INTRODUCTION

In this chapter, the committee considers the interactions between HIV, the world’s most important sexually transmitted infection (STI), and “classical” STIs (especially the curable bacterial STIs) that lead to mucosal inflammation and genital ulcers. There is a large literature that examines the biological, epidemiological, and behavioral aspects of HIV–STI interactions. This chapter highlights aspects of these interactions that may affect the trajectory of the ongoing STI epidemics in the United States. The chapter also examines how prevention and care programs to control the distinct, yet intertwined HIV and “classical” STI epidemics diverged, with profound adverse effects on the spread of STIs. Considering this history emphasizes opportunities to develop more efficient programs going forward that recognize the “syndemic” relationship between HIV, STIs, and viral hepatitis that can and should be addressed in an integrated fashion.

HISTORY

HIV was first recognized in 1981, in Los Angeles and New York City where reports of gay, bisexual, and other men who have sex with men (MSM) who acquired pneumocystis pneumonia and/or Kaposi’s sarcoma secondary to immunodeficiency foreshadowed the AIDS pandemic (CDC, 1981; Gottlieb et al., 1981, 1982; Masur et al., 1981). Given the initial clustering of cases, this syndrome was initially termed “gay-related immune deficiency,” and later renamed “acquired immunodeficiency syndrome” (Marx, 1982). The appearance of the same disease in persons with hemophilia (CDC, 1983; Gottlieb et al., 1982; Marx, 1983), neonates (Marx, 1983), injection drug using women and women sex workers (Harris et al., 1983; Masur et al., 1982), transfusion recipients (CDC, 1982), and children (Oleske et al., 1983; Rosner and Giron, 1983; Rubinstein et al., 1983) clarified the route(s) of transmission of the causal pathogen: sexual, blood-borne, and mother-to-child transmission during pregnancy, delivery, and breastfeeding (Royce et al., 1997).

In 1983 and 1984, the causative agent, a retrovirus named “human immunodeficiency virus,” was discovered and described, and antibody testing became available in 1985 (Gallo, 2002; Gallo and Montagnier, 2003). It was several years before it was accepted widely that HIV was primarily a sexually transmitted disease, however, and delays in prevention interventions contributed to the spread of the virus in both MSM and heterosexuals.

While HIV spread rapidly worldwide it attracted attention due to mounting morbidity and mortality in endemic regions and when it was shown to be indiscriminate in its potential to infect (e.g., children, women, blood product recipients, and celebrities). The aggressive and effective advocacy of lesbian, gay, bisexual, transgender, and queer (LGBTQ+) and other communities helped accelerate research, services, and policy changes (Shilts, 1987). The importance of advocacy in efforts to control the spread of HIV in the United States and worldwide is discussed later in this chapter.

HIV tests rendered the blood supply much safer (Weiss et al., 1985). Virus transmission remained an immense challenge nonetheless, through sexual, parenteral, and perinatal routes (Coates and Schechter, 1988; Royce et al., 1997; Vermund and Leigh-Brown, 2012). Although a worldwide pandemic ensued, the transmission of HIV per sexual encounter was recognized to be inefficient relative to other STIs. For example, gonorrhea transmission is very efficient, as it has a 20–53 percent chance of transmission from a woman infected with gonorrhea to a male partner through a single episode of vaginal intercourse (Hooper et al., 1978). By comparison, HIV transmission may occur just once in 300–1,000 sexual encounters involving someone with a chronic infection (Blower and Boe, 1993; Hollingsworth et al., 2008; Pinkerton et al., 2011; Powers et al., 2008; Røttingen and Garnett, 2002; Royce et al., 1997; Varghese et al., 2002).

