CSIRO PUBLISHING
Sexual Health, 2014, 11, 592–593 http://dx.doi.org/10.1071/SH14181
Letter
Lower sexually transmissible infection prevalence among lifetime exclusive women who have sex with women compared with women who have sex with women and men Christina A. Muzny A,B, Richa Kapil A, Erika L. Austin A, Edward W. Hook IIIA and William M. Geisler A A
Division of Infectious Diseases, University of Alabama at Birmingham, Birmingham, ZRB 242, 1530 3rd Avenue South, Birmingham, AL 35294, USA. B Corresponding author. Email: [email protected]
Abstract. Background: Sexually transmissible infection (STI) history, prevalence and seroprevalence among lifetime exclusive women who have sex with women (WSW) and an age-matched group of women who have sex with women and men (WSWM) was evaluated. Methods: Participants completed a study questionnaire and had genital specimens and sera collected for STI testing. Results: Twenty-one lifetime exclusive WSW and 42 WSWM were included. WSWM were more likely to report a history of prior STIs and be seropositive for chlamydia and HSV-2. Prevalent STIs were less common among WSW. Conclusions: While lifetime exclusive WSW are at risk of contracting STIs, WSWM are disproportionally affected. Healthcare providers should consider routine STI screening among WSW. Received 11 September 2014, accepted 3 October 2014, published online 1 December 2014
The risk for sexually transmissible infections (STIs) among lifetime exclusive women who have sex with women (WSW) (i.e. women who have never had sex with a man) is controversial,1–5 as little is known about STI transmission between women. Because many WSW also have a history of sex with men (WSWM) and continue to do so,5–7 it is difficult to determine the source of their STI(s). In a study of 163 African American WSW at the Jefferson County Department of Health (JCDH) STD clinic in Birmingham, Alabama, USA,8 we evaluated STI history, prevalence, and seroprevalence among a subset of lifetime exclusive WSW and an age-matched group of WSWM. This study was approved by the University of Alabama at Birmingham Institutional Review Board and the JCDH. Participants completed a questionnaire and provided genital specimens. These specimens were tested for trichomoniasis by culture and chlamydia and gonorrhea by a nucleic acid amplification test.8 Participants also had sera which was tested for herpes simplex virus type 2 (HSV-2), syphilis, HIV and chlamydia using the HerpeSelect® HSV-2 enzyme-linked immunosorbent assay (ELISA) (Focus Diagnostics, Cypress, CA, USA), the ZeusIFA fluorescent treponemal antibodyadsorption test, a HIV ELISA (Siemens, Malvern, PA, USA), and a chlamydia elementary body-based ELISA, respectively.9 Statistical analyses were performed by using Stata 12.1 (College Station, TX, USA). Of 163 WSW enrolled,8 21 were lifetime exclusive WSW and age-matched in a 1 : 2 ratio to 42 WSWM. The median age Journal compilation Ó CSIRO 2014
of all women was 22 years. There were no differences among groups with regards to lifetime number of female partners or ever having a female partner with an STI. Fifty-five per cent of WSWM reported having a male partner during the past year. Among lifetime exclusive WSW, only a single prior STI (trichomoniasis) was reported by one woman. In contrast, WSWM more often reported prior STIs: chlamydia and trichomoniasis were each reported by one-third (P = 0.003 and P = 0.013, respectively), gonorrhea by 17% (P = 0.085), and genital herpes and syphilis each by one WSWM. Prevalent STIs were less common among lifetime exclusive WSW (Table 1). Compared with lifetime exclusive WSW, a significantly higher proportion of WSWM were chlamydia seropositive (69% vs 33%, P = 0.007) and HSV-2 seropositive (36% vs 0%; P = 0.001). One of the WSWM had serologic evidence of syphilis; this is in contrast to none of the lifetime exclusive WSW. No participant was HIV seropositive. Our study suggests that while lifetime exclusive WSW are at risk of contracting STIs, the risk for WSWM is greater. This heightened risk among WSWM is consistent with previous studies.7,10 We have found that WSWM often engage in behaviours such as transactional sex, sex with a homosexual or bisexual man, sex with new or casual partners, group sex, and sex with partners known to have STIs.7 Chlamydia prevalence among WSW has traditionally been low;11 however, we have demonstrated a 12% prevalence in WSWM, and a recent study of women attending family planning clinics reported a prevalence of 7.1% among both WSW and www.publish.csiro.au/journals/sh
