GRAPHICAL ABSTRACT

INTRODUCTION

Human immunodeficiency virus (HIV) remains a severe infectious disease and a significant global public health concern. Without adequate medical care, the resulting immune system compromise can lead to acquired immunodeficiency syndrome (AIDS) and increased mortality risk. Each day, 4000 new HIV infections occur, and an estimated 650 000 individuals (500 000-860 000) die from HIV-related causes annually, equating to an average of about 1 person every minute [1]. The World Health Organization (WHO) recommends antiretroviral therapy (ART) for all individuals testing positive for HIV [2]. The provision of ART to people living with human immunodeficiency virus (PLHIV) has increased survival, improved quality of life, and decreased HIV transmission [1]. The Initiation of ART in Early Asymptomatic HIV Infection (INSIGHT START) study prompted a revision of international treatment guidelines, which occurred between 2012 and 2015 [3]. These guidelines now indicate that ART should be initiated for all PLHIV, regardless of disease stage or CD4 cell level, thus shortening the interval between diagnosis and ART initiation [4]. Moreover, more effective and easily tolerated ART, particularly second-generation integrase inhibitors, has become increasingly accessible and is now commonly used [5]. This has led to steady declines in AIDS incidence and mortality [6].

Before the implementation of combination ART in 1996, PLHIV faced significantly elevated mortality rates, primarily due to AIDS [7]. Subsequently, PLHIV in affluent nations began receiving ART. The effective inhibition of viral replication through ART has substantially reduced the likelihood of developing AIDS as well as mortality, significantly improving life expectancy. As deaths attributed to AIDS have declined, PLHIV are now living longer and facing a higher risk of mortality from other age-related factors, such as cardiovascular disease and cancer. Multi-country studies conducted by international organizations have demonstrated that initiating ART can effectively reduce disparities in addressing the HIV/AIDS epidemic across countries [8].

The WHO also recommends rapid ART initiation for all PLHIV. Rapid initiation refers to the prompt commencement of ART within 7 days, or as soon as feasible, for individuals recently diagnosed with HIV [9]. The implementation of rapid ART varies based on the specific conditions of the PLHIV and the resources available. Several programs in both low-income and middle-income countries (LMICs) and high-income countries have adopted rapid ART initiation [10]. Substantial evidence supports the benefits of rapid initiation methods, particularly in LMICs with high rates of HIV infection, delayed diagnosis, and limited healthcare availability. Several recent studies have shown that initiating ART sooner (including on the day of diagnosis) can lead to improved patient and program outcomes, such as fewer PLHIV lost to treatment before starting ART and decreased HIV-associated mortality rates [11-13]. The main objective of this study was to investigate the factors associated with mortality, including the time to ART initiation after diagnosis with HIV.

METHODS

Study Design and Data Source

This retrospective cohort analysis was conducted at Fatmawati General Hospital in Jakarta. Data were collected from electronic health records for PLHIV, namely the HIV/AIDS and Sexually Transmitted Infection Information System (Sistem Informasi HIV/AIDS dan IMS [SIHA]), from January 2018 to December 2022. The inclusion criteria for this study were adult PLHIV aged 18 years or older. In this study, 2 subsets of SIHA data were used: pre-ART and follow-up. The pre-ART data included 739 observations, while the follow-up data included 817 observations. After merging the data, 361 observations were identified as matching between the 2 datasets. PLHIV with incomplete data on variables relevant to this study were excluded. After cleaning the data, we included 326 participants in the analysis. The sample selection method is shown in Figure 1.

Measurements

The outcome for each participant was dichotomized into censored or death. Death was defined as the confirmed occurrence of mortality in PLHIV. Censoring included PLHIV (1) confirmed to be alive and still receiving ART, (2) lost to follow-up, or (3) transferred out. “Last-encounter censoring” was employed regarding PLHIV lost to follow-up or alive at the end of the study period. The definitions of “lost to follow-up” and “transferred out” were based on PLHIV status at the end of the study. We defined survival time as the duration, measured in months, that a PLHIV survived after initiating ART.

