Purpose of This Guideline

Date of current publication: November 4, 2022 Lead author: Meera Shah, MD, MPH, MS, AAHIVS Contributors: Maria Teresa (Tess) Timoney, MS, RN, CNM, and Jessica M. Atrio, MD, MSc Writing group: Steven M. Fine, MD, PhD; Rona M. Vail, MD; Joseph P. McGowan, MD, FACP, FIDSA; Samuel T. Merrick, MD; Asa E. Radix, MD, MPH, PhD; Charles J. Gonzalez, MD; Christopher J. Hoffmann, MD, MPH Committee: Medical Care Criteria Committee Date of original publication: July 10, 2018

This guideline on human papillomavirus (HPV) in individuals with HIV was developed by the New York State Department of Health AIDS Institute (NYSDOH AI) to inform primary care providers and other practitioners in New York State about HPV prevention, screening methods, diagnosis and presentation, and treatment in adults with HIV. This guideline aims to achieve the following goals:

• Increase the number of New York State residents with HIV who are screened and effectively treated for HPV-related dysplasia.
• Support the NYSDOH Prevention Agenda 2019-2024 by educating care providers on the importance of HPV vaccination and increasing the rate of 3-dose HPV immunization among individuals with HIV.
• Reduce the morbidity and mortality associated with HPV in people with HIV through early identification and treatment of potentially precancerous and cancerous lesions, when treatment is most likely to be effective.

Note on “experienced” and “expert” HIV care providers: Throughout this guideline, when reference is made to “experienced HIV care provider” or “expert HIV care provider,” those terms are referring to the following 2017 NYSDOH AI definitions:

• Experienced HIV care provider: Practitioners who have been accorded HIV Experienced Provider status by the American Academy of HIV Medicine or have met the HIV Medicine Association’s definition of an experienced provider are eligible for designation as an HIV Experienced Provider in New York State. Nurse practitioners and licensed midwives who provide clinical care to individuals with HIV in collaboration with a physician may be considered HIV Experienced Providers as long as all other practice agreements are met (8 NYCRR 79-5:1; 10 NYCRR 85.36; 8 NYCRR 139-6900). Physician assistants who provide clinical care to individuals with HIV under the supervision of an HIV Specialist physician may also be considered HIV Experienced Providers (10 NYCRR 94.2)
• Expert HIV care provider: A provider with extensive experience in the management of complex patients with HIV.

HPV-Associated Cancers

HPV-associated cancers: Cervical cancer rates have decreased because of a robust screening system in the United States that has been in place since the 1960s [NCI(a) 2022]. The incidence of anal cancer persists, particularly among men who have sex with men (MSM) with or without HIV and among women with HIV [Islami, et al. 2017; Palefsky 2017; Hessol, et al. 2013], and approximately 91% of anal cancers are thought to be caused by human papillomavirus (HPV) [CDC(b) 2022].

This committee has recommended anal screening for specific subpopulations of individuals with HIV since 2007 and recently expanded the recommendation to include anal cytology screening for MSM, cisgender women, transgender women, and transgender men who have HIV and are ≥35 years old. Anal Cancer HSIL Outcomes Research (ANCHOR) study investigators announced by press release in October 2021 that treatment of precancerous lesions reduced anal cancer risk among people with HIV [ANCHOR 2021]. Although screening tests are available for oropharyngeal cancers, the utility and benefits have not been established; therefore, screening other than visual inspection is not yet recommended (see American Dental Association: Evaluation of Potentially Malignant Disorders in the Oral Cavity Clinical Practice Guideline [2017] for more information). There are no routine screening tests or procedures for vulvar, vaginal, or penile cancers.

HPV types: There are many HPV types, some of which cause cancer (oncogenic) and others of which cause noncancerous disease (nononcogenic verruca vulgaris and condyloma acuminata). Approximately 30 different HPV types infect cells in the anus and genital tract, including the cervix, and may cause asymptomatic infection, condylomata acuminata (genital warts), squamous intraepithelial lesions (SILs), glandular cell abnormalities, and anal and cervical cancer or other genital carcinomas. HPV is also associated with oropharyngeal cancer [CDC(a) 2022; CDC(b) 2022]. HPV infection is often asymptomatic, and the time course from initial infection to the presence of lesions has not been determined, preventing a reliable method for determining the source and time of acquisition.

