Sexual Risk Behaviors Associated with Sexually Transmitted Infections in a US Military Population Living with HIV After the Repeal of “Don't Ask,Don't Tell”

Abstract

Risk behaviors associated with sexually transmitted infections (STIs) among people living with HIV (PLWH) have not been well characterized in the US military. We identified risk behaviors associated with a new STI in this population after the repeal of “Don't Ask, Don't Tell.” US Military HIV Natural History Study participants who completed the risk behavior questionnaire (RBQ) between 2014 and 2017 and had at least 1 year of follow-up were included (n = 1589). Logistic regression identified behaviors associated with incident STI in the year following RBQ completion. Overall, 18.9% acquired an STI and 52.7% reported condom use at last sexual encounter. Compared with those with no new sex partners, participants with between one and four or five or more new partners were 1.71 [1.25–2.35] and 6.12 [3.47–10.79] times more likely to get an STI, respectively. Individuals reporting low or medium/high perceived risk of STI were 1.83 [1.23–2.72] and 2.65 [1.70–4.15] times more likely to acquire a new STI than those reporting no perceived risk, respectively. Participants who preferred not to answer about sexual preference, number of new partners, or perceived STI risk were also more likely to acquire a new STI. Our study illustrates that despite regular access to health care and accurate perceptions of risk, rates of STI among PLWH remain high in the US military setting, as in others. Given the potential individual and public health consequences of STI coinfection after HIV, more work is needed to assess interventions aimed at sexual behavior change for PLWH.

Introduction

The most recent sexually transmitted disease (STD) surveillance report from the Centers for Disease Control and Prevention (CDC) states that since 2014, the number of chlamydia, gonorrhea, and syphilis cases in the United States has increased by 19%, 63%, and 71%, respectively, signifying the highest number of reported syphilis and gonorrhea cases since 1991 and the most chlamydia cases ever reported to the CDC.¹ Since the introduction of highly active antiretroviral therapies in 1996, people living with HIV (PLWH), and specifically men who have sex with men (MSM), have exhibited an increased risk for acquiring new sexually transmitted infections (STIs).² A systematic review of 37 studies measuring the prevalence of sexually transmitted coinfections among MSM living with HIV found the overall mean point prevalence for confirmed STIs to be 16.3%.³

Similarly, 77.6% of all male primary and secondary syphilis cases in the United States in 2018 were found in MSM; almost half of whom were also infected with HIV.¹ MSM with HIV are also more likely than MSM without HIV to test positive for gonorrhea and syphilis, according to the CDC's STD Surveillance Network (SSuN).¹ STI prevention is important for PLWH because STIs can result in potentially serious health consequences for this population. Antiretroviral therapy (ART) does not completely suppress HIV in semen of sexually active MSM,⁴ and STI coinfection can decrease CD4 count,⁵ increase viral load in the blood plasma,⁶ increase HIV shedding in genital tract secretions,⁷ and increase susceptibility to superinfection or reinfection.⁸ As a marker for sexual risk behavior, the presence of STI can also indicate risk of HIV transmission from those who are not virally suppressed.

The SSuN has also identified young adults and racial and ethnic minorities as high-risk groups with respect to STI acquisition in the United States. Given the large proportion of young, racially and ethnically diverse males that make up the US military, it may not seem surprising that rates of chlamydia, gonorrhea, and syphilis are on the rise in this setting.⁹ Like civilian populations in the United States, nearly half of PLWH in the US military acquire at least one STI after HIV diagnosis.^10

–13

While the US military may be young and racially diverse, its service members are socioeconomically stable compared with the general US population at highest risk for becoming infected with STDs, and military affiliation (as an active duty member, dependent, or retiree) confers open access to health care services and medications. Income inequality and disparities in access to health care have been shown to be strongly associated with an increased risk of STI,¹⁴ yet the US military provides an example of a population where these barriers are largely controlled but rates of STI are still high. This suggests that other factors, including risky sexual behaviors, play an equally important and independent role in the development of STIs, especially among MSM living with HIV.

Research focusing on the sexual behaviors of PLWH in the US military could improve the current understanding of factors affecting STI acquisition in a population with equal access to care, but studies have been limited. This is partially because the majority of PLWH in the military identify as lesbian, gay, bisexual, or transgendered (LGBT) and until 2011, this population was serving under the controversial “Don't Ask, Don't Tell” (DADT) policy.¹⁵ DADT allowed LGBT personnel to remain in the military if sexual orientation was not openly disclosed. Under DADT, data on sexual risk behaviors of PLWH in the military were not regularly collected,¹⁶ and this policy may have further contributed to the existing stigma surrounding PLWH in the military.^17,18 The repeal of DADT has provided a new opportunity to understand sexual behaviors of PLWH in the US military. This study aimed to determine the sexual behaviors associated with STI incidence in a cohort of PLWH from the Department of Defense (DoD) US Military HIV Natural History Study (NHS) in the period following repeal of DADT.

Methods

Study design and population

The NHS is an ongoing, longitudinal cohort study of active duty members, beneficiaries, and retirees from all service branches living with HIV who have been recruited from seven military medical centers in the United States and identified through routine and mandatory DoD screening. The NHS began enrollment in 1986, and previous publications have described this cohort in detail.¹⁹ The NHS is considered an incident cohort since the last documented HIV-negative test before a positive test is available for most participants. NHS participants were included in this analysis if they were 18 years or older, completed the baseline risk behavior questionnaire (RBQ) between March 2014 and December 2017 and remained in the study for at least 1 year after completing the survey. All NHS participants provided written informed consent, and Institutional Review Board approval for this study was obtained centrally and from each participating site.

Data collection

NHS study visits occur approximately every 6 months and include a medical record review, physical examination, laboratory measurements, and a medical history interview with a research coordinator. In 2006 STI screening was incorporated into routine visits at all study sites, including urine nucleic acid amplification testing (NAAT) for gonorrhea (GC) and Chlamydia (CT), serology for hepatitis B virus (HBV) and herpes simplex virus-2 (HSV-2), and screening for syphilis infection by a traditional or reverse algorithm, depending on the clinical practices of each study site. Although study sites now conduct routine oropharyngeal and anorectal GC/CT testing among MSM, only urogenital screening was available during the follow-up period for this analysis.

