Vaccine 32 (2014) 3936–3941
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How very young men who have sex with men view vaccination against human papillomavirus Huachun Zou a,b,∗ , Andrew E. Grulich c , Alyssa M. Cornall d,e , Sepehr N. Tabrizi d,e,f , Suzanne M. Garland d,e,f , Garrett Prestage c,g , Catriona S. Bradshaw a,b,h , Jane S. Hocking i , Andrea Morrow b , Christopher K. Fairley a,b,h,1 , Marcus Y. Chen a,b,h,1 a
School of Population and Global Health, University of Melbourne, Melbourne, Australia Melbourne Sexual Health Centre, Alfred Health, Melbourne, Australia c Kirby Institute, University of New South Wales, Sydney, Australia d Department of Microbiology and Infectious Diseases, Royal Women’s Hospital, Melbourne, Australia e Murdoch Children Research Institute, Melbourne, Australia f Department of Obstetrics and Gynaecology, University of Melbourne, Melbourne, Australia g Australian Research Centre in Sex, Health and Society, La Trobe University, Melbourne, Australia h Central Clinical School, Monash University, Melbourne, Australia i Centre for Women’s Health, Gender and Society, University of Melbourne, Melbourne, Australia b
a r t i c l e
i n f o
Article history: Received 4 March 2014 Received in revised form 2 May 2014 Accepted 7 May 2014 Available online 20 May 2014 Keywords: Human papillomavirus Men who have sex with men Attitude Vaccine
a b s t r a c t Background: HPV vaccination of men who have sex with men (MSM) prior to the commencement of sexual activity would have the maximum impact on preventing HPV and anal cancer in this population. However, knowledge and attitudes towards HPV vaccination among very young MSM have not been previously studied. Methods: Two hundred MSM aged 16 to 20 were recruited via community and other sources. Participants were asked about their knowledge and attitudes towards HPV and HPV vaccination. Results: Most (80%, 95% conﬁdence interval (CI) 72.2–87.2%) men were not willing to purchase the vaccine because of its cost (AUD$450). However, if the vaccine was offered to MSM free of charge, 86% (95% CI: 80–90%) reported they would be willing to disclose their sexuality to a health care provider in order to obtain the vaccine. Over half (54%, 95%: 47–61%) of men would only be willing to disclose their sexuality to receive the HPV vaccine after their ﬁrst experience of anal intercourse. The age at ﬁrst insertive anal intercourse and the age at ﬁrst receptive anal intercourse were 0.21 (IQR: −2.5 to 3.2) and 0.17 (IQR: −2.9 to 2.7) years earlier than the age that men would be willing to disclose their sexuality to receive the HPV vaccine, respectively. Willingness to receive the vaccine at a younger age was associated with younger age at ﬁrst insertive anal intercourse. Conclusion: Overall, very young MSM expressed high acceptance of HPV vaccination. Early, opportunistic vaccination of very young MSM may be feasible in settings where very young MSM have not been vaccinated through universal programs targeting school aged males. However, given HPV infections occur early on, the effectiveness of this approach will be less than vaccination targeting school aged boys. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction Studies have demonstrated that most adult men who have sex with men (MSM) have been infected with the human
∗ Corresponding author at: Corresponding author at: University of Melbourne, Melbourne Sexual Health Centre, 580 Swanston Street, Carlton 3055, VIC, Australia. Tel.: +61 3 9341 6263; fax: +61 3 9341 6269. E-mail address: [email protected]
(H. Zou). 1 Joint last authors. http://dx.doi.org/10.1016/j.vaccine.2014.05.043 0264-410X/© 2014 Elsevier Ltd. All rights reserved.