In the general U.S. population, HPV types 16 and 18 are responsible for approximately 70% of cases of cervical and anal SILs and cervical and anal cancers [Lowy and Schiller 2012; Steinbrook 2006] in addition to most oropharyngeal, vaginal, vulvar, and penile cancers [Saraiya, et al. 2015; Forman, et al. 2012; Grulich, et al. 2010; Bouvard, et al. 2009]. Nononcogenic HPV types 6 and 11 cause >90% of genital warts [CDC(a) 2021; Workowski, et al. 2021]. A wider range and higher prevalence of HPV types responsible for oncogenic and nononcogenic disease have been documented in people with HIV [Massad, et al. 2016; Kojic, et al. 2011; Clifford, et al. 2006]. HPV-associated cancers occur more often among people with HIV than in the general population [Liu, et al. 2018; Jemal, et al. 2013], and the distribution of HPV types responsible for SILs and warts also differs between these populations [Clifford, et al. 2006].

High-risk HPV types that are related to anogenital cancers include types 16, 18, 26, 31, 33, 35, 39, 45, 51, 52, 53, 56, 58, 59, 66, 67, 68, 69, 70, 73, and 82 [Guan, et al. 2012; Hariri, et al. 2012]. Although high-risk HPV types are detected in 99% of cervical cancers, types 16 and 18 are the most oncogenic [Clifford, et al. 2017; Keller, et al. 2015] and account for nearly 70% of all cervical cancers in the general population [CDC(a) 2021]. HPV type 16 is the most common high-risk type among individuals with or without HIV [Lin, et al. 2018]. Among individuals with HIV, cervical cancer is associated with types 16 and 18 and high-risk types 51, 52, 53, 56, 58, and 59 [McKenzie, et al. 2010]. High-risk HPV types other than type 16 are more common and are more frequently associated with anal cancer among MSM with HIV than MSM without HIV [Poynten, et al. 2021]. Infection with more than one HPV type occurs more frequently among individuals with HIV, and these individuals can be at risk of cervical and anal SILs and nonmalignant disease simultaneously [Castilho, et al. 2015; Clifford, et al. 2006].

Tobacco use: Tobacco use is an established contributor to the oncogenic potential of HPV and is an independent risk factor for acquisition and progression of cervical SILs [Collins, et al. 2010], anal neoplasia [Daling, et al. 2004], oropharyngeal cancer [NCI(b) 2022], and vulvar cancer in individuals with HIV [ACS 2018; Kutlubay, et al. 2013]. Some data suggest that HIV-related immune suppression can contribute to relapse and progression of HPV disease, and antiretroviral therapy-mediated immune reconstitution can lead to regression of SILs associated with HPV infection [Blitz, et al. 2013]. Other studies do not support this finding [Piketty, et al. 2013; Adler 2010].

HPV Prevention

Cervical and Anal Cancer Screening

Cervical cancer screening: Clinicians should perform cervical and anal cytologic screening for people with HIV according to the recommendations in the NYSDOH AI guidelines Screening for Cervical Dysplasia and Cancer in Adults With HIV and Screening for Anal Dysplasia and Cancer in Adults With HIV. HPV testing with cytologic screening enhances the identification of HPV-related cervical disease in individuals with HIV. Examination of the anogenital area of patients with HIV to assess for visible HPV lesions is necessary because HPV can also infect the urethra and the external genitalia [Ehrenpreis and Smith 2018; Leeds and Fang 2016; Tyerman and Aboulafia 2012; Weyers, et al. 2010]. Speculum examination of the vagina, neovagina, and cervix and anoscopic examination of the anus and lower rectum may also reveal lesions. There are currently no data on urethral screening and treatment, but referral to a urologist will facilitate appropriate assessment and management when this is a concern.

Anal cancer screening: Anal squamous intraepithelial lesions (SILs) have been associated with concurrent cervical SILs; however, they also occur independently. Anal cytology should be performed for all cisgender women with HIV [Gaisa, et al. 2017; Stier, et al. 2015; Hessol, et al. 2013; Kojic, et al. 2011], with or without cervical abnormalities, according to guidelines for adults with HIV. Although there are no specific data on transgender men or transgender women, anal screening is also recommended for these populations.

