Latino might be of any race. b Includes persons of unknown race/ethnicity.
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of AIDS diagnosis after HIV diagnosis within both 1 year and 3 years than MSMO. For Asians, MSMW had a higher percentage of AIDS diagnosis after HIV diagnosis within 1 year (40.8% vs 33.7%) than MSMO. For American Indian/Alaska Native (51.5% vs 42.7%) and Native Hawaiian/other Pacific Islander (56.7 vs 44.1%), MSMW had a higher percentage of AIDS diagnosis after HIV diagnosis within 3 years than MSMO. We conducted an additional analysis to determine whether the MSMW risk factor may be underreported in HIV surveillance. We reclassified males reported in NHSS as MSMW corresponding to the percentage in the NHSS-SHAS matched data set for NHSS MSMO that, according to SHAS, also had sex with women. We applied this correction for males diagnosed with HIV stratified by race/ethnicity to account for possible differences in underreporting across race/ethnicity categories. The number of diagnoses of MSMW and MSMO in the NHSS and the number of diagnoses adjusted by the distribution from the SHAS Project are shown in Table 3. Overall, comparing the NHSS data to the SHAS adjustment, the percentage of Black/African American, Hispanic/Latino, and White men who were MSMW increased: 30.7% to 74.7%, 25.1% to 65.1%, and 18.3% to 71.6%, respectively. For all racial/ethnic distributions, the number of diagnoses of MSMW for the SHAS-adjustment was more than 2.0 times that of NHSS.
DISCUSSION In 2011, MSM constituted the largest proportion (78.2%) of new HIV infections among adult and adolescent males diagnosed in the
United States, although they constituted an estimated 2.9% of the overall US male population aged 13 years and older.13 Of these, 26.4% were MSM who also had sex with women. For 2006 to 2010 data from the National Survey for Family Growth, among MSM, 43.9% identified as bisexual.14 HIV diagnoses increased among MSMO overall and were relatively stable for MSMW. Studies have shown that among MSMWs, less exclusive homosexual identification is associated with greater sexual risk behavior without disclosure with female partners.15 While overall decreases in HIV diagnoses have been observed among women during 2008 to 20111 and the magnitude of MSMW transmission is unknown, MSMW constitute a large percentage of persons with HIV and may require tailored prevention interventions. The National HIV/AIDS Strategy3 recommends intensifying HIV prevention efforts in communities where HIV is most heavily concentrated and targeting resources to gay and bisexual men, Blacks/African Americans, and Hispanics/Latinos. This includes effective communication strategies, expansion of HIV testing, and improved access to care and treatment services. CDC currently funds HIV prevention programs for young, minority MSM.16 Intensified interventions are needed to decrease HIV infections overall in MSMW who are less likely to identify with the MSM community and therefore may miss interventions traditionally targeted at MSM as well as reverse the increasing trends overall and particularly among young MSMO. Interventions should be tailored for MSMW and MSMO. As seen in our study, a larger percentage of MSMW were Black/ African American than MSMO. Additionally, for
MSMO, increases were observed for Black/ African American, Hispanics/Latinos, and multiple races. Interventions can be targeted specifically to these groups. MSMW interventions could also be targeted, for example, for those reporting using substances and sexual exchange which are reported more frequently than in heterosexuals and homosexuals.4,17 Furthermore, prevention efforts could address sexual behaviors such as unprotected vaginal intercourse as sex with a female may be perceived as less risky than sex with a male. CDC currently recommends routine annual testing for sexually active MSM aged 13 to 64 years.18 The percentage of undiagnosed HIV among MSM has been reported to be 25.7% for Blacks/African Americans, 22.9% for Hispanics/Latinos and 19.4% for Whites.19 In 2008, the National HIV Behavioral Surveillance System (NHBS) in 21 major US cities found that 18% of the MSM who identified themselves as bisexual tested positive for HIV. Of these, 63% were unaware of their status before testing.20 Such low awareness could be attributed to underestimating personal risk, fewer opportunities to get tested, or complacency that HIV treatment minimizes the impact of HIV disease. Persons unaware of their infection are 3.5 times as likely to transmit HIV than persons aware of their infection.21 Persons aware of their HIV infection can take steps to reduce risk behaviors, access medical care and treatment to improve length and quality of life, and reduce their infectiousness. Stronger efforts by HIV testing and prevention programs are necessary to ensure at least annual HIV testing for MSMW and to reach young and minority MSMO. Both MSMO and MSMW might also benefit from more
TABLE 3—Comparison of the Number of Diagnoses of MSMW and MSMO in the National HIV Surveillance System and the Number of Diagnoses Adjusted by the Supplement to the HIV/AIDS Surveillance Project by Race/Ethnicity: United States and 6 Dependent Areas, 2008–2011 NHSS
SHAS Adjustment
MSMW, No. (%)
MSMO, No. (%)
Total No.
MSMW, No. (%; 95% CI)
MSMO, No. (%; 95% CI)
Total No.
27 018
Race/ethnicity Black/African American
10 064 (30.7)
22 743 (69.3)
32 807
20 177 (74.7; 69.7, 79.7)
6841 (25.3; 20.3, 30.3)
Hispanic/Latinoa
5370 (25.1)
16 038 (74.9)
21 408
12 258 (65.1; 58.5, 71.7)
6577 (34.9; 28.3, 41.5)
18 835
White
6200 (18.3)
27 751 (81.7)
33 951
23 071 (71.6; 67.0, 76.3)
9131 (28.4; 23.7, 33.0)
32 202
Note. CI = confidence interval; MSMO = men who have sex with men only; MSMW = men who have sex with men and women; NHSS = National HIV Surveillance System; SHAS = Supplement to the HIV/AIDS Surveillance Project. The 6 US dependent areas were American Samoa, Guam, the Northern Mariana Islands, Puerto Rico, the Republic of Palau, and the US Virgin Islands. a Hispanic/Latino might be of any race.
