Prevalence and Associated Risk Factors of Hepatitis C Antibody and RNA among People Who Inject Drugs in Puerto Rico

Abstract

Introduction:

As a public health crisis, hepatitis C viral infection (HCV) is highly prevalent among people who inject drugs (PWID). We aimed to assess factors associated with HCV antibody (Ab) and HCV ribonucleic acid (RNA) positivity among PWID in Puerto Rico.

Methods:

The study recruited a total of 150 persons in rural and peri-urban community settings through the respondent-driven sampling method and administered a structured questionnaire. We conducted HIV and HCV testing using dried blood spots (DBS). We examined correlates of HCV infection with sociodemographics, drug use patterns, and injection practices using regression in bivariate and multivariable analysis.

Results:

Of the 150 participants, 89% were male; 11% were female; 72% identified as mixed race; and the median duration of drug injection was 17.8 years. The mean age was 43.1 years, with 64% of the population being from 23 to 45 years old. Among study participants (n=150), the prevalence of HCV Ab was 73%, and HCV RNA was 53%. Factors significantly associated with HCV Ab and RNA included older age, increasing years of injection, incarceration, injecting other people, and identifying as Black. The belief that syringe air blowing reduces HCV transmission was also independently associated with HCV Ab positivity.

Conclusions:

Our findings regarding risk factors associated with HCV infection show the need to enhance prevention and control strategies for reducing transmission among PWID. Direct-acting antiviral treatment, sustained access to harm reduction, and culturally tailored services will be required to substantially reduce rates of HCV. Community-based treatment models and treatment in correctional settings are needed.

1. Introduction

Hepatitis C (HCV) is a highly prevalent chronic viral infection among people who inject drugs (PWID) worldwide. Globally, of the estimated 14.8 million PWID, approximately 32.8% are infected with chronic HCV infection (Degenhardt et al., 2023), with 23–39% of new HCV infections associated with injection drug use (World Health Organization, n.d.). HCV is a major health problem, as untreated infected people are at risk of liver disease and associated mortality (Degenhardt et al., 2023, World Health Organization, n.d.). Worldwide, one in three HCV deaths are PWID-related (World Health Organization, n.d.). A recent systematic review of HCV and HIV among PWID show that, between 2017–2022, the prevalence of HCV among PWID surpassed that of HIV (Paintsil et al., 2010). Evidence has revealed that the differential in HCV and HIV prevalence among PWID may be related to microbiological characteristics that allow HCV to survive on surfaces outside of the body and remain infectious longer than HIV (Paintsil et al., 2010). In injection-drug-use settings, HCV has been shown to be 10 times more infectious than HIV, since HCV can live in a syringe and other contaminated injection equipment for up to two months (Paintsil et al., 2010).

HCV infection among PWID is mainly attributed to unsafe injection practices. Unsafe injection practices are behaviors that place PWID at increased risk for HCV transmission (Paintsil et al., 2010). The latter include sharing syringes and other injection preparation equipment and dividing drugs with a syringe previously used by another person. Use of shared injection equipment at shooting galleries, older age, injection frequency, years of injection, unstable housing, incarceration, financial insecurity, stigma, and lack of access to syringe services programs (SSPs) are also associated with a high risk of acquiring HCV (Doerrbecker et al., 2013; Eckhardt et al., 2017; Grebely & Dore, 2011; Hagan et al., 2001; Hahn et al., 2002; Larney et al., 2017; Pouget et al., 2011a; Thein et al,. 2008; Walters et al., 2023). Despite the increased risk of HCV for PWID, they are among those with the least access to HCV care and treatment worldwide (Bruggmann & Litwin, 2013; Grebely et al., 2009; Grebely et al., 2010; Lindenburg, et al., 2011; Mehta et al., 2018; Strathdee et al., 2005). Although PWID infected with HCV can achieve a sustained viral response after treatment with direct-acting antivirals, treatment remains inaccessible to many PWID. HCV care and treatment barriers among PWID include lack of health insurance, competing priorities, sobriety restrictions, transportation problems, financial constraints, drug-related stigma, negative experiences with medical providers, and unawareness regarding HCV status (Amoako et al., 2021; Austin et al., 2022; Fong et al., 2021; Grebely & Dore, 2011; Harris & Rhode 2013; Walters et al., 2023).

