Reaching Hard-to-Reach People Who Use Drugs: A Community-Based Strategy for the Elimination of Hepatitis C

Nicolas Nagot; Morgana D’Ottavi; Catherine Quillet; Anne Debellefontaine; Joëlle Castellani; Nicolas Langendorfer; Bertrand Hanslik; Sylvain Guichard; René Baglioni; Vincent Faucherre; Edouard Tuaillon; Georges-Philippe Pageaux; Didier Laureillard; Hélène Donnadieu-Rigole

doi:10.1093/ofid/ofac181

. 2022 Apr 14;9(6):ofac181. doi: 10.1093/ofid/ofac181

Reaching Hard-to-Reach People Who Use Drugs: A Community-Based Strategy for the Elimination of Hepatitis C

Nicolas Nagot ^1,^✉, Morgana D’Ottavi ², Catherine Quillet ³, Anne Debellefontaine ^4,⁵, Joëlle Castellani ⁶, Nicolas Langendorfer ⁷, Bertrand Hanslik ⁸, Sylvain Guichard ⁹, René Baglioni ¹⁰, Vincent Faucherre ¹¹, Edouard Tuaillon ¹², Georges-Philippe Pageaux ¹³, Didier Laureillard ^14,¹⁵, Hélène Donnadieu-Rigole ^16,¹⁷

PMCID: PMC9239554 PMID: 35774932

Abstract

Background

Elimination of hepatitis C virus (HCV) among people who use drugs (PWUD) remains a challenge even in countries in which HCV care is provided free of cost. We assessed whether an innovative community-based, respondent-driven sampling (RDS) survey, coupled with HCV screening and immediate treatment, could be efficient to detect and cure current PWUD with chronic HCV in a large city of Southern France.

Methods

At a community site with peers, PWUD (cannabis not included) were enrolled after confirmation by a urine drug test. Participants were then screened for hepatitis B virus, HCV, and human immunodeficiency virus and benefited from onsite HCV treatment evaluation and prescription. Peer support was provided during treatment, and a systematic visit was scheduled 12 weeks after the end of treatment. The cost of the intervention was estimated.

Results

Five hundred fifty-four participants were enrolled. Most were male (78.8%) with a median age of 39 years (interquartile range, 33–46). Cocaine (73.1%) and heroine (46.8%) were the main drugs consumed. Overall, 32.6% of PWUD (N = 181) were HCV seropositive, 49 (27.1%) of which had detectable HCV ribonucleic acid and were thus eligible for treatment. Ten of these patients had severe fibrosis. Hepatitis C virus treatment was initiated for 37 (75.5%) patients, 30 (81.1%) of whom completed their treatment and 27 (73.0%) achieved sustained viral response at week 12. The total cost was 161 euros € per screened patient and 1816€ per patient needing treatment.

Conclusions

A community-based RDS survey approach, involving peers, proved efficient and cost-effective to reach and cure PWUD for HCV. This innovative strategy could be key for the final step of HCV elimination.

Clinical trial registration. ClinicalTrials.gov, NCT04008927.

Keywords: Costs and cost analysis, drug users, hepatitis C, intervention, mass screening

Community-based, respondent-driven sampling with peer involvement is very efficient for HCV screening among PWUD. Same-day DAA eligibility check and prescription on site increases treatment initiation. This cost-effective strategy may allow us to achieve HCV elimination among PWUD.

In Europe, people who use drugs (PWUD) remain an important at-risk group for hepatitis C virus (HCV) infection [1]. Estimates from a modeling exercise with a 2018–2030 timeframe shows that people who inject drugs (PWID) could represent over 80% of HCV transmission in the Western European population [2]. Hepatitis C virus seroprevalence in PWUD ranges from 14% in the Czech Republic to 84% in Portugal, with various countries reporting rates exceeding 50% in 2015 [3–6]. To meet the goal of HCV elimination by 2030 [7], ie, reducing new infections and deaths by 90% and 65%, respectively, and treating 80% of those eligible, the World Health Organization and several expert associations highlight the urgent need to focus on HCV treatment in PWUD to prevent further HCV transmission from untreated individuals [2, 7, 8].

The strategy for HCV elimination in Europe relies almost exclusively on the healthcare system for testing and treating individuals. Hepatitis C virus screening and treatment (direct-acting antivirals [DAAs]) are free of charge in hospitals and addiction centers in most European countries for those covered by health insurance. The DAAs have proven to be very efficacious among PWUD and recorded a full recovery in 95% of cases [9]. However, many barriers (eg, structural, societal, etc) inhibit access to prevention, testing, and care among PWUD [10–13]. Therefore, many PWUD are left unscreened and untreated [14, 15], resulting in an uncontrolled HCV epidemic among PWUD [16]. Furthermore, in many countries—such as France—the absence of population-based data among PWUD makes it difficult to estimate progress towards HCV elimination in this particularly high-risk group [17].

A key challenge in HCV elimination can be attributed to PWUD being notably “hidden” and “hardly-reached” by the healthcare system. Innovative models for screening [18] and care, using new peer-led strategies, are therefore necessary [10, 19, 20]. To address this issue, recruitment of PWUD by other PWUD in their network has emerged as a promising strategy [21]. For instance, respondent-driven sampling (RDS) surveys, relying on both peer and financial incentives, have proven to be efficacious [22] for epidemiological purposes, or to control a large human immunodeficiency virus (HIV) outbreak as in Athens after the 2008 economic recession [23]. If the underlying assumptions of RDS surveys are met, the constituted sample can be considered representative of the study population [24].

Trust in healthcare workers is essential for marginalized populations. To build confidence and reach those who do not regularly (or ever) engage in healthcare services for HCV screening and care, the involvement of peers in the process as well as the designation of a neutral site (ie outside regular health services) may reduce stigma and reluctance to attend the habitual health/addiction care services. In addition, peers, when appropriately trained, can be very effective in delivering counseling and harm reduction activities [19].

The aim of our study was to assess whether a community-based RDS screening associated with immediate HCV treatment could be efficient in detecting and curing PWUD living with chronic HCV in a French city.

METHODS

Study Design

We implemented a demonstration project in the South of France to estimate the efficiency of our strategy, which aimed to identify and cure PWUD with chronic heaptitis C. We also estimated the PWUD population size using a capture-recapture method, and we calculated the cost of our intervention per person screened and per person treated (ClinicalTrials.gov Identifier NCT04008927).

Study Population

All current drug users aged 18 or above, living in the Montpellier metropolitan area (31 communes, ±500 000 inhabitants), were eligible to participate. Current drug use was defined as self-report of misused medication (eg methadone, buprenorphine, opiate drugs, methylphenidate, ketamine) or any illicit substance other than cannabis within the past 3 days and at least 10 times per month, confirmed by a positive urine drug test. We excluded the following persons: those who did not consent, those who were not recruited by the RDS survey method; those who did not have the capacity to understand the research; or those who were under guardianship.