Transgender individuals: It is important that care providers and facilities establish a safe and welcoming environment for transgender patients [UCSF 2016]. Approximately one-third of transgender or gender-diverse individuals assigned female sex at birth identify as nonbinary [National Center for Transgender Equality 2016]. Asking patients to provide details about all gender-affirming and gynecologic surgical procedures will help establish the need for screening for HPV-related cancers. For terminology and definitions related to transgender care, see University of California San Francisco Gender-Affirming Health Program.

Sexual history: Discussion of sexual health, including a patient’s history of sexually transmitted infections (STIs), is an important component of the baseline and annual assessments and is an opportunity to discuss a patient’s concerns and questions. The frequency of the sexual health assessment is based on risk factors. It is particularly important to use nonjudgmental, sex-positive language in this discussion to establish a strong connection and facilitate open discussion.

Presentation and Diagnosis of HPV Infection

Diagnosis of external condylomata acuminata is often made based on clinical appearance. The appearance of warts varies. Condylomata acuminata (genital warts) can be smooth and skin-colored or hyperpigmented papules or plaques that may be flat, hyperkeratotic, nodular, or exophytic. Symptoms may be absent or may include itching, bleeding, burning, and discomfort. Warts on the external genitalia and the cervix are commonly flat, plaque-like lesions but may also be exophytic and visible to the naked eye. Cervical lesions are best visualized by colposcopy. Penile lesions can occur along the shaft but may also occur along the penile urethra and be hidden from view.

Small external lesions are often treated without biopsy. Lesions that are atypical or variegated in color or shape require biopsy to exclude squamous intraepithelial lesions (SILs) or cancer. Clinicians should maintain a low threshold for obtaining biopsies of the following, which may indicate precancerous or cancerous lesions: atypical-appearing lesions; pigmented, internal, or condylomatous lesions; rapidly growing lesions; or lesions that fail to respond to standard treatment.

Manifestations of HPV infection in individuals with HIV infection may include the following [Wang and Palefsky 2019; Liu, et al. 2018; Clifford, et al. 2017; Palefsky 2017; Lillo, et al. 2001; Minkoff, et al. 2001; Palefsky(a), et al. 2001; Palefsky(b), et al. 2001; Frisch, et al. 2000; Palefsky, et al. 1998]:

• Condylomata acuminata, anal SILs, anal intraepithelial neoplasia, cervical SILs, and cervical intraepithelial neoplasia have all been reported to occur more frequently in people with HIV.
• With increased immunosuppression, there is evidence for increased risk of persistent and recurrent HPV infection and disease of the anal and genital tracts; decreased rates of spontaneous disease regression; increased severity of HPV disease; anal SILs and cervical SILs; and development of condylomata acuminata.
• HPV infection may be more difficult to treat and more likely to recur with advanced immunosuppression.
• Patients with more advanced immunosuppression have an increased relative risk of developing HPV-related invasive anogenital cancers.

Data are mixed regarding the contribution of HIV-related immune suppression to the relapse and progression of HPV disease and whether antiretroviral therapy (ART)-mediated immune reconstitution can lead to regression of SIL associated with HPV infection [Blitz, et al. 2013; Piketty, et al. 2013; Adler 2010]. Although there are cases of involution of mucocutaneous warts after initiation of ART, the prevalence or course of anogenital HPV disease is not altered significantly by ART [Lofgren, et al. 2015; Adler 2010].

HPV Treatment

The standard therapeutic approach to treating HPV-related nonmalignant lesions (condyloma/warts) and dysplasia (squamous intraepithelial lesions or above) in individuals with HIV is the same as that for individuals without HIV. Treatment of condyloma is aimed at removing symptomatic visible warts. However, some untreated warts may resolve spontaneously. There has been no evidence that any available treatment regimen eradicates HPV infection. Comparative efficacy trials of the different treatment options for patients with HIV have not been conducted. Treatment of precancerous lesions includes ablation, using cryotherapy or laser, and surgical or laser excision. These procedures should be performed only by experienced clinicians (for more information, see NYSDOH AI guideline Screening for Cervical Dysplasia and Cancer in Adults With HIV).

