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Prevention Research

Growing Acceptability of Undetectable = Untransmittable but Widespread Misunderstanding of Transmission Risk: Findings From a Very Large Sample of Sexual Minority Men in the United States

Rendina, H. Jonathon PhD, MPHa,b; Cienfuegos-Szalay, Jorge MPHa,b; Talan, Ali DrPHa; Jones, Stephen Scott BAa; Jimenez, Ruben H.a

Author Information
JAIDS Journal of Acquired Immune Deficiency Syndromes: March 1, 2020 - Volume 83 - Issue 3 - p 215-222
doi: 10.1097/QAI.0000000000002239
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Abstract

INTRODUCTION

Scientific consensus has been building for many years around the notion that successful antiretroviral treatment (ART) of HIV could suppress viral load (VL) to levels that would limit if not wholly avert HIV transmission, a phenomenon now known as treatment as prevention (TasP).1 In 2008, scientists at the Swiss National AIDS Commission were among the first to publicly state that individuals living with HIV who were consistently using ART and had an undetectable VL presented with a significant reduction in transmission risk,2 sparking a debate and a call to action to provide more empirical data.3 Initially, an analysis of annual surveillance data from San Francisco demonstrated that as VL levels within a defined community (ie, community VL) decreased, HIV incidence within that community also decreased.4 Three years later, the HIV Prevention Trials Network (HPTN) presented the results of HPTN-052, a phase-III randomized controlled study that followed 1763 serodifferent couples for over a decade. The study initially demonstrated a reduction of 96% in the likelihood of transmission occurring when ART was initiated early,5 and later analyses demonstrated no linked HIV transmissions within couples where the HIV-positive partner had durably suppressed VL.6,7

Although these landmark studies provided evidence for TasP, less was known in terms of serodifferent sexual minority men (SMM) couples and condomless anal sex (CAS). The PARTNER1 trial included 340 serodifferent male couples and demonstrated no linked transmissions when the HIV-positive partner's VL was suppressed.8 Two subsequent trials of serodifferent male couples—Opposites Attract with 234 couples9 and PARTNER2 with 783 couples—have confirmed no linked transmissions when the partner living with HIV was undetectable.10 The PARTNER2 findings were in the context of 76,088 recorded CAS acts, leading the authors to conclude that “the risk of HIV transmission in gay couples through condomless sex when HIV VL is suppressed is effectively zero.”10

Although scientific consensus regarding TasP has increased rapidly with these findings, the science of VL suppression and transmission risk has not been well disseminated, understood, or accepted among the general public and priority populations most affected by HIV. In 2016, the Prevention Access Campaign launched the slogan “Undetectable = Untransmittable” or “U = U” to promote advocacy for and education about these scientific breakthroughs. However, even with a recent commentary published by officials at the National Institute of Allergy and Infectious Diseases supporting TasP as scientifically sound,11 an official endorsement from the Centers for Disease Control that there is “effectively no risk,”12 and advocacy from more than 926 organizations across 99 countries,13 acceptance of the science surrounding VL transmission has been mixed. Dissemination and acceptance of this science through U = U and other messaging is critical for HIV prevention and a central component of the U.S. initiative toward “Ending the HIV Epidemic” by 2030.14 Thus, a greater understanding of barriers to uptake of this information among the general public is vital.

Only a handful of published studies to date have documented levels of and barriers to TasP and U = U acceptability among the general public. A Canadian study conducted between 2012 and 2015 assessed belief in TasP among 774 SMM found that support was greater among HIV-positive men (47.7%), with nearly all (93.9%) of HIV-negative men reporting to be skeptical and unaware of TasP.15 A study of 732 SMM in New York City conducted in 2016–2017 also found HIV-positive men to perceive TasP as more effective (58.3%) in comparison with HIV-negative men (34.4%).16 In the largest study to date with over 12,200 SMM conducted in 2016–2017,17 researchers found that far fewer (33.8%) HIV-negative and unknown-status SMM perceived the message as accurate compared with HIV-positive SMM (70.3%). These findings highlight that the potential HIV-preventive benefit of U = U is hindered due to gaps in acceptance, particularly by HIV status.