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frequent testing, such as every 3 to 6 months for those with risk factors of multiple or anonymous partners or illicit drug use.22 The findings in this report are subject to limitations. First, uncertainty1 in the statistical adjustment procedures applied to HIV surveillance data to account for reporting delay could result in an overestimation or underestimation of these results; however, this uncertainty is unlikely to affect the age and racial/ethnic categories disproportionately. Second, true temporal proximity of sex with males and sex with females for the MSMW classification is unknown. A male is classified as MSMW if at the time of diagnosis, he reported having a sexual history including at least 1 male partner and at least 1 female partner. A male may be classified as MSMW if he had sex with a female only once at a young age and has had sex exclusively with males thereafter. It is not truly known what proportion of the MSMW fall in this category. Because of not knowing enough about MSMW and current surveillance practices, it is difficult to assess how large the present MSMW population is and the resulting prevention needs and efforts. Our additional analysis, however, indicates that HIV case surveillance data may be underestimating MSMW. Comparing the SHAS Project to NHSS, 59.7% of cases initially classified in the NHSS as MSM were reclassified as MSMW as a result of the information obtained from the SHAS interview.4 This underreporting could be attributed to nondisclosure of risk from stigma toward MSMW from both MSM and men who have sex with women. In a study of 2941 young gay, bisexual, and other men who have sex with men using data from the NHBS, 61.3% disclosed male---male sexual attraction or behavior to a provider.23 Additionally, because the hierarchy to assign transmission category gives higher priority to having sex with a male, medical chart abstractors may not collect risk information for sex with a female in addition to having sex with a male; therefore the number of men in this category may be underreported. Risk factor ascertainment has been declining in recent years. Completeness for risk factor information was 72%. Though these data are adjusted for missing risk factor information, these data may not reflect the true number of MSMW with new HIV diagnoses. Our comparison of NHSS and SHAS data indicates this may
be the case and the race/ethnicity distributions may be different. SHAS has some limitations. Participation in the interview was voluntary. Characteristics of those who chose not to participate may differ from those who participated in the interview. As the SHAS data may not be representative of all those diagnosed with HIV, application of SHAS data to NHSS data should be interpreted with caution. Finally, although the SHAS adjustment indicates a number of men may be misclassified as MSMO in NHSS, this should not be interpreted as the number of men engaging in sexual activity with both men and women near the time of their HIV diagnosis. The sexual activity timelines for NHSS and SHAS were very long; information about sexual activity proximal to HIV diagnosis would be required to infer risk of possible onward transmission of risk to women. Nonetheless, comparison of the SHAS and NHSS data indicates the possibility that MSMW are underestimated and a reassessment of prevention efforts targeting this population may be warranted. The National HIV/AIDS Strategy calls for the support and strengthening of HIV surveillance activities to identify those populations at greatest risk needing to be targeted for prevention services. Data from the NHSS in turn aid in monitoring the impact of the National HIV/ AIDS Strategy. These data demonstrate that MSMO and MSMW, especially among youths, remain key targets for prevention efforts for reducing HIV incidence and decreasing racial disparities, principally for Blacks/African Americans and Hispanics/Latinos. Reducing HIV risk behaviors and increasing access to testing and referral to health care are important interventions for MSMO and MSMW to achieve the goals of the National HIV/AIDS Strategy. Intensified interventions are needed to decrease HIV infections overall and reverse the increasing trends among young and older MSMO. Additionally, stronger HIV testing efforts are needed for all MSMW, particularly for Blacks/African Americans. j
About the Authors Sonia Singh, Xiaohong Hu, and H. Irene Hall are with the Division of HIV/AIDS Prevention, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, GA. William Wheeler is with the Division of Nutrition, Physical Activity and Obesity
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Prevention, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention. Correspondence should be sent to Sonia Singh, PhD, MHS, Division of HIV/AIDS Prevention, Centers for Disease Control and Prevention, 1600 Clifton Road NE, MS E-47, Atlanta, GA 30329 (e-mail: [email protected]). Reprints can be ordered at http://www.ajph.org by clicking the “Reprints” link. This article was accepted March 26, 2014. Note. The findings and conclusions in this study are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.
Contributors S. Singh and H. I. Hall developed the analysis plan and led data interpretation and the writing and editing. X. Hu contributed to the analysis plan and performed the analyses. W. Wheeler contributed to the analysis plan, data interpretation, and the writing and editing.
Acknowledgments The authors acknowledge Patrick Sullivan who served as primary thesis advisor for William Wheeler’s master’s thesis, the foundation for this work.
Human Participant Protection This study used data collected as part of routine public health surveillance. It has been determined that public health surveillance is not research. No protocol approval was needed for this study.
References 1. Centers for Disease Control and Prevention. HIV Surveillance Report, 2011. 2013;23. Available at: http:// www.cdc.gov/hiv/surveillance/resources/reports/ 2011report/index.htm. Accessed August 2, 2013. 2. Centers for Disease Control and Prevention. Estimated HIV incidence in the United States, 2007---2010. HIV Surveillance Supplemental Report 2012;17(No. 4). Available at: http://www.cdc.gov/hiv/topics/ surveillance/resources/reports/#supplemental. Accessed August 12, 2013. 3. Office of National AIDS Policy. National HIV/AIDS Strategy for the United States. Available at: http://www. whitehouse.gov/administration/eop/onap/nhas. Accessed October 19, 2012. 4. Spikes PS, Purcell DW, Williams KM, Chen Y, Ding H, Sullivan PS. Sexual risk behaviors among HIV-positive Black men who have sex with women, with men, or with men and women: Implications for intervention development. Am J Public Health. 2009;99:1072---1078. 5. Jeffries WL IV. The number of recent sex partners among bisexual men in the United States. Perspect Sex Reprod Health. 2011;43(3):151---157. 6. Friedman MR, Wei C, Klem ML, Silvestre AJ, Markovic N, Stall R. HIV infection and sexual risk among men who have sex with men and women (MSMW): a systematic review and meta-analysis. PLoS ONE. 2014;9(1):e87139. 7. Chu SY, Peterman TA, Doll LS, Buehler JW, Curran JW. AIDS in bisexual men in the United States: epidemiology and transmission to women. Am J Public Health. 1992;82:220---224.