The primary independent variable was classified into 3 groups: within 7 days, 8-60 days, and more than 60 days. This categorization was based on the current WHO guidelines, which recommend starting ART in 7 or fewer days following HIV diagnosis, and on a study that defined early ART initiation as that occurring within 2 months [2,14]. Various socio-demographic and clinical factors were also included, namely age at ART enrollment, sex, education, employment status, marital status, HIV risk group, WHO clinical stage, treatment regimen at enrollment, site of HIV testing, CD4 cell count before initiating ART, tuberculosis post-exposure prophylaxis (TB-PEP), and opportunistic infection. HIV risk groups were categorized as heterosexual, homosexual, and others (including bisexual, transfusion, and injection drug users). Regarding the site of HIV testing, testing occurred at 2 locations: Fatmawati General Hospital and outer Fatmawati General Hospital. The WHO clinical stage was assigned as stage 1 through stage 4, according to WHO recommendations [15]. The treatment regimen at enrollment included 2 groups based on the nucleoside reverse transcriptase inhibitor regimen: zidovudine-based and tenofovir-based. CD4 cell counts before initiating ART were categorized into ≤200 cells/mm³ and >200 cells/mm³. The opportunistic infections included in this study were candidiasis, herpes simplex, herpes zoster, cytomegalovirus, toxoplasmosis, Pneumocystis jirovecii pneumonia, and diarrhea. PLHIV with 1 or more of these infections were defined as having an opportunistic infection.

Statistical Analysis

Descriptive statistics were presented as numbers and frequencies. The incidence of death was calculated relative to the person-time of the at-risk population, reported as the number of deaths per 1000 person-months of follow-up. In survival analysis, person-time is an estimate of the cumulative time at risk for all study participants, computed by multiplying the total population at risk by the average duration of risk exposure [16]. The enrollment date was defined as the date of ART initiation, and either death or censoring was recorded. Kaplan-Meier survival curves were employed to compare survival probabilities among categories of the primary independent variable, and the log-rank test was applied to compare the curves. Initially, a bivariate analysis was conducted to examine the candidate variables associated with mortality among PLHIV. Bivariate Cox regression was performed, and independent variables with p-values less than 0.25 were incorporated into the multivariable analysis. The associations from the bivariate analysis between the independent and outcome variables were presented as crude hazard ratios. Multiple Cox regression was then conducted at the 0.05 significance level to determine the net impact of each explanatory variable on the duration of survival among PLHIV. A p-value below 0.05 in the multivariable analysis was considered to indicate statistical significance. The results of these models were expressed as adjusted hazard ratios (aHRs) with 95% confidence intervals (CIs), and p-values were used to assess the strength of the associations and to determine statistical significance. Data analysis was performed using Stata/SE version 15.1 (StataCorp., College Station, TX, USA).

Ethics Statement

This study received ethical approval from the Institutional Review Board of Fatmawati General Hospital (approval No. PP.08.02/D.XXI.18/55/2023).

RESULTS

Table 1 shows the characteristics of the participants. Most participants were 18-39 years old (70.9%), male (81.0%), and employed (74.2%). Approximately half of the participants had higher education (47.6%). More than half of the respondents (56.4%) had never been married, and around half (50.6%) were classified as WHO clinical stage 3 at the initiation of ART. Most respondents (90.8%) received tenofovir-based ART.

As shown in Figure 2, the proportion of ART initiation within 7 days after diagnosis was 20.0% in 2018, decreased to 8.6% in 2019 and 6.0% in 2020, and then increased again, reaching 37.9% and 34.0% in 2021 and 2022, respectively. Conversely, the proportion of ART initiation between 8 days and 60 days increased from 64.3% in 2018 to 68.7% in 2020. The fraction initiating ART beyond 60 days increased in 2019 (25.9%) but progressively decreased in 2020, 2021, and 2022, with proportions of 25.4%, 13.8%, and 10.0%, respectively. From 2018 to 2022, the overall proportion of ART initiation within 7 days after diagnosis was 19.9%, compared to 19.0% for initiation after more than 60 days.

In this study, we followed 326 PLHIV receiving ART for a 5-year period. The estimated overall survival time for PLHIV was 52.61 months (95% CI, 50.87 to 54.34). Furthermore, the estimated survival times for PLHIV who initiated ART within 7 days, between 8 days and 60 days, and more than 60 days after diagnosis were 52.78 months (95% CI, 47.84 to 57.73), 53.40 months (95% CI, 51.26 to 55.55), and 49.62 months (95% CI, 46.24 to 53.00), respectively. The overall mortality rate in the cohort during the 11 148 person-months of observation was 5.11 per 1000 person-months of follow-up. Cumulatively, 57 PLHIV died, accounting for 17.4% of the total PLHIV population over 5 years. Of the total participants, 270 (82.6%) were censored, including 170 (57.6%) who were still being followed on ART, 19 (6.4%) who were lost to follow-up, and 49 (16.6%) who transferred to other health facilities. Figure 3 illustrates the Kaplan–Meier survival function for the entire study population over the 5 years following ART initiation. The probability of survival among respondents who initiated ART within 7 days of diagnosis was 81.0% (95% CI, 63.0 to 90.8). However, the survival probability decreased to 60.6% (95% CI, 38.5 to 76.9) for those who initiated ART between 8 days and 60 days and to 17.9% (95% CI, 3.4 to 41.7) for those who initiated ART more than 60 days after diagnosis. Throughout the follow-up period, a significant difference in survival probability was observed among the ART initiation groups (p=0.031, log-rank test).