papillomavirus (HPV) [1,2]. HPV results in a substantial burden of disease in MSM including anal and genital warts which are associated with signiﬁcant psychosocial burden and compromised quality of life [3,4]. In addition, HPV is associated with anal cancer which is more common among MSM, particularly those who are HIV positive [5,6]. Anogenital HPV detection is associated with anal sex with men and vaginal sex with women . The quadrivalent HPV vaccine has been shown to be effective in preventing infection with HPV types 6, 11, 16 and 18 in males together with genital warts and anal intraepithelial neoplasia, the precursor to anal cancer [8,9]. Data suggest that initial HPV
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infection among MSM occurs early, soon after their ﬁrst sexual experiences. In a study of very young MSM who were on average 2 years since their ﬁrst experience of anal intercourse, 31% had anal HPV infection. Of the infected men, 64% had at least one quadrivalent vaccine preventable anal HPV infection . HPV vaccination of school aged boys prior to the onset of any sexual activity would have the maximum impact on preventing HPV among men. However, to date, few countries have implemented universal school based male HPV vaccination programs despite an increasing number that have introduced universal female HPV vaccination. The Australian government implemented free HPV vaccination of school aged boys aged 12 and 13 in 2013. In the absence of a universal male vaccination program, an alternative strategy would be to opportunistically vaccinate young men who report sex with men. This may also be used as a “catch-up” strategy in countries which do introduce school-aged vaccination, in a manner analogous to young women. In order for such a vaccination approach to be successfully implemented, it is important to understand such men’s views about HPV and HPV vaccination. While some surveys have been undertaken among MSM, none have been obtained from very young MSM, who represent the main group that would need to be targeted . Our study aimed to investigate the knowledge and attitude towards HPV and HPV vaccination among very young MSM recruited from a range of sources. We also aimed to deﬁne the age that very young MSM would choose to obtain the HPV vaccine if they had to disclose their sexuality to a health care provider in order to obtain the vaccine.
2. Methods 2.1. Subjects and recruitment Participants in this study were those participating in the human papillomavirus in Young People Epidemiological Research (HYPER) Study which sought to determine the prevalence of HPV infection among MSM aged 16 to 20. We promoted the study at a range of sources in Melbourne. These include gay community organisations, such as (1) “Minus 18”, a young gay, lesbian, bisexual and transgender (LGBT) group of about 500 members, (2) LGBT student clubs in universities, and (3) “YAK”, a young LGBT social club; gay community media, such as (1) “Joy FM”, Australia’s national LGBT radio station, and (2) “MCV”, an LGBT magazine; gay community events, such as (1) “Mid-Summa”, LGBT Pride carnival, and (2) “Equal Love”, a campaign for same-sex marriage; gay social network on Facebook and Twitter; and sexual health clinics, such as the Melbourne Sexual Health Centre, Prahran Market Clinic and Family Planning Victoria Action Centre. Participants had to physically go to the Melbourne Sexual Health Centre. Questionnaire and biological sample collection for all eligible participants were conducted at the Melbourne Sexual Health Centre. To be eligible, participants had to be aged 16–20 years, having had or potentially will have oral or anal sex with other men and willing to attend 4 study visits across 12 months. Participants self-completed a questionnaire that captured information including social and demographic characteristics, sexual behaviours with both men and women, knowledge of HPV, and attitudes towards HPV vaccination. We used a few strategies to ensure a high retention rate, such as reimbursing a participant by $15, $15, $20 and $50 for their ﬁrst visit on day 1, second visit at month 3, third visit at month 6 and last visit at month 12; and offering free HPV vaccine at the end of the last visit. Details on recruitment methods and the STI testing protocol are described elsewhere . Participants were asked how likely it was that they would inform a doctor or nurse that they had sex with men in order to