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8. Department of Health and Human Services. Protection of human subjects, 45 CFR §46 (1974). 9. Centers for Disease Control and Prevention. Distinguishing Public Health Research and Public Health Nonresearch. Available at: http://www.cdc.gov/od/ science/integrity/docs/cdc-policy-distinguishing-publichealth-research-nonresearch.pdf. Accessed August 12, 2013. 10. Harrison KM, Kajese T, Hall HI, Song R. Risk factor redistribution of the national HIV/AIDS surveillance data: an alternative approach. Public Health Rep. 2008;123:618---627. 11. Wheeler W. Men Who Have Sex With Men and Women Among Men With Newly Diagnosed HIV Infections in the United States, 2001-2005 [master’s thesis]. Atlanta, GA: Rollins School of Public Health, Emory University; 2007. 12. Buehler JW, Diaz T, Hersh BS, Chu SY. The supplement to HIV-AIDS Surveillance project: an approach for monitoring HIV risk behaviors. Public Health Rep. 1996;111(suppl 1):133---137. 13. Purcell DW, Johnson CH, Lansky A, et al. Estimating the population size of men who have sex with men in the United States to obtain HIV and syphilis rates. Open AIDS J. 2012;6:98---107. 14. Chandra A, Mosher WD, Copen C, Sionean C. Sexual Behavior, Sexual Attraction, and Sexual Identity in the United States: Data From the 2006-2008 National Survey of Family Growth. National Health Statistics Reports; No. 36. Hyattsville, MD: National Center for Health Statistics; 2011. 15. Mutchler MG, Bogart LM, Elliott MN, et al. Psychosocial correlates of unprotected sex without disclosure of HIV-positivity among African-American, Latino, and White men who have sex with men and women. Arch Sex Behav. 2008;37(5):736---747. 16. Centers for Disease Control and Prevention. Available at: http://www.cdc.gov/msmhealth/msm-programs. htm. Accessed October 19, 2012. 17. Friedman MR, Kurtz SP, Buttram ME, et al. HIV risk among substance-using men who have sex with men and women (MSMW): findings from south Florida. AIDS Behav. 2014;18:111---119. 18. Branson BM, Handsfield HH, Lampe MA, et al. Revised recommendations for HIV testing of adults, adolescents and pregnant women in health-care settings. MMWR Morb Mortal Wkly Rep. 2006;55(no. RR-14):1---17. 19. Chen M, Rhodes PH, Hall IH, et al. Prevalence of undiagnosed HIV infection among persons aged ‡13 years — National HIV Surveillance System, United States, 2005---2008. MMWR Morb Mortal Wkly Rep. 2012;61: 57---64. 20. Centers for Disease Control and Prevention. Prevalence and awareness of HIV infection among men who have sex with men—21 cities, United States, 2008. MMWR Morb Mortal Wkly Rep. 2010;59(37):1201---1207. 21. Marks G, Crepaz N, Janssen RS. Estimating sexual transmission of HIV from persons aware and unaware that they are infected with the virus in the USA. AIDS. 2006;20:1447---1450. 22. Workowski KA, Bauer H, Bachman L, et al. Sexually transmitted disease treatment guidelines, 2010. MMMR Morb Mortal Wkly Rep. 2010;59(No. RR-12):1---110 . 23. Meites E, Krishna NK, Markowitz LE, Oster AM. Health care use and opportunities for human papillomavirus vaccination among young men who have sex with men. Sex Transm Dis. 2013;40(2):154---157.
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HIV Diagnoses Among Men Who Have Sex With Men and Women—United States and 6 Dependent Areas, 2008-2011 Sonia Singh, PhD, MHS, Xiaohong Hu, MS, William Wheeler, MPH, and H. Irene Hall, PhD, MPH
Men who have sex with men (MSM) constitute the majority of persons diagnosed with HIV in the United States. In 2011, 61.8% of HIV diagnoses were attributed to male-to-male sexual contact.1 Data from the Center for Disease Control and Prevention’s (CDC) National HIV Surveillance System indicate that MSM are the only risk group with significant increases in HIV incidence in recent years,2 and reducing HIV incidence is one of the 3 primary goals in the National HIV/AIDS Strategy.3 Some MSM also have sex with women (MSMW). Scant information compared to MSM exists on the epidemiology of MSMW, who have the potential to bridge HIV transmission risk from MSM to women. Some studies have reported bisexual compared to heterosexual men are more likely to exchange sex, use substances, experience forced sex, and have more sexual partners.4,5 A meta-analysis estimated that MSMW are more than 5 times as likely to be HIVpositive as men who have sex with women exclusively.6 In a previous analysis of National HIV Surveillance System (NHSS) data derived from AIDS cases reported nationally from June 1981 through June 1990, MSMW constituted 26% of all males diagnosed with AIDS, increasing from 23% in 1983 to 26% in 1989. Racial/ethnic distributions for MSMW included 41% Black/African American, 31% Hispanic/Latino and 21% White.7 Because of the unique attributes and behaviors of MSMW, it is important to characterize this population to guide tailored prevention efforts. We described HIV diagnoses among MSMW using NHSS data from 2008 through 2011. In particular, we estimated numbers, percentages, and trends of HIV diagnoses among MSMW.
METHODS Data from the NHSS were used to estimate numbers and percentages of MSMW and men who have sex with men only (MSMO) aged 13 years and older diagnosed with HIV from
Objectives. We sought to describe HIV diagnoses among men who have sex with men and women (MSMW), who have the potential to bridge HIV transmission risk from men who have sex with men (MSM) to women. Methods. Applying National HIV Surveillance System data for persons aged 13 years and older, we examined estimated numbers and percentages of HIV diagnoses among MSMW and MSM only (MSMO) from 2008 to 2011, and estimated the annual percentage change and 95% confidence intervals, by age and race/ethnicity. Results. In 2011, 26.4% of 30 896 MSM diagnosed with HIV infection also had had sex with women. A larger percentage of MSMW were Black/African American (44.5%) compared with MSMO (36.0%), and fewer MSMW were White (26.4%) compared with MSMO (36.2%); similar percentages were classified as either MWMW or MSMO among other racial/ethnic groups. Among MSMW, HIV diagnoses were relatively stable and MSMO increased more than 6% annually among those aged 13 to 29 years. Conclusions. Many MSM diagnosed with HIV infection had also had sex with women. Intensified interventions are needed to decrease HIV infections overall for MSMW and reverse the increasing trends among young MSMO. (Am J Public Health. 2014;104:1700–1706. doi:10.2105/AJPH.2014.301990)
2008 to 2011. For these analyses, we used data reported to the CDC as of June 30, 2012 from all 50 states, the District of Columbia and 6 US dependent areas with fully implemented confidential name-based HIV infection reporting by April 2008.1 These 6 US dependent areas consist of American Samoa, Guam, the Northern Mariana Islands, Puerto Rico, the Republic of Palau, and the US Virgin Islands. These are newly diagnosed cases that have been reported to the NHSS. They represent all known newly diagnosed cases, although there may be other newly diagnosed cases that have not yet been reported. A diagnosis of HIV infection could occur at any stage of disease. The 50 states, the District of Columbia, and the 6 US dependent areas report to the CDC National HIV Reporting System (NHSS) data. Physicians, other health care providers, and laboratories report persons diagnosed with HIV infection to state and local health departments which in turn report data to the CDC. Data are collected on case report forms additionally by medical record abstraction and notification from partner services interviews.
