Publications and Presentations

PLOS | November 29, 2019

The human papillomavirus (HPV) is the most common sexually transmitted infection worldwide. Gay, bisexual, and other men who have sex with men (GBM) living with HIV are disproportionately impacted by HPV-associated anal cancer, with rates about 100-fold that of the general population. Fortunately, HPV vaccination has proven efficacy in preventing both anogenital warts (condyloma) in males and anal pre-cancers (anal intraepithelial neoplasia; AIN) in GBM up to the age of 26. We conducted in-depth, semi-structured interviews with 25 HIV-positive gay men in Toronto to gain an understanding of their knowledge and experiences related to HPV and the HPV vaccine. These participants were part of The HPV Screening and Vaccine Evaluation (HPV-SAVE) Study, and received invitations to have anal cancer screening from their primary care doctors. Interviews were analyzed following a Grounded Theory Approach. Most participants had not received the HPV vaccine. Men described a lack of prior knowledge of the health consequences of HPV for GBM living with HIV and financial barriers to vaccine access. Participants did not articulate concerns about vaccine safety. Men frequently reported initial beliefs that HPV was predominantly—or exclusively—a risk for females or young girls, and thus they had not considered the vaccine to be necessary. Some participants remained uncertain if the current availability of the vaccine, and their newly acquired knowledge of its importance, was “too little, too late” because of their age and/or HPV exposure. Improving access and uptake of HPV vaccination requires addressing both financial barriers to access as well as increasing HPV health literacy levels, particularly by reframing the long-standing gendered associations of HPV. Physicians should provide clear, tailored messages regarding HPV vaccination.

International Journal for Equity and Health | October 17, 2019

Background

The human papillomavirus (HPV) is the most common sexually transmitted infection (STI) worldwide. Gay, bisexual, and other men who have sex with men (GBM), and GBM living with HIV in particular, are disproportionately impacted by HPV-associated cancers. The HPV vaccine, given early enough in life, may markedly reduce the likelihood of such cancers. In Canada, most provincial insurance programs only cover HPV vaccination for GBM up to the age of 26. Our objective was to understand physicians’ everyday experiences and challenges in recommending HPV vaccination to older GBM patients.

Methods

As part of the HPV Screening and Vaccine Evaluation (HPV-SAVE) Study, we conducted semi-structured interviews with 25 HIV-positive GBM patients who had received anal cancer screening and 15 service providers, including 13 physicians, who had arranged for anal cancer screening in the Canadian provinces of Ontario and British Columbia. In this analysis, we draw upon the 13 physician interviews, which were coded following Grounded Theory.

Results

Physicians strongly supported the HPV vaccine for all GBM and considered it to be important for the management of HIV-related care. However, the overall support for HPV vaccination among physicians did not translate into consistent recommendation practices. There were two overarching factors that limited the strength/frequency of physicians’ vaccine recommendation practices. First, cost/insurance coverage for some older patients impacted if and how the HPV vaccine was discussed. Second, physicians had diverse perspectives on both the prevention and therapeutic benefits of vaccinating older GBM and the reality that national guidelines are incongruent with publicly funded vaccine programs for vaccinating patients over 26 years old. These two interrelated factors have co-produced an apparent economic-evidentiary conundrum for many physicians regarding how and for whom to offer HPV vaccination.

Conclusion

Economic barriers coupled with evidentiary and guideline gaps have created clinical practice challenges for physicians and has resulted in different messages being communicated to some older GBM patients about how important HPV vaccination is for their health.