Cryotherapy, electrocautery, podophyllotoxin, interferon, imiquimod, cidofovir gel, trichloroacetic acid, and bichloroacetic acid have all demonstrated efficacy treating anogenital warts in patients without HIV. In a systematic review and meta-analysis, electrocautery and imiquimod were shown to be efficacious in treating anogenital warts in people with HIV [Werner, et al. 2017]. Controlled studies of other HPV interventions in people with HIV have not been done. Interferon, 5-fluorouracil, and podophyllotoxin are no longer preferred HPV treatments in the primary care setting because of low efficacy and toxicity that may limit their routine use [Lacey, et al. 2013]. The safety and efficacy of sinecatechins have not been evaluated in individuals with HIV and therefore should not be used [FDA 2007].

There are limited data on imiquimod use in pregnancy, but animal data suggest low risk of harm [Workowski, et al. 2021]. This drug can be used during pregnancy if no other options, including waiting until after delivery, are available. Because of a lack of safety data, podophyllin should not be used during pregnancy. Podofilox (podophyllotoxin) is contraindicated in pregnancy [Briggs, et al. 2017].

Data on treating HPV lesions of the neovagina, whether penile or colonic in origin, are limited to case reports and small case series. Standard, care provider-applied approaches to treatment should be used [Labanca and Mañero 2017; van der Sluis, et al. 2016; Matsuki, et al. 2015; Wasef, et al. 2005; Liguori, et al. 2004; Fiumara and Di Mattia 1973].

Clinicians often report poor clearance rates after therapy in patients with HIV [Richel, et al. 2013]. More than one application of therapy, more than one method of treatment (e.g., topical imiquimod followed by cryotherapy), or longer duration of treatment is often needed. Treatment length may vary, and frequent visits (as often as biweekly) are necessary to assess lesion regression and adverse effects. Topical treatments may cause adverse effects such as irritation and a burning sensation, which may affect treatment adherence. The response to treatment and its adverse effects should be evaluated throughout the course of therapy. The treatment approach may need to be changed if a patient has not improved substantially after standard therapy. There are no data available regarding effects of HPV treatment on HPV transmissibility.

When deciding whether to treat a patient with HIV for anogenital warts or refer the patient to a specialist, clinicians should consider their own experience and available resources, diagnostic certainty, anatomic site of lesions, potential adverse effects of treatment, and the patient’s ability to adhere to treatment.

Table 1, below, lists available treatment options for condyloma for patients with HIV.

Partner Exposure to HIV and HPV

Treatment of lesions solely for the prevention of future transmission cannot be recommended because the value of treatment in reducing infectivity is not known. However, sex partners of patients who have genital lesions might benefit from counseling and examination to assess the presence of genital warts and HPV-related dysplasia. Sex partners should also be evaluated for other sexually transmitted infections (STIs), including HIV, because HPV disease is transmitted sexually [Workowski, et al. 2021].

Clinicians should inform patients that any sex partner who does not have confirmed HIV infection should have routine HIV testing for early identification of HIV acquisition. If a patient with an HIV exposure presents within 36 hours, evaluation for non-occupational post-exposure prophylaxis (PEP) should occur. When possible, onsite availability of HIV testing and STI treatment for partners is ideal because it may increase the likelihood that partners will receive timely access to HIV testing and appropriate treatment, including HIV PEP and treatment for the STI as needed. Such strategies may also increase identification of individuals who require ongoing medical care. Partner education about reducing high-risk sexual behaviors, including counseling about the use of male/insertive and female/receptive condoms and making condoms visibly available in the clinic, may help further decrease the risk of transmission of both HIV and other STIs. Patients who remain at high risk of exposure after completing a course of non-occupational PEP and who are negative for HIV at the time of the 4-week test should be offered pre-exposure prophylaxis (PrEP), to begin immediately after the last dose of non-occupational PEP. Patient education about undetectable=untransmittable (U=U) as an HIV prevention strategy should stress that an undetectable HIV viral load prevents only the sexual transmission of HIV.

The NYSDOH Partner Services program provides assistance to individuals with HIV and care providers who would like help notifying a patient’s sex partner(s) of possible exposure to HIV, chlamydia, gonorrhea, or syphilis. Available options for partner notification include anonymous notification from the local health department, dual disclosure (patient disclosure with the help of Partner Services staff), and self-disclosure. Partner Services staff within local health departments work with patients to develop a plan to notify their partners, whether that plan includes staff notifying potentially exposed partners anonymously or helping patients who choose to tell their partners on their own develop a notification plan and strategy.

All Recommendations

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Supplementary Material

Supplement: Guideline Development and Recommendation Ratings