Collection of risk behavior data in the NHS began in March of 2014 through the RBQ. This analysis focused on responses collected from the baseline questionnaire through December 2017. The 20-min survey was administered annually on a tablet using a computer-assisted self-interview (CASI) format. The survey focused on five domains: (1) perceived health status; (2) drug and alcohol use; (3) condom use; (4) sexual history; and (5) most recent sexual encounter. The perceived health status section asked participants to estimate the number of poor physical and mental health days experienced in the last month and to classify general health as “excellent,” “good,” “fair,” or “poor.” The drug and alcohol section asked participants a series of multiple choice questions about the frequency and type of alcohol or drugs used in daily life. The condom use section also included multiple choice questions and focused on general practices such as where and how often condoms were accessed. This section also asked participants to assess their own risk of contracting an STI other than HIV. The sexual history section aimed to capture information about sexual experiences and risk behaviors of participants occurring in the last 3 months through a series of multiple choice questions and open-ended responses; it included questions about number of partners, relationship status, type of sexual activity, condom use, and the influence of drugs and/or alcohol during sex. The final section focusing specifically on most recent sexual encounter included multiple choice questions about when, with whom, and under what circumstances this most recent encounter took place. To ensure survey completeness, a response to each question was necessary to get to the next screen, but each question included a “prefer not to answer” (PNTA) option if the participant chose not to answer the question.

Primary outcome: incident STI

Participants were classified as having an incident STI if they had any new STI diagnosis during the 1-year period following RBQ completion. For GC and CT, a diagnosis was considered incident if it followed a negative test or occurred beyond 45 days from a previous diagnosis. For HBV, HSV-2, and syphilis, an incident diagnosis was defined as a positive test preceded by a negative test.

Covariates of interest: demographics, clinical characteristics, and risk behaviors

Relevant demographics and clinical characteristics were obtained from the regularly scheduled semiannual study visits, and included age, marital status, duty status, viral load, CD4 count, and ART status at time of RBQ completion, as well as age at HIV diagnosis, years since HIV diagnosis, sex, race, service branch, and initial military rank (often used a surrogate for education level²⁰). In this analysis, the risk behaviors of interest collected from the RBQ included alcohol use, drug use, MSM status, number of new sex partners, relationship to last sex partner, condom use at last sexual encounter, location of first encounter with last sex partner, and perceived STI risk.

Statistical analyses

Descriptive analyses were performed to compare baseline characteristics and RBQ responses by STI status, and are presented as frequencies (percentages) or medians [interquartile ranges (IQRs)] for categorical or continuous variables, respectively, with Chi-squared, Fisher's exact or Kruskal–Wallis test results reported as appropriate. Unadjusted and adjusted logistic regression models were used to investigate the association between odds of new STI and the covariates of interest. Covariates found to be significant in the descriptive analyses (p < 0.05) were considered for inclusion in the logistic regression models and a stepwise selection process was used to produce the final adjusted model. Results were reported as odds ratios (ORs) with 95% confidence intervals (CIs) and p values. Analyses were performed using SAS software, version 9.4 (Cary, NC).

Results

Cohort demographics

Table 1 summarizes the demographic and clinical characteristics of the 1589 participants included in this analysis. The study population was primarily male (94.2%) and on ART (96.8%). Caucasian participants comprised 38.5% of the population, whereas 44.9% were African American and 16.7% were either Hispanic or another race category. The median age at time of HIV diagnosis was 29.1 (IQR 24.8–35.6) and the median time since HIV diagnosis was 9.4 years (IQR 1.8–20.1). Approximately 60% of study participants were single, and the majority were either active duty or retired military personnel.

Table 1.

Demographic and Clinical Characteristics of Natural History Study Participants Completing the Baseline Risk Behavior Questionnaire Between 2014 and 2017, by Sexually Transmitted Infection Status

	Total	No incident STI	Any incident STI	p^*
Number of subjects	1589	1288	301
Gender				<0.0001
Male	1497 (94.2)	1199 (93.1)	298 (99.0)
Female	92 (5.8)	89 (6.9)	3 (1.0)
Race				0.0001
Caucasian	611 (38.5)	527 (40.9)	84 (27.9)
African American	713 (44.9)	557 (43.2)	156 (51.8)
Hispanic/other	265 (16.7)	204 (15.8)	61 (20.3)
Marital status at RBQ				0.0029
Married	633 (39.8)	536 (41.6)	97 (32.2)
Single	947 (59.6)	743 (57.7)	204 (67.8)
Missing	9 (0.6)	9 (0.7)	0 (0.0)
Age at HIV diagnosis (years)	29.1 [24.8–35.6]	29.7 [25.3–36.3]	26.7 [23.5–31.7]	<0.0001
Age at RBQ (years)	43.3 [30.5–51.9]	45.1 [32.8–53.2]	31.0 [25.5–42.9]	<0.0001
Service branch				0.8779
Air force	362 (22.8)	295 (22.9)	67 (22.3)
Army	380 (23.9)	312 (24.2)	68 (22.6)
Marines	119 (7.5)	93 (7.2)	26 (8.6)
Navy	686 (43.2)	553 (42.9)	133 (44.2)
Other	42 (2.6)	35 (2.7)	7 (2.3)
Duty status at RBQ				<0.0001
Active duty	679 (42.7)	481 (37.3)	198 (65.8)
Dependent	48 (3.0)	46 (3.6)	2 (0.7)
Retired	827 (52.0)	736 (57.1)	91 (30.2)
Other duty	35 (2.2)	25 (1.9)	10 (3.3)
Initial military rank				<0.0001
Enlisted	1246 (78.4)	977 (75.9)	269 (89.4)
Officer/warrant	187 (11.8)	163 (12.7)	24 (8.0)
Not applicable	156 (9.8)	148 (11.5)	8 (2.7)
Time from HIV diagnosis to RBQ (years)	9.4 [1.8–20.1]	11.7 [3.0–21.4]	2.1 [0.1–9.1]	<0.0001
Viral load at RBQ				<0.0001
Undetectable (<50 copies/mL)	1198 (75.4)	1018 (79.0)	180 (59.8)
Detectable (≥50 copies/mL)	379 (23.9)	258 (20.0)	121 (40.2)
Missing	12 (0.8)	12 (0.9)	0 (0.0)
CD4 at RBQ (cells/mm³)	575.0 [405.0–760.0]	574.0 [402.0–768.0]	579.0 [426.5–748.5]	0.5968
On ART at RBQ				0.0025
No	51 (3.2)	33 (2.6)	18 (6.0)
Yes	1538 (96.8)	1255 (97.4)	283 (94.0)

n (%) or median (IQR) for categorical and continuous variables, respectively. p values derived from Kruskal–Wallis test for continuous variables and Chi-squared or Fisher's exact test with Monte Carlo estimation for the exact p value for categorical variables.