Outcomes

Our primary outcome was the proportion of treated and cured PWUD (achieving a sustained viral response 12 weeks after the end of their treatment) among those identified with detectable HCV ribonucleic acid (RNA). Our secondary outcomes included the following: estimating the number and proportion of participants infected with HCV; the HCV cascade of care produced by this type of screening and treatment technique; and the cost per PWUD screened, HCV-infected, and cured.

Study Site

The main activities (screening etc) took place in a disused building, rented and rehabilitated for the duration of the study, and composed of 3 rooms and a courtyard with an enclosed canopy tent. The building was located at the back of the local university hospital campus with direct access from the exterior.

Study Procedures

Population Size Estimate

A capture-recapture method was used to estimate the PWUD population in the Montpellier metropolitan area. Two weeks before the beginning of enrollment in the study, 76 nail clippers with the ICONE study logo were distributed in the target population (any person fitting the study's inclusion criteria) by local nongovernmental organizations (NGOs), and they were instructed to hold on to the object. For the recapture phase, RDS survey participants once enrolled were asked whether they had been given a particular object by a member of the community and whether they could produce the said object. In the case of a positive response, in which the participant was unable to present the nail clipper, he/she was asked to describe it or recognize it from a selection of photos.

Peers

Five peers (former or current PWUD) from the community were recruited by community NGOs and trained on Good Clinical Practice, study procedures, risk reduction, and counseling for treatment compliance. Their role was to (1) welcome the participants, (2) inform them about the study, HCV transmission, and treatment, (3) administer a face-to-face questionnaire, and (4) provide individual support throughout the duration of HCV treatment uptake.

Seeds and Network Recruitment

The study was conducted according to standard RDS survey procedures [24]. Fifteen PWUD seeds, with distinct characteristics of interest (eg, gender, dwelling, age, sex work, and sexual behaviors), were identified in the community. They each needed to report a personal network size of at least 5 other PWUD. Seeds were formally enrolled and participated in all study procedures. They then each received 3 coupons to distribute within their network for the recruitment of new participants. Participants arriving at the study site were required to present a valid coupon to be eligible for inclusion. Each new PWUD enrolled in the study subsequently received 3 coupons to continue recruitment of additional participants in their respective networks. Participants could only enroll once in the study. Dissuasive biometric measures (wrist circumference and forearm length) were taken and recorded as a means to protect against multiple participations. Participants received honoraria for participation (50 euros [€] for transportation cost to the study site; the time spent at the research site; compensation for blood draws) and for any coupons returned via their personal network (20€ each; maximum 60 euros total for coupons returned).

Questionnaire, Hepatitis C Virus Assessment, Treatment Initiation, and Counseling

Once written informed consent was obtained, a urine sample was tested using a DOA-10 test cup (MB Biomedicals, Eschwege, Germany). After confirmation of participant eligibility, a face-to-face standardized questionnaire, including sociodemographic characteristics and drug use behaviors, was administered.

Participants then underwent a rapid test screening for HIV (INSTI VIH 1/2; Nephrotek, Boulogne-Billancourt, France), hepatitis B surface antigen (HBsAg) (TOYO VHB; Nephrotek), and HCV serology (TOYO VHC; Nephrotek). All participants with a positive HCV rapid test benefited from onsite HCV viral load quantification (Xpert HCV VL; point-of-care testing) and a liver fibrosis evaluation by a portable FibroScan. The results of the different tests were available within 90 minutes. An onsite physician consulted the patient and, if eligible for treatment, decided to initiate treatment with either glecaprevir/pibrentasvir for 8 weeks or sofosbuvir/velpatasvir for 12 weeks. Counterindications for treatment were as follows: pregnancy or breastfeeding, anticipated relocation for any period longer than 4 weeks in the 3 months after treatment initiation, taking counterindicated medication(s), allergies to any of the molecules in the antiviral regimen, and/or prognosis of death within the last 6 months. Only participants that were affiliated to and covered by the healthcare system could receive treatment. Those without health insurance were assisted by a social worker to gain access to the universal coverage plan. Because DAAs could not be delivered onsite by law, participants, often accompanied by a peer, were required to personally pick up their tablets from the pharmacy of their choosing. Once they initiated treatment, follow-up visits at week (W)2, W4, W8, and—for those with a 12-week treatment regimen—W12 were scheduled. During these visits, peers provided counsel for participants facing any treatment compliance issues and for harm reduction education. A final visit was scheduled to measure the sustained viral response (SVR) at W12 posttreatment completion. After 4 weeks of treatment, the participants were given the option to be referred to 1 of the 2 nearby addiction centers to continue his/her treatment and engage in addiction care.

Sample Size

Based on an HCV prevalence of 40%, recruiting 400 participants would allow a precision of ±5% in estimating the HCV prevalence in this population. Assuming that a third of HCV seropositive PWUD would require treatment, this sample size would provide a precision of ±3% around an estimated rate of 13% of PWUD needing treatment.

Data Analysis

People Who Use Drugs Population Size

The PWUD population size was estimated according to the Joint United Nations Programme for HIV/acquired immune deficiency syndrome recommendations [25]. Although the RDS survey was not implemented for epidemiological purposes, data are reported according to the relevant STROBE RDS recommendations [26]. To account for the study design and correlation between participants who were recruited by one another, RDS survey weighing is considered for the estimation of key outcomes [24]. Confidence intervals (CIs) for weighed estimates were obtained by a bootstrapping method. The RDS survey diagnostics, including homophily and equilibrium, were calculated and validated for the main participant characteristics.

The baseline participant characteristics and HCV viremia are described. Hepatitis C virus viremia, representing HCV transmission potential in the PWUD population, was defined as the proportion of PWUD with detectable HCV RNA among all participants, regardless of their HCV serology. The proportion of participants treated and cured (ie, achieving SVR12) among those identified with HCV, and among those who started treatment [27], were calculated.

Cost of the Intervention

All costs were collected by the research team, classified as variable (eg tests), fixed (eg rent) or staff (eg salaries). Costs related to research (eg data collection) were not considered. Costs for the tests and analysis devices (GeneXpert and Fibroscan) were depreciated over 10 years. The total cost of the RDS survey (with and without the follow-up visits) and the total cost per PWUD screened, HCV-infected, and cured were calculated. All costs were collected and presented in euros (2020).

Statistics

Statistical analyses were performed using both RDS Analysis Tool software (v7.1) and Stata software (version 16.1; StataCorp LP, College Station, TX).

Patient Consent Statement

The research protocol was approved by the “Comité de Protection des Personnes Sud Est V”, France. Individual written informed consent was obtained from all participants before their participation in the study.

RESULTS

Participant Enrollment

Between September 15 and November 27, 2020—when recruitment stopped for financial constraints—634 candidates passed through the RDS survey site, and 554 were included in the study (Figure 1). The main reason for exclusion was a drug consumption not meeting the established eligibility criteria (Figure 2).

Figure 1. — Recruitment rate per week of respondent-driven sampling survey, September 15, 2020 to November 27, 2020.

Figure 2. — Participants flow chart.

Abbreviations: AME, Aide médicale de l'Etat (Medical financial assistance from the government); HCV, hepatitis C virus; RDS, respondent-driven sampling; RNA, ribonucleic acid.