STI prevalence among lifetime exclusive WSW
Sexual Health
Table 1. Association between sex with men ever and STI diagnosis among African American women who have sex with women STI, sexually transmissible infection; WSW, women who have sex with women; WSWM, women who have sex with women and men; NAAT, nucleic acid amplification test. Results are presented as n (%) for both lifetime exclusive WSW and WSWM groups STI diagnosis
Serological evidence of STI Chlamydia trachomatis Herpes simplex virus type-2 Syphilis HIV Serological evidence of any STI NAAT evidence of STI Chlamydia trachomatis Neisseria gonorrhoeae Culture evidence of STI Trichomonas vaginalis Evidence of any STI
Lifetime exclusive WSW (n = 21) 7 0 0 0 7
(33) (0) (0) (0) (33)
Lifetime WSWM (n = 42) 29 15 1 0 32
P-value
(69) (36) (2) (0) (76)
0.007 0.001 1.00 – 0.001
0 (0) 0 (0)
5 (12) 2 (5)
0.160 0.548
1 (5) 8 (38)
9 (21) 33 (79)
0.144 0.001
WSWM.12 The high chlamydia seroprevalence among exclusive WSW (33%) and WSWM (69%) in this study suggests chlamydia transmission is even more common, underscoring the need for routine screening. No participant had HIV and only one WSWM had evidence of syphilis. HIV and syphilis transmission risk among female partners is not well known.13,14 With regards to HIV, WSW may be more likely to acquire this infection through injection drug use and sex with high-risk male partners.11 We found no serological evidence of HSV-2 among exclusive WSW; this is in contrast to a study that found a seroprevalence of 3% among 78 exclusive WSW.15 HSV-2 seroprevalence among WSWM was 35%, a result that is similar to population-based data.16 In conclusion, this study demonstrates that while lifetime exclusive WSW are at risk of contracting STIs, WSWM are disproportionally affected. Healthcare providers should consider routine STI screening among WSW. Conflicts of interest None declared. Acknowledgements This study was supported, in part, by a Developmental Award granted to Christina Muzny, M.D. from the American Sexually Transmitted Diseases Association. The authors thank Hanne Harbison, Saralyn Richter, Rhonda Whidden, Allison Whittington and Christen Press for their assistance in recruiting and enrolling patients for this study and Marga Jones for her assistance with data management. The authors also thank Dr. Nicholas Van Wagoner at the University of Alabama at Birmingham for performing the HSV-2 serological testing and Drs. Richard and Sandra Morrison from the University of Arkansas for Medical Sciences for supplying the gradient purified Chlamydia trachomatis elementary bodies for the ELISA antigen. Data from this study were presented, in part, as Poster #WP63 at the 2014 National STD Prevention Conference in Atlanta, GA on 10 June 2014.
593
References 1 Robertson P, Schachter J. Failure to identify venereal disease in a lesbian population. Sex Transm Dis 1981; 8: 75–6. doi:10.1097/ 00007435-198104000-00008 2 Johnson SR, Smith EM, Guenther SM. Comparison of gynecologic health care problems between lesbians and bisexual women. A survey of 2,345 women. J Reprod Med 1987; 32: 805–11. 3 Edwards A, Thin RN. Sexually transmitted diseases in lesbians. Int J STD AIDS 1990; 1: 178–81. 4 Marrazzo JM, Koutsky LA, Handsfield HH. Characteristics of female sexually transmitted disease clinic clients who report samesex behavior. Int J STD AIDS 2001; 12: 41–6. doi:10.1258/09564 62011916721 5 Marrazzo JM. Barriers to infectious disease care among lesbians. Emerg Infect Dis 2004; 10: 1974–8. doi:10.3201/eid1011.040467 6 Diamant AL, Schuster MA, McGuigan K, Lever J. Lesbians’ sexual history with men: implications for taking a sexual history. Arch Intern Med 1999; 159: 2730–6. doi:10.1001/archinte.159.22.2730 7 Muzny CA, Sunesara IR, Martin DH, Mena LA. Sexually transmitted infections and risk behaviors among African American women who have sex with women: does sex with men make a difference? Sex Transm Dis 2011; 38: 1118–25. doi:10.1097/OLQ.0b013e3182 2e6179 8 Muzny CA, Austin EL, Harbison HS, Hook EW 3rd. Sexual partnership characteristics of African American women who have sex with women: impact on sexually transmitted infection risk. Sex Transm Dis 2014; 41: 611–7. doi:10.1097/OLQ.0000000000000194 9 Geisler WM, Morrison SG, Doemland ML, Iqbal SM, Su J, Mancevski A, Hook EW, Morrison RP III. Immunoglobulinspecific responses to Chlamydia elementary