ART, antiretroviral therapy; IQR, interquartile range; RBQ, risk behavior questionnaire; STI, sexually transmitted infection.

Overall, 18.9% of all study participants (n = 301) were diagnosed with an incident STI within 1 year following RBQ completion. Of these, 28.6% were CT, 27.2% were syphilis, 29.9% were GC, 12.0% were HSV-2, and 7% were HBV. The proportion of NHS participants diagnosed with an incident STI within 1 year of survey completion increased from 11% in 2014 to 35% in 2016, and 27% of participants who completed the baseline RBQ in 2017 acquired a new STI.

Compared with participants without an incident STI, those with an incident STI were more likely to be younger, single, active duty, enlisted males who self-reported as African American or Hispanic (p < 0.0001). The median time since HIV diagnosis was also significantly shorter for the group with an incident STI (2.1 vs. 11.7 years, p < 0.0001). Most study participants were on ART (96.8%), but 6% of those with an incident STI were not on ART at the time of RBQ completion, compared with 2.6% without an incident STI (p = 0.0025). Finally, viral load was significantly different between the two groups, with 40.2% of those with an incident STI and 20% without an incident STI having a detectable viral load (<50 cells/mL) at the time of RBQ completion (p < 0.0001).

Description of risk behaviors

Table 2 summarizes the self-reported risk behaviors for the cohort, stratified by STI acquisition status. Alcohol use was significantly different by STI status, with a larger proportion of participants in the incident STI group reporting three or more drinks per day (36.5% vs. 27.3%, p = 0.0027). Drug use was rare in the study population and did not differ significantly between the two groups. Approximately three quarters of the study population reported ever engaging in MSM behavior while nearly 90% of those with an incident STI reported ever being MSM (p < 0.0001). The majority of participants reported no new sex partner in the last 3 months, but the proportion of participants with no new sex partner was significantly larger among those without an incident STI as compared with those with an incident STI (68.8% vs. 36.9%; p < 0.0001). A larger proportion of participants with an incident STI reported having at least one new sex partner in the last 3 months, with 13.6% reporting five or more new partners. Just over half of participants reported condom use at last sexual encounter (52.7), with an even smaller proportion using a condom in the incident STI group (49.5% vs. 53.4%, p = 0.0078). Of those with an incident STI, 15.3% and 32.9% reported anonymous or casual sex partners, respectively, compared with 8.4% and 22.7% of participants without an incident STI (p < 0.0001). Location of first encounter with last sex partner was also significantly different by STI status, with 53.5% of those with an incident STI meeting their last sex partner on the internet or through a social networking application, compared with 30.9% of participants without an incident STI (p < 0.0001). Perceived risk of STI was significantly higher in the incident STI group, with 71.8% of participants reporting some level of perceived risk, compared with 53.3% in the group without an incident STI (p < 0.0001).

Table 2.

Risk Behavior Questionnaire Results for Natural History Study Participants Completing the Baseline Survey Between 2014 and 2017, by Sexually Transmitted Infection Status

	Total	No incident STI	Any incident STI	p^*
Number of subjects	1589	1288	301
Alcohol use, typical number of drinks per day				0.0027
None	258 (16.2)	227 (17.6)	31 (10.3)
1–2	826 (52.0)	672 (52.2)	154 (51.2)
3+	462 (29.1)	352 (27.3)	110 (36.5)
PNTA	12 (0.8)	11 (0.9)	1 (0.3)
Missing	31 (2.0)	26 (2.0)	5 (1.7)
Hard drug use, ever				0.5937
No	1271 (80.1)	1026 (79.7)	246 (81.7)
Yes	175 (11.0)	144 (11.2)	31 (10.3)
PNTA	26 (1.6)	19 (1.5)	7 (2.3)
Missing	116 (7.3)	99 (7.7)	17 (5.6)
MSM, ever				<0.0001
No	256 (16.1)	243 (18.9)	13 (4.3)
Yes	1228 (77.3)	958 (74.4)	270 (89.7)
PNTA	88 (5.5)	74 (5.7)	14 (4.7)
Missing	17 (1.1)	13 (1.0)	4 (1.3)
Number of new sex partners, last 3 months (PNTA)				<0.0001
No new sex partner	997 (62.7)	886 (68.8)	111 (36.9)
1–4 people	465 (29.3)	328 (25.5)	137 (45.5)
5+ people	73 (2.1)	32 (2.5)	41 (13.6)
PNTA	127 (8.0)	108 (8.4)	11 (3.7)
Missing	20 (1.3)	19 (1.5)	1 (0.3)
Condom use, last sexual encounter				0.0078
No	542 (34.1)	417 (32.4)	125 (41.5)
Yes	837 (52.7)	688 (53.4)	149 (49.5)
PNTA	147 (9.3)	129 (10.0)	18 (6.0)
Missing	63 (4.0)	54 (4.2)	9 (3.0)
Relationship status, last sex partner				<0.0001
Anonymous	154 (9.7)	108 (8.4)	46 (15.3)
Casual	391 (24.6)	292 (22.7)	99 (32.9)
Main/steady	865 (54.4)	734 (57.0)	131 (43.5)
PNTA	121 (7.6)	105 (8.2)	16 (5.3)
Missing	58 (3.7)	49 (3.8)	9 (3.0)
Meeting location, last sex partner				<0.0001
At bar/club/restaurant	195 (12.3)	163 (12.7)	31 (10.6)
At work	89 (5.6)	85 (6.6)	4 (1.3)
Internet/social network	559 (35.2)	398 (30.9)	161 (53.5)
On temporary duty	12 (0.8)	6 (0.5)	6 (2.0)
On vacation	38 (2.4)	34 (2.6)	4 (1.3)
Through friends	290 (18.3)	240 (18.6)	50 (16.6)
Through gym/sports	37 (2.3)	34 (2.6)	4 (1.3)
Other	153 (9.6)	142 (11.0)	11 (3.7)
PNTA	166 (10.4)	143 (11.1)	23 (7.6)
Perceived STI risk				<0.0001
No risk	538 (33.9)	492 (38.2)	46 (15.3)
Low risk	612 (38.5)	492 (38.2)	120 (39.9)
Med/high risk	290 (18.3)	194 (15.1)	96 (31.9)
Don't know	82 (5.2)	61 (4.7)	21 (7.0)
PNTA	40 (2.5)	29 (2.3)	11 (3.7)
Missing	27 (1.7)	20 (1.6)	7 (2.3)

p Values were derived from Chi-squared or Fisher's exact test for categorical variables.