Respondent-Driven Sampling Survey Sample Validation

The RDS survey diagnostics were overall satisfactory. The number of waves to reach equilibrium was 2 for gender, 3 for HCV serology, and 3 for the type of PWUD (injecting drugs or not). Homophily, at a predefined threshold of 0.3, was reached for gender and HCV serology and was borderline for type of PWUD (injecting PWUD being more likely to recruit other injectors, which we considered appropriate given that injection is a major risk factor for HCV transmission in PWUD).

Population Size Estimate

The population of PWUD living in the Montpellier metropolitan area was estimated at 1559 (95% CI, 1099–2020).

Participant Characteristics

Most participants were male (78.8%) with a median age of 39 (interquartile range, 33–46), mostly coming from Western Europe (77.8%) and living from social benefits (62.8%) (Table 1). Cocaine (73.1%) and heroin (46.8%) were the main substances consumed according to participant self-declarations. Injection as a method of consumption was reported by 70.7% of HCV-seropositive, but only by 17.7% of HCV-seronegative, participants (P < .001). However, 82.6% of HCV-seronegative participants sniffed drugs versus 44.8% of HCV-seropositive PWUD (P < .001). More HCV-seropositive participants had previously been incarcerated (66.3% HCV-seropositive vs 45.3% HCV-seronegative; P < .001), took opioid replacement therapy (81.2% vs 50.1%, P < .001), and shared their injection materials (24.9% HCV-seropositive vs 5.1% HCV-seronegative; P < .001). Only 14.5% had no health insurance. Finally, more HCV-seropositive PWUD were infected with HIV (6.6% HCV-seropositive vs 1.3% HCV-seronegative; P = .001) and were HBsAg positive (3.9% HCV-seropositive vs 0.3% HCV-seronegative, P = .001). Overall, HCV seroprevalence stood at 32.6% (weighted population estimate, 28.7%; 95% CI, 21.8–35.8). The crude HCV viremia prevalence was 8.8% (95% CI, 28.8–36.8), and the weighted population estimate was 6.7% (95% CI, 3.3–11.1). Only 26.7% of participants reported having attended an addiction care center over the course of the previous year.

Table 1.

Characteristics of PWUD Enrolled in the RDS Survey

Category	Subcategory	Total	Anti-HCV Positive	Anti-HCV Negative	P Value^a,b
Category	Subcategory	N (%)	N (%)	N (%)	P Value^a,b
No. of participants		554 (100.0)	181 (32.7)	373 (67.3)
Sociodemographic Characteristics
Gender	Male	437 (78.8)	149 (82.3)	288 (77.2)	.304
	Female	115 (20.8)	31 (17.1)	84 (22.5)
	Transgender	2 (0.4)	1 (0.6)	1 (0.3)
Age	<30	97 (17.5)	12 (6.6)	85 (22.8)	.000^c
	30-39	190 (34.3)	59 (32.6)	131 (35.1)
	40–49	181 (32.7)	64 (35.4)	117 (31.4)
	≥50	86 (15.5)	46 (25.4)	40 (10.7)
Nationality by region	West European	431 (77.8)	126 (69.6)	305 (81.8)	.000^c
	East European	74 (13.4)	51 (28.2)	23 (6.2)
	North African	31 (5.6)	4 (2.2)	27 (7.2)
	Sub-Saharan African	17 (3.1)	–	17 (4.6)
	Other	1 (0.2)	–	1 (0.3)
Socioeconomic Characteristics
Sources of revenue^d	Professional activities	71 (12.8)	19 (10.5)	52 (13.9)	.255
	Benefits/Social minimums	348 (62.8)	110 (60.8)	238 (63.8)	.488
	Begging	130 (23.5)	61 (33.7)	69 (18.5)	.000^c
	Family	36 (6.5)	8 (4.4)	28 (7.5)	.167
	Illegal activities	81 (14.6)	31 (17.1)	50 (13.4)	.245
Living situation	Isolated	271 (48.9)	97 (53.6)	174 (46.7)	.129
	Cohabiting	83 (15.0)	19 (10.5)	64 (17.2)
	With family	61 (11.0)	48 (26.5)	91 (24.4)
	With friends	139 (25.1)	17 (9.4)	44 (11.8)
Dwelling	Stable	142 (25.6)	38 (21.0)	104 (27.9)	.005^c
	Temporary	185 (33.4)	59 (32.6)	126 (33.8)
	Squat	125 (22.6)	36 (19.9)	89 (23.9)
	Homeless	102 (18.4)	48 (26.5)	54 (14.5)
Ever been incarcerated	Yes	289 (52.2)	120 (66.3)	169 (45.3)	.000^c
Drug Use Behavior
Self-report of substance consumed in the past 6 months^d,e	Cocaine	405 (73.1)	134 (74.0)	271 (72.7)	.731
	Heroin	229 (46.8)	76 (42.0)	183 (49.1)	.118
	Analgesic opioid	176 (31.8)	77 (42.5)	99 (26.5)	.006^c
	Crack	236 (42.6)	62 (34.3)	174 (46.7)	.000^c
Method of consumption^d,e	Injected	194 (35.0)	128 (70.7)	66 (17.7)	.000^c
	Sniffed	389 (70.2)	81 (44.8)	308 (82.6)	.000^c
	Smoked	288 (52.0)	80 (44.2)	208 (55.8)	.011^c
	Ingested	435 (78.5)	141 (77.9)	294 (78.8)	.805
Taking ORT (methadone or buprenorphine, regardless whether taken as prescribed or not)	Yes	334 (60.3)	147 (81.2)	187 (50.1)	.000^c
Sharing injection materials^d	Yes	64 (11.6)	45 (24.9)	19 (5.1)	.000^c
	Needles	35 (6.3)	27 (14.9)	8 (2.1)	.000^c
	Syringes	42 (7.6)	33 (18.2)	9 (2.4)	.000^c
	Cottons/filters	44 (7.9)	31 (17.1)	13 (3.5)	.000^c
	Spoons/cups	45 (8.1)	32 (17.7)	13 (3.5)	.000^c
	Water/vials	42 (7.6)	31 (17.1)	11 (3.0)	.000^c
	Tourniquet	36 (6.5)	24 (13.3)	13 (3.2)	.000^c
	Other	19 (3.4)	1 (0.6)	2 (0.5)	.980
Health Status
Health insurance	Basic coverage plan	188 (33.9)	64 (35.4)	124 (33.2)	.197
	PUMA or AME^f	286 (51.6)	85 (47.0)	201 (53.9)
	None	80 (14.4)	32 (17.7)	48 (12.9)
Ever been hospitalized in a psychiatric hospital	Yes	145 (26.2)	62 (34.3)	83 (22.3)	.003^c
Positive HIV serology		17 (3.1)	12 (6.6)	5 (1.3)	.001^c
Detectable HBsAg		8 (1.4)	7 (3.9)	1 (0.3)	.001^‡
Positive HCV serology (crude)		181 (32.6)	181 (32.6)	…	–
Positive HCV serology (weighted)		181 (28.7)	181 (28.7)	…
Viremia prevalence (crude)		49 (8.8)	49 (8.8)	…
Viremia prevalence (weighted)		49 (6.7)	49 (6.7)	…
Liver fibrosis (elastography)	F0/F1 (2.5 ≤ LSM ≤ 7)	30 (69.8)^g	30 (69.8)^g	…
	F2 (7 < LSM ≤ 10)	3 (6.9)^g	3 (6.9)^g	…
	F3/F4 (LSM >10)	10 (23.3)^g	10 (23.3)^g	…

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Abbreviations: AME, aide médicale de l’Etat (medical financial assistance from the government); HBsAg, hepatitis B surface antigen; HCV, hepatitis C virus; HIV, human immunodeficiency virus; LSM, liver stiffness measurement; ORT, opioid replacement therapy; PUMA, Protection Universelle Maladie (universal health insurance); PWUD, people who use drugs; RDS, respondent-driven sampling.