obtain the HPV vaccine if it were available free of charge to MSM. Furthermore, they were asked at what age they would have felt comfortable doing this. Before enrolling in the study, participants were informed that HPV vaccination course was available as 3 doses over 6 months, at a cost of around AUD$450, the approximate cost of vaccination that adult Australian men are required to pay if they wanted the vaccine. As part of the study protocol, participants were offered vaccination against HPV at the completion of the HYPER study free of charge. 2.2. Measurement We designed a series of questions on the knowledge of and attitude towards HPV among participants. We asked 6 questions about participants’ knowledge of HPV: (1) Have you ever discussed HPV with your friends? (2) Is HPV the virus that causes genital warts? (3) Can HPV cause cancer of the cervix in women? (4) Does using condoms when having sex give 100% protection against HPV? (5) Can you tell if you have HPV? and (6) The HPV vaccination won’t work if a person is already sexually active? All these questions had three choices: “Yes”, “No” and “Unsure”. We asked 7 questions about participants’ attitudes towards HPV vaccination: (1) Do you think vaccinating young people against HPV would encourage them to become more sexually active? (2) Do you think HPV vaccination should be offered to boys and young men for free? (3) How likely would you have the HPV vaccine if you had to pay AUD$450 for it? (4) Why you are unlikely to have the HPV vaccine? (5) Would you tell a health professional that you had sex with men in order to obtain the vaccine if it was free for MSM? (6) Does your doctor know that you have sex with men? (7) What is your proposed age that you would feel comfortable disclosing sex with men to a doctor in order to obtain HPV vaccination for free? The ﬁrst two questions had three choices: “Yes”, “No” and “Unsure”. Questions 3 and 5 had three choices: “Likely”, “Neither likely nor unlikely” and “Unlikely”. Question 4 had four choices: “The vaccine is too expensive that I cannot afford”, “I am at low risk for HPV thus it’s unnecessary to have the vaccine”; “It’s hard to discuss it with my parents” and “Unsure”. Question 6 had three choices: “Yes”, “No” and “I do not have a doctor”. 2.3. Statistical analysis The sample size (n = 200) used in this study was designed to provide upper and lower 95% conﬁdence intervals (CI) of between 2 and 7% around expected proportion of men with HPV at each time point. Sample characteristics were compiled using descriptive statistics. Median and interquartile ranges (IQRs) were used for age at ﬁrst sex and age proposed by participants for receiving the HPV vaccine. Proportions were used for knowledge of HPV and attitudes towards the vaccine. Scatter plots were used to demonstrate age of ﬁrst insertive anal intercourse (IAI) and receptive anal intercourse (RAI) and age of HPV vaccine uptake. Univariate and multivariate logistic regression models with odds ratios (ORs) and 95% conﬁdence intervals (CIs) were used to explore factors associated with potential earlier uptake of HPV vaccine. Age, age at ﬁrst IAI, age at ﬁrst RAI, number of lifetime IAI partners, and number of lifetime RAI partners were included in the multivariate logistic regression. Statistical analyses were conducted using STATA 12.0 (StataCorp, Texas, USA). 3. Results 3.1. Participant characteristics In brief, 200 participants were recruited from September 2010 to August 2012. The median age of participants was 19. The majority
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of participants had previously had IAI (86.5%) or RAI (85.0%) with other men. The median age at which participants ﬁrst engaged in oral and anal intercourse with men was 16 and 17, respectively. The median age at ﬁrst oral and vaginal sex with women was 16 for both sexual practices. Participants who had experienced anal intercourse with men reported a median of 4 (interquartile range (IQR): 1–8) male anal intercourse partners in the past 12 months. Participants who had experienced vaginal sex with a woman reported a median of 2 (IQR: 1–4) female vaginal sex partners in the past 12 months. Among the 36 participants who had anal intercourse with men and vaginal intercourse with women, most (n = 22, 61%) ﬁrst had vaginal intercourse with women before they ﬁrst had anal intercourse with men. 3.2. Knowledge of and practice related to HPV Overall, the majority of participants could correctly answer HPV related questions that we asked (Table 1). One third of participants had previously discussed HPV with friends. Nearly all participants were aware that HPV can cause cervical cancer and genital warts. Most participants were correct in believing that condoms could not guarantee 100% protection against HPV. 3.3. Attitude towards and views on HPV vaccination Participants’s attitudes towards HPV vaccination are shown in Table 2. Only a minority were willing to purchase the vaccine at the cost of the vaccine in Australia at the time of the study: approximately AUD$450. This was mainly because they considered the vaccine as being too expensive. However, if the vaccine was offered free of charge to MSM, 85.5% of participants reported that they would have been willing to disclose their sexuality to a doctor or nurse in order to obtain the vaccine. Of the 174 men who had a regular doctor, 54.9% had already disclosed their sexuality to their doctors. 