We conducted a bivariate analysis to examine potential factors associated with mortality among PLHIV, as shown in Table 2. Variables with p-values less than 0.25 in the bivariate analysis—namely age, education, employment status, marital status, site of HIV testing, CD4 count before initiating ART, WHO clinical stage, and time to ART initiation—were included in the multivariable analysis. In addition, sex was included because of its importance as a socio-demographic factor. In the multivariable analysis, the time to ART after diagnosis was significantly associated with mortality among PLHIV. PLHIV who began ART within 7 days were less likely to die during the study period than those who started ART more than 60 days after diagnosis (aHR, 0.36; 95% CI, 0.14 to 0.93). Similarly, PLHIV who began ART in 8 days to 60 days faced lower mortality risk compared to those who started more than 60 days after diagnosis (aHR, 0.42; 95% CI, 0.22 to 0.81). PLHIV with CD4 counts greater than 200 cells/mm³ were less likely to die than those with counts of 200 cells/mm³ or less (aHR, 0.06; 95% CI, 0.01 to 0.43). In addition, PLHIV with lower clinical stages had a lower mortality risk than those with stage 4 disease, with aHRs of 0.35, 0.34, and 0.30 for stages 1, 2, and 3, respectively. PLHIV who received TB-PEP were less likely to die during the study compared to those who did not receive TB-PEP (aHR, 0.48; 95% CI, 0.27 to 0.85). Regarding demographic factors, older age was significantly associated with increased mortality among PLHIV (aHR, 1.91; 95% CI, 1.08 to 3.39).

DISCUSSION

This study examined rapid ART initiation among PLHIV and its association with mortality over a 5-year evaluation period. The proportion of rapid ART initiation among adults at Fatmawati General Hospital from 2018 to 2022 was 19.9%. A previous study in California between January 1, 2015, and December 31, 2020, reported a rapid ART initiation rate of 34.1%. In 2017, the WHO recommended that those diagnosed with HIV begin treatment within 7 days and, if possible, start ART on the day of diagnosis [9]. Most countries have officially adopted the WHO’s 2015 recommendation for universal HIV therapy. However, the implementation of ART varies based on each country’s policies [17]. The lower rate observed in our study compared to previous research may be attributed to factors such as insufficient time to adapt to an HIV diagnosis or inadequate efforts to eliminate structural obstacles. Facilitating prompt access to medical care following an HIV diagnosis may reduce the need for subsequent appointments, as PLHIV can achieve viral suppression more rapidly. Additionally, the expedited administration of ART may not allow sufficient time to address issues, such as HIV stigma and medical mistrust, that can impact medical engagement [18,19]. A similar finding was noted in a qualitative study conducted in San Francisco that examined the effectiveness of rapid ART; the study revealed that while PLHIV widely accepted the rapid ART approach, some expressed hesitation due to complex psychosocial and structural obstacles [20].

Our results revealed decreases in the proportion of rapid ART initiation in 2019 and 2020, which may be attributed in part to the coronavirus disease 2019 (COVID-19) pandemic. The pandemic has presented numerous obstacles to HIV care globally, potentially contributing to an increase in AIDS-related fatalities and a higher HIV transmission rate [21]. PLHIV must initiate ART as soon as possible after diagnosis to manage their condition and minimize the risk of transmitting the virus to others. Interruptions in care can hinder the capacity of PLHIV to adhere to medication regimens [22]. The pandemic may have exacerbated barriers to accessing HIV care and ART treatment in underserved communities with restricted access to healthcare facilities. Various pandemic-related factors potentially impeded access to HIV care, including quarantine and social distancing measures that restrict mobility and impact individuals’ ability to travel for ART refills. Economic disruptions due to imposed restrictions may also have affected the financial well-being of PLHIV [21-23]. However, a previous study in West Africa indicated that HIV clinics in two-thirds of the countries studied effectively ensured continued access to ART for PLHIV despite the challenges posed by the pandemic. Notably, the proportion of rapid ART initiation increased in 2021, likely due to health system adaptations during the COVID-19 pandemic, such as online appointments and individual ART delivery [24-26].

