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Published in final edited form as: AIDS Care. 2019 Apr 2;31(11):1376–1383. doi: 10.1080/09540121.2019.1601671

Identifying, linking, and treating people who inject drugs and were recently infected with HIV in the context of a network-based intervention

Mina Psichogiou a, George Giallouros b, Katerina Pantavou b, Eirini Pavlitina c, Martha Papadopoulou a, Leslie D Williams d, Andria Hadjikou b,e, Eleni Kakalou f, Athanasios Skoutelis f, Konstantinos Protopapas g, Anastasia Antoniadou g, George Boulmetis h, Dimitrios Paraskevis i, Angelos Hatzakis i, Samuel R Friedman d, Georgios K Nikolopoulos b
PMCID: PMC6818705  NIHMSID: NIHMS1056360  PMID: 30939897

Abstract

Identifying and linking people to care soon after HIV infection could limit viral transmission and protect their health. This work aims at describing the continuum of care among recently HIV-infected people who inject drugs (PWID) and participated in an intervention in the context of an HIV outbreak in Athens, Greece. The Transmission Reduction Intervention Project (TRIP) conducted risk network-based contact tracing and screened people for recent HIV infection. A comprehensive approach with a case management component that aimed to remove barriers to accessing care was adopted. Follow-up data on antiretroviral treatment (ART) and HIV-RNA levels were obtained from HIV clinics. TRIP enrolled 45 recently HIV-infected PWID (80% male) with a median viral load at recruitment of 5.43 log10 copies/mL. Of the recently infected persons in TRIP, 87% were linked to care; of these, 77% started ART; and of those on ART, 89% achieved viral load <200 copies/mL. TRIP and its public health allies managed to get most of the recently HIV-infected PWID who were identified by the program into care and many of them onto ART. This resulted in very low HIV-RNA levels. Treatment as prevention can work if individuals are aided in overcoming difficulties in entry to, or attrition from care.

Keywords: Continuum of care, treatment cascade, recent HIV infection, social network, HIV, outbreak

Introduction

Individuals who recently acquired HIV are very infectious (Brenner et al., 2007; Hollingsworth, Anderson, & Fraser, 2008; Marzel et al., 2016) because their viral load level is high, their immune response is suboptimal, and they are likely to still be engaged in risky behaviors (Cohen, Shaw, McMichael, & Haynes, 2011; Koopman et al., 1997). Reducing HIV infection in people who inject drugs (PWID) might be difficult without targeting recently HIV-infected PWID (Vasylyeva et al., 2016).

Laboratory tools (e.g., Limiting Antigen avidity (LAg) assay), have been developed to detect recent HIV infection (Duong et al., 2015; Nikolopoulos et al., 2017). Interventions based on social networks were effective in finding recently HIV-infected people (Green et al., 2017; Nikolopoulos et al., 2016). Treating HIV-infected persons with antiretroviral treatment (ART) significantly reduces HIV transmission (Cohen et al., 2011; Hull & Montaner, 2013; Jackson et al., 2003). However, linking recently HIV-infected persons to care and keeping them on ART are major challenges.

The aim of this work is to describe and depict the continuum of care of PWID diagnosed with recent HIV infection in Athens, Greece in the context of a risk network-based project with a comprehensive case management component.

Materials and methods

Project description

The Transmission Reduction Intervention Project (TRIP) used risk network-based contact tracing to target people who had recently been infected by HIV (i.e., in the past six months). This project has been described elsewhere (Friedman et al., 2014; Nikolopoulos et al., 2016). The logic underlying TRIP is that by recruiting and testing network contacts of people with recent HIV infection, more people who are recently infected and probably highly infectious are likely to be found. At its Athens, Greece site, the project was conducted between June 2013 and July 2015, in the context of a big HIV outbreak among PWID (Nikolopoulos et al., 2015; Paraskevis et al., 2013, 2015).

Eligible TRIP participants were those aged 18 years or older; able to answer the project questionnaire; and qualified for one of the project arms. TRIP participants were either seeds or network members. The term “seed” refers to a primary participant (index person) recruited by TRIP whose risk network members were subsequently traced. Network contacts were recruited for two steps from each seed, unless a new recent infection was found in the networks, in which case network tracing continued for two more steps.