3.4. Timing of HPV vaccination indicated by men An artiﬁcial line that simulates the scenario when age at ﬁrst anal intercourse exactly overlaps with age when participants would be willing to disclose their sexuality to get free vaccine was shown in Figs. 1 and 2. Superimposed is a scatter plot where each point represents an individual and their age at ﬁrst IAI (Figs. 1) or RAI (Figs. 2) and the age at which they reported willingness to disclose their sexuality in order to obtain free vaccine. The median age proposed by participants for disclosing their sexuality to a health care provider in order to obtain vaccination free of charge was 17 (IQR: 16–18). Over 90% of participants would have been willing to do so by the age of 20 under these circumstances. However, 54.0% would have disclosed only at an age that followed their ﬁrst experience of anal intercourse with a man. The proportion of participants who had ﬁrst had anal intercourse at least one month before they were willing to disclose their sexuality to obtain the vaccine was 71.5% (95% CI: 64.1–78.1%) for IAI and 69.4% (95% CI: 61.9–76.2%) for RAI. Among the 123 and 118 men who had had IAI and RAI before they were willing to disclose their sexuality to obtain free vaccine, the median number of IAI partners in the past 12 months was 3, and RAI partners in the past 12 months 4. The age at ﬁrst IAI was 0.21 (IQR: −2.5 to 3.2) years earlier than the age that men would be willing to disclose their sexuality to obtain free vaccine. The age at ﬁrst RAI was 0.17 (IQR: −2.9 to 2.7) years earlier than the age that participants would be willing to disclose their sexuality to receive the HPV vaccine. Seventy two percent (123/172) of participants who had ever had RAI would have commenced RAI before they would be willing to disclose their sexuality to obtain free vaccine, with a total
Fig. 1. Scatter plots of age at ﬁrst insertive anal intercourse and age when very young men who have sex with men would be willing to disclose their sexuality to receive the vaccine. Horizontal axis: age (years) when men would be willing to disclose sexuality to obtain vaccine. Vertical axis: age (years) when men ﬁrst had insertive anal intercourse (IAI). Age at ﬁrst IAI: age when men ﬁrst had IAI. Age at disclosure: age when men would be willing to disclose sexuality to obtain vaccine. Each hallow circle, rectangle and triangle represents an individual. The diagonal line is an artiﬁcial line that simulates the scenario when age at ﬁrst IAI equals to age when men would be willing to disclose sexuality to receive the vaccine. No one was less than 10 years old for ﬁrst IAI.
of 133 person years derived from age at ﬁrst IAI to age when they would be willing to disclose their sexuality to obtain free vaccine. Sixty nine percent (118/170) of participants who had RAI would commence IAI before they would be willing to disclose their sexuality to obtain free vaccine, with a total of 119 person years derived from age at ﬁrst RAI to age when they would be willing to disclose their sexuality to obtain the vaccine. Potential factors associated with willingness to receive the HPV vaccine free-of-charge earlier rather than later are shown in Table 3. By multivariate logistic regression, proposed earlier acceptance of vaccination was signiﬁcantly associated with: younger
Fig. 2. Scatter plots of age at ﬁrst receptive anal intercourse and age when very young men who have sex with men would be willing to disclose their sexuality to receive the vaccine. Horizontal axis: age (years) when men would be willing to disclose sexuality to obtain vaccine. Vertical axis: age (years) when men ﬁrst had receptive anal intercourse (RAI). Age at ﬁrst RAI: age when men ﬁrst had RAI. Age at disclosure: age when men would be willing to disclose sexuality to obtain vaccine. Each hallow circle, rectangle and triangle represents an individual. The diagonal line is an artiﬁcial line that simulates the scenario when age at ﬁrst RAI equals to age when men would be willing to disclose sexuality to receive the vaccine. No one was less than 10 years old for ﬁrst RAI.
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Table 1 Knowledge of and practice related to HPV among 200 very young men who have sex with men. Knowledge
Yes % (n)
No % (n)
Unsure % (n)
Did you ever discuss HPV with your friends? HPV is the virus that causes genital warts? HPV can cause cancer of the cervix in women? Using condoms when having sex gives 100% protection against HPV? Can you tell if you have HPV? The HPV vaccination won’t work if a person is already sexually active?