bodies in individuals with and at risk for genital chlamydial infection. J Infect Dis 2012; 206: 1836–43. doi:10.1093/infdis/jis621 10 Mercer CH, Bailey JV, Johnson AM, Erens B, Wellings K, Fenton KA, Copas AJ. Women who report having sex with women: British national probability data on prevalence, sexual behaviors, and health outcomes. Am J Public Health 2007; 97: 1126–33. doi:10.2105/AJPH. 2006.086439 11 Gorgos LM, Marrazzo JM. Sexually transmitted infections among women who have sex with women. Clin Infect Dis 2011; 53: S84–91. doi:10.1093/cid/cir697 12 Singh D, Fine DN, Marrazzo JM. Chlamydia trachomatis infection among women reporting sexual activity with women screened in Family Planning Clinics in the Pacific Northwest, 1997 to 2005. Am J Public Health 2011; 101: 1284–90. doi:10.2105/AJPH.2009. 169631 13 Kwakwa HA, Ghobrial MW. Female-to-female transmission of human immunodeficiency virus. Clin Infect Dis 2003; 36: e40–1. doi:10.1086/345462 14 Campos-Outcalt D, Hurwitz S. Female-to-female transmission of syphilis: a case report. Sex Transm Dis 2002; 29: 119–20. doi:10.1097/00007435-200202000-00010 15 Marrazzo JM, Stine K, Wald A. Prevalence and risk factors for infection with herpes simplex virus type-1 and -2 among lesbians. Sex Transm Dis 2003; 30: 890–5. doi:10.1097/01.OLQ.0000091151. 52656.E5 16 Xu F, Sternberg MR, Markowitz LE. Women who have sex with women in the United States: prevalence, sexual behavior and prevalence of herpes simplex virus type 2 infection-results from national health and nutrition examination survey 2001–2006. Sex Transm Dis 2010; 37: 407–13.
www.publish.csiro.au/journals/sh
Sexual Health, 2014, 11, 592–593 http://dx.doi.org/10.1071/SH14181
Letter
Lower sexually transmissible infection prevalence among lifetime exclusive women who have sex with women compared with women who have sex with women and men Christina A. Muzny A,B, Richa Kapil A, Erika L. Austin A, Edward W. Hook IIIA and William M. Geisler A A
Division of Infectious Diseases, University of Alabama at Birmingham, Birmingham, ZRB 242, 1530 3rd Avenue South, Birmingham, AL 35294, USA. B Corresponding author. Email: [email protected]
Abstract. Background: Sexually transmissible infection (STI) history, prevalence and seroprevalence among lifetime exclusive women who have sex with women (WSW) and an age-matched group of women who have sex with women and men (WSWM) was evaluated. Methods: Participants completed a study questionnaire and had genital specimens and sera collected for STI testing. Results: Twenty-one lifetime exclusive WSW and 42 WSWM were included. WSWM were more likely to report a history of prior STIs and be seropositive for chlamydia and HSV-2. Prevalent STIs were less common among WSW. Conclusions: While lifetime exclusive WSW are at risk of contracting STIs, WSWM are disproportionally affected. Healthcare providers should consider routine STI screening among WSW. Received 11 September 2014, accepted 3 October 2014, published online 1 December 2014
The risk for sexually transmissible infections (STIs) among lifetime exclusive women who have sex with women (WSW) (i.e. women who have never had sex with a man) is controversial,1–5 as little is known about STI transmission between women. Because many WSW also have a history of sex with men (WSWM) and continue to do so,5–7 it is difficult to determine the source of their STI(s). In a study of 163 African American WSW at the Jefferson County Department of Health (JCDH) STD clinic in Birmingham, Alabama, USA,8 we evaluated STI history, prevalence, and seroprevalence among a subset of lifetime exclusive WSW and an age-matched group of WSWM. This study was approved by the University of Alabama at Birmingham Institutional Review Board and the JCDH. Participants completed a questionnaire and provided genital specimens. These specimens were tested for trichomoniasis by culture and chlamydia and gonorrhea by a nucleic acid amplification test.8 Participants also had sera which was tested for herpes simplex virus type 2 (HSV-2), syphilis, HIV and chlamydia using the HerpeSelect® HSV-2 enzyme-linked immunosorbent assay (ELISA) (Focus Diagnostics, Cypress, CA, USA), the ZeusIFA fluorescent treponemal antibodyadsorption test, a HIV ELISA (Siemens, Malvern, PA, USA), and a chlamydia elementary body-based ELISA, respectively.9 Statistical analyses were performed by using Stata 12.1 (College Station, TX, USA). Of 163 WSW enrolled,8 21 were lifetime exclusive WSW and age-matched in a 1 : 2 ratio to 42 WSWM. The median age Journal compilation Ó CSIRO 2014
