Abstract
Background:
Unprotected oral sex may result in extragenital sexually transmitted infections (STIs). The purpose of this study was to describe sexual behaviors, barrier use, and chlamydia/gonorrhea (Ct/GC) positivity among young Black men who have sex with women, and to examine the potential influence of extragenital infections on genital infections.
Methods:
Young Black men who had vaginal sex were screened for Ct/GC in New Orleans, Louisiana from 08/14/2019 – 02/29/2020. Audio/computer-assisted self-interviews were used to collect data on demographics and sexual behaviors. Chi-square/Fisher’s Exact or t-test/Wilcoxon Rank tests were used to assess differences in behaviors by Ct/GC positivity.
Results:
Among 373 men studied, 619 female partnerships were reported in the past two months. Vaginal sex was reported in all partnerships per study protocol, receiving fellatio in 42.7%, performing cunnilingus in 35.7% and penile-anal sex in 5.9%. While 31.4% of the men consistently used condoms for vaginal sex with all partners, consistent barrier use was low during cunnilingus (0.5%) and fellatio (5.1%). Urethral infection rates among all men in the sample were 12.6% for Ct and 1.6% for GC. There was no significant difference in Ct/GC rates between those using and not using condoms consistently during vaginal sex (p= 0.38).
Conclusions:
Unprotected oral sex with female partners was common. The high rate of genital infection among men who used condoms consistently for vaginal sex suggests that oral infections could be serving as a reservoir of genital infection. Testing at all sites of exposure for youth who engage in heterosexual sex is merited.
Keywords: Chlamydia, gonorrhea, men who have sex with women, extragenital
Summary
Half of Black men (50%) who have sex with women in New Orleans engaged in oral sex and rates of urethral chlamydia and gonorrhea did not vary by condom use during vaginal sex, suggesting the possibility of extragenital exposure.
Introduction
Chlamydia trachomatis (Ct) is the most frequently reported bacterial sexually transmitted infection in the US, with more than 1.8 million cases reported in 2019.(1) Neisseria gonorrhoeae (GC) is a very common sexually transmitted infectious disease, with 1.6 million cases reported in 2018.(2) The risk of Ct is highest among young people, with two-thirds of infections occurring in people between 14–24 years of age.(3) Similarly, over half of GC cases are reported in individuals 15–24.(4) Nationally representative studies in the US have shown that Ct and GC rates are highest among Black people,(3) and that poverty, living in the southern US, and increased crime rates are also associated with increased rates of infection.(1, 5)
In addition to vaginal sex, Ct and GC can be transmitted through anal and oral sex, which may result in infection of the pharynx and rectum.(6) Moreover, it has been established that oral Ct and GC infections can be transmitted to the genital tract.(7) Since current guidelines only recommend extragenital screening for men who have sex with men (MSM), far less is known about these behaviors in men who have sex with women (MSW). (6)
Several studies have begun to investigate extragenital Ct and GC in individuals with sexual partners of a different sex, though most focus on female extragenital Ct and GC.(8–14) In population based studies of individuals with opposite sex partners, pharyngeal Ct rates have ranges from 0–22%, and pharyngeal GC rates have ranged from 0.4%–29%.(9, 14, 15)
Pharyngeal and anal Ct are of particular importance as they have the potential to serve as a reservoir of infection. Most pharyngeal infections (90%) are asymptomatic, suggesting that testing based on symptoms would not be effective.(16) As the duration of infection of pharyngeal Ct has been shown to be 667 days and that of rectal Ct is 579 days, these infections could persist long enough to be easily transmitted and remain undetected.(17) In comparison, approximately half of all genital Ct infections spontaneously clear in a year.(18)
Doxycycline is the first line of treatment for both genital and oral Ct.(6). Treatment failure for oral Ct with doxycycline is as low as 2%.(19) However, considering low barrier use during oral and anal sex among youth,(20) the risk of transmission prior to diagnosis and treatment is high through these routes. In contrast, a study examining condom use during one’s last genital sexual intercourse among African American men in the Deep South found rates between 56% and 65%.(21) For GC, ceftriaxone is the first line of treatment for both oral and genital infections.(6) However, there is mounting concern for antimicrobial resistance of GC, suggesting that treatment and infection clearance is important.(6) Hence, it would be important for clinicians to be aware of all sites of GC positivity to assess if treatment were effective.