32 (64) 89 (178) 96 (192) 7 (13) 12 (23) 2 (3)
66 (132) 3 (6) 1 (2) 83 (166) 63 (125) 86 (172)
2 (4) 8 (16) 3 (6) 11 (21) 26 (51) 13 (25)
Table 2 Attitudes towards and views on HPV vaccination among 200 very young men who have sex with men. Attitudes
Age men felt comfortable disclosing sex with men to a doctor in order to obtain HPV vaccination for free (median, IQR, yr)? Do you think vaccinating young people against HPV would encourage them to become more sexually active? Yes No Unsure Do you think HPV vaccination should be offered to boys and young men for free? Yes No Unsure How likely would you have the HPV vaccine if you had to pay AUD$450 for it? Likely Neither likely nor unlikely Unlikely Reasons why unlikely to have the HPV vaccine? Too expensive Thinks he is at low risk for HPV Hard to discuss with parents Unsure How likely would you tell a health professional that you had sex with men in order to obtain the vaccine if it was free for MSM? Likely Neither likely nor unlikely Unlikely Does your doctor know that you have sex with men? Yes No Don’t have a doctor
Table 3 Factors associated with potential earlier HPV vaccine uptake among 200 very young men who have sex with men. Variables
Age 16–18 19–20 Age at ﬁrst IAI ≤17 years >17 years Age ﬁrst RAI ≥17 years >17 years No. lifetime IAI partners ≤4 >4 No. lifetime RAI partners ≤4 >4
% men with potential earlier HPV vaccine uptake (n/N)
Adjusted odds ratio (95% CI)
77.8 (56/72) 36.7 (47/128)
3.3 (1.4–8.0) 1
70.0 (70/100) 23.6 (17/72)
3.8 (1.3–11.0) 1
65.4(70/107) 28.6 (18/63)
1.2 (0.4–3.5) 1
44.4 (44/99) 59.5 (44/74)
1 1.2 (0.5–2.8)
53.2 (50/94) 50.0 (38/76)
1 0.9 (0.4–2.2)
Notes: The median age that men thought they should receive the vaccine was 17 years. Men were considered to have potential earlier vaccine uptake if they proposed receiving the vaccine at 17 years of age or younger. CI: conﬁdence interval.
age (OR = 3.3, 95% CI: 1.4 to 8.0) and earlier commencement of IAI (OR = 3.8, 95% CI: 1.3 to 11.0). 4. Discussion To our knowledge this is the ﬁrst study on the views of very young MSM towards HPV vaccination. Most studies examining the
15 158 27
8 79 14
189 5 6
95 3 3
60 22 118
30 11 59
95 14 3 5
81 12 3 4
171 11 18
86 6 9
96 77 26
48 39 13
acceptability of HPV vaccination have focused on females and data on the acceptability of the HPV vaccine among MSM are scarce. The few existing studies were among older MSM where HPV vaccination would be less effective given more men will already have been infected with HPV. In an Australian study, the median age of men was 27, ranging from 19 to 71 ; in a Canadian study, the median age of men was 33, ranging from 19 to 83 ; in a Hong Kong study, half of participants were over 31 years old . In a Puerto Rican study only about 15 MSM aged under 26 were included and some of these men were HIV positive . Among the very young MSM in the study, the cost of the HPV vaccine was the greatest potential impediment against their willingness to be vaccinated. Most, however, accepted the concept of targeted HPV vaccination of MSM if it was available free of charge, even if this required disclosure of their sexuality to a doctor or nurse in order to receive the vaccine. The preventative impact of HPV vaccination is greatest in individuals not already infected with the vaccine HPV types. The early and high per partner transmission of HPV among very young MSM soon after their ﬁrst sexual experiences means that for maximal population protection early vaccination of this population is required . Among men in the HYPER study, who had not received the HPV vaccine, the proportion of participants with anal HPV of any type increased from 10% in participants reporting no prior RAI to 47% in participants reporting 4 or more RAI partners (ptrend < 0.001) . Moreover, the proportion with anal HPV type 16, the type most commonly associated with anal cancer, also increased from 0% in participants reporting no prior RAI to 8% in participants reporting 4 or more RAI partners (p-trend = 0.044) .