of all women was 22 years. There were no differences among groups with regards to lifetime number of female partners or ever having a female partner with an STI. Fifty-five per cent of WSWM reported having a male partner during the past year. Among lifetime exclusive WSW, only a single prior STI (trichomoniasis) was reported by one woman. In contrast, WSWM more often reported prior STIs: chlamydia and trichomoniasis were each reported by one-third (P = 0.003 and P = 0.013, respectively), gonorrhea by 17% (P = 0.085), and genital herpes and syphilis each by one WSWM. Prevalent STIs were less common among lifetime exclusive WSW (Table 1). Compared with lifetime exclusive WSW, a significantly higher proportion of WSWM were chlamydia seropositive (69% vs 33%, P = 0.007) and HSV-2 seropositive (36% vs 0%; P = 0.001). One of the WSWM had serologic evidence of syphilis; this is in contrast to none of the lifetime exclusive WSW. No participant was HIV seropositive. Our study suggests that while lifetime exclusive WSW are at risk of contracting STIs, the risk for WSWM is greater. This heightened risk among WSWM is consistent with previous studies.7,10 We have found that WSWM often engage in behaviours such as transactional sex, sex with a homosexual or bisexual man, sex with new or casual partners, group sex, and sex with partners known to have STIs.7 Chlamydia prevalence among WSW has traditionally been low;11 however, we have demonstrated a 12% prevalence in WSWM, and a recent study of women attending family planning clinics reported a prevalence of 7.1% among both WSW and www.publish.csiro.au/journals/sh
STI prevalence among lifetime exclusive WSW
Sexual Health
Table 1. Association between sex with men ever and STI diagnosis among African American women who have sex with women STI, sexually transmissible infection; WSW, women who have sex with women; WSWM, women who have sex with women and men; NAAT, nucleic acid amplification test. Results are presented as n (%) for both lifetime exclusive WSW and WSWM groups STI diagnosis
Serological evidence of STI Chlamydia trachomatis Herpes simplex virus type-2 Syphilis HIV Serological evidence of any STI NAAT evidence of STI Chlamydia trachomatis Neisseria gonorrhoeae Culture evidence of STI Trichomonas vaginalis Evidence of any STI
Lifetime exclusive WSW (n = 21) 7 0 0 0 7
(33) (0) (0) (0) (33)
Lifetime WSWM (n = 42) 29 15 1 0 32
P-value
(69) (36) (2) (0) (76)
0.007 0.001 1.00 – 0.001
0 (0) 0 (0)
5 (12) 2 (5)
0.160 0.548
1 (5) 8 (38)
9 (21) 33 (79)
0.144 0.001
WSWM.12 The high chlamydia seroprevalence among exclusive WSW (33%) and WSWM (69%) in this study suggests chlamydia transmission is even more common, underscoring the need for routine screening. No participant had HIV and only one WSWM had evidence of syphilis. HIV and syphilis transmission risk among female partners is not well known.13,14 With regards to HIV, WSW may be more likely to acquire this infection through injection drug use and sex with high-risk male partners.11 We found no serological evidence of HSV-2 among exclusive WSW; this is in contrast to a study that found a seroprevalence of 3% among 78 exclusive WSW.15 HSV-2 seroprevalence among WSWM was 35%, a result that is similar to population-based data.16 In conclusion, this study demonstrates that while lifetime exclusive WSW are at risk of contracting STIs, WSWM are disproportionally affected. Healthcare providers should consider routine STI screening among WSW. Conflicts of interest None declared. Acknowledgements This study was supported, in part, by a Developmental Award granted to Christina Muzny, M.D. from the American Sexually Transmitted Diseases Association. The authors thank Hanne Harbison, Saralyn Richter, Rhonda Whidden, Allison Whittington and Christen Press for their assistance in recruiting and enrolling patients for this study and Marga Jones for her assistance with data management. The authors also thank Dr. Nicholas Van Wagoner at the University of Alabama at Birmingham for performing the HSV-2 serological testing and Drs. Richard and Sandra Morrison from the University of Arkansas for Medical Sciences for supplying the gradient purified Chlamydia trachomatis elementary bodies for the ELISA antigen. Data from this study were presented, in part, as Poster #WP63 at the 2014 National STD Prevention Conference in Atlanta, GA on 10 June 2014.