This study investigated sexual behavior among a cohort of young Black men living in New Orleans, LA, including their rates of oral, vaginal, and anal sex. We examined barrier use for vaginal sex as compared to oral sex, as well as considered Ct and GC positivity rates in the context of this barrier use. It was hypothesized that barrier use will be lower for oral sex than for vaginal sex, and that if the risk of transmission of infection from the oral tract to the genital tract is high, Ct and GC positivity would be similar in those who report both inconsistent and consistent condom use during vaginal sex.
Methods
Study Background
Data was collected through the Check It program, a community-based Ct and GC screening program located in New Orleans, LA for young Black men ages 15–24 years who have sex with women. Methods have been described elsewhere,(22) but briefly, participants were recruited through venue-based methods (including barbershops, historically Black colleges and universities, job training programs, health fairs, and other community venues throughout New Orleans), peer referral, and social marketing strategies between May 2017 and May 2021.
Participants had to meet the following criteria to meet study eligibility: report having a penis, identify as African American or Black; be 15–26 years of age; live or spend most of their time in Orleans Parish; report having had vaginal sex with a woman in their lifetime; be able and willing to consent to study activities; speak and understand English; not have taken azithromycin in the 2 weeks prior to enrollment (as the data was collected when azithromycin was still the first line treatment); and not have previously enrolled in Check It.
After eligible participants provided informed consent, a survey was self-administered, a first catch urine sample was obtained, and contact information was documented. Participants received modest monetary compensation ($25 equivalent) in the form of a voucher for services at their recruitment site (e.g., haircut, food) or a gift card. STI status was assessed using nucleic acid amplification test (NAAT) Roche cobas®, which tests for both Ct and GC infection via urine specimens. Surveys were conducted with the audio computer-assisted self-interview (ACASI) software QDS™ Questionnaire Development System on laptops and tablets, for which participants had the option of using audio. The survey included questions on demographic characteristics, socio-economic status, sex education experiences, neighborhood environment, symptoms, STI history, STI fatalism, and health and sexual behaviors, including partner-specific questions. Study data were managed in REDCap hosted by Tulane University.(23)
Analytic Plan
For the purposes of the present analysis, data was limited to the participants who enrolled between August 14th, 2019 (when questions about extragenital sexual behaviors were added) and February 29th, 2020 (to avoid any changes in behavior attributed to the COVID-19 pandemic). Both demographic characteristics and risk behavior frequencies were tabulated to understand the extent to which risk was heterogenous in this population, and odds ratios and 95% confidence intervals were calculated. Finally, both demographic characteristics and risk behaviors were assessed in relation to STI positivity to understand the potential mechanisms for extragenital exposure.
Results
The mean age of the cohort was 19.8 years (SD: 2.4), with 42.3% aged 18 or younger. Just under twelve percent of participants had only completed high school, and another 61.7% had further education beyond the high school level. The median number of lifetime female partners reported was 5, though this ranged from 1 to 90 partners, and the average age of sexual debut was 15.1 (SD 1.8) years. Additionally, 9 individuals (2.4%) reported male partners in the last two months, and the same nine individuals were the only participants reporting any history of male sex partners. The median duration of partnerships reported as ongoing in the previous two months was 90 days; however, partnership duration ranged from 0 days to 12 years. About half of the men (45.3%) reported alcohol use in the past month and 61.1% reported drug use in the past month, of which 98% was marijuana use. Only 7% reported genital tract symptoms in the past two months.