P values are calculated for each class individually to account for nonindependent groups.

P values were calculated using Pearson’s χ² test of independence, with the threshold for statistical significance set at α < 0.05.

Cramér's V for statistically significant P values: age = 0.2547, region = 0.3312, begging as revenue = 0.1683, dwelling = 0.1517, ever been in jail = 0.1993, crack = −0.1176, analgesic opioids = 0.1612, injection = 0.5213, sniff = −0.3879, smoke = −0.1086, sharing injection materials = 0.2900, sharing needles = 0.2462, syringes = 0.2803, cottons = 0.2366, spoons = 0.2437, vials = 0.2512, tourniquet = 0.1911, ever been hospitalized in psych ward = 0.1281, HIV positive = 0.1438, detectable HBsAg = 0.1415.

Participants may be in more than 1 category.

Description of the 4 most common answers.

Universal health coverage scheme for resident in France.

43 of 49 PWID with RNA HCV⁺ realized a FribroScan at the 1st follow-up visit.

Among participants with detectable HCV RNA and available FibroScan data (N = 43), 30 (69.8%) had a liver stiffness measurement (LSM) ≤7, 3 (6.9%) were between 7 < LSM ≤ 10, and 10 (23.3%) had severe fibrosis (F3/F4, LSM > 10).

Participant Enrollment and Outcomes

Among the 181 HCV-seropositive PWUD, 49 had detectable HCV RNA and were eligible for treatment (Figure 2). Of the latter, 59.2% were already aware of their HCV status, 36.7% were newly diagnosed, and 37 of 49 (75.5%) initiated treatment, 30 of 37 (81.1%) of which collected their tablets for at least 2 months (under both medication regimens). Finally, 29 of 30 attended the W12 posttreatment visit and 27 achieved SVR12. Assuming those who did not attend the W12 posttreatment visit are not cured (although 2 of them collected all their tablets for the treatment duration), 73.0% (27 of 37) of those who initiated treatment achieved SVR12. Overall, our strategy enabled to cure at least 55% (27 of 49) of all PWUD who were identified with HCV during the RDS survey. It is interesting to note that among the 37 PWUD who started treatment, 20 had not attended any addiction center in the last year.

Cost of the Intervention

Implementing the survey for 554 participants cost 89 004€ (Table 2). The total cost per patient screened was 161€, and the total cost for identifying an HCV-infected patient was 1816€. The costs were mainly driven by the allowances given to the participants for both their initial visit and the returned coupons (almost 45% of the total RDS survey cost) (see Supplementary Table 1). The cost for follow-up visits stood at 825 691€ (Table 2), approximately 90% of which was allocated to the purchase of medication (see Supplementary Table 2). Finally, the cost per patient who completed treatment was 30 490€; the cost was 33 878€ per patient cured.

Table 2.

Costs Associated With the RDS Survey and Follow-up Visits

Category	N
Number of patients	554
Number of patients with chronic HCV eligible for treatment	49
Number of patients who completed the treatment	30
Number of cured patients	27
Total cost of RDS survey	89 004 €
Total cost per screened patient (at RDS survey)	161 €
Total cost to identify a patient with chronic HCV	1816 €
Total cost of the follow-up visits	825 691 €
Total cost of the intervention (RDS survey and follow-up visits)	914 695 €
Total cost per patient with chronic HCV	18 667 €
Total cost per patient who completed the treatment	30 490 €
Total cost per cured patient	33 878 €

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Abbreviations: HCV, hepatitis C virus; RDS, respondent-driven sampling.

DISCUSSION

Our community-based strategy proved efficient and cost-effective in rapid recruitment, screening, and treatment of a large number of PWUD with HCV. Approximately 33% of the estimated PWUD population in the city was screened for HCV within 11 weeks. Among those with detectable HCV RNA, most were fully recovered by the end of the study.

In most high-income countries where HCV testing and care are widely accessible and free of charge for patients, many PWUD with HCV have already been cured. This was the case in our study. In HepCare Europe—a large project addressing the various steps of the cascade of care in community addiction, homeless, and penitentiary services (ie, targeting not only PWUD) in 4 European cities—60.5% of 1074 participants (mainly PWUD) with a positive serology were infected with HCV (versus the 27.1% observed in our study) [28]. The ultimate challenge for HCV elimination consists of reaching and treating at least half of the remaining 40% of untreated PWUD (to attain a proportion of 80% of PWUD being treated), who are considered to be the most difficult to reach and engage in care in this especially high-risk community. The findings from our demonstration project suggest that our strategy can rapidly detect and treat a majority of these hard-to-reach PWUD.

Our strategy has been designed to improve the proportion of PWUD cured from HCV. To our knowledge, few alternative interventions have been able to address the entirety of the cascade of care (ie, from increased screening to full recovery), and they rarely report encouraging results. A randomized controlled trial in London tested outreach peer support to engage PWUD in care. Although this strategy resulted in modest improvement in engagement in HCV care, no participant achieved SVR12 [29]. In the HepCare project, the acceptance rate for testing was 75% [28]. Only 43.5% of those with detectable HCV RNA were initiated on a treatment regimen. Of note, HCV testing was done (1) in prisons and (2) in addiction and homelessness services. In Montpellier, as is the case in the rest of France, this strategy would be of limited benefit because prisoners and addiction center attendees are widely screened and treated. In Toronto, a randomized trial tested peer-led, point-of-care serological testing to target individuals in the community who had ever injected drugs in their lifetime. The results showed a poor uptake of HCV screening and a dismal engagement rate in care (3%) for those with positive serology, with no difference between study arms [30]. In Belgium, a similar peer outreach screening approach targeting PWUD resulted in major losses throughout the cascade of care with 63 of 425 (14.8%) testing HCV seropositive, 88.9% of whom were referred, and 66.1% of whom were finally linked to care and tested for HCV RNA. Among the 29 (78.4%) with chronic HCV, DAA treatment was initiated in only 17 (58%) with no report of SVR12 [31].

