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HIV Treatment as Prevention in a Developed Country Setting: The Current Situation and Future Scenarios for Australia

Murray, John M. PhD*,†

JAIDS Journal of Acquired Immune Deficiency Syndromes: December 1st, 2013 - Volume 64 - Issue 4 - p 409–416
doi: 10.1097/QAI.0b013e3182a6b20c
Epidemiology and Prevention

Objective: We investigated the current success of early HIV detection in Australia and the likely effectiveness of Treatment as Prevention.

Methods: HIV diagnoses data from the Australian National HIV/AIDS Registry were analyzed for CD4+ T-cell counts at diagnosis and for prior HIV testing. Mathematical modeling based on these data estimated future HIV prevalence and incidence under different scenarios of antiretroviral therapy (ART) usage.

Results: CD4+ T-cell counts significantly decreased with age (P < 0.0001) for men who have sex with men (MSM) and women in all HIV diagnoses, and for diagnoses at primary HIV infection (P < 0.02). This decrease with age meant that >50% of MSM aged 29 years and older are diagnosed with a CD4+ T-cell count <500 cells per cubic millimeters. Diagnosis during primary HIV infection has stabilized at 15% for MSM, with a lower percentage for older individuals (P = 0.002), but only 5% of women were diagnosed at this early stage. MSM older than 50 years were significantly less likely to have had an HIV test before diagnosis (P < 0.0001), whereas women of all ages at HIV diagnosis were less likely to have been tested than MSM. Mathematical modeling indicated that current levels of ART would see a continuing increase in HIV diagnoses among MSM. A 90% ART enrollment would result in an almost immediate decline in prevalence and would be cost effective in terms of person-years on ART by 2028.

Conclusion: Treatment as Prevention would be an effective intervention in Australia and other developed countries.

*School of Mathematics and Statistics, and

The Kirby Institute, University of New South Wales, Sydney, Australia.

Correspondence to: John M. Murray, School of Mathematics and Statistics, University of New South Wales, Sydney, New South Wales 2052, Australia (e-mail:

The Kirby Institute is funded by the Australian Government Department of Health and Ageing and is affiliated with the Faculty of Medicine, The University of New South Wales. The views expressed in this publication do not necessarily represent the position of the Australian Government.

The author has no conflicts of interest to disclose.

Received March 15, 2013

Accepted July 18, 2013

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Treatment as Prevention (TasP) and Test and Treat (TandT) programs have been discussed widely of late given the increasing evidence that alterations in antiretroviral therapy (ART) coverage in a number of regions and countries has significantly impacted on HIV incidence.1–8 These observational analyses have also been supported by the results of the HIV Prevention Trials Network (HPTN) 052 study and earlier investigations of HIV incidence in serodiscordant couples where HIV incidence was correlated with viral load.9,10 Treatment as Prevention has therefore been proposed as a means of further reducing HIV incidence beyond that achieved by current prevention programs, both for developing countries with high HIV prevalence and also for developed countries. In the developing country setting, TandT would reduce HIV incidence,9 and in the long run, also lower prevalence to an extent that the program may even be cost effective and, possibly, capable of eradicating the epidemic.5 Increased ART coverage has also been discussed as an intervention to curtail rising trends in HIV diagnoses in a number of developed countries,11 which have occurred despite universally available ART. These rises in HIV infections in developed countries have been attributed to a number of causes but, relevant to TasP, it is believed that increased ART coverage will lower HIV incidence and possibly even result in lower HIV prevalence. Hence, implicitly it is understood that insufficient ART uptake has contributed to these rising numbers of HIV infections. What the increase in ART coverage would need to be to reduce the epidemic to “minimal” levels is unclear, with mathematical models applied to South Africa producing divergent results as to the possible effectiveness of these programs.3