In addition to noting disparities by HIV status, research has also identified changes over time, with one Australian study of 1316 SMM noting an increasing belief in TasP from 2.6% in 2013 to 13.1% in 2015.18 These and other studies have noted other factors being associated with greater beliefs in TasP and U = U, including higher engagement in CAS, sex with serodifferent partners, more interaction with HIV prevention or treatment services (eg, more frequent HIV testing, use of PrEP, being prescribed, and adherent to ART), and drug use, as well as higher rates of belief among Black and Latino SMM.16,19,20

Since its launch in 2016, U = U's message has been gaining momentum. Data suggest both the awareness and acceptance of the science of viral suppression among SMM has been increasing over time. Yet, a broader understanding of viral suppression and belief in the U = U message is needed for the greatest benefit.15,18 Therefore, this study aimed to expand on previous work to provide ongoing surveillance of accuracy beliefs in the U = U message among SMM, compare changes over time, describe factors associated with these beliefs, and examine how beliefs in the U = U message are associated with perceived risk of HIV transmission during CAS with undetectable partners.

METHODS

Participants and Procedures

We gathered data during a 10-month span from November 2017 through September 2018 as part of ongoing efforts to screen participants into several research studies for SMM. We used online venues to advertise for these studies across the United States, including targeted banner advertisements on social media sites, pop-up and inbox advertisements on popular geotargeted sexual/dating networking apps, and targeted banner advertisements on web-based sexual/dating networking websites. Those who clicked any of the ads containing images and text (eg, “get a free at-home HIV test mailed to you”; “receive up to $275 for joining”) were directed to the secure survey. Those aged 18 years or older were directed to a page that contained informed consent while those who were aged 13–17 years were directed to an assent page, and the study received a waiver of parental consent. The informed consent/assent indicated the survey had no incentive, but they would be screened for multiple studies at once for which they could be compensated if they were eligible and enrolled. All procedures were approved by the institutional review board of the City University of New York.

Measures

Biomedical Status

Participants reported their HIV status as positive, negative, or unknown (“I don't know”), after which HIV-negative and status-unknown individuals were asked whether they were currently prescribed PrEP and HIV-positive individuals were asked whether their most recent VL test was undetectable, detectable, or unknown (“Not sure/don't remember”). We combined the answers to form 5 biomedical status groups: (1) HIV-negative/unknown, on PrEP; (2) HIV-negative, not on PrEP; (3) HIV status unknown, not on PrEP; (4) HIV-positive, undetectable; and (5) HIV-positive, detectable or unsure.

Sociodemographic Characteristics

We recorded whether participants were recruited from a social media website, a sexual/dating/social networking website (herein referred to as a “networking site”), or a sexual/dating/social networking app (herein referred to as a “networking app”). Participants self-reported their age, Hispanic/Latino ethnicity, racial identity based on U.S. census categories, gender identity, sexual orientation, zip code (which we recoded into the 4 primary regions of the United States), and their relationship status—for men in relationships, we asked the HIV status of their main partner, which we subsequently recoded into a seroconcordant or serodifferent relationship status. Participants in a relationship who reported an unknown HIV status for themselves or their partner were recoded as being in a serodifferent relationship.

HIV and STI Prevention and Treatment

HIV-negative and unknown-status participants reported the frequency with which they received HIV testing, which we recoded into a trichotomous variable of testing in the past 6 months, more than 6 months, or never tested.

ART Adherence

HIV-positive participants respond to a single validated item for assessing antiretroviral adherence21 ranging from 1 (very poor) to 6 (excellent), which was trichotomized into a variable indicating excellent adherence, less than excellent adherence, and currently not being on ART.

Club Drug Use

Participants were asked whether they had used cocaine, crack, crystal meth, ecstasy, GHB, and ketamine in the past 6 months, and we recoded responses into a dichotomous indicator of any recent club drug use.

Recent CAS

Participants were asked the number of casual male sexual partners they had in the previous 6 months and the number of times they engaged in insertive and receptive anal sex with and without a condom with these partners. We created a dichotomous indicator of any CAS with a casual male partner in the previous 6 months.

Month of Completion

To provide cross-sectional estimates of average change over time, we created a variable indicating the month the survey was completed (range: 1–10).

Perceived Accuracy of the U = U Message

We relied on measures used in previous research,17 in which participants were asked, “With regard to HIV-positive individuals transmitting HIV through sexual contact, how accurate do you believe the slogan U = U is?” Responses were on a Likert-type scale from 1 (completely inaccurate) to 4 (completely accurate) as well as a fifth option (I don't know what “undetectable” means). Within multivariable models, the fifth category was excluded, and higher scores indicate greater perceived accuracy of U = U.