We believe that the strategy we propose could be much more efficient for several reasons. The RDS survey approach is a powerful tool in reaching hard-to-reach PWUD [32, 33], whereas the peer outreach option tends to limit the testing coverage to more restricted networks. We were able to recruit ±33% of the whole PWUD population, including community members never before seen in addiction care centers. The RDS surveys also allow for an accelerated recruitment. For example, in Antwerp, 36 days of outreach screening in 18 locations recruited 425 PWUD over the course of 1 year, whereas we recruited a similar number in fewer than 3 months from 1 site [31]. Furthermore, the choice of a neutral, temporary site, outside of the usual health services, was likely a motivating factor for those reluctant to attend usual services. Beyond being a friendly environment with presence of peers and empathetic healthcare workers, this site provided the full HCV treatment eligibility check, using Xpert HCV VL and portable FibroScan. This “all-in-one” visit allowed eligible participants to leave the study site within 2 to 3 hours with a DAA prescription and peer-assisted referral to a pharmacy. This same-day assessment is crucial to reduce losses along the cascade of care [34]. Peer involvement, together with the choice of a temporary “test-and-treat” setting implemented within the community, were potentially instrumental in the success of our study.

As a result, the cost per person screened using our strategy (161€) was substantially lower compared to those reported by the HepCare project (from 194€ testing prisoners to 635€ in medication-assisted treatment clinics) [28]. Our findings confirm the high SVR12 success rates among PWUD initiating DAA as reported from other settings [14, 35].

Our approach could also provide, for the first time in France, a precise estimate of HCV serology and chronic HCV in the PWUD population. Although we could not estimate the elimination targets (new infections and HCV-related deaths could not be measured by design), we could assess our progress toward HCV elimination through the proportion of PWUD with detectable HCV RNA among those that are HCV seropositive (27.1%) and through the proportion of eligible PWUD who started treatment among those with detectable HCV RNA (75.5%). Therefore, our findings showed that RDS surveys are very close to achieve the World Health Organization HCV elimination target of 80% of those eligible.

Our study has several limitations. First, it was a demonstration project whose findings must be confirmed in other settings. Second, the intervention effectiveness relies on the assumption that participants identified with detectable HCV RNA would not have been initiated on DAA in the absence of the intervention. This assumption is likely true because few participants had any engagement in addiction or medical care over the past year. Finally, the total costs might be slightly underestimated because drug costs were only taken into account for those who completed their treatment.

A major improvement in this strategy would be the possibility to initiate DAAs directly on site. Although, to our knowledge, few other examples of this have been reported [36], research from the HIV field showed that both antiretroviral therapy initiation within the community [37] and prompt engagement in care proved efficacious in maintaining patients in care [38].

CONCLUSIONS

Our findings suggest that mass community-based HCV screening using an RDS survey coupled with same-day DAA eligibility onsite could be a cost-effective and efficient strategy to rapidly make the final step towards HCV elimination among PWUD in high-income settings.

Supplementary Data

Supplementary materials are available at Open Forum Infectious Diseases online. Consisting of data provided by the authors to benefit the reader, the posted materials are not copyedited and are the sole responsibility of the authors, so questions or comments should be addressed to the corresponding author.

Supplementary Material

ofac181_Supplementary_Data

Click here for additional data file.^{(25.5KB, zip)}

Acknowledgments

We are grateful to the members of the scientific advisory board (Dr. Perrine Roux) for their time and valuable comments. We also thank all participants for their contribution, the peers, and the staff of the different nongovernmental organizations (GROUPE SOS Solidarité, AMT CSAPA Arc en ciel, CAARUD Réduire les Risques-La Boutik, SOS Hépatites, and L’Avitarelle) for their collaboration and the Montpellier University Hospital for their assistance.

Author contributions. N. N. and H. D.-R. contributed to conceptualization. M. D. contributed to data curation, validation, and visualization. M. D. and J. C. contributed to formal analysis. N. N. and H. D.-R. contributed to funding acquisition. N. L., B. H., R. B., V. F., E. T., and D. L. contributed to investigation. N. N. contributed to methodology. S. G. contributed to project administration. G.-P. P. contributed to resources. C. Q. and A. D. supervised the work. N. N. and J. C. contributed to writing the original draft. All authors contributed to writing, reviewing, and editing the manuscript.

Disclaimer. The funding agency had no role in study design, data collection, analysis and interpretation, nor in writing of the manuscript and decision to submit it for publication.

Financial support. This work was funded by the Agence Nationale de Recherches sur le Sida et les Hépatites Virales – Maladies Infectieuses Emergentes (French National Agency for Research on AIDS, Viral Hepatitis and Infectious Emerging Diseases) (Grant number 95050).

Potential conflicts of interest. All authors: GPP received conference grants from Gilead, Abbvie, Ipsen and Astellas. HDR received conference grants from Gilead and Abbvie. SG received conference and consultancy fees from Gilead. BH received conference, consultancy and research grants from Gilead and Abbvie. No reported conflicts for other authors.

All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest.

Contributor Information

Nicolas Nagot, Pathogenesis and Control of Chronic & Emerging Infections, University of Montpellier, Montpellier, France.

Morgana D’Ottavi, Pathogenesis and Control of Chronic & Emerging Infections, University of Montpellier, Montpellier, France.

Catherine Quillet, Pathogenesis and Control of Chronic & Emerging Infections, University of Montpellier, Montpellier, France.

Anne Debellefontaine, Pathogenesis and Control of Chronic & Emerging Infections, University of Montpellier, Montpellier, France; Groupe SOS Solidarité, Montpellier, France.

Joëlle Castellani, Pathogenesis and Control of Chronic & Emerging Infections, University of Montpellier, Montpellier, France.

Nicolas Langendorfer, Department of Addiction Medicine, Montpellier University Hospital, Montpellier, France.

Bertrand Hanslik, Department of Addiction Medicine, Montpellier University Hospital, Montpellier, France.

Sylvain Guichard, Association of Marginality and Drug Addiction (AMT), Montpellier, France.

René Baglioni, Department of Addiction Medicine, Montpellier University Hospital, Montpellier, France.

Vincent Faucherre, Department of Addiction Medicine, Montpellier University Hospital, Montpellier, France.

Edouard Tuaillon, Pathogenesis and Control of Chronic & Emerging Infections, University of Montpellier, Montpellier, France.

Georges-Philippe Pageaux, Department of Hepatology and Gastroenterology, Montpellier University Hospital, Montpellier, France.

Didier Laureillard, Pathogenesis and Control of Chronic & Emerging Infections, University of Montpellier, Montpellier, France; Department of Infectious Diseases, Caremeau University Hospital, Nimes, France.

Hélène Donnadieu-Rigole, Pathogenesis and Control of Chronic & Emerging Infections, University of Montpellier, Montpellier, France; Department of Addiction Medicine, Montpellier University Hospital, Montpellier, France.