As a consequence of transient very high viral loads, before the host immune system can respond, acutely infected persons have far higher transmission probabilities (Pilcher et al., 2004b; Pinkerton et al., 2011), closer to those seen with bacterial STIs. Viral load (blood and genital tract) in someone with HIV can predict sexual transmission risk to an HIV-negative partner (Baeten et al., 2011; Chakraborty et al., 2001; Cohen et al., 2011; Fideli et al., 2001; Quinn et al., 2000). While patients with acute HIV infection have the highest viral load observed during the course of infection as the transmitted virus has rapid growth until restrained by evolving host defenses (Pilcher et al., 2004b), even chronically infected persons can be especially infectious if their viral loads are high, as with genital inflammation that recruits infected T-cells into the genital tract (Cohen et al., 2019; Passmore et al., 2016). Co-factors for the efficiency of sexual transmission continue to be elucidated (Council et al., 2020; Noël-Romas et al., 2020).

Blood-borne transmission among people who inject drugs is quite efficient because of the volume of infectious blood that can be derived from a person with untreated HIV (Degenhardt et al., 2010). The opioid crisis has contributed to a new wave of HIV in some parts of the United States, as illustrated by the Scott County, Indiana outbreak (Alpren et al., 2020; Crowley and Millett, 2017; Des Jarlais et al., 2020; Gonsalves and Crawford, 2018; Kishore et al., 2019; Peters et al., 2016).

While HIV spread is driven by the prevalence of unrecognized and untreated HIV infections (Cohen, 2006), co-factors and especially concomitant STIs enhance the efficiency of sexual HIV transmission, by increasing either the person’s infectiousness or the partner’s susceptibility (Baggaley and Hollingsworth, 2015; Blaser et al., 2014) (see Figure 5-1).

FIGURE 5-1

Intercurrent infections and HIV viral load: A conceptual example of someone who might be more infectious at different times in the course of their HIV infection, depending on coinfections, notably sexually transmitted infections. NOTE: HSV-2 = herpes (more...)

Sexual behaviors per se can affect the probability of transmission. For example, condomless anal intercourse leads to a transmission probability at least 10 times higher than penile-vaginal intercourse (Dosekun and Fox, 2010; Harman et al., 2013; Vermund and Leigh-Brown, 2012). It is generally believed that the density of lymphocytes and dendritic cells “defending” anal tissue (yet susceptible to HIV), and possibly the fragility of the anal and rectal mucosa and associated trauma, accounts for this risk (Harman et al., 2013; Kaul et al., 2008; Schneider et al., 1996).

Early in the pandemic, it was recognized that STIs (e.g., syphilis, herpes simplex virus type 2 [HSV-2], gonorrhea, and chlamydia) that were detected in people with HIV infection, might have amplified viral transmission through access provided by genital ulceration and mucosal inflammation (see Figure 5-1). Piot and Laga (1989, p. 624) focused on this idea in their early work in Zaire, stating that

Programs to control sexually transmitted diseases should be strengthened or initiated where they do not exist. Not only will this reduce the incidence of severe complications and sequelae of sexually transmitted disease, but it may also interfere with the spread of HIV. The two things not to do are to take the resources for AIDS prevention away from the general budget to control sexually transmitted diseases and to isolate the programs to prevent AIDS from those to control sexually transmitted diseases.

The relationship between well-known STIs and HIV was described as “epidemiologic synergy” to emphasize how each might exacerbate the transmission or pathogenicity of the other (Wasserheit, 1992). The synergy concept highlighted key populations that might be affected by both HIV and other STIs, including the challenges in treating STIs in persons with advanced HIV who might be profoundly immunosuppressed. According to this idea, STIs made people more susceptible to HIV and rendered people with HIV more infectious as well.

Interest in the relationship between STIs and HIV led to an explosion of research, including study of the biological basis for epidemiologic synergy (Galvin and Cohen, 2004). When the HIV pandemic began, the virus only could be studied by growth in tissue culture, a laborious procedure that required intensive safety precautions. Developing a polymerase chain reaction (PCR) assay that amplified viral RNA allowed HIV to be quantitated as the number of copies in blood or a bodily secretion. Using this technique, Mellors et al. (1996) were able to show that the HIV concentration in blood was correlated with the rate of clinical decline in the MultiCenter AIDS Cohort Study. In remarkably consistent landmark articles from Uganda and Zambia, studies of serodiscordant heterosexual couples (i.e., one partner with HIV and the other without) were able to correlate the blood concentration with the probability of heterosexual transmission (Fideli et al., 2001; Quinn et al., 2000). Subsequent field studies in Africa have helped define the concentration of HIV in mucosal secretions required for transmission (Baeten et al., 2011; Lingappa et al., 2010). Systematic reviews suggested the benefits of preventing coinfections, including STIs, in reducing HIV viral load and presumed HIV transmission risks (Modjarrad et al., 2008).