In this study, the timing of ART initiation was associated with mortality among PLHIV. Those who received rapid ART after diagnosis were less likely to die during the study period compared to those who started ART more than 60 days after diagnosis. PLHIV who began ART in 8-60 days also faced lower mortality risk compared to those who initiated ART more than 60 days post-diagnosis. Our findings align with those of several previous studies. Recent policy recommendations [13,27-29] have reinforced the urgency of early ART initiation. Reasons for delaying initiation include concerns about medication resistance, adverse effects, resource allocation, and PLHIV adherence. Research has shown that the potential clinical and public health benefits of promptly initiating ART outweigh the associated risks [29-32]. Our findings underscore the importance of initiating ART for PLHIV without delay, regardless of CD4 count.

The present study identified additional factors associated with reduced mortality risk, including a CD4 count greater than 200 cells/mm³ before initiating ART, a lower WHO clinical stage, and receipt of TB-PEP, consistent with previous studies. PLHIV with higher CD4 counts and lower clinical stage tend to exhibit fewer symptoms and stronger immune responses, contributing to reduced mortality [33-35]. Furthermore, findings regarding TB-PEP highlight the importance of preventing active tuberculosis, and this approach has the potential to decrease tuberculosis-related deaths in individuals with HIV [36].

Our study revealed that demographic factors, including education and employment status, were not significantly associated with mortality among PLHIV. A previous study in Brazil yielded a similar finding, which may be due to comparable access to healthcare across demographic groups [37]. In addition, the ART regimen was not significantly associated with mortality. Several previous studies have indicated no statistically significant difference in mortality or risk of disease progression between zidovudine-based and tenofovir-based regimens, suggesting similar efficacy for the initial treatment of HIV [38,39].

A key strength of our study is that all participants who started ART were sourced from a tertiary hospital, making the findings applicable to similar healthcare settings. However, this research also has several limitations. As this is an observational study, caution should be exercised when interpreting the findings. Participants’ decisions to initiate therapy may have been influenced by individual characteristics, such as medical comorbidities and social factors. Additionally, due to our reliance on medical records, we could not obtain certain potentially meaningful data, such as viral load outcomes, specific information regarding complications, and the underlying causes of mortality.

In conclusion, we found that the timing of ART initiation after diagnosis was associated with mortality. Specifically, earlier initiation of ART significantly reduced the risk of death. Our research also demonstrated that having a CD4 count greater than 200 cells/mm³ before starting ART, having a lower clinical stage, and receiving tuberculosis preventive therapy all contributed to lower mortality risk. The results indicate that rapid ART generally leads to better outcomes. However, it is crucial to ensure that PLHIV are well-informed when considering ART. Before offering rapid ART, PLHIV should undergo a thorough history, clinical examination, and diagnostic testing, if necessary, to identify any significant opportunistic infections. If clinical symptoms suggest tuberculosis or cryptococcal meningitis, ART initiation must be deferred to prevent potentially life-threatening paradoxical worsening of the existing disease. Further research is needed to identify additional predictors of mortality among PLHIV within a prospective cohort study design.

Notes

Conflict of Interest

The authors have no conflicts of interest associated with the material presented in this paper.

Funding

This study received funding from the Indonesia Endowment Fund for Education (LPDP).

Acknowledgements

The authors thank Fatmawati General Hospital for granting permission to utilize the data.

Author Contributions

Conceptualization: Mauleti IY, Saptarini I. Data curation: Mauleti IY, Wibisana KA, Syamsuridzal DP, Mulyati S. Formal analysis: Saptarini I. Funding acquisition: Lisdawati V, Saptarini I. Methodology: Mauleti IY, Saptarini I, Hendarwan H. Project administration: Saptarini I, Lisdawati V. Visualization: Mauleti IY, Hendarwan H, Saptarini I. Writing – original draft: Saptarini I. Writing – review & editing: Mauleti IY, Wibisana KA, Syamsuridzal DP, Mulyati S, Lisdawati V, Hendarwan H, Saptarini I.

Figure. 1.

Flow chart of study sample determination. PLHIV, people living with human immunodeficiency virus; ART, antiretroviral therapy.

Figure. 2.

Percentage of antiretroviral therapy (ART) initiations after diagnosis over the years.

Figure. 3.

Kaplan–Meier survival curves for patients with antiretroviral therapy (ART) initiation within 7 days, 8-60 days, and >60 days over the five-year follow-up period.

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Figure & Data

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