Puerto Rico has one of the highest HCV infection rates in the United States and Latin America, with an estimated HCV prevalence of 6.3% for adults aged 21 to 64 (Kershenobich et al., 2011; Pérez et al., 2007). In Puerto Rico, a history of drug use, especially drug injection, is the main risk for transmission of HCV. HCV antibody (Ab) prevalence among PWID in Puerto Rico has been reported at 78.4% in some rural locations and 76.5%−90% in San Juan, Puerto Rico’s capital (Abadie et al., 2016; Colón-López et al., 2022; Reyes et al., 2006). Injection of a speedball (the mixture of heroin and cocaine), pooling money to buy drugs, injecting in a shooting gallery (i.e., a location where PWID use drugs and rent, buy, or borrow injection equipment) and sharing injection equipment have been associated with HCV infection in Puerto Rico (Abadie et al., 2016; Colón-López et al., 2022; Reyes et al., 2006)

In this study, we aim to identify risk factors associated with HCV Ab and HCV ribonucleic acid (RNA) prevalence in PWID from rural and peri-urban areas (i.e., urban-rural hybrid; mixed and transition zones between rural and urban areas) in Puerto Rico. Understanding risk factors associated with HCV Ab and RNA prevalence may help drive treatment and prevention efforts for PWID in Puerto Rico.

2. Materials and Methods

2.1. Study Population and Recruitment

The study collected data from February 2022 to July 2022. Eligible participants reported having injected drugs in the last 90 days, aged ≥ 21 years, and living in Puerto Rico. The study recruited participants using respondent-driven sampling. We selected six initial participants (i.e., “seeds”) to begin coupon-based recruitment in Cidra (a rural municipality) and Caguas (a peri-urban municipality). The study identified seeds through street-based outreach. After the seeds provided informed consent and completed study requirements (i.e., a face-to-face interview in Spanish, dried blood spot collection for HIV, and HCV testing), they received three recruitment coupons to recruit the first wave of participants into the study. Subsequent waves of participants also received three recruitment coupons to recruit additional participants until the desired sample size of 150 was reached. Coupons contained the following information: a unique ID number, interview location, survey name (the target population and purpose of the study were not mentioned to prevent participants from being identified as people who use drugs), days and hours of study operation, and telephone number of recruitment and interview site). The coupons’ unique ID numbers enabled us to link recruiters and recruits.

2.2. Behavioral and Virological Assessments

Participants completed a screening assessment for eligibility that covered demographic information, injection drug use questions, and verification of injection track marks. After completing the screening assessment, the study obtained written informed consent from eligible participants, and the research assistant and study coordinator conducted interviews. Participants underwent a face-to-face interview, using a standardized questionnaire with sociodemographic and behavioral questions. The sociodemographic section contained questions related to age, gender, race, and housing situation. The behavioral questions requested information related to the following domains: substance use, drug injection history, injection practices, and injection-related HCV risk behaviors. Questions regarding injection-related HCV risk behaviors included questions such as the following: “Have you used a syringe that has been used by someone else?”, “Have you used a cotton, cooker, spoon, or water that has been used by someone else?”, “How many days in the past 30 days have you injected drugs?”, “How many times a day did you inject?” and “When you injected in the past 30 days, with how many people did you inject drugs that had been divided with a syringe?”.

Multiple-choice questions assessed the type of substance used and injected with that included heroin, cocaine, speedball, crack cocaine, xylazine, synthetic cannabinoids (commonly known in Puerto Rico as popurrí), and fentanyl, among other drugs. To assess injection assistance for another person who injects drugs, we asked participants, “Did you help to inject someone else?”, “How many people who inject drugs did you help to inject?”, and “Do you consider yourself a ganchero?”. A multiple-choice question that included places such as shooting galleries and abandoned buildings assessed drug injection locations. To assess belief regarding air-blowing, participants were asked whether the following statement was true or false: “You can avoid getting hepatitis C if you ‘air blow’ a syringe (i.e., take the plunger out of the barrel and blow air through the barrel a few times).”