The field staff consisted of 4 persons (a social worker, a person with a degree in psychology, an experienced interviewer, and a physician). The personnel received training in theory behind the project. The TRIP office was located in a building of the Greek Organization against Drugs in downtown Athens, near primary drug scenes and drug treatment facilities. This was helpful to the staff for identifying and recruiting people. Participants and staff could easily commute from the TRIP office to infectious disease clinics and opioid substitution treatment centers by using regular, fast, and inexpensive transportation means. The project office included separate rooms for participants’ reception, interviews, and blood sample collection thus allowing for privacy and confidentiality. A member of the staff managed the daily flow of participants. The intervention (interview, nomination of risk contacts, counseling, and referral) was implemented on a one-on-one basis.

People with recent HIV infection identified in TRIP were interviewed using a structured questionnaire, both at baseline and at follow-up (six months after enrollment). In order to achieve regular contact with the recently HIV-infected participants, the project staff established strong relationships with personnel at medical clinics, drug treatment centers, and with the participants, their friends, and relatives.

The recently HIV-infected participants were provided with standard counseling and were supported by the project staff to link themselves to care and/or to stay in care. Comprehensive strategies to facilitate linkage and retention to care included: (1) information support on where and how to contact facilities/services; (2) instrumental support by staff members who arranged appointments for the participants and/or accompanied them to clinics or other facilities; (3) provision of cues to action such as telephoning the participants or sending them text messages to remind them of appointments/medical exams; and (4) organized efforts to facilitate administrative procedures and assist the participants in obtaining legal documents, getting health insurance and benefits, finding a job, and getting legal advice.

TRIP has most of the elements of partner services as suggested by the United States (US) Centers for Disease Control and Prevention (CDC) (2008). These include linkage between surveillance/other programs and TRIP so as to identify and enroll HIV-undiagnosed index persons (for instance, many newly diagnosed PWID were referred to TRIP from the allied project Aristotle (Hatzakis et al., 2015)); priority to persons with acute/recent infection; conduct of interviews by trained staff in person in a private and comfortable environment to elicit enough information about partners of index cases (network contacts); use of the clustering method (for instance, eliciting information about and intervening at drug-using venues); offering partners (network contacts who were located and recruited) HIV testing; involvement as fast as possible after diagnosis to reduce risk for additional transmission; active collaboration with medical providers and prevention facilities; and monitoring and evaluation of the program (Morgan et al., 2018; Nikolopoulos et al., 2016; Smyrnov et al., 2018). In terms of discrepancies from the CDC recommendations, TRIP was not implemented by a public health department (though it could serve as an operational model for public health agencies); it only involved a kind of provider referral (network contacts in TRIP were informed about their potential exposure by the project staff only); it did not involve a protocol for screening for potential violence (though many items of the TRIP questionnaire asked about physical or other type of violence); it did not focus on other sexually transmitted infections; and it moved deeper in transmission networks, which, however, resembles to some degree the notions of social contacts, associates, cluster interviews, and social network approaches mentioned in the US CDC recommendations.

For all people recently infected with HIV in TRIP, further information on linkage to care, antiretroviral treatment, HIV-RNA levels (not regularly available), and mortality was retrieved by the attending physicians at the HIV clinics through the end of October 2016. Detailed data on Hepatitis C infection (HCV) was not collected but all participants diagnosed with HIV/HCV coinfection by medical providers were managed in accordance with the national guidelines.

A participant recently infected with HIV was considered as linked to care if he/she had visited an HIV clinic at least once following the HIV diagnosis. Virologic suppression was operationalized using cutoffs of 200 and 50 copies/mL.

Laboratory methods

Blood samples were tested for HIV antibodies by AxSYM HIV-1/2 gO (Abbott) and confirmed by Western Blot (MP Diagnostics). Recent HIV infection was detected by the LAg assay (Sedia™ Biosciences Corporation) (Duong et al., 2015). HIV-RNA was quantified in HIV positive samples in TRIP using Artus HI Virus-1 RG RT–PCR (Qiagen). HIV-RNA at HIV clinics was measured using Cobas Taqman HIV, PCR RNA, branched DNA 3.0, and Versant HIV-1 RNA 1.0 kPCR.