593
References 1 Robertson P, Schachter J. Failure to identify venereal disease in a lesbian population. Sex Transm Dis 1981; 8: 75–6. doi:10.1097/ 00007435-198104000-00008 2 Johnson SR, Smith EM, Guenther SM. Comparison of gynecologic health care problems between lesbians and bisexual women. A survey of 2,345 women. J Reprod Med 1987; 32: 805–11. 3 Edwards A, Thin RN. Sexually transmitted diseases in lesbians. Int J STD AIDS 1990; 1: 178–81. 4 Marrazzo JM, Koutsky LA, Handsfield HH. Characteristics of female sexually transmitted disease clinic clients who report samesex behavior. Int J STD AIDS 2001; 12: 41–6. doi:10.1258/09564 62011916721 5 Marrazzo JM. Barriers to infectious disease care among lesbians. Emerg Infect Dis 2004; 10: 1974–8. doi:10.3201/eid1011.040467 6 Diamant AL, Schuster MA, McGuigan K, Lever J. Lesbians’ sexual history with men: implications for taking a sexual history. Arch Intern Med 1999; 159: 2730–6. doi:10.1001/archinte.159.22.2730 7 Muzny CA, Sunesara IR, Martin DH, Mena LA. Sexually transmitted infections and risk behaviors among African American women who have sex with women: does sex with men make a difference? Sex Transm Dis 2011; 38: 1118–25. doi:10.1097/OLQ.0b013e3182 2e6179 8 Muzny CA, Austin EL, Harbison HS, Hook EW 3rd. Sexual partnership characteristics of African American women who have sex with women: impact on sexually transmitted infection risk. Sex Transm Dis 2014; 41: 611–7. doi:10.1097/OLQ.0000000000000194 9 Geisler WM, Morrison SG, Doemland ML, Iqbal SM, Su J, Mancevski A, Hook EW, Morrison RP III. Immunoglobulinspecific responses to Chlamydia elementary bodies in individuals with and at risk for genital chlamydial infection. J Infect Dis 2012; 206: 1836–43. doi:10.1093/infdis/jis621 10 Mercer CH, Bailey JV, Johnson AM, Erens B, Wellings K, Fenton KA, Copas AJ. Women who report having sex with women: British national probability data on prevalence, sexual behaviors, and health outcomes. Am J Public Health 2007; 97: 1126–33. doi:10.2105/AJPH. 2006.086439 11 Gorgos LM, Marrazzo JM. Sexually transmitted infections among women who have sex with women. Clin Infect Dis 2011; 53: S84–91. doi:10.1093/cid/cir697 12 Singh D, Fine DN, Marrazzo JM. Chlamydia trachomatis infection among women reporting sexual activity with women screened in Family Planning Clinics in the Pacific Northwest, 1997 to 2005. Am J Public Health 2011; 101: 1284–90. doi:10.2105/AJPH.2009. 169631 13 Kwakwa HA, Ghobrial MW. Female-to-female transmission of human immunodeficiency virus. Clin Infect Dis 2003; 36: e40–1. doi:10.1086/345462 14 Campos-Outcalt D, Hurwitz S. Female-to-female transmission of syphilis: a case report. Sex Transm Dis 2002; 29: 119–20. doi:10.1097/00007435-200202000-00010 15 Marrazzo JM, Stine K, Wald A. Prevalence and risk factors for infection with herpes simplex virus type-1 and -2 among lesbians. Sex Transm Dis 2003; 30: 890–5. doi:10.1097/01.OLQ.0000091151. 52656.E5 16 Xu F, Sternberg MR, Markowitz LE. Women who have sex with women in the United States: prevalence, sexual behavior and prevalence of herpes simplex virus type 2 infection-results from national health and nutrition examination survey 2001–2006. Sex Transm Dis 2010; 37: 407–13.
www.publish.csiro.au/journals/sh