After questionnaire completion, participants underwent counseling and testing for HIV and HCV. The study conducted HCV testing using dried blood spots (DBS). For DBS specimen samples, we collected capillary blood on a filter paper card (Whatman 903) by finger-prick using a single-use disposable lancet. The study sent DBS cards to the New York State Department of Health Wadsworth Center which tested DBS blood samples for HIV and HCV antibodies and HCV RNA. To assess HCV status, the laboratory tested first for HCV Ab. Participants who were positive for HCV Ab were tested for HCV RNA. The laboratory tested each DBS specimen for HCV antibodies using in-house-developed Luminex assays that screen for IgG antibodies. People who were HCV Ab positive were then tested for HCV RNA using the Aptima HCV Quant Dx test with modifications for DBS. The limit of detection for the HCV RNA assay with DBS is 250 IU/mL. Those positive for RNA were considered to have an active HCV infection. Research staff provided each participant with pre- and post-counseling, including risk reduction education, current available treatment options, and information on local services for follow-up diagnostic testing. To ensure participants’ confidentiality, their coupons, questionnaires, DBS cards, and test results were identified using a unique study identification number. Participants received a monetary incentive of $30 for completing the interview and $10 for each participant they referred who consented to participate in the study. The Institutional Review Board (IRB) at CUNY Graduate School of Public Health and Health Policy approved the study.

2.3. Measures

The sociodemographic variables used to investigate correlates of HCV antibody and RNA status included (1) age, (2) gender, (3) unhoused, (4) race, and (5) history of incarceration. The study categorized the variable age into three groups: (1) 23–35 years, (2) 36–45 years, and (3) 45–68 years. We defined unhoused as currently living on the streets, in a shelter, with friends or family, or in a car (yes or no). To assess their history of incarceration, we asked participants if they had ever been incarcerated (yes or no), and if yes, the number of times. Race is represented by (1) White, (2) Black, (3) American Indian, and (4) Mixed race.

The drug use and injection risk behavior variables used to investigate correlates of HCV infection were (1) years of injection, (2) type of drug used, (3) receptive sharing, (4) distributive sharing, (5) backloading, (6) engaging in caballo sessions, (7) injecting other PWID, (8) syringe air-blowing, (9) injecting in shooting galleries, (10) injecting in abandoned buildings, (11) ganchero, and (12) injection frequency. Years of injection referred to the number of years of injecting any illicit drug prior to the interview. The type of drug was defined by the kind of illicit drug injected. Receptive sharing was defined as using injection equipment in the last 12 months that had previously been used by another person. Distributive sharing was defined as giving used injection equipment to other people in the last 12 months. Backloading was defined as the use of a syringe to divide drugs. Participants were asked whether they had ever engaged in caballo sessions. Caballo refers to when PWID pool money to buy drugs and inject drugs together. Injecting another PWID was defined as a person who injects drugs and provides injection assistance to another person who injects drugs for free or a fee. A ganchero is a “hit doctor” who provides injection assistance for a fee (i.e., money or drug supply) to other PWIDs (Gelpí-Acosta et al., 2021). Syringe air-blowing refers to when a person who injects drugs blows air through a syringe (i.e., take the plunger out of the barrel and blow air through the barrel a few times) that had been used by someone else, to avoid contracting HCV. Shooting galleries are defined as locations typically managed by a person who uses drugs, where people go to inject drugs, and where they can purchase, rent, or borrow syringes and other injection equipment. Injecting in abandoned buildings or places is defined as injecting in an abandoned location that is not considered a shooting gallery. Injection frequency was measured by the number of days and times a given drug was injected in the past 30 days.

2.4. Statistical Analysis

The study identified associations between HCV seropositivity and participants’ selected behaviors and sociodemographic characteristics via bivariate and multivariate logistic regression. We selected independent variables based on previous research on risk factors associated with HCV among PWID and included demographic characteristics (i.e., gender, age, unhoused) and drug-use practices (i.e., frequency of drug use, types of drugs used, years of injection) (Belaunzarán-Zamudio et al., 2017; Guimarães et al., 2001; Hagan et al., 2001; Hahn et al., 2002; Kronfli et al., 2019; Pouget et al., 2011a; Spaulding et al., 2017). Bivariate analysis using simple logistic regression separately for HCV Ab and HCV RNA status determined the significant association with the selected independent variables. Variables with significant association (p ≤ 0.05) in the bivariate analyses were entered into two separate multiple logistic regression models to determine characteristics that predict HCV Ab status and again for HCV RNA status. The study performed all analyses using SPSS.

