In the current issue of Sexually Transmitted Diseases, Habel et al. examine the prevalence and correlates of oral sex and penile–anal intercourse (PAI) between male–female partners, reporting high endorsement of these behaviors in a nationally representative sample of US adolescents and adults aged 15 to 44 years.1 Unsurprisingly, more than 75% of women and men reported having given and received oral sex over their lifetime, with trivial proportions (6% of women and 7% of men) using a condom at their last oral sex encounter. Lifetime male–female PAI was reported by a significant minority of both women (33%) and men (38%), among whom only 21% and 30%, respectively, used a condom at last PAI.
To put these figures in context, a higher proportion of US adolescents and adults have had male–female PAI than have a Twitter account.2 In other words, Habel et al. highlight what is already widely known among sexual health researchers: for many women and men, male–female PAI is, simply, normal behavior. Yet despite the high lifetime endorsement of male–female PAI among US adult populations, now documented in multiple surveys,1,3–5 surprisingly little is known about the frequency or context in which it occurs, the prevalence of associated behaviors (e.g., use of condoms or lubricant), or about people's knowledge of PAI-specific risks of transmission of human immunodeficiency virus (HIV) and other sexually transmitted infections (STIs).
Receptive PAI is the riskiest sexual behavior for HIV acquisition due to formation of abrasions in the rectal mucosa, which also contains a high concentration of HIV-target cells.6 When engaging in PAI with an HIV-positive partner who is not virally suppressed, the HIV acquisition risk for the receptive partner is exacerbated by failure to use condoms,7 certain lubricants,8,9 and possibly presex or postsex hygiene practices (e.g., rectal douching10) that could further disrupt the rectal epithelium. The bulk of evidence on PAI and HIV/STI transmission is from studies conducted among men who have sex with men. As a result, the attributable fraction of PAI for women's HIV or STI risk is not well characterized. In clinical settings, male–female PAI is often dismissed or avoided in conversations about HIV/STI prevention.
In Habel et al's work, the most striking difference in endorsement of PAI among women was the increase in lifetime prevalence comparing the age groups of 15 to 19 years (11%) with those 20 to 24 years of age (32%). This increase occurs approximately at the transition from adolescence to adulthood and points both to a key window of exposure and to an important opportunity for sexual health education. US adolescents are the population most affected by increasing STI rates (particularly adolescent females),11 and they experience significant barriers to accessing sexual health services.12,13 Critically, more than 50% of HIV-positive youth in the United States are unaware of their status, are therefore not virally suppressed, and have increased risk of onward transmission to HIV-negative partners.14,15 Habel et al.'s findings reinforce the need for comprehensive sex education. Adolescents should be informed—before the period of increased engagement—how to have safe and healthy PAI and how to reduce the HIV/STI risks associated with it. However, PAI is rarely included in sex education curricula – despite recommendations that it should be16—and when it is, it is often the subject of protests.17,18
Valid measurement of male–female PAI is a critical first step for obtaining population-level estimates across and within age groups, which can then be used to estimate more reliable HIV/STI transmission risks associated with it. Indeed, current modeling analyses demonstrate that even if male–female PAI is relatively rare, it may still have a large impact on population-level HIV transmission dynamics in generalized epidemics.19 However, current models for high HIV prevalence regions in particular rely on sparse and likely incomplete data.20–24 Many epidemiological studies (which then inform mathematical modeling estimates) have not prioritized careful measurement of male–female PAI nor assessed its impact on their outcomes of interest.
When studies address whether a participant has engaged in PAI—often using anatomical or technical language, which may or may not be understood by the participant—they typically fail to collect data on behaviors occurring alongside PAI (including condom use, lubricant use, and rectal douching), use vague or inconsistent timeframes (ever, last 12 months, last 3 months, etc.), and do not capture detailed data about PAI with each partner (e.g., frequency and order of orifice exposure [e.g., vaginal sex following PAI]25). Habel et al. report lifetime endorsement, a measure distinct from current or consistent sexual practices. Among women who report lifetime PAI, is it a common part of their sexual experience, or a rare (or singular) event? Do some women engage in PAI out of curiosity, have an unpleasant experience, and subsequently never try it again? What proportion of women (or their partners) research how to safely and pleasurably engage in PAI before doing so? Do considerations related to avoiding pregnancy or menstrual fluid, or increasing sexual pleasure (for the woman or her partner), lead women to engage in PAI?