Statistical methods

Descriptive statistics included mean/median values and standard deviation/1st-3rd quartiles for quantitative variables, and frequencies/percentages for categorical variables. For all statistics about the time when an event occurred, calculations were made from baseline, which was the date people were recruited and HIV-RNA was measured for the first time in TRIP. The time of infection was obviously earlier than the baseline date (on average 3–4 months earlier given the properties of LAg).

Statistical comparisons were conducted using chi-squared tests, t-tests, one-way analysis of variance, and non-parametric tests (Wilcoxon rank-sum test, signed-rank test, and Kruskal–Wallis rank test).

A p-value less than .05 indicates statistical significance. All statistical analyses were performed in Stata 14 (Stata Corp., US).

Ethical statement

TRIP (ClinicalTrials.gov identifier: ) was approved by the Institutional Review Boards of the National Development and Research Institutes in New York City (NYC), US and of the Hellenic Scientific Society for the study of AIDS and Sexually Transmitted Diseases in Athens, Greece. All participants were informed about the project, were given the opportunity to ask questions about human subject protection, risks and benefits, and consented to the intervention.

Results

Forty-five recently HIV-infected persons (23 seeds and 22 network members of seeds), were enrolled. Figure 1 shows the continuum of care of these people by October 2016. They reported that they were injecting drugs, had a median age at recruitment of 35 years (1st–3rd quartiles: 30–43), and the majority were males (80%) (Table 1). Their median viral load at TRIP baseline was 5.43 log10 copies/mL (1st–3rd quartiles: 4.58–5.98), without statistically significant difference (p = .84) between seeds and network members.

Figure 1.

Figure 1.

Open in a new tab

Continuum of care of recently HIV-infected people who inject drugs and were enrolled in the Transmission Reduction Intervention Project (TRIP) in Athens, Greece (June 2013–July 2015; information updated October 2016). Percentages are out of the previous stage. Virologically suppressed are those on antiretroviral treatment (ART) with last HIV-RNA measurement less than 200 copies/mL.

Table 1.

Characteristics and outcomes of recently HIV-infected people who inject drugs and were enrolled in the Transmission Reduction Intervention Project (TRIP) in Athens, Greece (June 2013–July 2015; information updated October 2016).

Seeds
(n = 23)		 Network
members
(n = 22)		 Total
(n = 45)		 p-
value
Males 18 18 36 .77
(78.3%) (81.8%) (80%)
Age (median) (1st-3rd quartile) 38 34.5 35 .73
(30-43) (32-38) (30-43)
Infected by hepatitis C virus 20 14 34 .07
(87%) (63.6%) (75.6%)
Imprisonment 8 9 17 .67
(34.8%) (40.9%) (37.8%)
On drug treatment 14 8 22 .10
(60.9%) (36.4%) (48.9%)
Linked to HIV care 22 17 39 .07
(95.7%) (77.3%) (86.7%)
Antiretroviral treatment uptake 18 12 30 .09
(78.3%) (54.6%) (66.7%) .41a
(81.8%)a (70.6%)a (76.9%)a
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a

Of those linked to HIV care.

Six participants died (13.3%) between June 2013 and October 2016. Given the exact dates of death for three of these people, death occurred on average 21 months after the baseline TRIP interview. The exact cause of death was not available for all but one participant who died from drug overdose following his/her release from prison.

Thirty-nine participants (86.7%) paid at least one visit to an HIV clinic. The proportion of those linked to care was higher among the seeds (95.7%) than among the network members (77.3%) (p = .07). The median time between the date of first measurement of HIV-RNA at TRIP (baseline) and the date of first clinical visit was 56 days (1st–3rd quartiles: 36–132).

Nine PWID with recent HIV infection who were linked to care were not administered ART. Four of them came to the HIV clinic only once and did not start ART as there was no policy for same-day ART initiation. The other five, who visited the HIV clinic multiple times, had >500 CD4 T-cells/mm3 at diagnosis and did not receive ART according to the national guidelines (ART was recommended for those with CD4 T-cell count <350 cells/mm3) at the time TRIP was conducted (Lundgren et al., 2015; WHO, 2015). In addition, five of these nine participants were known to be in detention or imprisoned for some time after their baseline interview.