3. Results

The study recruited a total of 150 participants. Table 1 shows the characteristics of the sample. Most participants were male (89%); 72% considered themselves mixed race, 7% Black, 8% American Indian, and 13% White. The mean age of the participants was 43.1 years, with 64% of the study population being between 23 and 45 years old. The median number of years of injection was 17.8, and 45% were unhoused. The prevalence of HCV Ab was 73% (109/150) and HCV RNA was 53% (79/150). Regarding the frequency of drug injection in the past 30 days, 50.7% of the participants injected one to three times per day; 24.3% injected four to six times per day; and 25% injected seven or more times per day. The main drug injected was speedball (a mix of heroin and cocaine, 79%), followed by fentanyl alone (41%).

Table 1.

Sociodemographics and behavioral characteristics of people who inject drugs, n=150

Characteristic	N (%)
Gender
Female	17 (11.3)
Male	133 (88.7)
Age (SD)	43.1(10.5)
23–35	37 (24.7)
36–45	59 (39.3)
45–68	54 (36.0)
Race
White	19 (12.7)
Black	11 (7.3)
American Indian	12 (8.0)
Mixed Race	108 (72.0)
Unhoused, lifetime	112 (74.7)
Incarceration, lifetime	128(85.4)
Common Substance Use, lifetime
Crack	109 (72.7)
Synthetic Cannabinoids (i.e, K2)	68 (45.3)
Speedball	132 (88.0)
Heroin	120 (80.0)
Fentanyl	116 (77.3)
Xylazine	71 (47.3)
Years of injection
<=10 years	56 (37.3)
11–20 years	29 (19.3)
21+ years	65 (43.3)
Receptive syringe sharing, last 12months
Yes	45 (30.0)
No	105 (70.0)
Distributive syringe sharing, last 12 months
Yes	62(41.3)
No	88(58.7)
Receptive other injection equipment sharing, last 12 months
Yes	65(43.3)
No	85 (56.7)
Distributive other injection equipment sharing, last 12 months
Yes	77(51.3)
No	73 (48.7)
Ganchero (“hit doctor”)	47(31.3)
Injection risk behaviors, last 30 days
Injected drugs	148(98.6)
Injected in shooting galleries	98 (65.3)
Injected in abandoned places	32 (21.3)
Backloading	63(42.6)
Engaged in caballo sessions	80(54.1)
Injected other PWID	74 (50.0)
Daily injection frequency, last 30 days
1–3	75 (50.7)
4–6	36 (24.3)
7–10	23 (15.5)
11 or more	14 (9.5)
HIV/HCV status
HCV Antibody positive	109 (72.7)
HCV RNA positive	79 (52.7)
HIV Antibody positive	8 (5.3)

3.1. HCV Ab status and factors associated with HCV Ab

Bivariate and multivariable associations between participants’ characteristics and HCV antibody positivity are in Table 2. In the bivariate analysis, variables significantly associated with HCV antibody status included age, race, and incarceration. PWID identified as mixed race (OR=3.50, p=0.014), and Black (OR=11.11, p=0.035) were significantly more likely to be HCV Ab +. Also, participants ages 45–68 (OR=1.56, p=0.007) were significantly more likely to be HCV Ab + compared to those ages 23–35. Compared to those who have never been incarcerated, the odds of HCV Ab + were 7.73 (p= < .001) times higher among PWID who had been incarcerated three or more times. Drug use and some injection behaviors variables were significantly associated with increased HCV antibody positivity including 21 or more years of injection (OR=9.16, p= < .001), engaging in distributive sharing of other injection equipment with two or more people (OR=2.64, p=0.027), injecting 11 or more people in the last 30 days (OR=5.44, p=0.009), and believing that blowing air through syringes reduces HCV risk (OR=0.42, p=0.020). In the multivariable analysis, four factors remained significantly associated with HCV antibody positivity: having injected drugs 21 or more years (OR_a 10.76, p=0.001), being incarcerated ≥3 times (ORa_. 7.18, p=0.005), injecting 11 or more people in the last 30 days (OR_a 4.46, p=0.043), and correctly endorsing the belief that blowing air through used syringes will not reduce HCV risk (OR_a0.40, p=0.044).

Table 2.