References

1. Falla AM, Hofstraat SHI, Duffell E, Hahné SJM, Tavoschi L, Veldhuijzen IK. Hepatitis B/C in the countries of the EU/EEA: a systematic review of the prevalence among at-risk groups. BMC Infect Dis 2018; 18:79. [DOI] [PMC free article] [PubMed] [Google Scholar]
2. Trickey A, Fraser H, Lim AG, et al. The contribution of injection drug use to hepatitis C virus transmission globally, regionally, and at country level: a modelling study. Lancet Gastroenterol Hepatol 2019; 4:435–44. [DOI] [PMC free article] [PubMed] [Google Scholar]
3. European Monitoring Centre for Drugs and Drug Addiction . European drug report 2019: trends and developments. Available at: https://data.europa.eu/doi/10.2810/191370. Accessed 28 August 2021.
4. Nelson PK, Mathers BM, Cowie B, et al. Global epidemiology of hepatitis B and hepatitis C in people who inject drugs: results of systematic reviews. Lancet 2011; 378:571–83. [DOI] [PMC free article] [PubMed] [Google Scholar]
5. Wiessing L, Ferri M, Grady B, et al. Hepatitis C virus infection epidemiology among people who inject drugs in Europe: a systematic review of data for scaling up treatment and prevention. PLoS One 2014; 9:e103345. [DOI] [PMC free article] [PubMed] [Google Scholar]
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7. World Health Organization . Global health sector strategy on viral hepatitis 2016-2021. Available at: https://www.who.int/publications-detail-redirect/WHO-HIV-2016.06. Accessed 28 August 2021.
8. European Association for the Study of the Liver . EASL recommendations on treatment of hepatitis C 2016. J Hepatol 2017; 66:153–94. [DOI] [PubMed] [Google Scholar]
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10. Day E, Broder T, Bruneau J, et al. Priorities and recommended actions for how researchers, practitioners, policy makers, and the affected community can work together to improve access to hepatitis C care for people who use drugs. Int J Drug Policy 2019; 66:87–93. [DOI] [PubMed] [Google Scholar]
11. Falade-Nwulia O, Gicquelais RE, Astemborski J, et al. Hepatitis C treatment uptake among people who inject drugs in the oral direct-acting antiviral era. Liver Int 2020; 40:2407–16. [DOI] [PMC free article] [PubMed] [Google Scholar]
12. Iversen J, Grebely J, Catlett B, Cunningham P, Dore GJ, Maher L. Estimating the cascade of hepatitis C testing, care and treatment among people who inject drugs in Australia. Int J Drug Policy 2017; 47:77–85. [DOI] [PubMed] [Google Scholar]
13. Makarenko I, Artenie A, Hoj S, et al. Transitioning from interferon-based to direct antiviral treatment options: a potential shift in barriers and facilitators of treatment initiation among people who use drugs? Int J Drug Policy 2019; 72:69–76. [DOI] [PubMed] [Google Scholar]
14. Grebely J, Dalgard O, Conway B, et al. Sofosbuvir and velpatasvir for hepatitis C virus infection in people with recent injection drug use (SIMPLIFY): an open-label, single-arm, phase 4, multicentre trial. Lancet Gastroenterol Hepatol 2018; 3:153–61. [DOI] [PubMed] [Google Scholar]
15. Lazarus JV, Sperle I, Maticic M, Wiessing L. A systematic review of hepatitis C virus treatment uptake among people who inject drugs in the European region. BMC Infect Dis 2014; 14(Suppl 6):S16. [DOI] [PMC free article] [PubMed] [Google Scholar]
16. Matičič M, Lombardi A, Mondelli MU, Colombo M, ESCMID Study Group for Viral Hepatitis (ESGVH) . Elimination of hepatitis C in Europe: can WHO targets be achieved? Clin Microbiol Infect 2020; 26:818–23. [DOI] [PubMed] [Google Scholar]
17. Brouard C, Pillonel J, Boussac M, et al. French hepatitis C care cascade: substantial impact of direct-acting antivirals, but the road to elimination is still long. BMC Infect Dis 2020; 20:759. [DOI] [PMC free article] [PubMed] [Google Scholar]
18. Katzman C, Mateu-Gelabert P, Kapadia SN, Eckhardt BJ. Contact tracing for hepatitis C: The case for novel screening strategies as we strive for viral elimination. Int J Drug Policy 2019; 72:33–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
19. Henderson C, Madden A, Kelsall J. ‘Beyond the willing & the waiting’—The role of peer-based approaches in hepatitis C diagnosis & treatment. Int J Drug Policy 2017; 50:111–15. [DOI] [PubMed] [Google Scholar]
20. Lambert JS, Murtagh R, Menezes D, et al. ‘HepCheck Dublin’: an intensified hepatitis C screening programme in a homeless population demonstrates the need for alternative models of care. BMC Infect Dis 2019; 19:128. [DOI] [PMC free article] [PubMed] [Google Scholar]
21. Falade-Nwulia O, Ward KM, McCormick S, et al. Network-based recruitment of people who inject drugs for hepatitis C testing and linkage to care. J Viral Hepat 2020; 27:663–70. [DOI] [PMC free article] [PubMed] [Google Scholar]
22. Des Jarlais DC, Duong Thi H, Khuat Thi Hai O, et al. Ending an HIV epidemic among persons who inject drugs (PWID) in a middle-income country: extremely low HIV incidence among PWID in Hai Phong, Viet Nam. AIDS 2020; 34:2305–11. [DOI] [PMC free article] [PubMed] [Google Scholar]
23. Sypsa V, Psichogiou M, Paraskevis D, et al. Rapid decline in HIV incidence among persons who inject drugs during a fast-track combination prevention program after an HIV outbreak in Athens. J Infect Dis 2017; 215:1496–505. [DOI] [PMC free article] [PubMed] [Google Scholar]
24. Heckathorn DD, Semaan S, Broadhead RS, Hughes JJ. Extensions of respondent-driven sampling: A new approach to the study of injection drug users aged 18–25. AIDS Behav 2002; 6:55–67. [Google Scholar]
25. UNAIDS . Guidelines on estimating the size of populations most at risk to HIV. Available at: https://www.unaids.org/en/resources/documents/2011/2011_Estimating_Populations. Accessed 1 September 2021.
26. White RG, Hakim AJ, Salganik MJ, et al. Strengthening the reporting of observational studies in epidemiology for respondent-driven sampling studies: “STROBE-RDS” statement. J Clin Epidemiol 2015; 68:1463–71. [DOI] [PMC free article] [PubMed] [Google Scholar]
27. Latham Ned H, Doyle Joseph S, Palmer Anna Y, et al. Staying hepatitis C negative: A systematic review and meta-analysis of cure and reinfection in people who inject drugs. Liver International 2019; 39(12):2244–60. doi: 10.1111/liv.v39.12. [DOI] [PubMed] [Google Scholar]
28. Avramovic G, Reilly M, Cullen W, et al. HEPCARE EUROPE- A case study of a service innovation project aiming at improving the elimination of HCV in vulnerable populations in four European cities. Int J Infect Dis 2020; 101:374–79. [DOI] [PubMed] [Google Scholar]
29. Stagg HR, Surey J, Francis M, et al. Improving engagement with healthcare in hepatitis C: a randomised controlled trial of a peer support intervention. BMC Med 2019; 17:71. [DOI] [PMC free article] [PubMed] [Google Scholar]
30. Broad J, Mason K, Guyton M, Lettner B, Matelski J, Powis J. Peer outreach point-of-care testing as a bridge to hepatitis C care for people who inject drugs in Toronto, Canada. Int J Drug Policy 2020; 80:102755. [DOI] [PubMed] [Google Scholar]
31. Busschots D, Kremer C, Bielen R, et al. Identification and treatment of viral hepatitis C in persons who use drugs: a prospective, multicenter outreach study in Flanders, Belgium. Harm Reduct J 2021; 18:54. [DOI] [PMC free article] [PubMed] [Google Scholar]
32. Abdul-Quader AS, Heckathorn DD, McKnight C, et al. Effectiveness of respondent-driven sampling for recruiting drug users in New York City: findings from a pilot study. J Urban Health 2006; 83:459–76. [DOI] [PMC free article] [PubMed] [Google Scholar]
33. Collier MG, Garfein RS, Cuevas-Mota J, Teshale EH. Comparison of three popular methods for recruiting young persons who inject drugs for interventional studies. J Urban Health 2017; 94:587–91. [DOI] [PMC free article] [PubMed] [Google Scholar]
34. Alavi M, Poustchi H, Merat S, et al. An intervention to improve HCV testing, linkage to care, and treatment among people who use drugs in Tehran, Iran: the ENHANCE study. Int J Drug Policy 2019; 72:99–105. [DOI] [PubMed] [Google Scholar]
35. Cunningham EB, Hajarizadeh B, Amin J, et al. Adherence to once-daily and twice-daily direct-acting antiviral therapy for hepatitis C infection among people with recent injection drug use or current opioid agonist therapy. Clin Infect Dis 2020; 71:e115–24. [DOI] [PubMed] [Google Scholar]
36. Kamali I, Barnhart DA, Nyirahabihirwe F, et al. Initiation of hepatitis C treatment in two rural Rwandan districts: a mobile clinic approach. BMC Infect Dis 2021; 21:220. [DOI] [PMC free article] [PubMed] [Google Scholar]
37. Eshun-Wilson I, Awotiwon AA, Germann A, et al. Effects of community-based antiretroviral therapy initiation models on HIV treatment outcomes: a systematic review and meta-analysis. PLoS Med 2021; 18:e1003646. [DOI] [PMC free article] [PubMed] [Google Scholar]
38. Labhardt ND, Ringera I, Lejone TI, et al. Effect of offering same-day ART vs usual health facility referral during home-based HIV testing on linkage to care and viral suppression among adults with HIV in Lesotho: the CASCADE Randomized Clinical Trial. JAMA 2018; 319:1103–12. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