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All data were collected as part of routine HIV surveillance and as mandated by federal, state or local laws or regulations, ethical review or approval for this analysis is waived.8,9 A MSMW was defined as a person who, at the time of HIV diagnosis, had a history of having sex with at least 1 male as well as a history of having had sex with at least 1 female. A MSMO was defined as a person who, at the time of HIV diagnosis, had a history of having sex with at least 1 male but not sex with a female. MSM comprised both MSMW and MSMO. MSM was defined as a person who, at the time of HIV diagnosis, had a history of either having sex with at least 1 male but not sex with a female or both sex with at least 1 male and sex with at least 1 female. We examined trends in reported HIV diagnoses with estimated numbers and percentages for 2008 and 2011, and estimated annual percentage change (EAPC) and 95% confidence intervals (CIs). Data were stratified by age at diagnosis, race/ethnicity (American Indian/ Alaska Native, Asian, Black/African American, Hispanic/Latino ethnicity [regardless of race], Native Hawaiian or other Pacific Islander,
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White, or multiple races), and year of HIV diagnosis. Data were adjusted for reporting delays and missing risk factor information but not for incomplete reporting.1,10 We determined concurrent diagnosis of HIV infection and stage 3 (AIDS). Concurrent diagnosis is defined as a diagnosis of stage 3 (AIDS) within 3 months of HIV diagnosis. We used a standardized Kaplan---Meier survival method to determine time to an AIDS diagnosis after receiving an HIV diagnosis from 1996 through 2009. Cases were followed through 2010. Estimates of the percentage of persons diagnosed with HIV who later had an AIDS diagnosis after one year and after 3 years were calculated by age at diagnosis, race/ethnicity, and year of diagnosis. For HIV surveillance, there is a presumed hierarchy for risk factor ascertainment that a specific risk factor is most likely responsible for transmission. The hierarchy gives priority to having sex with a male. Persons with more than 1 reported risk factor for HIV infection are classified in the transmission category first
listed in the hierarchy with the exception of MSM and intravenous drug use, which together constitute 1 category. Risk factor information is collected from medical records as well as notification during partner services interviews. It is possible that there is an underreporting of risk factors in the medical records. Furthermore, once a risk factor is identified during chart review, it is possible that no further inquiry is performed for additional risk factors such as sex with a female in addition to having sex with a male. To assess whether the MSMW risk factor is underestimated in HIV surveillance, we conducted an additional analysis applying selfreported risk factor information. Self-reported data from the Supplement to HIV/AIDS Surveillance (SHAS) Project for the years 2000 to 2004 including 9 states were used to adjust for diagnoses among MSMW. We determined the percentage of cases classified in SHAS as MSMW and MSMO that were classified differently in NHSS, regardless of stage of disease at diagnosis, and applied this distribution
to our case counts to explore potential underestimation.11 SHAS was an extension to the National HIV Surveillance System. It was a cross-sectional project to supplement behavioral surveillance data routinely collected in NHSS. Personal interviews were conducted for persons aged 18 years and older newly diagnosed with HIV. Participants were asked questions on sociodemographics, drug and alcohol use, sexual behavior, HIV diagnosis and treatment and use of social services. Details of the study’s recruitment, methods, and questionnaire are reported elsewhere.4,12 Data were collected in 13 states (Arizona, Colorado, Connecticut, Delaware, Florida, Georgia, Kansas, Michigan, Minnesota, New Jersey, New Mexico, South Carolina, and Washington) and Los Angeles County, representing a mixture of moderate and high HIV prevalence areas. Of these 13 states, 9 were conducting confidential, name-based HIV diagnosis reporting (Arizona, Colorado, Kansas, Michigan, Minnesota, New Jersey, New Mexico, and South Carolina) at the time of the project. At that time, from a national perspective, persons
TABLE 1—Estimated HIV Diagnoses and Estimated Annual Percentage Change (EAPC) Among MSMW and MSMO by Selected Characteristics: United States and 6 Dependent Areas, 2008–2011 MSMW Characteristic
Diagnosed in 2008, No. (%)
MSMO
Diagnosed in 2011, No. (%)
EAPC (95% CI)
Diagnosed in 2008, No. (%)
Diagnosed in 2011, No. (%)
EAPC (95% CI)
Age, y 13–19
466 (5.6)
387 (4.7)
–5.6 (–11.3, 0.6)
1050 (5.2)
1277 (5.6)
6.3 (2.2, 10.6)
20–24
1348 (16.2)
1421 (17.4)
1.5 (–2.2, 5.4)
3514 (17.5)
4933 (21.7)
12.3 (10.0, 14.7)
25–29 30–39
1229 (14.8) 2029 (24.4)
1263 (15.5) 1872 (23.0)
–0.3 (–4.5, 4.1) –3 (–6.5, 0.6)
3317 (16.6) 5239 (26.2)
4175 (18.4) 5241 (23.0)
7.0 (4.5, 9.5) –0.6 (–2.6, 1.4)
40–49
2020 (24.3)
1872 (23.0)
–3.4 (–7.2, 0.5)
4775 (23.8)
4594 (20.2)
–2.7 (–4.9, –0.5)
50–59
913 (11.0)
993 (12.2)
1.9 (–4.0, 8.1)
1652 (8.2)
1993 (8.8)
5.6 (1.7, 9.8)
‡ 60
304 (3.7)
341 (4.2)
3.9 (–6.8, 15.8)
484 (2.4)
535 (2.4)
2.8 (–5.1, 11.4) –1.5 (–14.4, 13.4)
Race/ethnicity American Indian/Alaska Native Asian Black/African American Hispanic/Latinoa Native Hawaiian/Other Pacific Islander White Multiple races Total
35 (0.4)
23 (0.3)
–8 (–25.9, 14.4)
96 (0.5)
96 (0.4)
154 (1.9)
194 (2.4)
5 (–6.7, 18.1)
427 (2.1)
511 (2.2)
3811 (45.9) 1956 (23.5)
3625 (44.5) 2004 (24.6)
–2.4 (–5.1, 0.4) 0.3 (–3.3, 4.1)
6816 (34.0) 4271 (21.3)
8185 (36.0) 5262 (23.1)
16 (0.2)
12 (0.1)
–11.5 (–33.6, 18.0)
42 (0.2)
49 (0.2)
2150 (25.9)
2149 (26.4)
–0.7 (–3.7, 2.4)
8057 (40.2)
8226 (36.2)
186 (2.2)
140 (1.7)
–8.2 (–18.4, 3.3)
8308 (100)
8148 (100)
–1.3 (–3.1, 0.5)
321 (1.6)
418 (1.8)
20 029 (100)
22 748 (100)
5.1 (–1.9, 12.6) 5.9 (4.0, 7.8) 6.2 (4.0, 8.5) 2.7 (–14.1, 22.8) 0.0 (–1.5, 1.5) 8.8 (1.0, 17.1) 3.6 (2.6, 4.7)
Note. CI = confidence interval; MSMO = men who have sex with men only; MSMW = men who have sex with men and women. The number of diagnoses was adjusted for reporting delays and missing risk factor information but not for incomplete reporting. Because column totals were calculated independently of the values for the subpopulations, the values in each column might not sum to the column total. The 6 US dependent areas were American Samoa, Guam, the Northern Mariana Islands, Puerto Rico, the Republic of Palau, and the US Virgin Islands. a Hispanic/Latino might be of any race.