Just as PCR was a game changer for monitoring disease progression and treatment response, rapid, affordable, point-of-care (POC) diagnostics were a key to expanded HIV treatment and prevention (Manoto et al., 2018). The advent of these technologies for HIV diagnosis and management starkly contrasts with modern-day approaches to classical STIs, in which POC tests are only now emerging, and at a slow pace and high cost compared to POC tests for HIV (see Chapter 7).

Using PCR, investigators were able to demonstrate that STIs reversibly increased the concentration of HIV in genital secretions, supporting the theory that the higher viral concentrations evoked by STIs increased HIV transmission (Cohen et al., 1997; Johnson and Lewis, 2008). STIs also lowered the viral threshold for HIV transmission, with STI-induced denuded mucosa and epithelium (rich in inflammatory cells) increasing HIV acquisition (Galvin and Cohen, 2004; Mayer and Venkatesh, 2011). Furthermore, STIs increase the number of inflammatory cells available and the expression of critical receptors on such cells, further facilitating HIV infection (Galvin and Cohen, 2004; Sheffield et al., 2007). HIV variants less fit for growth were shown to persist as a cause of infection in the presence of an STI coinfection (Carlson et al., 2014). The emerging paradigm suggested that people with unrecognized or untreated STI–HIV coinfection might first transmit the more efficient “classical” STIs, causing enough inflammation in the sexual partner to set the stage for subsequent HIV transmission. In an effort to stem the global HIV pandemic, therapeutic studies of treatment of STIs to reduce HIV transmission efficiency were conducted.

CONSEQUENCES OF STIs IN PEOPLE LIVING WITH HIV

STIs among people living with HIV represent a significant risk for reproductive tract sequelae for themselves and their sexual partners. While STIs may cause fewer reproductive complications in MSM, bridging STIs to the heterosexual male population and to women has been demonstrated (Williamson et al., 2019). Additionally, the rise in syphilis among women has led to a dramatic rise in congenital syphilis, both in the United States and worldwide (Liew et al., 2021; Schmidt et al., 2019). Currently, CDC (Barrow et al., 2020) and WHO (2016) treatment and prevention guidelines recommend frequent testing for and treatment of STIs, but HIV—given its potential lethality, incurability, and high prevalence—remains a far greater funding and programmatic priority from governments and foundations alike (Barrow et al., 2020).

STIs are used to represent markers of sexual behavior. A history of an STI is often required to enroll in HIV prevention trials and to justify PrEP. HIV prevention trials rarely target both HIV and STIs, focusing on HIV as the most serious of all the STIs. While an STI may indicate higher-than-average HIV risk, the trends of STIs and HIV may not be in sync. For example, as ART and PrEP use expands, HIV incidence has declined, perhaps a “treatment as prevention” effect. At the same time, STI rates continue to rise.

Recently, the White House has launched Ending the HIV Epidemic: A Plan for America, with four pillars (Fauci et al., 2019):

• Diagnose all individuals with HIV as early as possible after infection;
• Treat HIV infection rapidly and effectively to achieve sustained viral suppression;
• Prevent at-risk individuals from acquiring HIV, including the use of PrEP and syringe exchange programs; and
• Rapidly detect and respond to emerging clusters of HIV infection to reduce new transmissions.