Keywords: Human papillomavirus (HPV), HPV vaccination, HIV, Gay, bisexual, and other men who have sex with men (GBM), Qualitative, Physician practices

Social Science & Medicine | January 2020

The social science literature on medical screening has documented a notable disjuncture between the promises of population-based screening programs and the complex realities of their rollout in everyday practice. We contribute to this scholarship by examining how healthcare providers confront numerous uncertainties associated with the implementation of anal cancer screening programs in Canada given the absence of standardized national evidence-based guidelines. The data was derived from in-depth interviews conducted with 13 physicians and 2 clinical researchers about anal cancer screening for gay, bisexual and other men who have sex with men living with HIV, the minority sub-population at the highest risk for HPV-associated anal cancer. Despite having unknown utility and low specificity, an initial anal Pap test was used to triage patients into anal dysplasia clinics for high-resolution anoscopy. This process led to technological skepticism toward the Pap's accuracy, diagnostic ambiguity related to the interpretation of the cytology results and increased patient anxiety regarding abnormal results. Physicians navigated a tension between wanting to avoid exposing their patients to additional uncertainties caused by screening and pre-cancer treatment and wanting to ensure that their patients did not develop anal cancer under their care. A high number of abnormal anal Pap results paradoxically reintroduced some of the capacity issues that the Pap was meant to resolve, as the existing dysplasia clinics were incapable of seeing all patients with abnormal results. We define this sequence as the epistemic-capacity paradox, a dynamic whereby seeking evidence to improve healthcare capacity simultaneously produces evidence that introduces capacity challenges and generates additional uncertainty. The epistemic-capacity paradox demonstrates the limitations of evidence-based medicine frameworks at determining best practices in the context of rarer health conditions affecting minority sub-populations, where smaller population numbers and limited institutional support pose systemic challenges to the acquisition of sufficient evidence.

URL: https://www.sciencedirect.com/science/article/pii/S0277953619306380

Journal of Oral Oncology | October 6, 2014

Objectives

To examine the risk and trends of HPV-related and HPV-unrelated Head and Neck Squamous Cell Carcinoma (HNSCC) in HIV-infected individuals and assess whether immunosuppression (measured through CD4 cell count) and other risk factors impact HNSCC risk.

Materials and methods

Incident HNSCCs at HPV-related and HPV-unrelated anatomic sites were detected in HIV-infected participants from pooled data from 17 prospective studies in the North American AIDS Cohort Collaboration on Research and Design (NA-ACCORD) between 1996 and 2009. HNSCC cases were validated using chart review or cancer registry matching. Risk factors for incident HPV-related and HPV-unrelated HNSCC were explored using mixed effects Poisson regression in a full prospective analysis, and the effect of CD4 prior to cancer diagnosis was examined in a nested case control analysis.

Results

66 HPV-related and 182 HPV-unrelated incident HNSCCs were detected among 82,375 HIV-infected participants. Standardized incidence ratios (SIRs) for both HPV-related (SIR = 3.2, 95%CI = 2.5–3.4) and HPV-unrelated (SIR = 3.0, 95%CI = 2.5–4.1) HNSCC were significantly elevated in HIV-infected individuals compared with the US general population. Between 1996 and 2009, the age-standardized HPV-related HNSCC incidence increased non-significantly from 6.8 to 11.4 per 100,000 person-years (p-trend = 0.31) while the age-standardized incidence of HPV-unrelated HNSCC decreased nonsignificantly from 41.9 to 29.3 per 100,000 person-years (p-trend = 0.16). Lower CD4 cell count prior to cancer diagnosis was significantly associated with increased HPV-related and HPV-unrelated HNSCC risk.

Conclusion

The standardized incidence of HPV-related and HPV-unrelated HNSCC are both elevated in HIV-infected individuals. Immunosuppression may have a role in the development of both HPV-related and HPV-unrelated HNSCC.

Keywords: Head and Neck Squamous Cell Carcinoma, HPV, CD4 T cell count, NA-ACCORD, HIV, Oropharyngeal cancer

Virology Journal | October 23, 2012

BACKGROUND:

Human papillomavirus type 97 (HPV97) DNA was detected in nearly 5% of anal samples collected from HIV-seropositive men living in Montreal, Canada. The rate of detection of HPV97 in the genital tract of Canadian women is unknown. Whether HPV97 is a local epidemic in HIV-seropositive men living in Montreal is also unknown. The prevalence of human papillomavirus type 97 (HPV97) was assessed in cervicovaginal cells from women living in Canada and in anal samples from HIV-seropositive men living in Toronto.