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a
with AIDS from participating sites had a demographic profile that approximated the national profile of persons reported with AIDS. All analyses were conducted using SAS version 9.3 (SAS Institute, Cary, NC).
1400 -2.4 (-6.2, 1.5)
1200 1000 800 600 3.3 (-4.4, 11.6)
400 200
4.5 (-3.6, 13.4)
0
2008
2009
2010
2011
Year Black/African American Hispanic/Latino White
b 4000 3500
Number of Diagnoses
Of an estimated 50 007 persons aged 13 years and older diagnosed with HIV during 2011, 8148 (16.3%) were MSMW and 22 748 (45.5%) were MSMO. In 2011, among MSMW diagnosed with HIV, 4.7% were aged 13 to 19 years, 32.9% aged 20 to 29 years, 23.0% aged 30 to 39 years, 23.0% aged 40 to 49 years, 12.2% aged 50 to 59 years, and 4.2% aged 60 years and older (Table 1). A similar distribution of age at diagnosis was observed for MSMO. A larger percentage of MSMW were Black/African American (44.5%) compared with MSMO (36.0%), and fewer MSMW were White (26.4%) compared with MSMO (36.2%). By race, the proportion of new diagnoses among MSMW were as follows: 10.8% for American Indian/Alaska Native, 19.9% for Asian, 15.7% for Black/African American, 18.2% for Hispanic/Latino, 15.0% for Native Hawaiian/Other Pacific Islander, 15.6% for White, and 17.0% for multiple races. The most common facilities of diagnosis for MSMW were inpatient hospital (18.2%) and private physician’s office (17.0%). The most common facilities of diagnosis for MSMO were private physician’s office (22.8%) and inpatient hospital (13.5%). From 2008 to 2011, the number of diagnoses among MSMW was relatively stable over time, although for MSMO there was an increase (EAPC = 3.6; 95% CI = 2.6, 4.7; Table 1). For MSMO, increases were observed for those younger than 29 years and for those aged 50 to 59 years (EAPC = 5.6; 95% CI = 1.7, 9.8) while a decrease was observed for ages 40 to 49 years (EAPC = –2.7; 95% CI = –4.9, –0.5). Overall, for MSMW, there were no significant changes over time by race/ ethnicity, while for MSMO, there were increases for Blacks/African Americans (EAPC = 5.9; 95% CI = 4.0, 7.8), Hispanics/Latinos (EAPC = 6.2; 95% CI = 4.0, 8.5) and multiple races (EAPC = 8.8; 95% = 1.0, 17.1). From 2008 to 2011, among MSMW aged 13 to 24 years, the number of HIV diagnoses for all
Number of Diagnoses
RESULTS
3000 11.4 (8.7, 14.2)
2500 2000 1500 8.8 (4.6, 13.1)
1000 500 0
10.4 (5.9, 15.1)
2008
2010
2009
2011
Year Note. MSMO = men who have sex with men only; MSMW = men who have sex with men and women. The number of diagnoses was adjusted for reporting delays and missing risk factor information but not for incomplete reporting. Numbers in parentheses indicate 95% confidence intervals. The 6 US dependent areas were American Samoa, Guam, the Northern Mariana Islands, Puerto Rico, the Republic of Palau, and the US Virgin Islands. Hispanic/Latino might be of any race.
FIGURE 1—Estimated HIV diagnoses and estimated annual percentage change (EAPC) by race/ethnicity and year of diagnosis among 13- to 24-year-old (a) MSMW and (B) MSMO: United States and 6 dependent areas, 2008–2011
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races/ethnicities were relatively stable (Figure 1a). The number of diagnoses in 2011 in this age group was higher among Black/African American MSMW (1143) and Hispanic/Latino MSMW (348) than among White MSMW (251). For MSMO aged 13 to 24 years, increases were observed in Blacks/African Americans, Hispanics/Latinos, and Whites
(Figure 1b). The number of diagnoses in 2011 among Black/African American MSMO (3476) was higher than among Hispanic/Latino MSMO (1244) and White MSMO (1228). In 2010, 33.1% of MSMW and 24.4% of MSMO had a concurrent diagnosis of HIV infection and stage 3 (AIDS). Overall, MSMW had higher percentages of AIDS diagnosis after
HIV diagnosis within 1 year (40.6% vs 35.0%) and within 3 years (47.9% vs 41.1%) compared to MSMO (Table 2). At all age groups, MSMW had higher percentages of AIDS diagnosis after HIV diagnosis, both within 1 year and 3 years than MSMO. Black/African American, Hispanic/Latino, White, and multiple-race MSMW had higher percentages
TABLE 2—Percentages of MSMW and MSMO Who Receive a Diagnosis of AIDS 1 Year and 3 Years After Receiving Their Initial Diagnosis of HIV Infection by Selected Characteristics: United States and 6 Dependent Areas, 1996–2009 MSMW
Characteristic Age, y 13–19
MSMO
HIV Diagnosis, No. (%)
AIDS Diagnosis 1 Year After HIV Diagnosis, % (95% CI)
AIDS Diagnosis 3 Years After HIV Diagnosis, % (95% CI)
HIV Diagnosis, No. (%)
AIDS Diagnosis 1 Year After HIV Diagnosis, % (95% CI)
AIDS Diagnosis 3 Years After HIV Diagnosis, % (95% CI)
3020 (4.5)
18.1 (16.2, 20.1)
26.6 (24.4, 28.9)
5456 (3.4)
14.5 (13.0, 15.9)
21.4 (19.8, 23.0)
20–29
18 571 (27.5)
26.5 (25.9, 27.2)
