HPV Clinical Research and Vaccines. Rachel Winer, PhD, MPH Department of Epidemiology University of Washington

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1 HPV Clinical Research and Vaccines Rachel Winer, PhD, MPH Department of Epidemiology University of Washington

2 Epidemiology of HPV The most common STD in the US and worldwide 80% sexually active adults in the US infected with at least one HPV type by age 50 1 Estimated incidence: 6.2 million per year 1 1. Centers for Disease Control and Prevention. Rockville, Md: CDC National Prevention Information Network; 2004

3 Worldwide HPV Prevalence Global estimate* 10% Africa 22% Central America/Mexico 20% North America 11% Europe 8% Asia 8% *based on 78 studies worldwide de Sanjose et al (2007) Lancet Infect Dis Age-adjusted HPV prevalence

4 Role of HPV in Cancers % HPV Cx Anal Vulva/Vaginal Penile Oral Trottier H et al, Public Health Genomics 2009

5 Estimated Lifetime Risk of HPV- Related Lesions Genital warts 1 in 15 adults Abnormal Pap (routine Pap testing) 1 in 3 women Cervical cancer Regions with routine Pap testing < 1 in 100 women Regions without routine Pap testing ~ 1 in 25 women Other genital cancers <1 in 100 adults Anal cancer ~ 1 in 25 men who have sex with men ~20% of head & neck cancers <1 in 400 adults

6 Annual Global Burden of HPV- Related Cancers 530,000 cervical cancers (270,000 deaths) 88% in developing countries 97,200 non-cervical cancers (51,000 in men and 46,000 in women), including penile, vaginal, vulvar, anal, oropharyngeal

7 Global Perspective on Cervical Cancer 5 th most common cancer in humans 3 rd most common cancer in women Relatively early age of death Median of 57 yrs versus 72 yrs for all cancers

8 Age-Standardized Rates of New Cases of Cervical Cancer per 100,000 Women, 2002 Agosti J and Goldie S. N Engl J Med 2007;356:

9 Relative Contribution of HPV Types to the Global Burden of Cervical Cancer Other 53.5% 70.7% 77.4% 80.3% 82.9% 85.2% 87.4% 88.8% 90.1% 91.3% 92.3% 93.0% 93.6% 94.1% 94.4% 100% Muñoz IJC 2004

10 Modes of HPV Transmission SKIN contact, not blood or bodily fluids Sexual Intercourse (vaginal or Anal) (most common route) Genital (non-penetrative), oral, digital contact Non-sexual Mother to newborn (vertical transmission - rare) Auto-innoculation probably important for site-to-site transmission

11 Female Risk of Acquiring Genital HPV Infection from her First Male Sex Partner Winer et al. J Infect Dis 2008;197: Cumulative Incidence of Genital HPV Infection Months* *From date of first reported vaginal intercourse with a male partner (Women were censored at reported date of a second sex partner)

12 Duration of HPV Infections Vast majority of infections resolve spontaneously (90% within 2 years) Can t be sure whether an infection has cleared or become latent

13 Duration of HPV Infections In newly sexually active female university students, 90% of new infections cleared within 2 years (half cleared within 9.4 months). 1 19% of cleared infections were re-detected within 1 year. 1 Winer et al. Cancer Epi Bio Prev 2011; 20:

14 Risk Factors for HPV Infection in Women Recent new partners Increased risk with new partners reported in the past year Time having known a partner before sex Women knowing their partners for <8 month at greater risk than women knowing their partners for 8 months Sex partner s number of previous partners Increased risk with one or more previous partners Even greater risk if the number of previous partners was unknown! Inconsistent condom use with new partners

15 Association between incident HPV infection and condom use over the past 8 months (Winer et al. N Eng J Med 2006; 354: ) Newly sexually active HPV naïve female university students who used condoms consistently (100% of time) reduced their risk of acquisition by 70%.* Those who used condoms at least half the time reduced their risk of acquisition by 50%.* *Compared to those who used condoms <5% of the time, adjusting for numbers of new partners and numbers of partners new partners.