Of course, measurement of PAI is also challenging outside of the US. In sub-Saharan Africa specifically, studies have generated highly-varied estimates of lifetime male–female PAI: 10% to 20% of “general population” men and women, 5% to 15% of adolescents, and 16% to 43% of female sex workers.26 However, we suggest that these estimates may be biased, not only from the limitations common to all sexual health research (recall, embarrassment, judgment and stigma), but also from participant misunderstanding. No standardized tool exists to measure PAI, a specific term for PAI is not present in some languages, and slang terminology varies across geographical regions, populations, and age groups. Some surveys use vague language to maximize cultural sensitivity and to avoid offending participants, but such descriptions can also be confusing. A handful of highly informative qualitative studies26–30 have explored these issues and have uncovered significant misunderstanding: as 1 example, during in-depth interviews conducted after a large HIV trial, many women in South Africa, Uganda, and Zimbabwe realized that they had overreported PAI in the earlier trial because of confusion between PAI and vaginal intercourse “from behind.”28 Qualitative studies have also reported low knowledge about the HIV risk associated with male–female PAI, with respondents in some studies explaining that they sometimes choose PAI over vaginal sex specifically because they believe that it carries a lower HIV risk.26,27,29,30 Future studies on this topic must develop, pilot, and refine comprehensive, unambiguous, culturally appropriate data collection instruments that capture not only the prevalence but also the context, correlates, and consequences of male–female PAI.
A final point concerns terminology and the power of our chosen words, as clinicians and scientists, to inform or inhibit our ability to do meaningful work. Habel et al., like many studies on this topic, use the term “heterosexual anal sex” throughout their article; here, we use “male–female PAI,” in accordance with terminology guidelines from the American Psychological Association.31 As with every research topic, we must thoughtfully characterize the populations and behaviors we study. Women who engage in PAI may not identify as heterosexual, and assuming all women who report sex with men are heterosexual mischaracterizes an important subset of women who do not identify as such, falls short of ethical and social awareness within research, and may have damaging consequences to public health messaging and community engagement. “Male–female PAI,” although an improvement over “heterosexual anal sex,” is still inadequate, as gender nonconforming, gender queer, and nonbinary identities remain excluded.
According to Habel et al., approximately 40% of US adults have had PAI by age 35 years. Clearly, consensual PAI can be a healthy, ordinary sexual experience, and both sexual health education and research efforts would be improved by framing this behavior not only as a mechanism of disease transmission. Yet education and research are built on data, and as described above, significant gaps currently exist in our knowledge of male–female PAI in the United States and globally. A more thoughtful discussion about PAI among women will inform HIV prevention efforts (e.g., community education, HIV preexposure prophylaxis guidelines) and HIV/STI screening and treatment (e.g., screening women for extragenital STIs that would be missed if testing only occurs in urogenital sites). Finally, sexual health researchers must consistently and thoughtfully measure male–female PAI to generate a more nuanced understanding of this behavior and its implications for HIV/STI acquisition and transmission.
1. Habel MA, Leichliter JS, Dittus PJ, et al. Heterosexual anal and oral sex in adolescents and adults in the United States, 2011–2015. Sex Transm Dis 2018; 45:775–782.
2. Smith A, Anderson M. Internet and technology: Social media use in 2018. Pew Research Center 2018. http://www.pewinternet.org/2018/03/01/social-media-use-in-2018/
3. Herbenick D, Reece M, Schick V, et al. Sexual behavior in the United States: Results from a national probability sample of men and women ages 14–94. J Sex Med 2010; 7(Suppl 5):255–265.
4. Leichliter JS, Chandra A, Liddon N, et al. Prevalence and correlates of heterosexual anal and oral sex in adolescents and adults in the United States. J Infect Dis 2007; 196:1852–1859.
5. Satterwhite CL, Kamb ML, Metcalf C, et al. Changes in sexual behavior and STD prevalence among heterosexual STD clinic attendees: 1993–1995 versus 1999–2000. Sex Transm Dis 2007; 34:815–819.
6. Fox J, Fidler S. Twenty-five years of antiretroviral drug development: Progress and prospects. (January 01, 2010). Sexual transmission of HIV-1 Antiviral Research 85, 1:276–285.
7. Darrow WW, Jaffe HW, Curran JW. Passive anal intercourse as a risk factor for AIDS in homosexual men. Lancet 1983; 2:160.
8. Sudol KM, Phillips DM. Relative safety of sexual lubricants for rectal intercourse. Sex Transm Dis 2004; 31:346–349.
9. Phillips DM, Sudol KM, Taylor CL, et al. Lubricants containing N-9 may enhance rectal transmission of HIV and other STIs. Contraception 2004; 70:107–110.