Recent analysis of HIV incidence among 16,667 individuals followed from 2004 to 2011 in South Africa estimated that even a moderate 30%–40% community ART coverage reduced risk of HIV infection by 38% compared with individuals in a community with low ART coverage of <10%.12 TasP can significantly lower HIV incidence in communities with high HIV prevalence. It is less clear what the impact would be in developed countries with comparatively low HIV prevalence. Here, we consider the possible impact of TasP in Australia. Australia was chosen for a number of reasons for estimation of TasP in a developed country setting: approximately 90% of HIV diagnoses in Australia occur through a single mode of transmission among MSM so that estimating impact of TasP in this 1 group will have a large impact on the entire HIV epidemic in Australia. Australia is widely recognized as being able to identify primary HIV infection (PHI) cases and has contributed extensively to international studies involving PHI. The ability to identify HIV infection early is paramount to any program that intends to treat its way out of endemic HIV because it reduces levels of undiagnosed infection and, in particular, is likely to lower transmissions within PHI that have been estimated to contribute between 9% and 15% of new HIV infections.13–15 Finally, Australia has from the very beginning of the epidemic collected extensive data describing new HIV infections and deaths from AIDS. These data allow a characterization of the HIV epidemic in great detail.

Here, we describe how successful Australia has been in diagnosing early HIV infection, levels of prior testing in individuals who are eventually diagnosed, numbers and ages of individuals living with HIV infection, ART uptake and its impact on HIV diagnoses, and importantly, how each of these factors differs by age group. We determine these levels in MSM, by far the largest group among HIV diagnoses, and in women for a comparison of effectiveness of HIV diagnosis across genders and modes of transmission. Finally, we estimate how the size of the epidemic will change with current ART levels and the levels required to lower HIV prevalence.

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Data on age (in 5-year age groups), CD4+ T-cell count at HIV diagnoses, whether the individual was diagnosed at PHI (defined as an evolving Western Blot, a seroconversion illness, or a negative HIV test within the previous 12 months), and time from a previous negative HIV test were extracted where available for all 30,486 HIV diagnoses from the National HIV/AIDS Registry that listed diagnoses throughout Australia from 1980 to 2010. Consistent with previous classifications,16 numbers of MSM were determined from the exposure categories “Male homosexual contact,” “Male homosexual contact and injecting drug use,” and male “Other/Undetermined.” Numbers of women were extracted from the Registry for all exposure categories, with the 2 largest categories being “Heterosexual contact,” and “From a high prevalence country.”17 Data were sorted by year of diagnosis, gender, and mode of transmission.

The discrete-time dynamic method used to estimate numbers and ages of individuals living with HIV infection has previously been described.16,17 Briefly, for each year from 1980 until the end of 2010, numbers and ages of new HIV diagnoses by gender and mode of transmission were accumulated numerically over time, assuming aging of adults so that they progressed over 5-year age groups from 15 to 75 years of age and older. Numbers of deaths after AIDS were also obtained from the National HIV/AIDS Registry. The number of individuals living with HIV in year i + 1, age group a, and exposure group g (here MSM and female), H (i + 1, a, g), was then estimated from those who were already diagnosed progressing with age in the 5-year age groups; new diagnoses for that year, age group, and exposure group obtained from the HIV Registry data I (i, a, g); minus individuals in each group dying following AIDS determined from the AIDS Registry data A (i, a, g); and also subject to natural annual mortality rates in the general community in each age group and gender μ(a, g)18:

For predictions of numbers of MSM living with HIV in the future, we followed a similar procedure. For each year after 2010, the number living in an age group in a subsequent year was given by aging current individuals by 1 year, adding the estimated number of new infections contributed by individuals not on ART in that year (values based on means and standard deviations of ratios described below) and subtracting estimates of deaths after an AIDS diagnosis, and deaths from other causes. The proportion of deaths because of AIDS per year was given by the proportion in 2010 within that age group, gender, and mode of transmission. We used Latin Hypercube sampling based on these mean ratios and their standard deviations of new infections per individual not on ART to generate 100 sample ratios (for each scenario of ART usage) predicting HIV incidence and prevalence for the next 15 years.

Statistical comparisons between 2 groups were performed with the Wilcoxon rank sum test, whereas those over multiple groups were performed with the Kruskal–Wallis test. All calculations were performed with MATLAB R2012b (The MathWorks, Inc., Natick, MA).