34.5 (33.8, 35.2)
44 941 (27.9)
23.3 (22.9, 23.7)
30.3 (29.8, 30.7)
30–39
21 997 (32.6)
41.9 (41.2, 42.6)
49.2 (48.5, 50.0)
57 383 (35.6)
36.5 (36.1, 36.9)
42.5 (42.1, 42.9)
40–49
15 840 (23.5)
49.7 (48.9, 50.5)
56.5 (55.7, 57.3)
38 884 (24.1)
43.8 (43.3, 44.3)
49.1 (48.6, 49.6)
50–59
6005 (8.9)
56.9 (55.6, 58.2)
63.0 (61.7, 64.3)
11 724 (7.3)
47.9 (47.0, 48.9)
53.0 (52.0, 54.0)
‡ 60
2000 (3.0)
62.0 (59.8, 64.2)
67.1 (64.9, 69.3)
2842 (1.8)
53.1 (51.3, 55.0)
58.8 (56.9, 60.6)
343 (0.5) 642 (1.0)
39.3 (35.1, 43.5) 40.8 (37.5, 44.1)
51.5 (47.2, 55.8) 44.2 (40.9, 47.5)
659 (0.4) 2316 (1.4)
36.3 (33.0, 39.6) 33.7 (31.6, 35.8)
42.7 (39.4, 46.0) 40.2 (38.0, 42.4) 45.2 (44.7, 45.7)
Race/ethnicity American Indian/Alaska Native Asian Black/African American
30 045 (44.6)
40.0 (39.4, 40.5)
48.3 (47.7, 48.9)
43 689 (27.1)
38.4 (37.9, 38.9)
Hispanic/Latinoa
14 168 (21.0)
47.0 (46.2, 47.9)
53.8 (52.9, 54.6)
31 039 (19.3)
38.5 (37.9, 39.1)
44.7 (44.2, 45.3)
42.6 (38.8, 46.5)
56.7 (52.9, 60.4)
37.4 (33.3, 41.4)
44.1 (40.0, 48.1)
Native Hawaiian/Other Pacific Islander White
79 (0.1)
265 (0.2)
20 821 (30.9)
36.6 (35.9, 37.3)
42.7 (42.0, 43.4)
80 613 (50.0)
31.9 (31.6, 32.2)
37.5 (37.2, 37.9)
1325 (2.0)
40.6 (38.1, 43.1)
50.4 (47.8, 53.0)
2621 (1.6)
35.8 (34.0, 37.6)
43.3 (41.4, 45.1)
1996 1997
2413 (3.6) 2278 (3.4)
49.1 (47.0, 51.1) 46.6 (44.4, 48.7)
54.9 (52.8, 57.0) 51.9 (49.8, 54.1)
5269 (3.3) 4891 (3.0)
50.1 (48.6, 51.6) 46.1 (44.6, 47.7)
55.0 (53.5, 56.5) 50.7 (49.1, 52.3)
1998
3226 (4.8)
44.4 (42.6, 46.1)
49.9 (48.2, 51.7)
6232 (3.9)
43.4 (42.1, 44.6)
48.3 (47.0, 49.6)
1999
4167 (6.2)
43.5 (42.0, 44.9)
50.5 (49.0, 52.0)
7175 (4.5)
41.8 (40.6, 42.9)
47.1 (46.0, 48.3)
2000
4563 (6.8)
42.9 (41.5, 44.4)
50.2 (48.8, 51.7)
8350 (5.2)
39.9 (38.8, 40.9)
45.4 (44.4, 46.5)
2001
4999 (7.4)
40.9 (39.6, 42.3)
49.2 (47.8, 50.6)
10 682 (6.6)
35.9 (35.0, 36.8)
42.4 (41.5, 43.3)
2002
5133 (7.6)
40.1 (38.8, 41.4)
48.5 (47.2, 49.8)
11 140 (6.9)
34.8 (33.9, 35.6)
42.2 (41.3, 43.1)
2003
5586 (8.3)
42.2 (40.9, 43.4)
50.4 (49.1, 51.7)
13 527 (8.4)
37.0 (36.2, 37.8)
43.9 (43.1, 44.8)
2004 2005
5928 (8.8) 6022 (8.9)
41.1 (39.9, 42.3) 40.5 (39.3, 41.7)
48.0 (46.8, 49.3) 47.3 (46.1, 48.6)
14 726 (9.1) 15 175 (9.4)
35.1 (34.4, 35.9) 33.4 (32.6, 34.1)
41.8 (41.0, 42.6) 40.0 (39.2, 40.8)
2006
5946 (8.8)
38.7 (37.5, 39.9)
46.4 (45.1, 47.6)
15 637 (9.7)
31.8 (31.1, 32.5)
37.7 (37.0, 38.5)
2007
6003 (8.9)
36.8 (35.5, 38.0)
44.0 (42.7, 45.2)
16 241 (10.1)
29.3 (28.6, 30.0)
35.3 (34.6, 36.1)
2008
5672 (8.4)
37.0 (35.7, 38.3)
NA
16 305 (10.1)
29.6 (28.9, 30.3)
NA
2009
5497 (8.2)
35.1 (33.8, 36.4)
NA
15 880 (9.8)
30.3 (29.5, 31.0)
NA
Totalb
67 433 (100.0)
40.6 (40.2, 40.9)
47.9 (47.5, 48.3)
161 230 (100.0)
35.0 (34.8, 35.2)
41.1 (40.9, 41.4)
Multiple races Year of HIV diagnosis
Note. CI = confidence interval; MSMO = men who have sex with men only; MSMW = men who have sex with men and women; NA = not available. Data were not adjusted for reporting delays and reflect estimates of the probability that persons will have AIDS 1 year and 3 years after their initial HIV diagnosis, as determined by the standardized Kaplan–Meier method. The 6 US dependent areas were American Samoa, Guam, the Northern Mariana Islands, Puerto Rico, the Republic of Palau, and the US Virgin Islands. a Hispanic/Latino might be of any race. b Includes persons of unknown race/ethnicity.
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of AIDS diagnosis after HIV diagnosis within both 1 year and 3 years than MSMO. For Asians, MSMW had a higher percentage of AIDS diagnosis after HIV diagnosis within 1 year (40.8% vs 33.7%) than MSMO. For American Indian/Alaska Native (51.5% vs 42.7%) and Native Hawaiian/other Pacific Islander (56.7 vs 44.1%), MSMW had a higher percentage of AIDS diagnosis after HIV diagnosis within 3 years than MSMO. We conducted an additional analysis to determine whether the MSMW risk factor may be underreported in HIV surveillance. We reclassified males reported in NHSS as MSMW corresponding to the percentage in the NHSS-SHAS matched data set for NHSS MSMO that, according to SHAS, also had sex with women. We applied this correction for males diagnosed with HIV stratified by race/ethnicity to account for possible differences in underreporting across race/ethnicity categories. The number of diagnoses of MSMW and MSMO in the NHSS and the number of diagnoses adjusted by the distribution from the SHAS Project are shown in Table 3. Overall, comparing the NHSS data to the SHAS adjustment, the percentage of Black/African American, Hispanic/Latino, and White men who were MSMW increased: 30.7% to 74.7%, 25.1% to 65.1%, and 18.3% to 71.6%, respectively. For all racial/ethnic distributions, the number of diagnoses of MSMW for the SHAS-adjustment was more than 2.0 times that of NHSS.