Of the participants, 27.6% reported always using a condom during vaginal sex. A little over one-third (35.7%) of men reported performing cunnilingus at least once in the last two months, and 42.7% reported receiving fellatio. Of those who reported performing cunnilingus with their female partners, only 9.8% had ever used protection and only two individuals reported doing so consistently. Of those who reported receiving fellatio, 27.0% reported using a condom at least some of the time, with only 5.1% reporting consistent condom use during oral sex. 50.1% reported either fellatio or cunnilingus and, of these, 5.6% reported using condoms consistently during these acts. Only 5.9% of participants reported penile-anal sex with a female partner in the previous two months; data on barrier use during oral-anal sex was not collected. Among those with male partners, 5 (55.5%) had both given fellatio and received fellatio, though none reported consistent condom use during oral sex. Full demographic characteristics and reported sexual behaviors are available in Table 1.
Table 1:
Characteristics of the Cohort
| Characteristic | Men enrolled through February 2020 (n=373) N, % |
|---|---|
|
| |
| Age (mean years, SD) | 19.8 (2.4) |
| 18 or younger | 158 (42.4%) |
| Education Level | |
| Less than High School | 6 (1.6) |
| High School Student | 95 (25.5) |
| High School Graduate | 42 (11.3) |
| More Than High School | 230 (61.7) |
| Total female sexual partners (mean, SD) | 10.0 (14.4) |
| At least one male partner reported | 9 (2.4%) |
| Age at sexual debut (mean years, SD) | 15.1 (1.8) |
| Mean duration of partnership (mean days, SD) | 299.8 (514.1) |
| Alcohol use in past month | 169 (45.3%) |
| Binge drinking in past two months | 102 (27.3%) |
| Any drug use in past month | 228 (61.1%) |
| Marijuana use in past month | 223 (59.8 %) |
| Health insurance | 274 (73.5%) |
| Tested for Ct/ GC ever | 161 (43.2%) |
| Ct/ GC symptoms in previous two months | 26 (7.0%) |
| Condoms always used during vaginal sex | 103 (27.6%) |
| Any extragenital sex | 191 (51.2%) |
| Oral sex given to female (cunnilingus) | 133 (35.7%) |
| Oral sex given to female with barrier ever (n=133) | 13 (9.8%) |
| Oral sex given to female with barrier consistently (n=133) | 2 (0.5%) |
| Oral sex received (fellatio) | 159 (42.7%) |
| Oral sex received with a condom ever (n=159) | 493 (27.0%) |
| Oral sex received with a condom consistently (n=159) | 19 (5.1%) |
| Anal sex with a female partner | 22 (5.9%) |
| Oral or Anal Sex with a Man in last two months | 9 (2.4%) |
Consistent condom use for vaginal sex was associated with younger age (p=0.001), having shorter partnership durations (p=0.001), not using marijuana (p=0.004) or other drugs (p=0.002), not performing cunnilingus (p=0.003), and using a barrier among those receiving oral sex (p<0.001). Participant social and sexual behaviors were assessed in relation to their Ct and GC test results. Total number of female partners (p=0.002) and genital tract symptoms in the past two months (p<0.001) were associated with a greater likelihood of Ct, GC, and Ct & GC positivity. None of the following variables were associated with Ct or GC positivity: age, education, binge drinking, health insurance, drug use, age of sexual debut, average partnership duration, consistent condom use during vaginal sex, condom use during oral sex, dental dam use during oral sex, engaging in oral sex, engaging in anal sex, or reporting a male partner. These findings are reported in Tables 2 and 3.