10. Carballo-Diéguez A, Bauermeister JA, Ventuneac A, et al. The use of rectal douches among HIV-uninfected and infected men who have unprotected receptive anal intercourse: Implications for rectal microbicides. AIDS Behav 2008; 12:860–866. Epub 2007 Aug 18.
11. Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep 2015; 64.
12. Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance 2016. Atlanta: U.S. Department of Health and Human Services, 2017.
13. Tilson EC, Sanchez V, Ford CL, et al. Barriers to asymptomatic screening and other STD services for adolescents and young adults: Focus group discussions. BMC Public Health 2004; 4–21.
14. Centers for Disease Control and Prevention. HIV in Youth. Atlanta: U.S. Department of Health and Human Services, 2018.
15. Centers for Disease Control and Prevention (CDC). Vital signs: HIV infection, testing, and risk behaviors among youths—United States. MMWR Morb Mortal Wkly Rep 2012; 61:971–976.
16. The American College of Obstetricians and Gynecologists. Comprehensive sexuality education. Committee opinion no. 678. Obstet Gynecol 2016; 128:e227–e230.
17. CBS News. N.C. school district votes to end widely used sex education program amid outcry. CBS Interactive Inc 2018; 14. https://www.cbsnews.com/news/debate-over-planned-parenthood-sex-education-program-north-carolina/
18. CBS News. Parents protest “graphic” sex ed curriculum in Calif. Schools. CBS News Interactive 2017; 30. https://www.cbsnews.com/news/parents-protest-graphic-sex-ed-curriculum-changes-cupertino-california-schools/
19. Leynaert B, Downs AM, de Vincenzi I. Heterosexual transmission of human immunodeficiency virus: Variability of infectivity throughout the course of infection. European Study Group on heterosexual transmission of HIV. Am J Epidemiol 1998; 148:88–96.
20. Maheu-Giroux M, Baral S, Vesga JF, et al. Anal intercourse among female sex workers in Côte d'Ivoire: Prevalence, determinants, and model-based estimates of the population-level impact on HIV transmission. Am J Epidemiol 2018; 187:287–297.
21. O'Leary A, DiNenno E, Honeycutt A, et al. Contribution of anal sex to HIV prevalence among heterosexuals: A modeling analysis. AIDS Behav 2017 Oct; 21:2895–2903.
22. Baggaley RF, White RG, Boily MC. HIV transmission risk through anal intercourse: Systematic review, meta-analysis and implications for HIV prevention. Int J Epidemiol 2010; 39:1048–1063.
23. Boily MC, Baggaley RF, Wang L, et al. Heterosexual risk of HIV-1 infection per sexual act: Systematic review and meta-analysis of observational studies. Lancet Infect Dis 2009; 9:118–129.
24. Powers KA, Poole C, Pettifor AE, et al. Rethinking the heterosexual infectivity of HIV-1: A systematic review and meta-analysis. Lancet Infect Dis 2008; 8:553–563.
25. Gorbach PM, Pines H, Javanbakht M, et al. Order of orifices: Sequence of condom use and ejaculation by orifice during anal intercourse among women. Implications for HIV transmission J Acquir Immune Defic Syndr 2014; 67:424–429.
26. Duby Z, Colvin C. Conceptualizations of heterosexual anal sex and HIV risk in five east African communities. J Sex Res 2014; 51:863–873.
27. Duby Z, Hartmann M, Montgomery ET, et al. Sexual scripting of heterosexual penile-anal intercourse amongst participants in an HIV prevention trial in South Africa, Uganda and Zimbabwe. Cult Health Sex 2016; 18:30–44.
28. Duby Z, Hartmann M, Mahaka I, et al. Lost in translation: Language, terminology, and understanding of penile-anal intercourse in an HIV prevention trial in South Africa, Uganda, and Zimbabwe. J Sex Res 2016; 53:1096–1106.
29. Duby Z, Hartmann M, Montgomery ET, et al. Condoms, lubricants and rectal cleansing: Practices associated with heterosexual penile-anal intercourse amongst participants in an HIV prevention trial in South Africa, Uganda and Zimbabwe. AIDS Behav 2016; 20:754–762.
30. Mtenga S, Shamba D, Wamoyi J, et al. How long-distance truck drivers and villagers in rural southeastern Tanzania think about heterosexual anal sex: A qualitative study. Sex Transm Infect 2015; 91:576–580.
31. American Psychological Association. Avoiding heterosexual bias in language. Reprint: Committee on lesbian and gay concerns, 1991. Avoiding heterosexual bias in language. American Psychologist 1991; 46:973–974.