Correlates of HCV Antibody positive serostatus among people who inject drugs, n=150

	Overall	HCV Antibody +	HCV Antibody -	Unadj.OR(95%CI)	p value	Adj.OR(95%CI)	p value
N(%)	150(100.0)	109(72.7)	41(27.3)
Gender
Female	17 (11.3)	10 (9.2)	7 (17.1)	ref	ref
Male	133 (88.7)	99 (90.8)	34 (82.9)	2.04(0.72–5.78)	0.180
Age (mean,sd)	43.1 (10.5)	44.5 (9.9)	39.6 (11.4)		0.011
23–35	37 (24.7)	21 (19.3)	16 (39.0)	ref	ref
36–45	59 (39.3)	43 (39.4)	16 (39.0)	2.05 (0.86–4.87)	0.105	0.94 (0.30–2.98)	0.921
45–68	54 (36.0)	45 (41.3)	9 (22.0)	1.56 (1.13–2.16)	0.007	0.93 (0.57–1.52)	0.771
Race
White	19 (12.7)	9 (8.3)	10 (24.4)	ref	ref	ref	ref
Black	11 (7.3)	10 (9.2)	1 (2.4)	11.11(1.18–104.81)	0.035	10.88 (0.69–171.53)	0.090
American Indian	12 (8.0)	8 (7.3)	4 (9.8)	2.22 (0.50–9.96)	0.188	1.29 (0.22–7.59)	0.777
Mixed Race	108(72.0)	82 (75.2)	26 (63.4)	3.50 (1.29–9.55)	0.014	2.36 (0.70–7.91)	0.165
Incarceration
None	22 (14.7)	10 (9.2)	12 (29.3)	ref	ref	ref	ref
1 to 2	61 (40.7)	41 (37.6)	20 (48.8)	2.46 (0.91–6.65)	0.076	2.37 (0.67–8.41)	0.180
3 or more	67 (44.7)	58 (53.2)	9 (22.0)	7.73 (2.59–23.10)	<.001	7.18 (1.83–28.19)	0.005
Common Substance Use, lifetime
Crack
No	41 (27.3)	33 (30.3)	8 (19.5)	ref	ref
Yes	109 (72.7)	76 (69.7)	33 (80.5)	0.56 (0.23–1.43)	0.191
Synthetic Cannabinoids (i.e, K2)
No	82 (54.7)	62 (56.9)	20 (48.8)	ref	ref
Yes	68 (45.3)	47 (43.1)	21 (51.2)	0.72 (0.35–1.48)	0.375
Speedball
No	18 (12.0)	10 (9.2)	8 (19.5)	ref	ref
Yes	132 (88.0)	99 (90.8)	33 (80.5)	2.40 (0.87–6.59)	0.089
Heroin
No	30 (20.0)	25 (22.9)	5 (12.2)	ref	ref
Yes	120 (80.0)	84 (77.1)	36 (87.8)	0.47 (0.17–1.32)	0.150
Fentanyl
No	34 (22.7)	27 (24.8)	7 (17.1)	ref	ref
Yes	116 (77.3)	82 (75.)	34 (82.9)	0.63 (0.25–1.57)	0.318
Xylazine
No	79 (52.7)	56 (51.4)	23 (56.1)	ref	ref
Yes	71 (47.3)	53 (48.6)	18 (43.9)	1.21(0.59–2.49)	0.606
Years of injection (mean, sd)	17.8(12.4)	20.8(11.9)			<.001
<=10 years	56 (37.3)	29 (26.6)	27 (65.9)	ref	ref	ref	ref
11–20 years	29 (19.3)	21 (19.3)	8 (19.5)	2.44 (0.93–6.44)	0.071	1.83 (0.55–6.05)	0.321
21+ years	65 (43.3)	59 (54.1)	6 (14.6)	9.16 (3.40–24.64)	<.001	10.76 (2.57–44.96)	0.001
Receptive syringe sharing
No	105 (70.0)	72 (66.1)	33 (80.5)	ref	ref	ref
Yes	45 (30.0)	37 (33.9)	8 (19.5)	2.12 (0.89–5.05)	0.090
Receptive other injection equipment sharing 1
0	85 (56.7)	58 (53.2)	27 (65.9)	ref	ref
1	27 (18.0)	19 (17.4)	8 (19.5)	1.11 (0.43–2.84)	0.835
2 or more	38 (25.3)	32 (29.4)	6 (14.6)	2.48 (0.93–6.64)	0.070
Distributive syringe sharing
0	73 (48.7)	47 (43.1)	26 (63.4)	ref	ref
1	25 (16.7)	19 (17.4)	6 (14.6)	1.75 (0.62–4.93)	0.289
2 or more	52 (34.7)	43 (39.4)	9 (22.0)	2.64 (1.11–6.27)	0.027
Ganchero (hit doctor)
No	103 (68.7)	70 (64.2)	33 (80.5)	ref	ref
Yes	47 (31.3)	39 (35.8)	8 (19.5)	2.30 (0.97–5.46)	0.060
Injection risk behaviors, last 30 days
Injected in abandoned places
No	118 (78.7)	90 (82.6)	28 (68.3)	ref	ref
Yes	32 (21.3)	19 (17.4)	13 (31.7)	0.46 (0.20–1.04)	0.061
Engaged in caballo sessions
0	68 (45.9)	55 (50.9)	13 (32.5)	ref	ref
1–10	51 (34.5)	33 (30.6)	18 (45.0)	0.46 (0.20–1.04)	0.062
11 or more	29 (19.6)	20 (18.5)	9 (22.5)	0.56 (0.21–1.48)	0.240
Injected other PWID
0	74 (50.0)	47 (43.5)	27 (67.5)	ref	ref	ref	ref
1–10	43 (29.1)	33 (30.6)	10 (25.0)	1.92 (0.83–4.49)	0.130	1.76 (0.61–5.10)	0.297
11 or more	31 (20.9)	28 (25.9)	3 (7.5)	5.44 (1.51–19.95)	0.009	4.46(1.05–18.95)	0.043
Syringe-air blowing reduces HCV 3
Incorrect answer	82 (54.7)	66 (60.6)	16 (39.0)	ref	ref	ref	ref
Correct answer	68(45.3)	43(39.4)	25(61.0)	0.42(0.20–0.87)	0.20	0.40 0.16–0.98)	0.44