DISCUSSION In 2011, MSM constituted the largest proportion (78.2%) of new HIV infections among adult and adolescent males diagnosed in the
United States, although they constituted an estimated 2.9% of the overall US male population aged 13 years and older.13 Of these, 26.4% were MSM who also had sex with women. For 2006 to 2010 data from the National Survey for Family Growth, among MSM, 43.9% identified as bisexual.14 HIV diagnoses increased among MSMO overall and were relatively stable for MSMW. Studies have shown that among MSMWs, less exclusive homosexual identification is associated with greater sexual risk behavior without disclosure with female partners.15 While overall decreases in HIV diagnoses have been observed among women during 2008 to 20111 and the magnitude of MSMW transmission is unknown, MSMW constitute a large percentage of persons with HIV and may require tailored prevention interventions. The National HIV/AIDS Strategy3 recommends intensifying HIV prevention efforts in communities where HIV is most heavily concentrated and targeting resources to gay and bisexual men, Blacks/African Americans, and Hispanics/Latinos. This includes effective communication strategies, expansion of HIV testing, and improved access to care and treatment services. CDC currently funds HIV prevention programs for young, minority MSM.16 Intensified interventions are needed to decrease HIV infections overall in MSMW who are less likely to identify with the MSM community and therefore may miss interventions traditionally targeted at MSM as well as reverse the increasing trends overall and particularly among young MSMO. Interventions should be tailored for MSMW and MSMO. As seen in our study, a larger percentage of MSMW were Black/ African American than MSMO. Additionally, for
MSMO, increases were observed for Black/ African American, Hispanics/Latinos, and multiple races. Interventions can be targeted specifically to these groups. MSMW interventions could also be targeted, for example, for those reporting using substances and sexual exchange which are reported more frequently than in heterosexuals and homosexuals.4,17 Furthermore, prevention efforts could address sexual behaviors such as unprotected vaginal intercourse as sex with a female may be perceived as less risky than sex with a male. CDC currently recommends routine annual testing for sexually active MSM aged 13 to 64 years.18 The percentage of undiagnosed HIV among MSM has been reported to be 25.7% for Blacks/African Americans, 22.9% for Hispanics/Latinos and 19.4% for Whites.19 In 2008, the National HIV Behavioral Surveillance System (NHBS) in 21 major US cities found that 18% of the MSM who identified themselves as bisexual tested positive for HIV. Of these, 63% were unaware of their status before testing.20 Such low awareness could be attributed to underestimating personal risk, fewer opportunities to get tested, or complacency that HIV treatment minimizes the impact of HIV disease. Persons unaware of their infection are 3.5 times as likely to transmit HIV than persons aware of their infection.21 Persons aware of their HIV infection can take steps to reduce risk behaviors, access medical care and treatment to improve length and quality of life, and reduce their infectiousness. Stronger efforts by HIV testing and prevention programs are necessary to ensure at least annual HIV testing for MSMW and to reach young and minority MSMO. Both MSMO and MSMW might also benefit from more
TABLE 3—Comparison of the Number of Diagnoses of MSMW and MSMO in the National HIV Surveillance System and the Number of Diagnoses Adjusted by the Supplement to the HIV/AIDS Surveillance Project by Race/Ethnicity: United States and 6 Dependent Areas, 2008–2011 NHSS
SHAS Adjustment
MSMW, No. (%)
MSMO, No. (%)
Total No.
MSMW, No. (%; 95% CI)
MSMO, No. (%; 95% CI)
Total No.
27 018
Race/ethnicity Black/African American
10 064 (30.7)
22 743 (69.3)
32 807
20 177 (74.7; 69.7, 79.7)
6841 (25.3; 20.3, 30.3)
Hispanic/Latinoa
5370 (25.1)
16 038 (74.9)
21 408
12 258 (65.1; 58.5, 71.7)
6577 (34.9; 28.3, 41.5)
18 835
White
6200 (18.3)
27 751 (81.7)
33 951
23 071 (71.6; 67.0, 76.3)
9131 (28.4; 23.7, 33.0)
32 202
Note. CI = confidence interval; MSMO = men who have sex with men only; MSMW = men who have sex with men and women; NHSS = National HIV Surveillance System; SHAS = Supplement to the HIV/AIDS Surveillance Project. The 6 US dependent areas were American Samoa, Guam, the Northern Mariana Islands, Puerto Rico, the Republic of Palau, and the US Virgin Islands. a Hispanic/Latino might be of any race.
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frequent testing, such as every 3 to 6 months for those with risk factors of multiple or anonymous partners or illicit drug use.22 The findings in this report are subject to limitations. First, uncertainty1 in the statistical adjustment procedures applied to HIV surveillance data to account for reporting delay could result in an overestimation or underestimation of these results; however, this uncertainty is unlikely to affect the age and racial/ethnic categories disproportionately. Second, true temporal proximity of sex with males and sex with females for the MSMW classification is unknown. A male is classified as MSMW if at the time of diagnosis, he reported having a sexual history including at least 1 male partner and at least 1 female partner. A male may be classified as MSMW if he had sex with a female only once at a young age and has had sex exclusively with males thereafter. It is not truly known what proportion of the MSMW fall in this category. Because of not knowing enough about MSMW and current surveillance practices, it is difficult to assess how large the present MSMW population is and the resulting prevention needs and efforts. Our additional analysis, however, indicates that HIV case surveillance data may be underestimating MSMW. Comparing the SHAS Project to NHSS, 59.7% of cases initially classified in the NHSS as MSM were reclassified as MSMW as a result of the information obtained from the SHAS interview.4 This underreporting could be attributed to nondisclosure of risk from stigma toward MSMW from both MSM and men who have sex with women. In a study of 2941 young gay, bisexual, and other men who have sex with men using data from the NHBS, 61.3% disclosed male---male sexual attraction or behavior to a provider.23 Additionally, because the hierarchy to assign transmission category gives higher priority to having sex with a male, medical chart abstractors may not collect risk information for sex with a female in addition to having sex with a male; therefore the number of men in this category may be underreported. Risk factor ascertainment has been declining in recent years. Completeness for risk factor information was 72%. Though these data are adjusted for missing risk factor information, these data may not reflect the true number of MSMW with new HIV diagnoses. Our comparison of NHSS and SHAS data indicates this may
be the case and the race/ethnicity distributions may be different. SHAS has some limitations. Participation in the interview was voluntary. Characteristics of those who chose not to participate may differ from those who participated in the interview. As the SHAS data may not be representative of all those diagnosed with HIV, application of SHAS data to NHSS data should be interpreted with caution. Finally, although the SHAS adjustment indicates a number of men may be misclassified as MSMO in NHSS, this should not be interpreted as the number of men engaging in sexual activity with both men and women near the time of their HIV diagnosis. The sexual activity timelines for NHSS and SHAS were very long; information about sexual activity proximal to HIV diagnosis would be required to infer risk of possible onward transmission of risk to women. Nonetheless, comparison of the SHAS and NHSS data indicates the possibility that MSMW are underestimated and a reassessment of prevention efforts targeting this population may be warranted. The National HIV/AIDS Strategy calls for the support and strengthening of HIV surveillance activities to identify those populations at greatest risk needing to be targeted for prevention services. Data from the NHSS in turn aid in monitoring the impact of the National HIV/ AIDS Strategy. These data demonstrate that MSMO and MSMW, especially among youths, remain key targets for prevention efforts for reducing HIV incidence and decreasing racial disparities, principally for Blacks/African Americans and Hispanics/Latinos. Reducing HIV risk behaviors and increasing access to testing and referral to health care are important interventions for MSMO and MSMW to achieve the goals of the National HIV/AIDS Strategy. Intensified interventions are needed to decrease HIV infections overall and reverse the increasing trends among young and older MSMO. Additionally, stronger HIV testing efforts are needed for all MSMW, particularly for Blacks/African Americans. j
About the Authors Sonia Singh, Xiaohong Hu, and H. Irene Hall are with the Division of HIV/AIDS Prevention, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, GA. William Wheeler is with the Division of Nutrition, Physical Activity and Obesity
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Prevention, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention. Correspondence should be sent to Sonia Singh, PhD, MHS, Division of HIV/AIDS Prevention, Centers for Disease Control and Prevention, 1600 Clifton Road NE, MS E-47, Atlanta, GA 30329 (e-mail: [email protected]). Reprints can be ordered at http://www.ajph.org by clicking the “Reprints” link. This article was accepted March 26, 2014. Note. The findings and conclusions in this study are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.