Perceived Risk of Transmission With an Undetectable Partner

Participants were asked, “What is the risk that an HIV+ man who is currently undetectable could transmit HIV sexually to his partner through topping?” The question was repeated for receptive sex, replacing the final word with “bottoming.” Participants responded on a sliding scale from 0% to 100% in intervals of 1%, with anchors only at the extremes of “no risk” and “complete risk.”

Statistical Analyses

We used SPSS 24 to examine sociodemographic characteristics of the sample and compared those characteristics between the HIV-negative, HIV-positive, and unknown status participants using χ2 tests of independence. Next, multivariable regression analyses were run with cross-sectional responses to perceived accuracy of the message as the outcome; one model was run for SMM who identified as HIV-positive and another for those who identified as HIV-negative/unknown status. Because of the 4-point nature of the scale response, we ran an ordinal (ie, proportional odds) logistic regression of the accuracy ratings for each, excluding those who responded that they were unsure what undetectable meant. Finally, we examined perceived accuracy of U = U in relation to perceived risk of transmission during condomless sex with undetectable male partners using χ2 tests of independence and graphical representations of the data.

RESULTS

Overall, 204,816 individuals submitted an eligible age and reached the survey consent/assent, of whom 157,587 provided consent/assent and 123,373 completed the survey in its entirety. We removed 9427 responses that were duplicate responses of previous surveys. An additional 2199 individuals did not provide valid regional data, identify as male, report male-identified casual or main partners, or identify as a sexual minority. A total of 111,747 SMM provided full data on the measures focused on in this manuscript and thus constituted the analytic sample.

Sociodemographic characteristics of the sample are presented in Table 1. Participants ages ranged from 13 to 88 years, with an average age of 34.5 years (Median = 32.0). Looking by HIV status (without consideration of biomedical status), we saw significant sociodemographic differences between the 3 groups on all variables examined. Perceived accuracy of U = U is fully broken down in Table 1—collapsing the categories, we saw that 53.8% of HIV-negative men and 39.0% of HIV status-unknown men perceived U = U to be somewhat or completely accurate compared with the vast majority (83.9%) of HIV-positive men.

T1
TABLE 1.:
Demographic Characteristics and Comparisons by HIV Status

Table 2 reports the stratified regression results for the ordinal accuracy belief outcome, as well as the unadjusted percentage who endorsed belief in U = U (accurate or completely accurate) for each subgroup comparison to translate these findings into more meaningful indicators of practical significance. Among HIV-negative/unknown SMM, those on PrEP had substantially higher beliefs in the accuracy of U = U than those not on PrEP. Similarly, in the model for HIV-positive SMM, those who reported their most recent VL result was undetectable had substantially higher perceptions of the accuracy of U = U. Across both models, there were some notably consistent findings. The odds of moving up 1 point on the accuracy scale (which ranged from 1 to 4) were, on average, 1.0% higher per month for HIV-negative/unknown men and 2.0% higher per month for HIV-positive men. Men recruited from networking apps had lower perceived accuracy than those from social media, queer-identified men had higher and bisexually identified men had lower perceived accuracy than gay-identified men, and men partnered in a serodifferent relationship had higher perceived accuracy than single men.

T2
TABLE 2.:
Multivariable Analyses Examining Perceived Accuracy of U = U Message

Within the model for HIV-negative and status-unknown men, we found that Black men had higher perceived accuracy than men who identified as Asian, Hawaiian Native, or Pacific Islander, those who identified as Native American or Alaskan Native, and those who identified as Multiracial, but did not differ from White men. Straight-identified men had lower perceived accuracy than gay-identified men, men from the Midwest had higher perceived accuracy than those from the Northeast, and men partnered in seroconcordant relationships had higher perceived accuracy than single men. We also found that recent club drug use and recent CAS were both significantly associated with higher perceived accuracy; HIV testing less often than every 6 months or never testing was associated with significantly lower perceived accuracy compared with men who tested every 6 months or more often.

Within the model for HIV-positive men, fewer significant differences emerged. Men from a networking site had significantly lower perceived accuracy than those from social media. Also, self-reported adherence less than excellent or not being prescribed ART were associated with significantly lower perceived accuracy compared with men who reported excellent adherence.