ofac181_Supplementary_Data

Click here for additional data file.^{(25.5KB, zip)}

[ofac181-B1] 1. Falla AM, Hofstraat SHI, Duffell E, Hahné SJM, Tavoschi L, Veldhuijzen IK. Hepatitis B/C in the countries of the EU/EEA: a systematic review of the prevalence among at-risk groups. BMC Infect Dis 2018; 18:79. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B2] 2. Trickey A, Fraser H, Lim AG, et al. The contribution of injection drug use to hepatitis C virus transmission globally, regionally, and at country level: a modelling study. Lancet Gastroenterol Hepatol 2019; 4:435–44. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B3] 3. European Monitoring Centre for Drugs and Drug Addiction . European drug report 2019: trends and developments. Available at: https://data.europa.eu/doi/10.2810/191370. Accessed 28 August 2021.

[ofac181-B4] 4. Nelson PK, Mathers BM, Cowie B, et al. Global epidemiology of hepatitis B and hepatitis C in people who inject drugs: results of systematic reviews. Lancet 2011; 378:571–83. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B5] 5. Wiessing L, Ferri M, Grady B, et al. Hepatitis C virus infection epidemiology among people who inject drugs in Europe: a systematic review of data for scaling up treatment and prevention. PLoS One 2014; 9:e103345. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B6] 6. Hope VD, Eramova I, Capurro D, Donoghoe MC. Prevalence and estimation of hepatitis B and C infections in the WHO European Region: a review of data focusing on the countries outside the European Union and the European Free Trade Association. Epidemiol Infect 2014; 142:270–86. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B7] 7. World Health Organization . Global health sector strategy on viral hepatitis 2016-2021. Available at: https://www.who.int/publications-detail-redirect/WHO-HIV-2016.06. Accessed 28 August 2021.

[ofac181-B8] 8. European Association for the Study of the Liver . EASL recommendations on treatment of hepatitis C 2016. J Hepatol 2017; 66:153–94. [DOI] [PubMed] [Google Scholar]

[ofac181-B9] 9. D’Ambrosio R, Degasperi E, Colombo M, Aghemo A. Direct-acting antivirals: the endgame for hepatitis C? Curr Opin Virol 2017; 24:31–7. [DOI] [PubMed] [Google Scholar]

[ofac181-B10] 10. Day E, Broder T, Bruneau J, et al. Priorities and recommended actions for how researchers, practitioners, policy makers, and the affected community can work together to improve access to hepatitis C care for people who use drugs. Int J Drug Policy 2019; 66:87–93. [DOI] [PubMed] [Google Scholar]

[ofac181-B11] 11. Falade-Nwulia O, Gicquelais RE, Astemborski J, et al. Hepatitis C treatment uptake among people who inject drugs in the oral direct-acting antiviral era. Liver Int 2020; 40:2407–16. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B12] 12. Iversen J, Grebely J, Catlett B, Cunningham P, Dore GJ, Maher L. Estimating the cascade of hepatitis C testing, care and treatment among people who inject drugs in Australia. Int J Drug Policy 2017; 47:77–85. [DOI] [PubMed] [Google Scholar]

[ofac181-B13] 13. Makarenko I, Artenie A, Hoj S, et al. Transitioning from interferon-based to direct antiviral treatment options: a potential shift in barriers and facilitators of treatment initiation among people who use drugs? Int J Drug Policy 2019; 72:69–76. [DOI] [PubMed] [Google Scholar]

[ofac181-B14] 14. Grebely J, Dalgard O, Conway B, et al. Sofosbuvir and velpatasvir for hepatitis C virus infection in people with recent injection drug use (SIMPLIFY): an open-label, single-arm, phase 4, multicentre trial. Lancet Gastroenterol Hepatol 2018; 3:153–61. [DOI] [PubMed] [Google Scholar]

[ofac181-B15] 15. Lazarus JV, Sperle I, Maticic M, Wiessing L. A systematic review of hepatitis C virus treatment uptake among people who inject drugs in the European region. BMC Infect Dis 2014; 14(Suppl 6):S16. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B16] 16. Matičič M, Lombardi A, Mondelli MU, Colombo M, ESCMID Study Group for Viral Hepatitis (ESGVH) . Elimination of hepatitis C in Europe: can WHO targets be achieved? Clin Microbiol Infect 2020; 26:818–23. [DOI] [PubMed] [Google Scholar]