16 HPV in mid-adult women Are mid-adult women at risk for new HPV infections, or are the majority of new infections due to reactivation or persistence of infections acquired at younger ages? It is impossible to distinguish between new infection and reactivation. There are no perfect markers of prior infection.

17 Worldwide meta-analysis (DeSanjose et al, Lancet Infect Dis 2007;7:453-9) Figure 3. World estimates of the age-specific HPV prevalence by country-specific development status

18 Possible Explanations for Secondary Peaks in Prevalence in Older Women Increased persistence or reactivation of latent infections due to age-related / post-menopausal immune senescence New acquisition due to contact w/ new sex partners Changing sexual behaviors among middle-aged women and their partners Birth cohort differences in sexual behaviors In areas with good cervical cancer screening programs, treatment of HPV-related lesions may contribute to lower prevalence in middle-aged women (censoring effect).

19 Risk of incident high-risk HPV infection in female mid-adult online daters (n=421) 1 Sexual activity in prior 6 months Not sexually active with male partners Sex with 1 male partner who was not new Sex with new partner(s) or multiple partners Hazard Ratio ( ) 3.0 ( ) 1 Winer et al. Abstract presented at IPV 2011 conference, Berlin, Germany.

20 HPV Reactivation from Latency In HIV+ women who were not recently sexually active, low CD4+ T-cell count was associated with increased HPV incidence. 1 Age-related / post-menopausal immune senescence may contribute to increased persistence or reactivation of latent infections. 1 Strickler et al. J Natl Cancer Inst 2005;97:

21 Does Re-infection Occur? Neutralizing antibodies likely protect against re-infection with the same HPV type. Difficult to distinguish re-infection from reactivation. Limited epidemiologic data for and against.

22 Incidence of Genital HPV Infection by Anatomic Site Among Sexually Active Male University Students (18-23 Years Old) (Partridge et al. JID, 2007;196: ) Cumulative incidence of HPV infection 1.0 Glans Scrotum Fingernails XXXXX Shaft Urine

23 Circumcision and HPV? A meta-analysis of 21 studies (including 2 RCTs in Africa) showed that HPV was less prevalent in circumcised than uncircumcised men (OR=0.6, 95% CI: ) 1 No effect on HPV acquisition or clearance A longitudinal in young heterosexual men showed no effect on overall HPV acquisition, but multi-focal genital infection was more common in uncircumcised men. 2 Does it affect men s susceptibility to infection and/or infectivity and persistence? 1 Albero et al, Sex Transm Dis 2012; 39: Vanbuskirk et al, Sex Transm Dis 2011; 38:

24 HPV in non-genital sites

25 HPV in Fingers HPV detected on fingers of 38% of women and 64% of men with genital warts. 1 The 2-year cumulative incidence of HPV in fingernail tips was 32% in male university students. 2 14% of fingernail tip samples from female university students were HPV+. 3 The same HPV type was concurrently detected in 60% of vaginal samples. Re-detection at the next visit was less common in fingernail tip samples (15%) than in vaginal samples (73%). 1 Sonnex et al. Sex Transm Infect 1999;75: Partridge et al. J Infect Dis 2007;196: Winer et al. Cancer Epi Bio Prev 2010;19:

26 HPV in Fingers True infection? Deposition? Autoinnoculation?

27 Autoinnoculation In a small study of 25 heterosexual couples, the rate of autoinnoculation (between genitals, anus, hands) in men was comparable to the rate of female-tomale transmission. 1 In female university students, vaginal HPV infections tended to precede cervical infections. 2 1 Hernandez et al. Emerging Infectious Diseases 2008;14: Winer et al. AJE 2003;157:

28 Oral HPV

29 Oral HPV HPV linked to oropharyngeal squamous cell carcinomas (OSCCs) (~90% due to HPV16) 1 Incidence of OSCCs is increasing and expected to surpass that of cervical cancer by D Souza et al. N Engl J Med 2007;356(19): Chaturvedi et al. J Clin Oncol 2011;29(32):