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From the 30,486 HIV diagnoses recorded in the Australian National HIV/AIDS Registry from 1980 to 2010, we investigated how quickly HIV diagnoses have been made and, in particular, the current level of success in early identification of HIV infection. Age is an important factor, especially relevant to TasP in Australia because CD4+ T-cell counts at HIV diagnosis for MSM significantly decrease with age (P < 0.0001; Table 1). For MSM diagnosed with HIV infection during the last decade, median CD4+ T-cell count at HIV diagnosis decreased from 520 cells per cubic millimeters in 15- to 19-year olds to 130 cells per cubic millimeters for those older than 75 years of age (Fig. 1A). Based on fitting these median values for each age group with a linear model, the percentage of MSM who would present with a CD4+ T-cell count <500 cells per cubic millimeters increases linearly with age.





Hence, >50% of MSM 29 years or older at HIV diagnosis would be recommended to commence ART based on a 500 CD4+ T cells per cubic millimeters guideline. On these figures, programs that aim to commence ART at least at this 500 CD4+ T cell per cubic millimeters level will struggle to enroll even 50% of MSM at diagnosis with CD4 counts more than this value, especially in the older age groups.

CD4+ T-cell counts at HIV diagnosis for women also significantly decrease with age (P < 0.0001; Fig. 1B). Women newly diagnosed were more likely to present with a lower CD4+ T-cell count, and median CD4+ T-cell counts at HIV diagnosis for 11 of the 13 age groups were lower for women than for MSM (P = 0.01, signed rank test).

Although the likelihood of early diagnosis has increased over the course of the epidemic for MSM, it has stabilized at only 15% of MSM diagnosed at PHI (Fig. 1C), with older MSM significantly less likely to be diagnosed in this stage (P = 0.002). This improvement in early diagnoses is also reflected by the average age of MSM diagnosed during PHI roughly overlapping the average age of diagnoses in chronic stages of HIV infection (CHI), whereas there was a 4-year age difference between PHI and CHI diagnoses in 1995 (Fig. 2A). In contrast, the percentage of women diagnosed in PHI has remained at 5% over the last 20 years and has not changed with time (P = 0.9).



CD4+ T-cell counts at PHI differed significantly with age (P = 0.003 MSM and P = 0.02 women) being lower for MSM, 55 years and older, and for women, 60 years and older than their younger counterparts (Table 1). Significant differences between CD4 counts at PHI compared with all diagnoses occurred for age groups from 25 to 59 years for MSM and for ages 20–39 years plus 60–64 years for women (Table 1).

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HIV Testing

MSM aged 50 years and older at diagnosis were significantly less likely to have been tested at all, even over the last decade: a median of 32% of MSM aged 50 and older had previously been tested for HIV, compared with 44% and 45% of the 2 youngest groups (P < 0.0001; Fig. 1D). Having previously been tested did increase the likelihood of presenting with a higher CD4 count at diagnosis in 2010 for MSM diagnosed in CHI (mean 519 CD4+ T cells per cubic millimeters compared to 362 CD4+ T cells per cubic millimeters for those not previously tested). Women were much less likely to have been previously tested. Over the last decade, the youngest female group exhibited the highest testing percentages of 16% (compared with 44% in this same age group for MSM), but this was not significantly different to levels in the other age groups (P = 0.1).

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Spare Capacity for ART

Uptake of ART among MSM decreased in Australia between 1997 and 2007,19 with younger diagnosed men being significantly more likely to delay commencement of therapy. Although 80% of MSM who were 50 years and older with diagnosed HIV infection in 2007 surveyed in the Gay Community Periodic Surveys were enrolled for ART, this figure was only 25% for MSM younger than 30 years (Fig. 2B). This delay in the commencement of ART for younger MSM is consistent with their diagnoses at higher CD4+ T-cell counts (Table 1) (Fig. 1) and postponement of ART until CD4-guided commencement times are reached. Approximately 50% of the 30- to 39-year age groups were diagnosed with <500 CD4+ T cells per cubic millimeters (Fig. 1), and approximately this same percentage of 30- to 39-year olds were receiving ART (Fig. 2B).

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The Size and Age-Profile of the HIV Epidemic in Australia

Using the diagnoses and death notifications within the National HIV/AIDS Registry, we used a mathematical procedure involving aging of diagnoses over time with AIDS and non-AIDS estimated deaths to determine numbers of MSM and women living with HIV infection over time (see Methods16). According to these calculations, numbers of MSM living with HIV infection plateaued briefly in 1994, when deaths mostly from AIDS closely matched numbers of new diagnoses (Fig. 3), but from that time, numbers have increased because of lower AIDS mortality with the introduction of combination ART in the mid 1990s plus ongoing HIV incidence. The number of women living with HIV infection from all exposure categories is also increasing in size and age (Fig. 3).