Contributors S. Singh and H. I. Hall developed the analysis plan and led data interpretation and the writing and editing. X. Hu contributed to the analysis plan and performed the analyses. W. Wheeler contributed to the analysis plan, data interpretation, and the writing and editing.
Acknowledgments The authors acknowledge Patrick Sullivan who served as primary thesis advisor for William Wheeler’s master’s thesis, the foundation for this work.
Human Participant Protection This study used data collected as part of routine public health surveillance. It has been determined that public health surveillance is not research. No protocol approval was needed for this study.
References 1. Centers for Disease Control and Prevention. HIV Surveillance Report, 2011. 2013;23. Available at: http:// www.cdc.gov/hiv/surveillance/resources/reports/ 2011report/index.htm. Accessed August 2, 2013. 2. Centers for Disease Control and Prevention. Estimated HIV incidence in the United States, 2007---2010. HIV Surveillance Supplemental Report 2012;17(No. 4). Available at: http://www.cdc.gov/hiv/topics/ surveillance/resources/reports/#supplemental. Accessed August 12, 2013. 3. Office of National AIDS Policy. National HIV/AIDS Strategy for the United States. Available at: http://www. whitehouse.gov/administration/eop/onap/nhas. Accessed October 19, 2012. 4. Spikes PS, Purcell DW, Williams KM, Chen Y, Ding H, Sullivan PS. Sexual risk behaviors among HIV-positive Black men who have sex with women, with men, or with men and women: Implications for intervention development. Am J Public Health. 2009;99:1072---1078. 5. Jeffries WL IV. The number of recent sex partners among bisexual men in the United States. Perspect Sex Reprod Health. 2011;43(3):151---157. 6. Friedman MR, Wei C, Klem ML, Silvestre AJ, Markovic N, Stall R. HIV infection and sexual risk among men who have sex with men and women (MSMW): a systematic review and meta-analysis. PLoS ONE. 2014;9(1):e87139. 7. Chu SY, Peterman TA, Doll LS, Buehler JW, Curran JW. AIDS in bisexual men in the United States: epidemiology and transmission to women. Am J Public Health. 1992;82:220---224.
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8. Department of Health and Human Services. Protection of human subjects, 45 CFR §46 (1974). 9. Centers for Disease Control and Prevention. Distinguishing Public Health Research and Public Health Nonresearch. Available at: http://www.cdc.gov/od/ science/integrity/docs/cdc-policy-distinguishing-publichealth-research-nonresearch.pdf. Accessed August 12, 2013. 10. Harrison KM, Kajese T, Hall HI, Song R. Risk factor redistribution of the national HIV/AIDS surveillance data: an alternative approach. Public Health Rep. 2008;123:618---627. 11. Wheeler W. Men Who Have Sex With Men and Women Among Men With Newly Diagnosed HIV Infections in the United States, 2001-2005 [master’s thesis]. Atlanta, GA: Rollins School of Public Health, Emory University; 2007. 12. Buehler JW, Diaz T, Hersh BS, Chu SY. The supplement to HIV-AIDS Surveillance project: an approach for monitoring HIV risk behaviors. Public Health Rep. 1996;111(suppl 1):133---137. 13. Purcell DW, Johnson CH, Lansky A, et al. Estimating the population size of men who have sex with men in the United States to obtain HIV and syphilis rates. Open AIDS J. 2012;6:98---107. 14. Chandra A, Mosher WD, Copen C, Sionean C. Sexual Behavior, Sexual Attraction, and Sexual Identity in the United States: Data From the 2006-2008 National Survey of Family Growth. National Health Statistics Reports; No. 36. Hyattsville, MD: National Center for Health Statistics; 2011. 15. Mutchler MG, Bogart LM, Elliott MN, et al. Psychosocial correlates of unprotected sex without disclosure of HIV-positivity among African-American, Latino, and White men who have sex with men and women. Arch Sex Behav. 2008;37(5):736---747. 16. Centers for Disease Control and Prevention. Available at: http://www.cdc.gov/msmhealth/msm-programs. htm. Accessed October 19, 2012. 17. Friedman MR, Kurtz SP, Buttram ME, et al. HIV risk among substance-using men who have sex with men and women (MSMW): findings from south Florida. AIDS Behav. 2014;18:111---119. 18. Branson BM, Handsfield HH, Lampe MA, et al. Revised recommendations for HIV testing of adults, adolescents and pregnant women in health-care settings. MMWR Morb Mortal Wkly Rep. 2006;55(no. RR-14):1---17. 19. Chen M, Rhodes PH, Hall IH, et al. Prevalence of undiagnosed HIV infection among persons aged ‡13 years — National HIV Surveillance System, United States, 2005---2008. MMWR Morb Mortal Wkly Rep. 2012;61: 57---64. 20. Centers for Disease Control and Prevention. Prevalence and awareness of HIV infection among men who have sex with men—21 cities, United States, 2008. MMWR Morb Mortal Wkly Rep. 2010;59(37):1201---1207. 21. Marks G, Crepaz N, Janssen RS. Estimating sexual transmission of HIV from persons aware and unaware that they are infected with the virus in the USA. AIDS. 2006;20:1447---1450. 22. Workowski KA, Bauer H, Bachman L, et al. Sexually transmitted disease treatment guidelines, 2010. MMMR Morb Mortal Wkly Rep. 2010;59(No. RR-12):1---110 . 23. Meites E, Krishna NK, Markowitz LE, Oster AM. Health care use and opportunities for human papillomavirus vaccination among young men who have sex with men. Sex Transm Dis. 2013;40(2):154---157.
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