MSM, men who have sex with men; PNTA, prefer not to answer.

Odds of incident STI

Table 3 reports the unadjusted and adjusted odds of incident STI and 95% CIs resulting from the univariate and multivariate logistic regression models. In the unadjusted analyses, every 10-year increase in age was associated with 47% decreased odds of acquiring a new STI (OR = 0.53 [0.47–0.60]). In addition, each additional year since HIV diagnosis was associated with a 7% decrease in odds of acquiring a new STI (OR = 0.93 [0.91–0.94]). Compared with Caucasians, African Americans and Hispanic/other were almost twice as likely to become infected with a new STI (OR = 1.76 [1.31–2.35]) and OR = 1.88 [1.30–2.71], respectively), and married participants were 34% less likely than single participants to acquire an STI (OR = 0.66 [0.51–0.86]). Participants on active duty were more than three times as likely to acquire an STI than those who were nonactive duty (OR = 3.23 [2.48–4.20]), and enlisted military personnel were 87% more likely to become infected with an STI than officers (OR = 1.87 [1.19–2.93]). Participants on ART were 59% less likely to acquire a new STI than those not on ART (OR = 0.41 [0.23–0.75]) and similarly, those with a detectable viral load were more than two and a half times more likely to acquire an STI than those who had reached undetectable status (OR = 2.65 [2.03–3.47]). Participants who were ever MSM or who PNTA the question pertaining to MSM status were greater than five and three times more likely than those who were never MSM to acquire a new STI (OR = 5.27 [2.97–9.35] and OR = 3.54 [1.59–7.86], respectively). Participants who reported using a condom at last sexual encounter were 28% less likely to acquire a new STI compared with those who reported using a condom (OR = 0.72 [0.55–0.94]). Participants reporting between one and four new sex partners in the last 3 months were more than three times as likely to contract an STI (OR = 3.33 [2.52–4.41]), and participants reporting five or more new sex partners were more than ten times as likely to contract an STI than individuals with no new sex partner (OR = 10.23 [6.19–16.91]). Participants who reported their last sex partner to be casual or anonymous were more likely to acquire a new STI than those who reported their last sexual partner to be a main/steady partner (OR = 1.90 [1.42–2.55] and OR = 2.39 [1.61–3.53], respectively). Compared with participants reporting no perceived risk of STI, individuals reporting low or medium/high perceived risk were 2.61 [1.82–3.75] and 5.29 [3.59–7.81] times more likely to acquire a new STI infection in the unadjusted model, respectively. Individuals reporting unknown risk for STI or who PNTA the perceived risk question were also more likely to become newly infected with an STI (OR = 3.68 [2.06–6.58] and OR = 4.06 [1.90–8.65], respectively).

Table 3.

Odds of Incident Sexually Transmitted Infection for Natural History Study Participants Who Completed the Risk Behavior Questionnaire Between 2014 and 2017

	Unadjusted^*				Adjusted^*
	OR	LCL	UCL	p	OR	LCL	UCL	p
Age at RBQ (per 10 years)	0.53	0.47	0.60	<0.0001	0.74	0.60	0.92	0.0064
Race
Caucasian	Reference
African American	1.76	1.31	2.35	0.0001	1.72	1.23	2.40	0.0017
Hispanic/other	1.88	1.30	2.71	0.0008	1.39	0.91	2.12	0.1334
Marital status
Single	Reference
Married	0.66	0.51	0.86	0.0021
Year from HIV diagnosis to RBQ (per year)	0.93	0.91	0.94	<0.0001	0.97	0.94	1.00	0.0311
Viral load
Undetectable (<50 copies/mL)	Reference
Detectable (≥50 copies/mL)	2.65	2.03	3.47	<0.0001	1.61	1.16	2.23	0.0041
CD4 at RBQ (cells/mm³)	1.00	1.00	1.00	0.5263
On ART at RBQ
No	Reference
Yes	0.41	0.23	0.75	0.0033
Service
Air force	Reference
Army	0.96	0.66	1.39	0.8286
Marines	1.23	0.74	2.05	0.4239
Navy	1.06	0.76	1.47	0.7305
Other	0.88	0.38	2.07	0.7704
Active duty status
Nonactive duty	Reference
Active duty	3.23	2.48	4.20	<0.0001
Initial rank
Officer/warrant	Reference
Enlisted	1.87	1.19	2.93	0.0063
Alcohol use, typical number of drinks per day
None	0.60	0.39	0.90	0.0143	0.81	0.51	1.31	0.3957
1–2	Reference
3+	1.36	1.03	1.80	0.0280	0.80	0.58	1.11	0.1767
PNTA	0.40	0.05	3.10	0.3778	0.43	0.05	3.86	0.4498
Condom use, last sexual encounter	Reference	0.55	0.94	0.017	0.93	0.68	1.27	0.6463
No	0.72	0.27	0.79	0.0049	0.61	0.32	1.18	0.142
Yes	0.47
PNTA
MSM, ever
No	Reference
Yes	5.27	2.97	9.35	<0.0001	3.60	1.96	6.62	<0.0001
PNTA	3.54	1.59	7.86	0.0019	3.30	1.36	7.97	0.0081
Number of new sex partners, last 3 months
No new sex partner	Reference
1–4 people	3.33	2.52	4.41	<0.0001	1.66	1.21	2.28	0.0016
≥5 people	10.23	6.19	16.91	<0.0001	5.93	3.35	10.47	<0.0001
PNTA	3.82	1.81	8.04	0.0004	2.98	1.22	7.27	0.0168
Relationship status, last sex partner
Main/steady	Reference
Casual	1.90	1.42	2.55	<0.0001
Anonymous	2.39	1.61	3.53	<0.0001
PNTA	0.85	0.49	1.49	0.5787
Meeting location, last sex partner
Through friends	Reference
At a bar/club/restaurant	0.94	0.58	1.53	0.8108
Internet/social network	1.94	1.36	2.77	0.0003
Other	0.37	0.19	0.74	0.0046
PNTA	0.77	0.45	1.32	0.3436
Perceived STI risk
No risk	Reference
Low risk	2.61	1.82	3.75	<0.0001	1.91	1.28	2.84	0.0014
Medium/high risk	5.29	3.59	7.81	<0.0001	2.72	1.74	4.28	<0.0001
Don't know risk	3.68	2.06	6.58	<0.0001	1.96	1.03	3.73	0.0413
PNTA	4.06	1.90	8.65	0.0003	2.55	1.00	6.48	0.0489

LCL and UCL in the unadjusted and adjusted models refer to lower confidence level and upper confidence interval, respectively.