Table 2:
Characteristics of the cohort by Condom Use During Vaginal Sex
| Characteristic | Consistent Condom use (n=117) n (%) | Inconsistent Condom use (n=252) n (%) | OR (95% CI) | p-value |
|---|---|---|---|---|
|
| ||||
| Age (mean years, SD) | 19.0 (2.4) | 20.2 (2.3) | 1.2 (1.1, 1.4) | 0.001 1 |
| Age category | ||||
| 15–18 | 61 (59.2) | 81 (33.8) | 1.0 (ref) | <0.001 2 |
| 19–24 | 42 (40.8) | 159 (66.3) | 2.7 (1.7, 4.3) | |
| Educationl Level | ||||
| High School or Less | 47 (42.7) | 84 (35.0) | 1.0 (ref) | 0.1662 |
| More Than High School | 63 (57.3) | 156 (65.0) | 1.4 (0.8, 2.2) | |
| Total female sexual partners (mean, SD) | 7.4 (11.6) | 11.7 (15.2) | 1.0 (1.0, 1.0) | 0.001 1 |
| At least one male partner reported | 0 (0) | 8 (3.3) | 0.9 (0.7, 1.0) | 0.1133 |
| Age at sexual debut (mean years, SD) | 15.1 (1.8) | 15.15 (1.8) | 1.0 (0.9, 1.1) | 0.9773 |
| Mean duration of partnership (mean days, SD) | 147.1 (291.7) | 343.8 (502.9) | 1.0 (1.0, 1.0) | 0.001 1 |
| Alcohol use in past month | 39 (37.9) | 120 (50.0) | 1.6 (1.0, 2.6) | 0.1022 |
| Binge drinking in past two months | 20 (19.4) | 75 (31.3) | 1.8 (1.1, 3.1) | 0.0732 |
| Any drug use in past month | 49 (47.6) | 162 (67.5) | 2.1 (1.3, 3.4) | 0.002 2 |
| Marijuana use in past month | 49 (47.6) | 158 (66.8) | 1.9 (1.2, 3.1) | 0.004 2 |
| Health insurance | 83 (80.6) | 169 (70.4) | 0.4 (0.2, 1.1) | 0.5162 |
| Tested for Ct/GC ever | 41 (40.2) | 111 (46.4) | 1.3 (0.8, 2.0) | 0.2262 |
| Ct/ GC symptoms in previous two months | 6 (5.8) | 19 (7.9) | 1.3 (0.5, 3.1) | 0.6442 |
| Oral sex given to female | 29 (28.2) | 108 (45.0) | 2.7 (1.4, 5.5) | 0.003 2 |
| Oral sex given to female with barrier (n=133) | 1(3.6) | 12 (11.3) | 0.3 (0.04, 10.7) | 0.3003 |
| Oral sex received | 40 (38.8) | 123 (51.2) | 2.1 (0.9, 4.9) | 1.1042 |
| Oral sex received with a condom (n=159) | 16 (41.0) | 27 (22.5) | 0.08 (0.02, 0.2) | <0.001 3 |
| Anal sex with a female partner | 5 (4.9) | 17 (7.1) | 1.6 (0.6, 4.5) | 0.2702 |
| Oral or Anal Sex with a Man in last two months (n=9) | 0 (0) | 8 (3.3) | 2.1 (1.7, 2.7) | 0.1702 |
Wilcoxon Rank-Sum Test
Chi-square Test
Fisher’s Exact Test
OR of more than high school versus high school or less
Table 3:
Characteristics of the cohort by Ct/GC Positivity
| Characteristic | Ct/ GC Negative (n=339) n (%) | Ct/GC Positive (n=53) n (%) | OR (95% CI) | p-value |
|---|---|---|---|---|
|
| ||||
| Age (mean years, SD) | 19.7 (2.4) | 20.2 (2.1) | 1.1 (0.9, 1.2) | 0.1221 |
| Age category | ||||
| 5–18 | 139 (43.7) | 17 (34.0) | 1.0 (ref) | 0.2202 |
| 19–24 | 179 (56.3) | 33 (66.0) | 1.5 (0.8, 2.8) | 0.2202 |
| Education level | ||||
| High School or Less | 122 (38.4) | 192 (38.0) | 1.0 (ref) | 1.03 |
| More Than High School | 196 (61.6) | 31 (62.0) | 1.0 (0.5, 1.9) | |
| Total female sexual partners (mean, SD) | 9.2 (13.5) | 15.2 (18.9) | 1.02 (1.01, 1.04) | 0.002 3 |
| At least one male partner reported | 7 (2.2) | 1 (2.0) | 1.1 (0.9, 1.4) | 1.03 |
| Age at sexual debut (mean years, SD) | 15.2 (1.8) | 14.9 (1.7) | 0.9 (0.8, 1.1) | 0.3273 |
| Mean duration of partnership (mean days, SD) | 296.6 (470.3) | 345.4 (754.8) | 1.0 (1.0, 1.0) | 0.9963 |
| Alcohol use in past month | 144 (45.3) | 24 (48.0) | 1.1 (0.6, 2.0) | 0.4172 |
| Binge drinking in past two months | 85 (26.7) | 16 (32.0) | 1.3 (0.7, 2.5) | 0.4962 |
| Any drug use in past month | 191 (60.1) | 35 (70.0) | 1.4 (0.8, 2.8) | 0.3182 |