Thirty participants (66.7% of the 45 people with recent HIV infection or 76.9% of those linked to care) started ART. The proportion of those who began ART was 81.8% among the seeds and 70.6% among the network members (p = .41). The median time from the day HIV-RNA was measured at baseline for TRIP to the day ART was administered, was 9.8 months (1st–3rd quartiles: 3.7–17.7).

For 18 individuals on ART, viral load results were available after ART initiation. The latest median HIV-RNA measurement, on average taken 14.4 months (1st–3rd quartiles: 5.8–20.6) after ART initiation and 19.5 months (1st–3rd quartiles: 11.2–24.7) after baseline, was 1.70 log10 copies/mL (10th—90th percentiles: 1.60—2.69) and significantly reduced from baseline (p < .001). The proportions of the 18 participants with HIV-RNA levels below 200 and 50 copies/mL were 88.9% (n = 16), and 83.3% (n = 15), respectively. Four participants who were never linked to care but came to TRIP offices for the scheduled follow-up visit (on average 10 months after baseline), had a non-significant (p = .47) decrease in HIV-RNA levels from baseline (5.38 log10 copies/mL; 1st–3rd quartiles: 3.98–5.72) to follow-up (4.61 log10 copies/mL; 1st–3rd quartiles: 3.87–5.27) and viral load levels higher than 200 copies/mL.

Discussion and conclusion

TRIP identified 45 people with recent HIV infection over its course. Despite difficulties in the context of an HIV outbreak in Athens, Greece, during very hard economic and social conditions (Bonovas & Nikolopoulos, 2012; Nikolopoulos et al., 2015), the project and its allies among the medical, social, and public health services had managed, as of October 2016, to get 87% of the recently HIV-infected participants into care and around two thirds on ART, which resulted in significantly lower viral load levels and likely in fewer HIV transmissions.

TRIP staff were successful at helping almost 90% of the recently HIV-infected participants enter care within approximately two months after baseline. This is important as PWID are more likely than non-drug users to experience delays in health care entry, which in turn are associated with heightened morbidity and mortality (Meyer, Althoff, & Altice, 2013; Thompson et al., 2012). To achieve the goal of early connection to care, the TRIP staff and their allies implemented an active referral process with many components including establishing close contact with both the participants and their relatives or friends, which included regular phone calls or text messages, and assistance in arranging appointments to the clinics and in dealing with problems related to health insurance coverage, social benefits, legal issues, and access to medical facilities. Intensive case management like that adopted in TRIP is recommended, as it has been shown to work better than passive referral (Gardner et al., 2005; Meyer et al., 2013; Thompson et al., 2012). The goals were achieved despite the implementation of TRIP in the middle of a severe financial crisis that was accompanied by significant cuts in public health spending (Bonovas & Nikolopoulos, 2012; Nikolopoulos et al., 2015). These cuts reduced the capacity of clinics to offer timely and adequate services adapted to PWID and their needs; important HIV services including HIV-RNA testing were not regularly available; and the provision of HIV treatment to all HIV infected individuals was adopted with delay. The increased death rate among the recently HIV-infected PWID in TRIP (13.3%) may reflect the impact of structural factors, such as extreme poverty and heightened rates of homelessness (Sypsa et al., 2017).