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On average men in the HYPER study reported their ﬁrst anal intercourse around the age of 17 . Studies show that the age at ﬁrst anal intercourse has fallen progressively among younger cohorts of MSM . Men in the HYPER study indicated that they would have been willing to disclose their sexuality in order to obtain free HPV vaccination on average at the age of 17, that is, at the same age as when they ﬁrst engaged in anal intercourse and potential exposure to anogenital HPV infection. About half of participants had already been sexually active before the age at which they were willing to access the vaccine if this required disclosure. This raises the question as to how effective selective vaccination of MSM would be in preventing HPV acquisition. Ideally vaccination would precede the onset of any sexual activity but the reality is that at present, there are no countries other than Australia that offer free, universal school based HPV vaccine programs. There are limitations to this study. The ﬁndings in this study may not apply to other populations of young MSM. We provided periodic monetary incentive and HPV vaccine at the end of the study. As a result this sample might be skewed towards men who were less economically independent and/or those who were more likely to accept vaccine and other interventions. The men in this study, predominantly urban and educated very young MSM, were participating in a study of HPV infection which offered free HPV vaccination at the conclusion of the study. This may have biased towards those more positively disposed toward HPV vaccination. Men were also well informed about HPV. It is possible that men with less knowledge of HPV and HPV vaccination may have different attitudes to the vaccine. Over half of men had already disclosed their sexuality to their doctor for other reasons suggesting that many of the men in this study were comfortable discussing their sexuality for health related reasons. The willingness to disclose sexuality to obtain the vaccine may be lower in settings where disclosure of sexuality may be more difﬁcult or stigmatizing. The questionnaire was designed by our research team and validity and reliability were not tested before the research. The age at which participants reported being comfortable receiving the vaccine was a hypothetical one and may be different in the reality. Earlier uptake of the vaccine was associated with younger age and also higher sexual risk: younger age at ﬁrst IAI or RAI and a higher number of lifetime IAI partners. It is possible that participants who were more willing to accept the vaccine earlier on were at least partly driven by a higher self-perceived risk for sexually transmitted infection. Overall acceptance of HPV vaccination in this young population of MSM and willingness to disclose their sexuality in order to obtain it indicates that opportunistic vaccination of young MSM may be feasible. However, the effectiveness of this approach depends on whether vaccination can occur early enough to prevent infection. Given the potential consequences of HPV infection in MSM including anal cancer, further research into how this could be implemented including how parents, schools, and health care providers can best support early vaccination of young MSM is warranted. School-based vaccination program offers a tremendous opportunity for affording protection against the four types included in the quadrivalent HPV vaccine.
Funding The HYPER Study was supported by a research grant from the Investigator Initiated Studies Program of Merck Sharp & Dohme Corp. The opinions expressed in this paper are those of the authors and do not necessarily represent those of Merck Sharp & Dohme Corp. CKF has received honoraria from CSL Biotherapies and Merck and research funding from CSL Biotherapies. CKF owns shares in CSL Biotherapies the manufacturer for Gardasil. JSH has received
an honorarium from CSL Biotherapies and is an investigator on an Australian Research Council funded project (LP0883831) that includes CSL Biotherapies as a research partner. AEG has received honoraria and untied research funding from CSL Biotherapies, and has received honoraria from Merck and Sanoﬁ-Pasteur MSD. SMG has received advisory board fees and grant support from CSL and GlaxoSmithKline, and lecture fees from Merck, GSK and Sanoﬁ Pasteur; in addition, she has received funding through her institution to conduct HPV vaccine studies for MSD and GSK. SMG is a member of the Merck Global Advisory Board as well as the Merck Scientiﬁc Advisory Committee for HPV. None of this relates to this speciﬁc work. MC has received a research grant from Merck.
Conﬂict of interest statement All other authors have no potential conﬂicts of interest.
Acknowledgements We would like to extend our thanks to the following organisations and individuals for their support for the HYPER study: Minus18; ALSO Foundation; YAK; the Action Centre, Family Planning Victoria, queer clubs in the University of Melbourne, RMIT, Monash University, Deakin University, Latrobe University, Victoria University; Joy FM; MCV; Rainbow Network Victoria; Gay and Lesbian Health Victoria; CAN Resource Centre; Prahran Market Clinic; Tim Read; Lenka Vodstrcil; David Lee; Matiu Bush; Mark Chung; Helen Henzell; Helen Kent; Julie Silvers; Rabia Thomson; staff at the Melbourne Sexual Health Centre; Ed Yap; David Towl; Greg Adkins; Amanda Grattan and Merck Australia; TaNisha Evans; Sneha Kishnani; Houda Abdo and Tania Tabone.
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