OR, odds ratio.

The stepwise selection process resulted in age, race, time since HIV diagnosis, viral load, MSM status, number of new sex partners, and perceived STI risk being kept in the adjusted multivariate model. Despite being significant in the univariate analyses, alcohol and condom use did not significantly affect odds of incident STI in the adjusted model, nor did active duty status, rank, ART status, relationship status, or meeting location. Since alcohol and condom use were hypothesized to significantly affect odds of incident STI, they were kept in the adjusted model despite dropping out as a result of the stepwise selection process. Nevertheless, the resulting ORs remained nonsignificant and did not greatly change the magnitude or direction of the relationships between the other covariates and odds of incident STI.

Discussion

This is the first study to utilize STI screening results and risk behavior data from all branches of the US military to identify risk behaviors associated with incident STI in a cohort of PLWH with equal access to health care in the post-DADT era. The rate of infection in this setting was high and regular condom use was not common, despite continued education efforts and guidance provided to leaders and medical professionals in the military setting.²¹ Younger age, non-Caucasian race, shorter time since HIV diagnosis, detectable viral load, ever engaging in MSM behavior, increased number of new sex partners, and higher perceived risk for STI were associated with increased odds of acquiring a new STI in the year following RBQ completion.

Our finding that 18.9% of PLWH in the NHS acquired a new STI in the year following RBQ completion contrasts slightly with that of an earlier study of STIs among PLWH in the US military conducted in 2013 that found the proportion experiencing a new STI among PLWH in this population to be 23.7% in the 10 years since HIV diagnosis.¹³ Since our study utilized STI screening results from a longitudinal cohort study and Tzeng et al.¹³ relied on surveillance data from the Defense Medical Surveillance System and International Classification of Diseases (ICD)-9 codes, this difference in incidence may be partially due to differences in study populations and the way STIs were ascertained in each study. In addition, Tzeng et al.¹³ measured STI incidence beginning immediately after HIV diagnosis, whereas the median time from HIV infection to RBQ completion in our study was >9 years, and half of the new STIs in the prior study occurred in the 1st year following HIV diagnosis.

Nevertheless, a recent report focusing on STI trends suggests that rates of infection in the broader military population are increasing,²² and our results support this finding since incident STI rates more than doubled over the study period. It is also important to consider that while the rate of STI acquisition after HIV diagnosis in the US military may appear higher than the rate found in some civilian populations of PLWH,²³ this difference may be due to ascertainment bias resulting from active screening practices in the NHS and military, as well as differences in access to care, since the US military requires annual medical examinations for PLWH and therefore provides more opportunities for STI screening.^24

–27 However, comparative studies have identified that military service members are at increased risk for STI compared with geographically similar civilians.²⁸

This analysis found that although condom use was significantly associated with decreased odds of acquiring a new STI in the univariate analysis, the association was not significant after adjustment. This may be due to the association of condom use with other covariates in the adjusted model, such as number of new sex partners or perceived risk. For instance, less than five percent of the study population reported five or more new sex partners in the last 3 months and it is possible that those with fewer new sex partners were less likely to use condoms. Similarly, perceived STI risk may be mediating some of the effect between condom use and odds of new STI, or this covariate may serve as a surrogate for condom use.

The relationship between perceived STI risk and other risky sexual behaviors was provisionally explored as a follow-up to this analysis and is described in Supplementary Fig. S1. Supplementary Fig. S1a stratifies condom use by levels of perceived STI risk and shows that only 40% of those who reported medium or high perceived STI risk used a condom at last sexual encounter, compared with nearly 60% of those reporting no or low risk of STI. The stepwise multivariate model selected the strongest variables and identified independent information contained within them, but if perceived STI risk is a sufficient surrogate for condom use, this may explain the lack of significance in the multivariate model. In addition, nearly 10% of the study population responded PNTA when asked about condom use. It is possible that these participants were more likely not to be using condoms and that our results may therefore be biased toward a null effect.

It is also important to note that condom use was relatively low for the entire study population, with only half of study participants reporting condom use at last sexual encounter. Previous research has shown that individual beliefs about viral load and the effectiveness and availability of ART are associated with changes in risky sex behaviors, such that those who believe undetectable viral load and regular use and availability of ART to be protective against HIV transmission are more likely to engage in unprotected sex.²⁹ Condom use may be low in our study population since nearly all the participants were on ART and three quarters were virally suppressed. Since condom use at last sexual encounter did significantly affect odds of incident STI in the univariate analysis, it is important for efforts aimed at promoting consistent condom use to continue in the DoD population living with HIV, as it is for all PLWH, regardless of viral suppression status.

Viral suppression is strongly correlated with good ART adherence,^30,31 while poor adherence may be associated with an increased likelihood of engaging in risky sexual behaviors.³² It is therefore understandable that a detectable viral load was associated with an increased odds of incident STI in our study. On the other hand, research has also shown that for PLWH on ART, STI diagnoses can be associated with the belief that an HIV suppression means it is less likely for partners to become infected during unsafe sex, easier to relax about unsafe sex and safer to have condomless sex.³³ Since 2016, HIV prevention campaigns such as the “Undetectable = Untransmissible” (U = U) initiative have emphasized that achieving viral suppression through ART adherence reduces the risk of sexual HIV transmission to zero,³⁴ and subsequent studies have confirmed this protective effect of ART.³⁵

Nevertheless, careful attention must be paid to the messaging surrounding risk behaviors that may increase the odds of new STI, such as condom use, relationship status (e.g., casual or anonymous encounters) and number of new or concurrent sex partners. The increased rates of STI observed in our study coincide with a 70% viral suppression rate for NHS participants diagnosed between 1996 and 2010³⁶ and a 90% viral suppression rate for those diagnosed between 2010 and 2015.³⁷ In the era of “treatment as prevention,” detectable viral load should be thought of as a risk factor for HIV transmission as well as STI acquisition, and counseling about risky sexual behaviors and promotion of safe sex practices, with a focus on preventing STIs, should continue to be emphasized for PLWH who achieve and maintain viral suppression.