^1.Number of people from whom other injection equipment was received.

^2.Number of people to whom other injection equipment was distributed.

^3.Participants were asked the statement “You can avoid getting hepatitis C if you “air blow” a syringe was true or false. The correct answer is “false”, indicating that syringe-air blowing is an unsafe practice.

3.2. HCV RNA status and factors associated with HCV RNA

Table 3 shows bivariate and multivariable associations between variables and HCV RNA outcomes. In the bivariate analysis, detectable RNA was significantly associated with being male (OR=3.01, p=0.049), older age (45–68 years old; OR=1.69, p=0.001), injecting drugs for 21 years or more (OR=5.99, p= < .001), history of incarceration (1–2 times incarcerated; OR=4.45, p=0.016), being Black (OR=12.60 ,p=0.007) or mixed race (OR=3.50, p=0.024), and having injected 11 or more people in the past 30 days (OR=3.81, p=0.006). Compared to those who have never been incarcerated, being incarcerated three or more times also increased the odds of testing HCV RNA+ (OR=9.20, p= < .001). In the multivariable model, the following variables remained significantly associated with testing HCV RNA +: injecting for 21 years or more (OR_a=4.29, p=0.016), being Black (OR_a=16.12, p=0.016), and having been incarcerated 1–2 times (OR_a= 8.40, p=0.006) and 3 or more times (OR_a=15.13, p=0.001)

Table 3.