| Marijuana use in past month | 186 (58.5) | 35 (70.0) | 1.6 (0.8, 3.0) | 0.2412 |
| Health insurance | 238 (74.8) | 32 (60.4) | 0.4 (0.2, 1.0) | 0.2342 |
| Tested for Ct/ GC ever | 134 (42.4) | 25 (50.0) | 1.5 (0.8, 2.7) | 0.556 |
| Ct/ GC symptoms in previous two months | 17 (5.3) | 9 (18.0) | 4.0 (1.7, 9.7) | <0.001 2 |
| Condoms always used during vaginal sex | 90 (28.3) | 12 (24.0) | 1.2 (0.6, 2.4) | 0.3842 |
| Oral sex given to female | 115 (36.2) | 17 (34.0) | 0.9 (0.4, 2.4) | 0.6282 |
| Oral sex given to female with barrier (n=145) | 12 (10.3) | 1 (5.9) | 1.84 (0.2, 51.7) | 0.9612 |
| Oral sex received | 138 (43.3) | 20 (40.0) | 0.8 (0.2, 2.4) | 0.6522 |
| Oral sex received with a condom (n=174) | 37 (26.8) | 5 (25.0) | 0.8 (0.2, 4.0) | 0.8642 |
| Anal sex with a female partner | 20 (6.3) | 1 (2.0) | 0.3 (0.0, 2.3) | 0.3323 |
| Oral or Anal Sex with a Man in last two months (n=9) | 7 (2.2) | 1 (2.0) | 0.9 (0.1, 7.5) | 1.03 |
T-test
Chi-square test
Wilcoxon Rank-Sum Test
There was no significant difference in Ct/GC rates between those engaging only in vaginal sex and those engaging in both vaginal and oral sex, stratified by condom use consistency during vaginal sex (χ2 = 1.93, p= 0.14). Among those having vaginal sex only, it appeared that there was a beneficial effect of consistent condom use although the difference in Ct/GC rates between using condoms consistently (8%) and those not doing so (19%) was not significant, p=0.10. Similarly, among those having vaginal sex and oral sex, there was no difference in Ct/GC rates between using condoms consistently (16%) and those not doing so (13%), p=0.56. Among those using condoms consistently, there was no significant difference in Ct/GC rates between those having vaginal sex only and those having vaginal and oral sex, p=0.22. Similarly, among those using condoms consistently, there was no significant difference in Ct/GC rates between those having vaginal sex only and those having vaginal and oral sex, p=0.25. These findings are reported in Figure 1. Only 10% of the sample reported receiving fellatio but not performing cunnilingus in the past two months and 13% of the sample reported performing cunnilingus but not receiving fellatio; thus, those having any type of oral sex were categorized together for the purpose of sample size.
Figure 1: Ct and GC positivity by sexual behavior and condom use during vaginal sex (N=373).
-p-value overall: 0.38
-p-value among those having condomless sex, between those having vaginal sex only and those having vaginal and oral sex: 0.25
-p-value consistently using condoms during vaginal sex between those having vaginal sex only and those having vaginal and oral sex: 0.22
-p-value among those having vaginal sex only, between condom use status: 0.10
-p-value among those having vaginal sex and oral sex, between condom use status: 0.56
Discussion
This study examined the sexual behaviors, barrier usage, and Ct and GC positivity rates among a cohort of young Black men living in New Orleans, Louisiana. The goal of the study was to understand the potential for extragenital exposure on genital chlamydia and gonorrhea transmission. As shown in Figure 1, condom use during vaginal sex tended to conferred protection for those who engaged in vaginal sex only but not for those who engaged in both vaginal and oral sex, suggesting that extragenital transmission is potentially occurring in this population.