Finally, we found that perceived accuracy of U = U was strongly linked to perceived risk of HIV transmission during CAS with a known undetectable partner. Figures 1 and 2 show the distribution of perceived risk within a histogram for the overall sample and within box-and-whisker plots stratified by perceived accuracy of U = U, with standard notation for median and quartiles and single points for means within each group. As shown in the histogram on the left of Figure 1, only 10% of the sample overall perceived transmission risk to be zero when the undetectable partner was insertive during CAS, and in Figure 2, this was slightly higher at 14% when the undetectable partner was receptive. However, these proportions were 31.0% and 39.0%, respectively, among the group who perceived U = U to be completely accurate. Perceived accuracy of U = U was associated with significantly lower perceived risk of HIV transmission during CAS with an undetectable partner whether he is in the insertive (χ2 = 31,223.38, P < 0.001) or receptive (χ2 = 25,704.95, P < 0.001) position.

F1
FIGURE 1.:
Distribution of reported risk of HIV transmission during CAS when an undetectable HIV-positive individual is the insertive partner for the sample overall (histogram) and stratified by perceived accuracy of U = U (box-and-whisker plots).
F2
FIGURE 2.:
Distribution of reported risk of HIV transmission during CAS when an undetectable HIV-positive individual is the receptive partner for the sample overall (histogram) and stratified by perceived accuracy of U = U (box-and-whisker plots).

DISCUSSION

In this study, we examined perceived accuracy of U = U among a large and diverse sample of SMM in the United States to inform ongoing TasP implementation efforts to reduce HIV transmission. Similar to previous studies, the current findings demonstrated that HIV-positive men continue to be more likely to consider TasP messaging as accurate compared with HIV‐negative and unknown‐status men. Among HIV-positive men, 4 in 5 considered the message to be somewhat or completely accurate, compared with approximately 1 in 2 of HIV-negative and unknown-status men.

Compared with previous work15–17 we found that across all biomedical statuses, SSM were more likely to perceive U = U as somewhat or completely accurate, suggesting a positive shift in acceptance. In this study, 53.8% of HIV-negative men and 39% of HIV status-unknown men perceived U = U to be somewhat or completely accurate. These rates of perceived accuracy show quite a shift for HIV-negative/unknown SMM since a study in 2016–2017 with over 12,200 SMM,17 where one-third reported the message as accurate. In addition, we observed the average odds of a 1-point increase on the accuracy scale (ranging from 1 to 4) being 1% higher per month for HIV-negative/unknown men and 2% by month for HIV-positive men.

Even with these advancements, there are SMM—particularly HIV-negative and unknown-status—who continue to rate U = U messaging as inaccurate. The present results echo previous studies showing that men who report more risk behavior and more engagement with HIV treatment and prevention were more likely to believe in the accuracy of U = U.17 Specifically, recent CAS was a strong predictor of higher perceived accuracy of U = U among the HIV-negative SMM. Because reporting higher accuracy of U = U may indicate better understanding of the nuanced per-act risk associated with different types of sexual behavior, aggregate measures of CAS that do not delineate subtypes with higher and lower risk may be higher among this group despite the potential for reduced risk of transmission overall. Relatedly, more frequent HIV testing was associated with significantly higher perceived accuracy among the HIV-negative SMM. These finding suggest that HIV prevention services continue to have the intended effect of increasing HIV prevention knowledge.

More striking, the growing acceptance of TasP messaging has led to an almost ubiquitous belief that TasP is accurate among SMM living with HIV, contributing to the growing gap between U = U perceptions among HIV-positive and HIV-negative or HIV-status-unknown men. In this study, 83.9% of HIV-positive men perceived U = U to be somewhat or completely accurate, compared with other research that found lower rates of acceptance among this group (47.7%,15 58.3%,16 and 70.3%17). Among the SMM living with HIV, the two most salient factors associated with accuracy beliefs were about treatment engagement—those who reported their most recent VL test was detectable or were unsure what their most recent result was and those who either reported suboptimal adherence or not being prescribed ART had significantly lower accuracy beliefs than those who reported an undetectable result and excellent adherence. One potential reason for this is simply lack of knowledge or understanding around the underlying risk levels of different behaviors, which may be driven by lower engagement in and contact with HIV care. Another possibility is that this group reacts differently to the potential social and personal consequences of U = U, which has yet to be empirically explored in published work.