Correlates of positive RNA among people who inject drugs, n=150

	Overall	HCV RNA +	HCV RNA-	Unadj.OR(95%CI)	p value	Adj.OR(95%CI)	p value
N (%)	150(100.0)	79(52.7)	71(47.3)
Gender
Female	17 (11.3)	5 (6.3)	12 (16.9)	ref	ref
Male	133 (88.7)	74 (93.7)	59 (83.1)	3.01 (1.004–9.02)	0.049	0.73 (0.18–2.92)	0.657
Age (mean, sd)	43.1 (10.5)	45.8 (9.9)	40.1 (10.4)		0.001
23–35	37 (24.7)	13(16.5)	24 (33.8)	ref	ref	ref	ref
36–45	59 (39.3)	27(34.2)	32 (45.1)	1.59 (0.67–3.63)	0.305	0.65(0.20–2.13)	0.480
45–68	54 (36.0)	39 (49.4)	15 (21.1)	1.69 (1.25–2.28)	0.001	1.29(0.82–2.01)	0.272
Race
White	19 (12.7)	5 (6.3)	14 (19.7)	ref	ref	ref	ref
Black	11 (7.3)	9 (11.4)	2 (2.8)	12.60 (2.00–79.44)	0.007	16.12 (1.69–153.73)	0.016
American Indian	12 (8.0)	5 (6.3)	7 (9.9)	2.00 (0.43–9.29)	0.376	1.11 (0.19–6.55)	0.906
Mixed race	108 (72.0)	60 (75.9)	48 (67.6)	3.50 (1.18–7-10.40)	0.024	2.25 (0.63–8.00)	0.211
Unhoused, lifetime
No	38 (25.3)		25 (31.6)	13 (18.3)	ref	ref
Yes	112 (74.7)		54 (68.4)	58 (81.7)	0.48(0.23–1.04)	0.063
Incarceration
None	22 (14.7)	4 (5.1)	18 (25.4)	ref	ref	ref	ref
1 to 2	61 (40.7)	30 (38.0)	31 (43.7)	4.35 (1.32–14.37)	0.016	8.40 (1.82–38.69)	0.006
3 or more	67 (44.7)	45 (57.0)	22 (31.0)	9.20 (2.78–30.48)	<.001	15.13 (3.20–71.64)	<.001
Common Substance Use, lifetime
Crack
No	41 (27.3)	22 (27.8)	19 (26.8)	ref	ref
Yes	109 (72.7)	57 (72.2)	52 (73.2)	0.95 (0.46–1.94)	0.947
Synthetic
Cannabinoids(i.e, K2)
No	82 (54.7)	46 (58.2)	36 (50.7)	ref	ref
Yes	68 (45.3)	33 (41.8)	35 (49.3)	0.74(0.39–1.41)	0.356
Speedball
No	18 (12.0)	9 (11.4)	9 (12.7)	ref	ref
Yes	132 (88.0)	70 (88.6)	62 (87.3%)	1.13(0.42–3.02)	0.809
Heroin
No	30 (20.0)	17 (21.5)	13 (18.3)	ref	ref
Yes	120 (80.0)	62 (78.5)	58 (81.7)	0.82(0.37–1.83)	0.624
Fentanyl
No	34 (22.7)	20 (25.3)	14 (19.7)	ref	ref
Yes	116 (77.3)	59 (74.7)	57 (80.3)	0.72(0.33–1.57)	0.415
Xylazine
No	79 (52.7)	40 (50.6)	39 (54.9)	ref	ref
Yes	71 (47.3)	39 (49.4)	32 (45.1)	1.19(0.62–2.26)	0.599
Years of injection(mean, sd)	17.8 (12.4)	22.4 (12.0)	12.7 (10.7)		<.001
<=10 years	56 (37.3)	17 (21.5)	39 (54.9)	ref	ref	ref	ref
11–20 years	29 (19.3)	15 (19.0)	14 (19.7)	2.46 (0.98–6.20)	0.057	2.31(0.72–7.38)	0.158
21+ years	65 (43.3)	47 (59.5)	18 (25.4%)	5.99(2.73–13.16)	<.001	4.29 (1.31–14.06)	0.016
Receptive syringe sharing, last 12months
No	105 (70.0)	51 (64.6)	54 (76.1)	ref	ref
Yes	45 (30.0)	28 (35.4)	17 (23.9)	1.74 (0.85–3.56)	0.127
Injected other PWID
0	74 (50.)	35 (44.9)	39 (55.7)	ref	ref	ref	ref
1–10	43 (29.1)	19 (24.4)	24 (34.3)	0.88 (0.41–1.87)	0.738	0.78 (0.31–1.98)	0.599
11 or more	31 (20.9)	24 (30.8)	7 (10.0)	3.81 (1.47–9.90)	0.006	5.47(1.70–17.60)	0.004