Providing ART to PWID is crucial for their survival (Wood et al., 2008). Around 67% of people with recent HIV infection in TRIP (or 77% of those who were linked to care) began ART, a proportion that is better than that reported for PWID in other settings (Escudero et al., 2017; Heimer et al., 2017) but lower than the overall national estimate for 2013 of 82% (Gourlay et al., 2017). The national figure in Greece, however, was determined by the predominance of men who have sex with men in the Greek epidemic, who have been shown to have better outcomes than drug injectors in obtaining HIV-related care (Helleberg, Häggblom, Sönnerborg, & Obel, 2013; Lourenço et al., 2014; Risher, Mayer, & Beyrer, 2015; Van Beckhoven et al., 2014). ART initiation, despite being earlier than that reported in other studies (Mehta, Kirk, Astemborski, Galai, & Celentano, 2010), was not timely, as, on average, the recently infected PWID in TRIP started ART around 10 months after their first HIV-RNA measurement in the project. Structural factors including socioeconomic status, health insurance coverage, unstable accommodation, health-care delivery systems, individual behaviors and beliefs, patient-provider relationship, clinicians’ attitudes to ongoing injecting and likely adherence, and their experience in treating PWID are associated with ART use (Knowlton et al., 2010; Mehta et al., 2010; Meyer et al., 2013; Westergaard, Ambrose, Mehta, & Kirk, 2012). Delays in ART initiation among the recently HIV-infected people in TRIP could also be attributed to the prevailing treatment guidelines at the time of the study, which recommended ART initiation for those with CD4 T-cell count <350 cells/mm3. Recommendations and clinical practice have changed since then.

ART uptake influences infectiousness among PWID (Wood, Milloy, & Montaner, 2012). In a study on drug injectors in NYC, half of the transmissions were attributed to undiagnosed HIV positives and one-third to HIV-diagnosed who had not begun ART (Escudero et al., 2017). Research suggests that HIV-infected people with virologic suppression are significantly unlikely to transmit HIV to others (Escudero et al., 2017; Rodger et al., 2016; Skarbinski et al., 2015); and if PWID are adherent to ART, their virologic response does not differ from that of non-injectors (Wood et al., 2003). PWID in TRIP who started ART attained virologic suppression, with more than 80% having less than 50 copies/mL at their last HIV-RNA measurement.

Various barriers exist in the continuum of care of HIV-infected PWID (Meyer et al., 2013). Even PWID who are initially linked to care and have suppressed their viral load are likely to show, in the long-term, lapses and attrition in care (Westergaard, Hess, Astemborski, Mehta, & Kirk, 2013). Active drug use, concomitant psychosocial problems including polydrug use and abuse in adulthood, homelessness, and legal issues with frequent arrests and incarceration episodes affect engagement to care (Joseph et al., 2015; Kerr et al., 2014; Meyer et al., 2013; Milloy et al., 2012; Mizuno et al., 2015; Palepu et al., 2004; Thompson et al., 2012; Westergaard et al., 2013). Around 40% of the recently HIV-infected people in TRIP spent some time in detention or in prison after their baseline visit to TRIP offices. Policy reform following discussions involving all stakeholders including the department of health, public health agencies, medical and public health communities, the police, and organizations of people living with HIV and of PWID are necessary to avoid law enforcement interference with essential medical management (Degenhardt et al., 2014; Wolfe, Carrieri, & Shepard, 2010). An integrated approach to care from HIV diagnosis to ART initiation and retention should adapt service delivery models of care to PWID, address social problems, offer social support, and provide treatment for drug addiction and mental disorders (Bachireddy et al., 2014; Meyer et al., 2013; Reddon et al., 2014; Thompson et al., 2012).

Limitations of this analysis include the small sample size, and the unavailability of some post-ART initiation HIV-RNA measurements. Despite these, this is the only study we are aware of that has reported on the continuum of care for PWID with recent HIV infection. TRIP used laboratory and risk network-based tools to find recently HIV-infected people who were probably highly infectious. Yet, diagnosis is not enough to reduce further HIV transmission. It is imperative to achieve viral suppression by treating HIV with ART. The multidisciplinary TRIP staff and their collaborators in clinics and social services adopted an intensive case management strategy, which resulted in a high proportion of people recently infected with HIV entering care, and in a substantial number of them receiving effective ART. Our findings highlight the urgent need to develop and deliver targeted interventions addressing structural, interpersonal, and individual-level factors that cause delays and affect engagement in or disengagement from care.

Acknowledgments

Funding

This intervention was financially supported by the United States (US) National Institute on Drug Abuse (NIDA) (DP1 DA034989). The Greek Organization against Drugs provided facilities for interviews and blood collection.

Footnotes

Disclosure statement

The authors declare no conflict of interest.

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