This analysis also supports the findings from CDC and others that MSM, and specifically MSM living with HIV, are at increased risk for a new STI. The Medical Monitoring Project (MMP) is an HIV surveillance system in the United States designed to provide estimates of behavioral and clinical characteristics of PLWH receiving medical care. One MMP study of HIV/STD prevention services utilized by PLWH found that only 52% received any HIV/STD prevention service and that MSM were less likely to receive risk-reduction interventions compared with non-MSM populations,³⁸ despite being identified as a high-risk group. Since the DoD provides equal access to health care services for all its members, our study suggests that more research is needed to understand the barriers to utilization and uptake of STD prevention services such as counseling and behavior change strategies for MSM (with and without HIV) in the military.

Our study also found that those who chose PNTA were at a greater risk for acquiring an STI than those who identified as never MSM. Although this group comprised only 6% of our study population, the finding suggests that some MSM may still be experiencing high levels of perceived and/or personal stigma in the post-DADT era that could in turn increase the risk of STI. Similarly, participants who chose not to reveal how many new sex partners they had in the last 3 months and those who PNTA the question about perceived STI risk were also more likely to acquire a new STI. Increased efforts should therefore be made to better understand and reduce stigma attached to MSM and other risky sexual behaviors for PLWH within and outside of the US military.

A final noteworthy finding from this study was the strong correlation between increased levels of perceived STI risk and increased odds of incident STI. The perceived risk is a core concept for several well-respected behavior change models, including the Health Belief Model,³⁹ the AIDS Risk Reduction Model,⁴⁰ and the Information–Motivation–Behavioral Skills Model.⁴¹ STI prevention interventions grounded in these conceptual frameworks focus on increasing the perceived risk of STIs to reduce rates of infection. Our results suggest that accurately perceiving one's own risk of STIs is possible, and the US military may provide a unique opportunity to study how this can be achieved. However, perceived STI risk did not correlate with decreased odds of STI incidence in our analysis, and risk awareness alone may not be enough for lowering rates of STIs.

In fact, a larger proportion of participants reporting medium/high levels of perceived STI risk did not use condoms, engaged in casual or anonymous sex, and had five or more sex partners in the last 3 months, as depicted in the Supplementary Fig. S1. This supports the notion that study participants were able to accurately assess their risk for a new STI and suggests that additional work must be done in this and other populations to promote safer sex practices and mitigate the STI risk. Several meta-analyses of interventions aimed at reducing risky sexual behaviors have been conducted in recent years. One such review by Herbst et al. found that successful interventions were (1) based on theoretical models; (2) included interpersonal skills training; (3) incorporated several delivery methods; and (4) were delivered over multiple sessions spanning a minimum of 3 weeks.⁴² Another review confirmed the effectiveness of grounding behavioral interventions in theoretical models, and suggested that matching the gender or ethnicity of the communicator to the intervention recipients and tailoring the intervention to specific risk groups were effective ways to reduce HIV/STIs.⁴³ Peer-led interventions have also been shown in some studies to reduce unprotected sex among MSM.⁴⁴ Military medical centers offer the infrastructure and access to resources necessary to support the development, improvement, and evaluation of such interventions to reduce rates of STI for those with and without HIV.

There are some limitations to this study. One limitation is that participants included in this analysis were living with HIV for a median of 9 and a 0.5 years before completing the RBQ. As a result, the effect of any STIs acquired in the years leading up to the implementation of the RBQ were not captured in this analysis. In addition, younger age is known to be associated with a proclivity for risk taking behaviors,^45,46 but the earlier risk profiles of NHS participants included in this study were not reflected in the results due to the long interval between HIV diagnosis and RBQ completion. Nevertheless, this study clearly describes the current risk behavior profile of the cohort and emphasizes that risk of coinfection with an STI continues in the decades following HIV infection. A second limitation of this study is that extragenital testing was not utilized to diagnose STIs, and extragenital testing with NAAT has been shown to significantly increase the number of identified GC or CT infections in MSM.⁴⁷

On the other hand, this study may be slightly overestimating the incidence of some STIs such as syphilis, since false-positive nontreponemal test results due to a serofast status are possible.⁴⁸ The potential for recall bias must be considered in this study, but it seems unlikely that the effect of recall bias on participant responses to the RBQ was different between those with and without an incident STI. Social desirability bias is also often a consideration in survey-based research and can lead to underreporting of risk behaviors,⁴⁹ and we sought to minimize the effects of social desirability bias by utilizing the CASI format to administer the RBQ, including the PNTA option and making responses anonymous to the study coordinators. In fact, the effect of social desirability bias in this study was likely small, since participants reporting higher levels of perceived risk were also more likely to report engaging in several risky sexual behaviors.

Lastly, this study only included cross-sectional results from the baseline questionnaire. An annual follow-up version of the RBQ is currently being administered to NHS participants and future analyses will be able to report updated rates of STI in the cohort as well as address changes in risk behaviors over time.

This study underscores the relatively high rates of STI and the ongoing engagement in risky sexual behaviors after HIV diagnosis in a predominantly MSM population living with HIV in the US military in the DADT era, despite accurate perceptions of STI risk. Given the growing rates of STIs in the US military and civilian populations and the potentially serious health consequences associated with sexually transmitted coinfections among PLWH, future work should focus on developing and testing new interventions aimed at changing sexually risky behaviors in the era of “U = U.”

Footnotes

Acknowledgments

The authors would like to thank the NHS study participants, study site staff and leadership, as well as the members of the Infectious Disease Clinical Research Program (IDCRP) HIV Working Group for collecting and reviewing study data and ensuring effective protocol operations. The IDCRP HIV Working Group includes: Brooke Army Medical Center, Fort Sam Houston, TX: W. Bradley; S. Merritt; T. Merritt; Lt Col J. Okulicz; C. Olsen; C. Rhodes; and T. Sjoberg; Madigan Army Medical Center, Joint Base Lewis McChord, WA: C. Baker; S. Chambers; R. Colombo; COL T. Ferguson; LTC A. Kunz; and C. Schofield; National Institute of Allergy and Infectious Diseases, Bethesda, MD: J. Powers; COL (Ret.) E. Tramont; Naval Medical Center Portsmouth, Portsmouth, VA: S. Banks; L. Illinik; CAPT K. Kronmann; T. Lalani; and R. Tant; Naval Medical Center San Diego, San Diego, CA: S. Cammarata, CDR J. Curry; N. Kirkland; CAPT R. Maves; and CAPT (Ret.) G. Utz; Tripler Army Medical Center, Honolulu, HI: COL M. Price; Uniformed Services University of the Health Sciences, Bethesda, MD: B. Agan; COL (Ret.) N. Aronson; CAPT T. Burgess; X. Chu; C. Estupigan; H. Hsieh; A. Noiman; E. Parmelee; D. Tribble; X. Wang; and S. Won; Walter Reed Army Institute of Research, Silver Spring, MD: LTC J. Ake; T. Crowell; S. Peel; and Walter Reed National Military Medical Center, Bethesda, MD: I. Barahona; LTC J. Blaylock; C. Decker; A. Ganesan; and LTC(P) R. Ressner. The authors would also like to thank Camille Estupigan for her editorial assistance.