30 Oral HPV Prevalence U.S. survey of healthy individuals aged years 1 : Any HPV: 6.9% HPV16: 1% Prevalence higher in men (10.1%) than in women (3.6%) Bimodal age distribution (peak prevalence in adults aged and years) 1 Gillison et al. JAMA 2012; 15(307):

31 Oral HPV Transmission Oral HPV is predominantly sexually transmitted. Oral HPV prevalence 8-fold higher in sexually experienced individuals, and associated with lifetime numbers of sex partners. 1 Link between oral sex behaviors/open mouth kissing partners and oral HPV is inconclusive. Smoking, immunsuppression, and genital HPV infection have also been associated with oral HPV. Data on oral HPV acquisition and natural history are lacking. 1 Gillison et al. JAMA 2012; 15(307):

32 HPV Vaccination

33 Prophylactic HPV Vaccines Two vaccines based on L1 capsid (shell) protein of HPVs Bivalent HPV16/18, HPV2 Cervarix GlaxoSmithKline Regulatory approval in 50+ countries Quadrivalent HPV6/11/16/18, HPV4 Gardasil Merck Regulatory approval in 100+ countries

34 Diagram of a Prophylactic Vaccine Randomize & blind Trial Disease Vaccinated Follow-up Target Population No Disease Disease Unvaccinated Follow-up prevalent infection (include or exclude?) No Disease

35 Populations Used to Evaluate Gardasil Sero (+) and/or PCR (+) to the relevant vaccine HPV type at day 1 PCR (+) to the relevant vaccine HPV type during the vaccination phase PPE = Per-protocol efficacy ITT = intention to treat PPE Population Excluded Excluded ITT General Population Included Included Protocol violators Excluded Included <3 Doses Excluded Included Case counting 1 month Postdose 3 1 month Postdose 1 Cytology abnormal day 1 Included Included

36 Phase III Randomized Clinical Trials of HPV6/11/16/18 (Merck) or HPV16/18 (GSK) L1 VLP Vaccines in Susceptible Women (~16 to 25 Yrs) Merck Vaccine GlaxoSmithKline Vaccine (NEJM 2007;357:19) Efficacy (Lancet 2009;374:301) Efficacy Vaccine Placebo (95% CI) Vaccine Placebo (96% CI) HPV 16/18- CIN % % (85-99) (86-98) HPV6/11/16/18- Genital warts % (86-99) Merck Vaccine: HPV6/11/16/18 L1 VLP with injections 0, 2, 6 mo. (3 years FU) GSK Vaccine: HPV16/18 L1 VLP with injections 0, 1, 6 mo. (3 year FU)

37 Reduction in HPV16/18-Related CIN2/3+ and Cervical Treatments: ITT Analysis of All Vaccinated Females (~15-26 years), Catch-Up Vaccination Population Paavonen Lancet 2009, Muñoz JNCI 2010 Endpoint Vaccine Cases Placebo Cases Disease or Treatment Reductions due to HPV4 or HPV2 Vaccination CIN2+ HPV4 Vaccine % HPV2 Vaccine % RX Procedures HPV4 Vaccine % HPV2 Vaccine % HPV4 Vaccine N = 17,622, HPV2 Vaccine N = 20,583

38 Prophylactic Efficacy Against HPV 6/11/16/18- Related Genital Lesions in Susceptible Men (16-26 years old) Giuliano NEJM 2011; 364: Palefsky NEJM 2011; 365: Endpoint HPV6/11/16/18 Vaccine (n = 1,397) Placebo (n = 1,408) Vaccine Efficacy (95% CI) HPV6/11/16/18- Genital Warts % (67, 98) (n = 194) (n = 208) AIN in MSM % (40, 93) Susceptible (per protocol)= seronegative, < 6 partners, HPV DNA negative at enrolment, all 3 vaccinations