Average ages of new HIV diagnoses peaked in 2006, and since then, newly diagnosed MSM have become younger on average (Fig. 2A). This is consistent with the increasing numbers of younger MSM not enrolled on ART and the role they play in new infections.19

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How Much Increased ART is Required?

For Australian MSM, the best correlate in terms of duplicating numbers and average ages of new HIV diagnoses was the group of MSM with diagnosed HIV infection but who were not taking ART.19 The mean number per year (and standard deviation) of new HIV diagnoses per HIV+ MSM not on ART for the years 1998–2007 for each age group (15–29, 30–39, 40–49, 50+ years) was given by: 0.198 (0.021), 0.176 (0.015), 0.155 (0.019), and 0.162 (0.028). A ratio of 0.198 for the 15- to 29-year age group implies that 1 new HIV diagnosis will arise annually for every 5 individuals in this age group with diagnosed untreated HIV infection.

Taking these ratios of estimates of new infections per diagnosed but untreated MSM, incorporating numbers for each age group, and projecting into the future while incorporating ageing between groups and expected AIDS and non-AIDS deaths (see Methods), allows us to estimate the impact of different levels of ART. This approximation omits explicit contributions from treated individuals with unsuppressed virus and from undiagnosed individuals, but implicitly incorporates their contributions through these ratios. Based on 2007 levels of ART usage for each age group (Fig. 2B), numbers of MSM living with HIV infection is expected to increase by 34% during the next 10 years (Figs. 4A, D), whereas annual new diagnoses will increase by 36%. The majority of this increase is because of a growth in new HIV diagnoses in the younger than 30 years bracket, so that under these ART levels, the average age of MSM living with HIV peaks at approximately 47 years in 2022 and begins to decrease after this time implying a significant expansion of the epidemic.



Scenarios assuming the higher ART usage observed in 1997 produce lower incidence and prevalence, whereas with a uniform 80% of MSM enrolled on ART from 2013, a level that has consistently been achieved by older diagnosed MSM (Fig. 2B), numbers of MSM living with HIV would peak in 2023 before decreasing. Each of these first 3 scenarios sees a sizable expansion of older MSM living with diagnosed HIV infection by 2025, as continuing infection ages through to this group (Figs. 4D–F). Simulations with 90% ART usage in each age group is estimated by our projections to reduce numbers of individuals living with HIV almost immediately (Fig. 4G). This loss of numbers with high levels of ART is because of natural mortality of those living with HIV infection, here taken to be community death rates rather than any high loss from AIDS deaths, plus 70% fewer new HIV infections as a result of expanded treatment.

Although higher ART enrollment increases person-years and cost of ART early in these scenarios, by 2020, all scenarios are estimated to result in virtually equivalent levels of annual person-years of ART (Fig. 4C). By the year 2028 and beyond, the 90% ART scenario requires the lowest cumulative ART person-years and becomes extremely cost effective on this basis alone.

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By definition, undiagnosed levels are hard to accurately quantify. Approximately 25% of individuals living with HIV infection are thought to be unaware of their status in the United States.20 Testing rates among MSM in Australia are among the highest in the world,21 so it would be expected that the undiagnosed percentage of MSM and other groups would be lower than elsewhere. The testing rates, markers of PHI, and CD4+ T-cell counts at HIV diagnosis determined from the National HIV/AIDS Registry data suggest that there is also a reasonable proportion of MSM in Australia who are undiagnosed. Although men and women in older age groups at HIV diagnosis have lower CD4+ T-cell counts consistent with findings from other countries,22,23 this is not entirely representative of poorer surveillance of these individuals because their PHI CD4+ T-cell counts also decrease with age. CD4+ T-cell counts for all MSM diagnoses differed by approximately 100 cells per cubic millimeters or more compared with PHI counts for 30- to 59-year olds indicating that surveillance over all ages can improve.