Author Disclosure Statement

No competing financial interests exist.

Funding Information

This study was conducted by the Infectious Disease Clinical Research Program (IDCRP), a Department of Defense (DoD) program executed by the Uniformed Services University of the Health Sciences (USUHS) through a cooperative agreement with The Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc. (HJF). This project has been supported in whole, or in part, with federal funds from the National Institute of Allergy and Infectious Diseases, National Institutes of Health (NIH), under Inter-Agency Agreement Y1-AI-5072, and from the Defense Health Program, US Department of Defense, under award HU0001190002.

Supplementary Material

Supplementary Figure S1

References

Centers for Disease Control and Prevention. Sexually Transmitted Diseases Surveillance. 2018. Atlanta, GA: U.S. Department of Health and Human Services, 2019. Available at: https://www.cdc.gov/std/stats18/default.htm (Last accessed February 10, 2020 ).

Dougan

, Evans

, Elford

. Sexually transmitted infections in Western Europe among HIV-positive men who have sex with men. Sex Transm Dis, 2007; 34:783–790.

Kalichman

, Pellowski

, Turner

. Prevalence of sexually transmitted co-infections in people living with HIV/AIDS: Systematic review with implications for using HIV treatments for prevention. Sex Transm Infect, 2011; 87:183–190.

Politch

, Mayer

, Welles

, et al. Highly active antiretroviral therapy does not completely suppress HIV in semen of sexually active HIV-infected men who have sex with men. AIDS, 2012; 26:1535–1543.

Buchacz

, Patel

, Taylor

. Syphilis increases HIV viral load and decreases CD4 cell counts in HIV-infected patients with new syphilis infections. AIDS, 2004; 18:2075–2079.

Duffus

, Mermin

, Bunnell

. Chronic herpes simplex virus type-2 infection and HIV viral load. Int J STD AIDS, 2005; 16:733–735.

Rotchford

, Strum

, Wilkinson

. Effect of coinfection with STDS and of STD treatment on HIV shedding in genital-tract secretions: Systematic review and data synthesis. Sex Transm Dis, 2000; 27:243–248.

Blackard

, Mayer

. HIV superinfection in the era of increased sexual risk-taking. Sex Transm Dis, 2004; 31:201–204.

Stahlman

, Javanbakht

, Cochran

, et al. Self-reported STIs and sexual risk behaviors in the U.S. military: How gender influences risk. Sex Transm Dis, 2014; 41:359–364.

10.

Spaulding

, Lifson

, Iverson

, et al. Gonorrhea of Chlamydia in a US-Military HIV-Positive Cohort. Sex Transm Infect, 2012; 88:266–271.

11.

Ganesan

, Fieberg

, Agan

, et al. Results of a 25-year longitudinal analysis of the serologic incidence of syphilis in a cohort of HIV infected patients with unrestricted access to care. Sex Transm Dis, 2012; 39:440–448.

12.

Chun

, Fieberg

, Hullsiek

, et al. The epidemiology of hepatitis B virus infection in a U.S. cohort of HIV-infected individuals during the last 20 years. Clin Infect Dis, 2011; 50:426–436.

13.

Tzeng

, Clark

, Garges

, et al. Epidemiology of sexually transmitted infections among human immunodeficiency virus positive United States military personnel. J Sex Transm Dis, 2013; 2013:610258.

14.

Harling

, Subramanian

, Barnighausen

, Kawachi

. Income inequality and sexually transmitted infections in the United States: Who bears the burden?. Soc Sci Med, 2014; 102:174–182.

15.

Under Secretary of Defense. Memorandum. Subject: Repeal of “Don't Ask Don't Tell.” Washington, DC: Department of Defense, 2011.

16.

Hakre

, Scoville

, Pacha

, et al. Brief Report: Sexual risk behaviors of HIV seroconverters in the U.S. army, 2012–2014. J Acquir Immune Defic Syndr, 2015; 70:456–461.

17.

Pierce

. The lived experiences of HIV-positive soldiers in the United States

Army

. Dissertation. New Mexico State

University

, 2013. Available at: https://search.proquest.com/openview/c6729ec440c0d59972181dddae83386b/1?pq-origsite=gscholar&cbl=18750&diss=y (Last accessed February 12, 2020 ).

18.

Brodine

, Shaffer

, Starkey

, et al. Drug resistance patterns, genetic subtypes, clinical features and risk factors in military personnel with HIV-1 seroconversion. Ann Intern Med, 1999; 131:502–506.

19.

Agan

, Ganesan

, Byrne

, et al. The U.S. military HIV natural history study: Informing military HIV care and policy for over 30 years. Mil Med, 2019; 184(Suppl. 2):6–17.

20.

Congress of the United States Congressional Budget

Office

. Educational Attainment and Compensation of Enlisted

Personnel

. Washington

: Congressional Budget

Office

, 2004. Available at: https://www.cbo.gov/sites/default/files/cbofiles/ftbdocs/51xxdoc5108/02-23-enlistedpersonnel.pdf (Last accessed February 12, 2020 ).

21.

Navy and Marine Corps Public Health Center Sexual Health and Responsibility

Program

. Targeted Condom Access for Disease and Pregnancy

Prevention

. Portsmouth

: Navy and Marine Corps Public Health

Center

, 2018. Available at: https://www.med.navy.mil/sites/nmcphc/Documents/health-promotion-wellness/reproductive-and-sexual-health/targeted-condom-access-for-disease-and-pregnancy-prevention.pdf (Last accessed February 12, 2020 ).

22.

Military Health Communications

Office

. Sexually Transmitted Infections on the Rise in the

Military

. Fairfax

: Health.Mil, 2019. Available at: https://health.mil/News/Articles/2019/06/26/Sexually-transmitted-infections-on-the-rise-in-military (Last accessed February 12, 2020 ).