Self-reported condom use can be subjected to social desirability bias; however, the use of computer assisted self-administered surveys (CASI) likely reduced the potential bias.(24) Also, the finding that consistent condom use among men who engaged in vaginal sex only did show a trend for protection suggests that self-reported condom use was accurate. It is possible that those reporting condom use consistently during vaginal sex likely contracted Ct or GC either from a previous partner or through non-vaginal sex. Given the low prevalence of anal sex overall (6%), it is unlikely that anal sex was driving much of the vaginal infections. The only factors that were significantly associated with Ct and GC positivity were the man’s total number of sex partners and the presence of Ct/GC symptoms, consistent with previously reported literature.(25–27) This further bolsters our assertation that self-reported behaviors were accurate.
We posit that oral sex increased vaginal Ct and GC transmission in this cohort, particularly since condom use during oral sex was low (27%) and dental dam use was even lower (10%). It is also worth noting that there was no significant difference in Ct/GC positivity when stratified by both the types of sexual acts (oral and vaginal sex or just vaginal) and condom use during vaginal sex. This suggests that a combination of both genital and extragenital exposures is likely driving positivity rates, with inconsistent condom use contributing to the spread of Ct and GC. Though the difference in Ct/GC rates by condom use among those having only vaginal sex was not statistically significant, there did appear to be a trend of lower infections in the group have only vaginal sex with consistent condom use. Similarly, there appeared to be a trend where those having vaginal sex only were less likely to be Ct/GC positive, than those having both oral and vaginal sex, among those using condoms consistently during vaginal sex. Both trends support the hypothesis of extragenital exposure.
This study suggests that screening individuals reporting opposite sex partnerships and engaging in oral sex for pharyngeal Ct/GC could be beneficial in interrupting the transmission of these STIs and reinforces the use of doxycycline for the treatment of Ct, to target potential extragenital infections. The wide range in number of partners and duration of partnerships also suggests a very heterogeneous environment of sexual behavior. Moreover, receiving fellatio and performing cunnilingus were common behaviors in this study population, and often reciprocal behaviors, though barrier use during these acts was low—findings which are consistent with what has been previously reported in a nationally representative study.(20)
The low use of barrier methods during extragenital sexual acts may be indicative of lower perceived risk during these activities. Hence, those consistently using condoms during vaginal sex may not believe themselves to be at risk of Ct/GC, despite having the same rates as those not using condoms consistently during vaginal sex. Alternatively, individuals may consistently use condoms for vaginal sex to avoid pregnancy, rather than solely to avoid STI exposure. This driver of condom use would also explain the difference in rates between condom use during vaginal versus extragenital sex. Additionally, a few men reported male partners, meaning that they may bridge sexual networks and have additional risks in terms of STI exposure. Extragenital screening could therefore be an important tool in such a diverse environment of sexual behavior.
This study had several strengths and a few limitations. The study captured many different elements of sexual behavior, which are useful in conceptualizing the landscape of sexual behavior amongst this population. However, this sample was relatively small, single site, only among Black young men, and oropharyngeal tests were not conducted, meaning that further research along with extragenital testing is needed to confirm the present findings. Finally, the present study focused on men as the index cases, meaning that their reported partnership information was not confirmed by their partners. Further research to examine a multi-gendered cohort may be useful in detecting differences in sexual behaviors and outcomes among young people in general. Additionally, the use of network data may be illustrative of network-level trends in Ct/GC prevalence.
Extragenital Ct and GC infections could explain the positive test results among those reporting consistent condom use during vaginal sex. Oral sex was a common behavior among the present cohort of young Black men in New Orleans, LA, though barrier use during these acts was quite low. As such, screening for extragenital Ct and GC based on exposure history among heterosexual partnerships may be useful in interrupting community transmission and reducing rates of infection in the community.
Support:
NICHD/NIAID R01HD086794
Footnotes
Conflicts of interest: The authors have no conflicts of interest to report.
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