FINDINGS:

Cervicovaginal lavages collected from 904 women (678 HIV-seropositive, 226 HIV-seronegative) women living in Canada and anal cells collected from 123 HIV-seropositive men living in Toronto were tested for the presence of HPV97 with PCR. HPV97-positive samples were further tested by PCR-sequencing for molecular variant analysis to assess if all HPV97-positive men were infected with the same strain. All cervicovaginal samples were negative for HPV97. HPV97 was detected in anal samples from 6 HIV-seropositive men (4.9%, 95% confidence interval 2.0-10.5%), of whom five had high-grade and one had low-grade anal intraepithelial neoplasia, in addition to 2 to 8 HPV genital genotypes per sample. Four HPV97 variants were defined by four variation sites in the viral control region.

CONCLUSION:

These findings indicate that HPV97 infects in the anal canal of HIV-seropositive men but is not detected in the genital tract of women.

URL: https://www.ncbi.nlm.nih.gov/pubmed/23092191

AIDS | 13 March, 2011

OBJECTIVE:

To assess the cost-effectiveness of high-resolution anoscopy (HRA), anal cytology, and anal human papillomavirus (HPV) detection in screening for histologic high-grade anal intraepithelial neoplasia (AIN 2/3) in HIV-positive MSM.

DESIGN:

Participants were 401 HIV-positive MSM who were screened for anal cancer in a tertiary care HIV clinic.

METHODS:

A decision analytical model was used to determine the cost-effectiveness of three anal cancer screening strategies: the direct use of HRA; HRA only if anal cytology was abnormal; and HRA only if oncogenic HPV was present. The model included the use of different thresholds for abnormal cytology and also combined cytology and HPV testing. The outcome was the number of AIN 2/3 cases detected. Costs were estimated from institutional data and sensitivity/specificity of cytology and HPV tests were obtained from the screening study.

RESULTS:

The costs ($ US) per procedure for HRA, cytology, and HPV testing were $193, $90, and $95, respectively. The direct use of HRA was the most cost-effective strategy. It detected 98 individuals with AIN 2/3 and had a cost-effectiveness of $809 per AIN 2/3 case detected. Using probabilistic sensitivity analysis, three other strategies had similar costs per case detected and might be as cost-effective as HRA.

CONCLUSION:

In HIV-infected MSM, the direct use of HRA is the most cost-effective strategy for detecting AIN 2/3. The higher cost per use for HRA was offset by the high sensitivity and low specificity of HPV and cytology testing.

URL: https://www.ncbi.nlm.nih.gov/pubmed/21139488

AIDS | June 1, 2010

OBJECTIVE:

To assess anal oncogenic human papillomavirus (HPV) and anal cytology as screening tests for detecting high-grade anal intraepithelial neoplasia (AIN 2+), as this is an immediate anal cancer precursor.

DESIGN:

Cross-sectional study of 401 HIV-positive men who have sex with men (MSM). The endpoint was histologically confirmed AIN 2+ obtained by high-resolution anoscopy. Cytology and biopsy specimens were assigned random numbers and independently assessed by two pathologists.

METHODS:

We did concomitant anal cytology, anal HPV testing and HRA with directed biopsies without knowing the results of each intervention. The main outcome measures were the sensitivity, specificity, negative predictive value and positive predictive value of anal cytology and oncogenic HPV for the detection of AIN 2+.