23.

Lucar

, Hart

, Rayeed

, et al. Sexually transmitted infections among HIV-infected individuals in the District of Columbia and estimated HIV transmission risk: Data from the DC cohort. Open Forum Infect Dis, 2018; 5:0fy017.

24.

Department of the Army . Identification Surveillance, and Administration of Personnel Infected with Human Immunodeficiency Virus. Army Regulation 600-110. Headquarters, Department of the Army. 2014. Available at: https://www.army.mil/e2/downloads/rv7/r2/policydocs/r600_110.pdf (Last accessed February 12, 2020 ).

25.

Secretary of the Air

Force

. Human Immunodeficiency Virus

Program

. Instruction 44-178. Headquarters

, Air

Force.

2014. Available at: http://static.e-publishing.af.mil/production/1/af_sg/publication/afi44-178/afi44-178.pdf (Last accessed February 12, 2020 ).

26.

Department of

Defense

. Instruction on Medical Standards for

Appointment

, Enlistment, or Induction into the Military

Services.

2018. Available at: https://www.med.navy.mil/sites/nmotc/nami/arwg/Documents/WaiverGuide/DODI_6130.03_JUL12.pdf (Last accessed February 12, 2020 ).

27.

Department of the

Navy

. Management of Human Immunodeficiency

Virus

, Hepatitis B

Virus

, and Hepatitis C Virus Infections in the Navy and Marine

Corps

. Instruction 5300.30E. Department of the

Navy.

2012. Available at: www.public.navy.mil/surfor/IDCorpsmen_Docs/Hepatitis_B_C_HIV_INST_5300.30E.pdf (Last accessed February 12, 2020 ).

28.

Sena

, Miller

, Hoffman

, et al. Trends of gonorrhea and chlamydial infections during 1985–1996 among active duty soldiers at a US army installation. Clin Infect Dis, 2000; 30:742–748.

29.

Crepaz

, Hart

, Marks

. Highly active antiretroviral therapy and sexual risk behavior: A meta-analytic review. JAMA, 2004; 292:224–236.

30.

Nieuwkerk

, Oort

. Self-reported adherence to antiretroviral therapy for HIV-1 infection and virologic treatment response: A meta-analysis. J Acquir Immune Defic Syndr, 2005; 38:445–448.

31.

Bangsberg

, Perry

, Charlebois

, et al. Non-adherence to highly active antiretroviral therapy predicts progression to AIDS. AIDS, 2001; 15:1181–1183.

32.

Kalichman

, Rompa

. Treatment adherence and unprotected sex practices among persons receiving antiretroviral therapy. Sex Transm Infect, 2003; 79:59–61.

33.

Kalichman

, Eaton

, Cherry

. Sexually transmitted infections and infectiousness beliefs among people living with HIV/AIDS: Implications for HIV treatment as prevention. HIV Med, 2010; 11:502–509.

34.

Prevention Access

Campaign

. Undetectable = Untransmittable Consensus

Statement

. Department of Health and Human Services

Panel

, Published

July

. 2016. Updated May 2019. Available at: https://www.preventionaccess.org/consensus (Last accessed February 15, 2020 ).

35.

LeMessurier

, Traversy

, Varsaneux

, et al. Risk of sexual transmission of human immunodeficiency virus with antiretroviral therapy, suppressed viral load and condom use: A systematic review. CMAJ, 2018; 190:E1350–E1360.

36.

Guest

, Weintrob

, Rimland

, et al. A comparison of HAART outcomes between the US military HIV Natural History Study (NHS) and HIV Atlanta Veterans Affairs Cohort Study (HAVACS). PLoS One, 2013; 8:e62273.

37.

Anglemyer

, Haber

, Noiman

, et al. HIV care continuum and meeting 90-90-90 targets: Cascade of care analysis of a U.S. military cohort. Mil Med, 2020; 185:e1147–e1154.

38.

Mizuno

, Zhu

, Crepaz

, et al. Receipt of HIV/STD prevention counseling by HIV-infected adults receiving medical care in the United States. AIDS, 2014; 28:407–415.

39.

Janz

, Becker

. The health belief model: A decade later. Health Educ Q, 1984; 11:1–47.

40.

Catania

, Kegeles

, Coates

. Towards an understanding of risk behavior: An AIDS risk reduction model (ARRM). Health Educ Q, 1990; 17:53–72.

41.

Fisher

, Fisher

, Williams

, et al. Empirical tests of an information-motivation-behavioral skills model of AIDS-preventive behavior with gay men and heterosexual university students. Health Psychol, 1994; 13:238–250.

42.

Herbst

, Sherba

, Crepaz

, et al. A meta-analytic review of HIV behavioral interventions for reducing sexual risk behavior of men who have sex with men. J Acquir Immune Defic Syndr, 2005; 39:228–241.

43.

Covey

, Rosenthal-Stott

HES

, Howell

. A synthesis of meta-analytic evidence of behavioral interventions to reduce HIV/STIs. J Behav Med, 2016; 39:371–385.

44.

Shaodong

, Lin

, Amico

, et al. Efficacy of peer-led interventions to reduce unprotected anal intercourse among men who have sex with men: A meta-analysis. PLoS One, 2014; 9:e90788.

45.

Stall

, Barrett

, Bye

, et al. A comparison of younger and older gay men's HIV risk-taking behaviors: The communication technologies 1989 cross sectional survey. J Acquir Immune Defic Syndr, 1992; 5:682–687.

46.

Mata

, Josef

, Hertwig

. Propensity for risk taking across the life span and around the globe. Psychol Sci, 2016; 27:231–243.

47.

Barbee

, Dombrowski

, Kerani

, Golden

. Effect of nucleic acid amplification testing on detection of extragenital gonorrhea and chlamydial infections in men who have sex with men sexually transmitted disease clinic patients. Sex Transm Dis, 2014; 41:168–172.

48.

Centers for Disease Control and Prevention. 2015. Sexually Transmitted Diseases Treatment Guidelines. Division of STD Prevention, National Center of HIV/AIDS, Viral Hepatitis, STD and TB Prevention, 2015. Available at: https://www.cdc.gov/std/tg2015/syphilis.htm (Last accessed February 12, 2020 ).

49.

Kelly

, Soler-Hampejsek

, Mensch

, et al. Social desirability bias in sexual behavioral reporting: Evidence from an interview mode experiment in Rural Malawi. Int Perspect Sex Reprod Health, 2013; 39:14–21.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.03 MB