Women newly diagnosed were more likely to present with a lower CD4+ T-cell count. Because CD4+ T cell counts tend to be higher in women than men of the same age without HIV infection,24 women in Australia may have been undiagnosed for longer, although a contributing aspect may be the cohort that have emigrated from high prevalence countries.17,25

Among gay socially engaged men, it is the younger age group those are most likely to have never been tested for HIV (22% for the 30 years and younger age group) with much lower percentages for other age groups.21 This was in contrast to our findings, where the 50 years and older age group was less likely to have been tested. The approximate 60% of diagnoses with no reported prior HIV test also differs significantly from these community-based surveys. Although the exact proportions of prior HIV testing may be underreported in these databases, it is unlikely to be greatly in error considering that individuals with no reported prior HIV test also presented with lower CD4 counts (362 vs. 519 CD4+ T cells per cubic millimeters), and older MSM were less likely to be diagnosed in PHI. Our results highlight lower testing in older MSM that can be improved, especially since the population living with HIV infection is ageing. Certainly, testing among women in Australia can be improved as rates of prior testing were considerably lower than among MSM.

The delay in ART commencement for younger individuals is possibly a consequence of CD4-guided recommendations and where younger individuals are more likely to present with higher CD4+ T-cell counts. TasP will need to offer incentives for these younger individuals, in particular, to commence ART. ART is now recommended for all adults in the United States regardless of CD4 count and with increasing strength of that recommendation with lower CD4 counts.26 Our calculations add support to these recommendations that increased ART will not only be beneficial to the individual on ART, who will be subject to less immune destruction and risk of opportunistic infections, but also to the community at large.

The richer the available data, the fewer free parameters required in a mathematical model to describe those data. This is the case here where the detailed information on 30,486 HIV diagnoses and 6819 deaths after an AIDS diagnosis allowed estimation of how numbers and ages of those living with HIV infection have changed in Australia between 1980 and 2010. Settings where the data are less descriptive require models with more uncertain parameters and with additional assumptions on the underlying dynamics that naturally lead to a greater uncertainty in their predictions.3 Our model provides the simplest and most extensive description of the HIV epidemic in Australia to date. This same model with inclusion of how new diagnoses relate to ART levels,19 also enables an estimate of HIV diagnoses into the future, while maintaining the age, and gender groupings contained within the original data. A related model was used to estimate burdens of neurocognitive impairment and dementia in the future,17 a concern in many developed countries with a sizable older age cohort living with HIV infection. A limitation of our procedure is that we have not explicitly included HIV transmission from individuals on ART nor from an undiagnosed group. However, the ratios correlating all the annual new diagnoses to numbers of individuals not on ART implicitly incorporates contributions from both these sectors because it incorporates data of all diagnoses. A further limitation is that our calculations have used estimates of new HIV diagnoses as a surrogate for new infections. Given there is some delay between infections proceeding to diagnosis, any effect on prevalence of increased ART coverage will also be delayed in comparison to our calculations.

Our analysis indicates that treating at 80% levels, a value that has been consistently achieved by older MSM in Australia, can result in a peaking of HIV prevalence in 10 years' time, without any requirement for expanded testing. Treating at 90% over all age groups will result in an almost immediate decrease in HIV prevalence, and would be cost neutral in terms of ART by 2028, while providing substantial benefits in terms of infections avoided. It should be noted that these treatment levels refer to those diagnosed at current testing levels, and any expansion in testing programs with concurrent enrollment on ART will only improve these outcomes. Expansion of ART usage among injection drug users may be more difficult given they are less likely to access health care and exhibit poorer HIV treatment outcomes,27 so that additional support would be required in countries where injection drug users comprise a substantial component of those living with HIV infection.

In summary, younger individuals are more likely to be diagnosed with higher CD4+ T-cell counts and choose to delay ART, thus providing a sector for increased ART enrollment for TasP. On the other hand, older individuals were significantly less likely to have been tested and be diagnosed early in infection, providing a more resistant sector for these programs but who would correspondingly benefit from TandT. Expanding ART enrollment for all age groups, in particular for younger individuals, is required if rising HIV incidence is to be curtailed. A level of 90% ART usage will significantly lower incidence and prevalence and becomes cost effective on a simple pill count basis within 15 years. Treatment as Prevention to ART levels that can substantially impact both HIV incidence and prevalence is feasible and beneficial in a developed world setting.

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      Treatment as Prevention; Test and Treat; Australia; mathematical model; CD4; age

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