[ofac181-B17] 17. Brouard C, Pillonel J, Boussac M, et al. French hepatitis C care cascade: substantial impact of direct-acting antivirals, but the road to elimination is still long. BMC Infect Dis 2020; 20:759. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B18] 18. Katzman C, Mateu-Gelabert P, Kapadia SN, Eckhardt BJ. Contact tracing for hepatitis C: The case for novel screening strategies as we strive for viral elimination. Int J Drug Policy 2019; 72:33–9. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B19] 19. Henderson C, Madden A, Kelsall J. ‘Beyond the willing & the waiting’—The role of peer-based approaches in hepatitis C diagnosis & treatment. Int J Drug Policy 2017; 50:111–15. [DOI] [PubMed] [Google Scholar]

[ofac181-B20] 20. Lambert JS, Murtagh R, Menezes D, et al. ‘HepCheck Dublin’: an intensified hepatitis C screening programme in a homeless population demonstrates the need for alternative models of care. BMC Infect Dis 2019; 19:128. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B21] 21. Falade-Nwulia O, Ward KM, McCormick S, et al. Network-based recruitment of people who inject drugs for hepatitis C testing and linkage to care. J Viral Hepat 2020; 27:663–70. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B22] 22. Des Jarlais DC, Duong Thi H, Khuat Thi Hai O, et al. Ending an HIV epidemic among persons who inject drugs (PWID) in a middle-income country: extremely low HIV incidence among PWID in Hai Phong, Viet Nam. AIDS 2020; 34:2305–11. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B23] 23. Sypsa V, Psichogiou M, Paraskevis D, et al. Rapid decline in HIV incidence among persons who inject drugs during a fast-track combination prevention program after an HIV outbreak in Athens. J Infect Dis 2017; 215:1496–505. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B24] 24. Heckathorn DD, Semaan S, Broadhead RS, Hughes JJ. Extensions of respondent-driven sampling: A new approach to the study of injection drug users aged 18–25. AIDS Behav 2002; 6:55–67. [Google Scholar]

[ofac181-B25] 25. UNAIDS . Guidelines on estimating the size of populations most at risk to HIV. Available at: https://www.unaids.org/en/resources/documents/2011/2011_Estimating_Populations. Accessed 1 September 2021.

[ofac181-B26] 26. White RG, Hakim AJ, Salganik MJ, et al. Strengthening the reporting of observational studies in epidemiology for respondent-driven sampling studies: “STROBE-RDS” statement. J Clin Epidemiol 2015; 68:1463–71. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B27] 27. Latham Ned H, Doyle Joseph S, Palmer Anna Y, et al. Staying hepatitis C negative: A systematic review and meta-analysis of cure and reinfection in people who inject drugs. Liver International 2019; 39(12):2244–60. doi: 10.1111/liv.v39.12. [DOI] [PubMed] [Google Scholar]

[ofac181-B28] 28. Avramovic G, Reilly M, Cullen W, et al. HEPCARE EUROPE- A case study of a service innovation project aiming at improving the elimination of HCV in vulnerable populations in four European cities. Int J Infect Dis 2020; 101:374–79. [DOI] [PubMed] [Google Scholar]

[ofac181-B29] 29. Stagg HR, Surey J, Francis M, et al. Improving engagement with healthcare in hepatitis C: a randomised controlled trial of a peer support intervention. BMC Med 2019; 17:71. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B30] 30. Broad J, Mason K, Guyton M, Lettner B, Matelski J, Powis J. Peer outreach point-of-care testing as a bridge to hepatitis C care for people who inject drugs in Toronto, Canada. Int J Drug Policy 2020; 80:102755. [DOI] [PubMed] [Google Scholar]

[ofac181-B31] 31. Busschots D, Kremer C, Bielen R, et al. Identification and treatment of viral hepatitis C in persons who use drugs: a prospective, multicenter outreach study in Flanders, Belgium. Harm Reduct J 2021; 18:54. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B32] 32. Abdul-Quader AS, Heckathorn DD, McKnight C, et al. Effectiveness of respondent-driven sampling for recruiting drug users in New York City: findings from a pilot study. J Urban Health 2006; 83:459–76. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B33] 33. Collier MG, Garfein RS, Cuevas-Mota J, Teshale EH. Comparison of three popular methods for recruiting young persons who inject drugs for interventional studies. J Urban Health 2017; 94:587–91. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B34] 34. Alavi M, Poustchi H, Merat S, et al. An intervention to improve HCV testing, linkage to care, and treatment among people who use drugs in Tehran, Iran: the ENHANCE study. Int J Drug Policy 2019; 72:99–105. [DOI] [PubMed] [Google Scholar]

[ofac181-B35] 35. Cunningham EB, Hajarizadeh B, Amin J, et al. Adherence to once-daily and twice-daily direct-acting antiviral therapy for hepatitis C infection among people with recent injection drug use or current opioid agonist therapy. Clin Infect Dis 2020; 71:e115–24. [DOI] [PubMed] [Google Scholar]

[ofac181-B36] 36. Kamali I, Barnhart DA, Nyirahabihirwe F, et al. Initiation of hepatitis C treatment in two rural Rwandan districts: a mobile clinic approach. BMC Infect Dis 2021; 21:220. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B37] 37. Eshun-Wilson I, Awotiwon AA, Germann A, et al. Effects of community-based antiretroviral therapy initiation models on HIV treatment outcomes: a systematic review and meta-analysis. PLoS Med 2021; 18:e1003646. [DOI] [PMC free article] [PubMed] [Google Scholar]

[ofac181-B38] 38. Labhardt ND, Ringera I, Lejone TI, et al. Effect of offering same-day ART vs usual health facility referral during home-based HIV testing on linkage to care and viral suppression among adults with HIV in Lesotho: the CASCADE Randomized Clinical Trial. JAMA 2018; 319:1103–12. [DOI] [PMC free article] [PubMed] [Google Scholar]

PERMALINK

Reaching Hard-to-Reach People Who Use Drugs: A Community-Based Strategy for the Elimination of Hepatitis C

Nicolas Nagot

Morgana D’Ottavi

Catherine Quillet

Anne Debellefontaine

Joëlle Castellani

Nicolas Langendorfer

Bertrand Hanslik

Sylvain Guichard

René Baglioni

Vincent Faucherre

Edouard Tuaillon

Georges-Philippe Pageaux

Didier Laureillard

Hélène Donnadieu-Rigole

Abstract

Background

Methods

Results

Conclusions

METHODS

Study Design

Study Population

Outcomes

Study Site

Study Procedures

Population Size Estimate

Peers

Seeds and Network Recruitment

Questionnaire, Hepatitis C Virus Assessment, Treatment Initiation, and Counseling

Sample Size

Data Analysis

People Who Use Drugs Population Size

Cost of the Intervention

Statistics

Patient Consent Statement

RESULTS

Participant Enrollment

Figure 1.

Figure 2.

Respondent-Driven Sampling Survey Sample Validation

Population Size Estimate

Participant Characteristics

Table 1.

Participant Enrollment and Outcomes

Cost of the Intervention

Table 2.

DISCUSSION

CONCLUSIONS

Supplementary Data

Supplementary Material

Acknowledgments

Contributor Information

References

Associated Data

Supplementary Materials

ACTIONS

PERMALINK

RESOURCES

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