39 Prophylactic Efficacy Against HPV 6/11/16/18-Related Genital Lesions in Endpoint HPV6/11/16/18- Men (16-26 years old) ITT Analysis Giuliano NEJM 2011; 364: Palefsky NEJM 2011; 365: HPV6/11/16/18 Vaccine (n = 2,032) Placebo (n = 2,033) Vaccine Efficacy (95% CI) Genital Warts (47, 80) AIN in MSM (n = 275) 38 (n = 276) (26, 67) ITT= <6 partners, at least 1 vaccine, serostatus + or -

40 Additional Findings Neither vaccine acts therapeutically to induce regression of established lesions Protection is HPV-type restricted Both vaccines show partial protection against HPV-31 A 9-valent HPV vaccine is in phase III trials Duration of protection is unknown although current evidence supports durability Strong protection 6 to 8 years after VLP antibody levels have reached a plateau The few vaccine failures not related to low antibody titers Antigen challenge at 5 years stimulates an anamnestic response (characteristic of vaccine with long-lasting protection) Generally safe and well-tolerated (surveillance is ongoing)

41 Population-level Effectiveness

42 Vaccine Coverage Coverage of US adolescent females is <40% Coverage in countries with school-based vaccination programs: Scotland (12-18 yr old females) - 90% England (12-13 yr old females) - 80% Australia (12-18 yr old females) - 80% Preliminary efficacy data from Australian STD Clinic: ~50% genital wart prevalence in young women, ~ 20% in young men, and no in young MSM Fairley STI 2009

43 Read T R H et al. Sex Transm Infect doi: /sextrans by BMJ Publishing Group Ltd. Reused with permission

44 Cervical Cancer Mortality Hao Int J Health Geogr 2006 African Americans Non-Hispanic Whites

45 Women (25+ Yrs of Age) with Abnormal Pap Tests and Scheduled Treatment Tabnak Cancer Causes Control 2009 on-line Scheduled for treatment Race/Ethnicity Adjusted Odds Ratio White 1.00 African American 0.43* Asian 0.44* Hispanic *P *

46 HPV Vaccination Among 10,082 Girls (9-18 Yrs. of Age) Dempsey Vaccine 2009 Race Dose 1 % eligible girls vaccinated Dose 2 % eligible girls vaccinated Dose 3 % eligible girls vaccinated Received all 3 doses White 28% 82% 77% 17.7% African American 34%* 60%* 61%* 12.4%* *P < for all racial comparisons

47 Cervical Cancer in Developing Global inequity Countries By 2020, 90% of cervical cancer cases will be in developing world Largest single cause of years of life lost to cancer in the developing world Devastating effect on the well-being of families Effective Pap screening, diagnosis and treatment programs have failed despite 40 years of repeated attempts

48 Global Incidence and Mortality of Cervical Cancer Incidence Mortality Cervix uteri (all ages) ASR Cases ASR Deaths Africa , ,671 Asia , ,735 Europe , ,812 Oceania , Central America , ,124 North America , ,796 South America , ,402 World , ,505 ASR = age-standardized rate per 100,000. Ferlay J, et al. GLOBOCAN 2002 Cancer Incidence, Mortality and Prevalence Worldwide. IARC CancerBase; Lyon, 2004.

49 HPV Vaccine: Global Perspective and Cost-effectiveness Cost-effectiveness countries with GDP of less than $1,000 per capita Probably need to price at no more than $1 to $2 per dose GAVI added HPV vaccination in 2011 and negotiated a price of $5 per dose for Gardasil Rwanda started a national cervical cancer prevention program in 2011 Achieved 93% coverage in 6 th grade girls (school-based vaccination program)

50 Unanswered Questions What is the duration of HPV vaccine protection? 3 doses VS 2 doses? Does HPV vaccination prevent HPV-related oropharyngeal cancers? How effective is HPV vaccination in HIV+ adolescents and young adults? Who should be vaccinated? Girls and Boys? Older adults? How can disparities in cervical cancer prevention (US and globally) be eliminated?

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