This was the first published study of which we are aware to assess both U = U beliefs and perceived transmission risk during sex with undetectable partners and links lower belief in the accuracy of U = U to a fundamental misunderstanding of the underlying rates of transmission with undetectable partners. It is critical to note that reaching high rates of undetectable status has been shown to be the most effective method for curbing the HIV epidemic, in addition to having health and social benefits for people living with HIV themselves.8,15,22,23 Moreover, uptake of TasP and U = U for HIV-negative individuals is highly cost-effective, requiring no more than an accurate understanding of risk and the ongoing successful treatment of people living with HIV. Despite this, previous work shows much higher public awareness of and confidence in PrEP and condoms than VL suppression for risk reduction.16,19,24,25

Communication about the science of VL suppression must be unequivocal to ensure the risk-reducing benefits of VL suppression reach their full potential for effectiveness and to reduce HIV stigma. Psychological literature suggests that framing is important, and a switch from change in risk to the degree of protection may also prove critical to increasing success of U = U messaging. Clear and consistent messaging about the effectiveness of U = U is critical—based on the fundamental misunderstanding of base rates of risk and psychological literature on framing, we recommend language that uses relative rather than overall risk (ie, moving from “no risk to complete reduction in risk”) and uses protection-enhancing rather than risk-reducing framing. In other words, describing U = U as being 100% effective in protecting against HIV transmission may enhance acceptability among the groups who have been slower to accept the message to date.

STUDY STRENGTHS AND LIMITATIONS

We were able to recruit a large and diverse sample of SMM from across the United States, including adolescents (aged 13-17), and with a large enough sample to separately examine a diverse range of racial and ethnic backgrounds and sexual identities. At the same time, data collected were cross-sectional and self-reported, and thus, we were unable to confirm factors such as reported HIV status or levels of ART adherence for SMM who reported were HIV-positive. Although we showed average perceptions being somewhat higher for each subsequent month of data collection, our cross-sectional data cannot longitudinally elucidate the within-person changes in perceived accuracy of the U = U message over time. Although our sample was large, we had a relatively small proportion who identified as transgender men and no female-identified participants, preventing us from assessing beliefs among these groups or the general population. Finally, although several precautions were taken to safeguard the online recollection and validity of our data and we have a large sample, the online survey was anonymous and drew heavily from app-based recruitment and thus may not generalize to the broader population of SMM in the United States.

CONCLUSIONS

Among SMM in the United States, we found a greater proportion believe the message compared with similar previous research, with the overall proportion who believed the U = U message exceeding half for the first time in the published literature. In addition to showing an average monthly trend for increasing accuracy beliefs, we demonstrated growing consensus around the accuracy among SMM living with HIV. At the same time, SMM living with HIV who showed less engagement with HIV care, as evidenced by a recent detectable VL, ART non-adherence, or not being prescribed ART, had significantly lower beliefs. Several factors were associated with accuracy beliefs among HIV-negative SMM, with those more engaged in HIV prevention (ie, on PrEP, more frequent HIV testing) and those engaging in potentially higher risk behaviors (ie, CAS, drug use) rating the message as more accurate. In this study, perceived risk of HIV transmission with an undetectable partner was skewed well above zero, even among those who rated U = U as completely accurate. Individuals often misperceive and exaggerate base rates of risk,26 and a focus on the effectiveness in averting risk (ie, a relative risk reduction or degree of effectiveness) would mirror language used for PrEP and condoms and allow comparability among them. Taken together, these findings suggest people believe antivirals are more effective as PrEP than as TasP and highlight the need for clear and compelling messaging about the science of viral suppression showing complete protection against HIV transmission during condomless sex with a partner who is durably suppressed and adherent to treatment. Finally, providers are a necessary partner in disseminating TasP and U = U science, and data suggest that even physicians may be more strongly influenced by relative risk information than absolute risk.27

ACKNOWLEDGMENTS

The authors are grateful for the support of the Principal Investigators and NIH staff for each of the awards that supported data collection for this study, our dedicated research team at Hunter College, and our participants who volunteered their time.

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Keywords:

treatment as prevention; men who have sex with men; viral load; public health; risk factors

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