While treatment of HIV/AIDS is a key pillar, STI control is not explicitly included in this strategy, which may represent a missed opportunity for better integration of management of HIV, STIs, and viral hepatitis. Importantly, before leaving office, the Trump administration’s Office of the Assistant Secretary for Health at the Department of Health and Human Services (HHS) published an HIV National Strategic Plan (HIV-NSP) in January 2021 (HHS, 2020a). Additionally, President Biden, in December 2020, committed his administration to updating the National HIV/ AIDS Strategy for the United States (the most recent iteration covered 2015–2020) (KFF, 2020), which may presumably start with a review of the HIV-NSP. The HIV-NSP, however, is focused on the 48 U.S. counties responsible for half of all HIV diagnoses, along with the District of Columbia and San Juan, Puerto Rico, and 7 rural states with HIV risks derived from the opioid epidemic and other concerns. The Office of the Assistant Secretary for Health also updated the National Viral Hepatitis Action Plan (HHS, 2020c) and recently released the first-ever federal STI National Strategic Plan (STI-NSP, see Chapter 12 for more information) (HHS, 2020b). The STI-NSP emphasizes coordination with Ending the HIV Epidemic (EHE) (HHS, 2020b) (see Box 5-1 and additional discussion later in this chapter).

BOX 5-1

Example of Synergies Between Ending the HIV Epidemic (EHE) from the 2020 STI National Strategic Plan.

IMPORTANT LESSONS FROM THE HIV PANDEMIC

The worsening spread of STIs motivated the request for this report and is linked to the novel STI-NSP (HHS, 2020a). The committee believes there are important lessons to be learned from historical and ongoing attempts to control the spread of HIV. First, successes in treating and preventing HIV reflect unique, sustained, and powerful advocacy by affected communities. The rise of the Gay Men’s Health Crisis and other community-based organizations across the country, along with establishment of local and national activist and advocacy organizations, including the AIDS Coalition to Unleash Power, the National Association of People with AIDS, NMAC (formerly the National Minority AIDS Council), the Latino Commission on AIDS, the Black AIDS Institute, and the Treatment Action Group in the 1980s and 1990s, books and dramatic works, such as And the Band Played On (book and movie), The Normal Heart and Angels in America (plays), Philadelphia (movie), and celebrity disclosure of HIV infection (e.g., Rock Hudson, Liberace, Arthur Ashe, Magic Johnson, Greg Louganis, Freddie Mercury, and Charlie Sheen) inspired massive commitments to treating and preventing HIV. The late Surgeon General C. Everett Koop’s ”Understanding AIDS” mailing to all U.S. households by CDC in 1986 acknowledged HIV as a major public health problem and urged Americans to seek testing (Koop, 1986). This was a remarkable moment: the Surgeon General with CDC, independent of the White House, acknowledged an STI, urged all Americans to get tested, and advocated for healthier sexual behaviors to the entire U.S. population.

Effective advocacy ultimately led to resources for HIV treatment and infection at a level that has been unavailable for STIs and many other infectious diseases. In 1990, the Ryan White Comprehensive AIDS Resources Emergency Act was enacted, named for a courageous young boy with hemophilia who died from HIV and whose family was ostracized; his family were tireless in their search to access government resources and showed understanding and compassion for people with HIV. This critical and remarkably successful legislation was the first attempt to mount a nationwide response to the care and treatment needs of people with HIV by expanding funding for high-prevalence cities and metropolitan areas and providing funding to states and HIV primary care clinics in areas with lower prevalence, which has allowed for high-quality care for more than half of the people living with HIV in the United States.

In 2003, President Bush developed the President’s Emergency Plan for AIDS Relief with broad bipartisan support, providing resources to address global HIV prevention and treatment. These substantial funding commitments, nationally and globally, resulted in advances in diagnostics and therapies that fundamentally shifted outcomes, notably in Africa.

Moreover, the rise in the number of persons living with HIV or AIDS that accompanied breakthroughs in treatment has sustained a level of advocacy and attention to HIV that is perhaps unparalleled relative to other health conditions, at least before the COVID-19 pandemic. Public health messaging centers on positive messages from diverse individuals living with HIV, including celebrities and prominent people from all walks of life and HIV-negative allies among civic leaders, faith leaders, elected officials, athletes, and celebrities.