RESULTS:

Cytology was abnormal in 67% of patients: high-grade squamous intraepithelial lesion, 12%; low-grade squamous intraepithelial lesion, 43% and atypical squamous cells of undetermined significance, 12%. Biopsies were abnormal in 68% of patients: AIN 2+, 25% and AIN 1, 43%. HPV was detected in 93% with multiple HPV types in 92% and oncogenic HPV types in 88%. Test performance characteristics for the detection of AIN 2+ using any abnormality on anal cytology were: sensitivity 84%, specificity 39%, negative predictive value 88% and positive predictive value 31%; using oncogenic HPV: sensitivity 100%, specificity 16%, negative predictive value 100% and positive predictive value 28%.

CONCLUSION:

Anal cytology and HPV detection have high sensitivity but low specificity for detecting AIN 2+. HIV-positive men who have sex with men have a high prevalence of AIN 2+ and require high-resolution anoscopy for optimal detection of high-grade anal dysplasia.

URL: https://www.ncbi.nlm.nih.gov/pubmed/20442633

Health, Risk & Society | 17 September, 2019

HPV-associated anal cancer is one of the most prevalent non-AIDS defining cancers affecting gay men living with HIV. Drawing on interviews with 25 HIV-positive gay men living in Toronto in 2017, we explored their responses to anal cancer as a comorbidity risk and the necessity of preventative screening. These participants had previously been screened for anal cancer through a clinical trial. The majority of our sample did not initially consider anal cancer a health priority. They relied on narratives of living with HIV – that is, on their HIV biographies – to make sense of anal cancer’s significance given their self-described lack of knowledge. This included references to personal-level narratives of the biographical disruption and revision associated with a HIV diagnosis, as well as reflections on community-level and socio-historical trends in the HIV epidemic. Drawing on these narratives, some started to accept anal cancer as a significant comorbidity risk, while others remained ambivalent. Those who began to accept anal cancer as significant integrated it into their HIV biographies to present anal cancer as a threat to the ontological security they have gained managing HIV in an era of effective treatment and to position themselves as pragmatic, responsible health-seekers. Others drew on their HIV biographies to vocalise resistance to chronic risk and medicalisation. Our analysis points to the fundamental role narratives play on everyday risk perception practices, health decision-making and, for those managing a chronic illness, on securing ontological security and presenting a coherent self-identity under conditions of expanding risks and prevention possibilities.

AIDS | 21 February, 2020 

Our objective was to quantify the extent of anal cancer screening among men receiving HIV specialty care in Ontario, Canada and evaluate factors associated with screening.

SETTING:

Cross-sectional questionnaire within a multi-site clinical HIV cohort.

METHODS:

A questionnaire assessing knowledge and experience with HPV-associated diseases and their prevention was administered in 2016-2017 to 1677 men in the Ontario HIV Treatment Network Cohort Study. We used logistic regression to identify factors associated with having discussed screening with a healthcare provider and self-reported receipt of screening (digital anorectal exams [DARE]; anal cytology or anoscopy). Results reported as adjusted odds ratios (aOR) with 95% confidence intervals (CI).

RESULTS:

40% of men reported ever having had anal cytology/anoscopy, and 70% had ever had DARE. After accounting for differences in age, sexual orientation, years since HIV diagnosis, previous diagnosis with AIDS, knowing someone with HPV-associated cancer, comfort discussing anal health, education and income, the proportion screened differed by self-identified race. Compared to White men, Asian men were less likely to have discussed screening with a healthcare provider (aOR=0.48 95% CI:0.29,0.80) or to have been screened by DARE (aOR=0.27 95% CI:0.17,0.44) or anal cytology/anoscopy (aOR=0.51 95% CI:0.31,0.83); and African, Caribbean or Black men (aOR=0.47 95% CI:0.31,0.70) were less likely to have had DARE. Results were consistent when restricting the analyses to gay, bisexual and other men who have sex with men.

CONCLUSION:

Our findings highlight the potential for disparities in anal cancer screening that need to be considered when developing guidelines and screening programs to reduce the burden of anal cancer among men living with HIV and ensure health equity.

URL: https://www.ncbi.nlm.nih.gov/pubmed/32097251

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