Trends in genital warts by socioeconomic status after the introduction of the national HPV vaccination program in Australia: analysis of national hospital data

In a previous analysis of this data, we found that the rate of genital warts admissions had decreased in school-aged girls (12–17 years), and in both young women and men (18–26 years) since the introduction of the NHVP [12]. In this further analysis, we found these reductions appear to be similar across different socioeconomic groups for teenaged-girls (10–19 years) and young women (20–29 years), and generally also for young men (20–29 years), residing both inside and outside major cities. This is the first study in Australia to examine HPV vaccine impact within subgroups based on socioeconomic or geographic factors, and one of only a small number of studies internationally to have examined vaccine impact within sociodemographic subgroups of females [12, 16]. Our findings that reductions in teenaged-females were very similar across different socioeconomic areas, including inside and outside major cities, is consistent with initial estimates of vaccine uptake from the first target age-group of young females (aged 12–13 years in 2007) which reported that uptake was relatively equal across these different groups [3]. Similar national data are not available for young women who accessed the vaccine through primary care, as the NHVP Register data is known to under-report uptake in this group [17], however data from two states suggest some potential differences. Based on data extracted from the NHVP Register for women residing in Victoria, three-dose uptake was reported as 33.4 % in the most disadvantaged areas and 38.0 % in the least disadvantaged areas [4], and in a NSW-based study of young women with a recent negative cervical screening test, self-reported uptake of one or more vaccine doses was associated with higher socioeconomic status and living outside inner regional areas [5]. We found no significant difference in the estimated reductions between women living in more versus less disadvantaged areas, although the cohorts which we examined differ slightly from those examined in the Victorian (females aged 18–26 years in 2007) and the NSW (females both aged 20–29 in 2008–2009 and 26 years or younger in mid-2007) studies. The last year of data examined here includes those aged 20–29 in July 2010-June 2011, who were potentially aged from 16–26 in mid-2007. The inclusion of slightly younger cohorts (aged 16–17 in 2007; predominantly offered vaccination at school) may potentially weaken differences in uptake between more and less disadvantaged areas if these differences were smaller in the school-based catch-up than in the community (in the youngest age group vaccinated at school, dose 1 uptake differed by only 1.2 % which is smaller than differences in the Victorian and NSW studies) [3–5]. Additionally the SES associated with the area of residence of these younger cohorts of women at the time of their hospital admission may not be the same as it was when they were vaccinated, as young women could have moved since that time. Furthermore as our results are for impact, they may not reflect exactly the same patterns as uptake, due to indirect protection effects [18]. Our finding that reductions in young men were also very similar across different socioeconomic areas, including inside and outside major cities, is also reassuring. An identified difference in the relative reduction in young men by SES within major cities appeared to be driven by differences in anal warts. No difference was observed in admissions involving only non-anal sites, which may more closely reflect indirect protection from female-only vaccination if MSM are over-represented in admissions involving anal warts.

A major strength of this study is that it uses data from a large, comprehensive and routinely-collected national dataset.

A limitation of this study is that is ecological, and vaccination status of admitted individuals is not known. However, an analysis of the same data over a longer period found the substantial reductions in admissions involving genital warts since mid-2007 were confined to young females and males, and the observed reduction did not appear to be a continuation of a pre-existing decline in either group [12]. This study is also ecological in relation to measuring socioeconomic status, since this represents the socioeconomic characteristics of the admitted individual’s area of residence, rather than the personal characteristics of the admitted individual (which were not available). However this is a widely-used approach and SLAs are the smallest area for which socioeconomic, health and population are available. Differences could also have been masked by classifying women into two SES groups rather than smaller groups such as quintiles; however an initial analysis by SES quintile also found very little difference between groups (data not shown). Another limitation was the extent of missing data on socioeconomic status prior to July 2006, and on remoteness area prior to July 2005. In order to address this, our primary analysis was restricted to use data from July 2006 on, and admission rate ratios (which used earlier years) were a secondary analysis. The findings were consistent across both the primary and secondary analyses, however, and an additional sensitivity analysis we undertook suggested that the subset we used had not biased the results (Additional file 1).

As genital warts are predominantly managed in primary care or sexual health clinics [19], these admissions data will only represent a fraction of warts cases. Admissions involving a primary diagnosis of genital warts likely represent more serious cases of warts which have not responded to earlier treatment, or where surgical treatment is not as readily available on an outpatient basis. Admissions where warts were a contributing (but not primary) diagnosis were generally for another purpose (for example treatment of cervical abnormalities in women, as previously described in the Methods). Therefore, the absolute admission rates and variation in these by SES and remoteness area could potentially relate to a combination of access and behavioural issues; for example a greater choice of treatment options outside hospitals in major cities. As the main purpose of this analysis was to examine whether the relative reduction (if any) in admission rates varied by SES, these potentially access-related differences are not likely to affect our findings unless there was a change in service usage unrelated to vaccination during the same time period; however this seems unlikely given that no changes were observed in older females.

Australia has had an organised, government-subsidised cervical screening program in place since 1991, and yet, while the program has been successful in reducing both cervical cancer incidence and mortality, socioeconomic and geographic disparities persist in cervical cancer [20]. Lower socioeconomic status is associated with lower participation in cervical screening and higher cervical cancer incidence and mortality [20]. Residing in outer regional areas of Australia is associated with higher cervical cancer mortality compared to more urban areas of Australia [20] (but not incidence, suggesting treatment variation may be a factor) [21]; while residing in remote or very remote regions is associated with both higher incidence and mortality [13]. In contrast, the uptake of school-based HPV vaccination [3] and, as reported here, its impact on genital warts, appears to have been relatively equal across socioeconomic groups including in different remoteness areas. This is potentially due to high school-participation rates [22]; the relative ease of vaccine administration (three doses) compared to repeated cervical cancer screening over many years; comparatively smaller (if any) out of pocket costs; and fewer issues of access (which for example are potentially a factor in poorer cancer survival in more remote areas) [21]. This suggests that the school-based HPV vaccination program in Australia may play an important role in reducing disparities in cervical cancer, which exist even in the context of an organised screening program and publicly-subsidised healthcare more broadly. The finding of relatively equal vaccine uptake in Australia [3, 4] is consistent with data from other countries suggesting that school-based programs result in more equitable uptake across socioeconomic strata [23–26], implying our findings on impact may also have relevance for other settings. It is therefore very important to continue to monitor both HPV vaccine uptake and impact in subgroups to ensure that the results observed to date continue. It will also be useful to assess the impact of HPV vaccination on cervical abnormalities by socioeconomic status and remoteness area to ascertain whether these findings for genital warts are also observed in cervical cancer precursors; however as records of cervical abnormalities on screening registers only include women who attend for screening and screening attendance varies by SES [13], this approach will have some limitations. Therefore monitoring of genital warts in population subgroups is likely to continue to be useful, and will additionally offer the opportunity to examine vaccine impact in subgroups of males, who have been included in the HPV vaccination program since 2013.