These observations need to be compared with historical efforts at STI control; classical STIs have simply never received the same funding or national awareness. There has been no parallel movement or awareness, with rare literary exceptions like the 1882 Henrik Ibsen play Ghosts (shocking and reviled at the time of its release) and the little-known 1993 play In the Clap Shack by well-known novelist William Styron. While an Internet search will find many celebrities diagnosed with HSV-2, chlamydia, gonorrhea, syphilis, and other STIs, none speak out in advocacy for prevention and control as is seen for HIV. Advocacy organizations exist² but are not anywhere near as successful in defining STIs as an important cause worthy of public attention as HIV community-based and policy-oriented groups have been. In fact, comedy routines discussing STIs may actually have an opposing effect: leading people to be less concerned about STI severity and prevention. For example, Saturday Night Live’s Weekend Update on October 12, 2019, parodied that STIs have a relatively low negative impact on quality of life compared to other infectious diseases, such as influenza (SNL, 2019). Although such content is designed for entertainment, trivializing the harms of STIs likely also influences viewers’ attitudes/beliefs and behaviors. The STI epidemic’s growth reflects many social, biological, and behavioral forces; limited resources for public awareness and risk reduction education, and limited investments in surveillance, screening, and treatment, also contribute to STI spread.

CONCLUSIONS

This chapter has sought to provide historical information about HIV and emphasize the inextricable linkage between HIV, classical STIs, and viral hepatitis. Ultimately, HIV and many types of viral hepatitis are most importantly STIs. While the committee was not charged with providing policy recommendations related to HIV, it offers a series of conclusions (see Box 5-2 for examples of potential synergies between HIV and STI prevention, treatment, and control):

BOX 5-2

Examples of Potential Synergies Between HIV and STI Prevention, Treatment, and Control.

Conclusion 5-1: STIs and HIV are inextricably linked. Over the past 40 years, however, they frequently have been addressed in silos by the U.S. public health system even though they are very often detected concomitantly.

Conclusion 5-2: There are opportunities for greater synergies for HIV and STIs that would improve prevention, treatment, and linkage to care for both. STI and HIV service integration at the client level and program integration at the federal, state, and local levels will enhance the prevention and care of both. Furthermore, increased education for HIV providers regarding treatment and prevention of STIs is needed.

Conclusion 5-3: Significant federal investments have been made toward screening individuals for HIV, yet when such screening is not integrated with screening for bacterial STIs, it represents a missed opportunity. Conversely, it is equally important to assess HIV status among those diagnosed with a bacterial STI; and for those with HIV infection, screening for other STIs should be elevated as a priority within routine clinical management of HIV.

Conclusion 5-4: Ending the HIV Epidemic (EHE) has the potential to drive significant improvements in the health of communities affected by STIs; therefore, targets for STI reduction could be added to the EHE Plan in partnership with CDC. While this initiative is supporting STI clinics, the absence of more central consideration of STIs in the EHE has the potential to limit the achievements of EHE goals and sustain ongoing transmission of these infections.

In past decades, STIs and HIV have mostly been addressed by the U.S. public health system in “silos” even though they are very often detected in combination. Advances in HIV can be ascribed to funding and growth of a massive community of researchers, clinical and community-based services providers, and people living with HIV and their advocates. In addition, the rapidity of scientific progress for new diagnostic, therapeutic, and preventative tools contrasts to comparatively indolent progress for other STIs, despite their clinical recognition for centuries and their microbiological characterization for many decades. Progress with HIV underscores what can be done if a problem is confronted and prioritized; programmatic successes with HIV serve to emphasize the promise for substantially improved STI control. Yet, public health support for STIs has lagged the demands of the rising incidence in the United States, contributing to the rise of STIs and a relative dearth of vaccine research, innovative diagnostics, and improved treatments. Unfortunately, success in preventing and treating HIV has likely contributed to STI spread in some populations, as concern around HIV infection has diminished. STIs cannot be seen as simply an annoyance or inevitability, given the seriousness of STI long-term sequelae, including infertility. STI and HIV service integration will enhance the prevention and care of both.

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