4. Discussion

The results from this research indicate that older age, more years of drug injection, injecting others, a history of incarceration, and identifying as Black were all significantly associated with HCV exposure and HCV RNA. In addition, believing that blowing air through a used syringe could prevent HCV exposure was associated with HCV antibody positivity in the adjusted analysis. Although distributive and receptive sharing of injection paraphernalia have been strongly associated with HCV Ab infection among PWID, in this study, only receptive sharing of injection paraphernalia (excluding syringes) in the bivariate analysis was found to be significantly associated with HCV Ab (Abadie et al., 2016; Reyes et al., 2006). This finding may be a consequence of underreporting due to the fear of stigma associated with sharing injection equipment on the island. Previous epidemiological studies conducted in Puerto Rico have also reported speedball use as a correlate to HCV Ab among Puerto Rican PWID (Colón-López et al., 2022; Reyes et al., 2006). Although participants who reported speedball use had odds of HCV Ab two times higher than those who reported never using a speedball, we did not find a significant association. Increased risk for HCV among unhoused PWID has also been documented (Pouget et al., 2011b). While the vast majority of participants reported having been unhoused, lack of housing was not found to be a significant driver of HCV infections.

Our findings suggest that prisons in Puerto Rico are high-risk environments for HCV and possibly for other blood-borne infections. Studies in Russia, Brazil, and North America have identified prisons as a high-risk environment for HCV and HIV transmission since drug use and sharing of contaminated drug injection equipment is common in these settings (Belaunzarán-Zamudio et al., 2017; Guimarães et al., 2001; Kronfli et al., 2019; Spaulding et al., 2017). This finding is consistent with findings from a qualitative study conducted among migrant Puerto Rican PWIDs in New York, who reported that unsafe practices such as injection equipment sharing are common in corrections facilities in Puerto Rico (Gelpí-Acosta et al., 2019). Therefore, prisons could be strategic venues for screening and treating PWID while they are incarcerated. Additionally, our results demonstrate that there is an association between the belief that blowing air through a syringe that has been previously used by others and the reduced risk of HCV exposure. This finding is partly aligned with a research study of Puerto Ricans who were born in Puerto Rico and began injecting drugs in Puerto Rico and later migrated to New York City (Gelpí-Acosta et.al, 2019). These migrants hold the same beliefs and engage in similar risky injection practices, although they are more applicable to HIV in the case of this study. Gelpí-Acosta et. al. (2019) found that Puerto Rican PWID who migrated from Puerto Rico to New York City believed that water-rinsing (i.e., cleaning used syringes with water, commonly known in Puerto Rico as chambonear) and air-blowing reduced HIV transmission. Furthermore, studies conducted among Puerto Rican PWID living in Puerto Rico and New York have shown that PWID in Puerto Rico are more likely to die from an HIV-related condition and engage in HIV and HCV-conducive risk behaviors (e.g., injecting in shooting galleries and sharing injection equipment) than their counterparts in New York (Deren et al., 2004; Finlinson et al., 2006; Mino et al., 2011). Moreover, PWID in Puerto Rico are less likely to have access to drug treatment services and syringe service programs than Puerto Rican PWID in New York (Finlinson et al., 2000; Mino et al., 2011).

There were trending correlations between being HCV Ab+ and engaging in multiple caballo sessions. Fifty-four percent of participants reported having engaged in caballo sessions, and 31.3% reported being a ganchero. Previous qualitative studies among Puerto Rican PWID conducted in New York and Puerto Rico have suggested the latter as risk factors for HCV (Abadie & Dombrowsky, 2020; Gelpí-Acosta et al., 2021). Since experiences of drug use are partly informed by social and contextual factors (Zinberg, 1986), people who use drugs in Puerto Rico are equipped in different ways to manage the negative consequences associated with this behavior. Poverty among Puerto Rican PWID increases the risks of being a ganchero, sharing injection equipment, and engaging in caballo sessions. For example, a drug injector with very limited income could resort to caballo sessions as a way to have access to drugs. Likewise, a person who injects drugs could become a ganchero as a means to generate income or secure access to drugs provided by those who receive their services.

Indeed, most PWID in Puerto Rico live in a context plagued with poverty and its associated vulnerabilities. Furthermore, they experience the scarcity of HCV prevention and health-related services daily, especially in rural communities. Several scholars have documented the role of social determinants of health as important factors predicting the chances of acquiring infectious diseases such as HCV (Abdul-Quader et al., 2013; Kim et al., 2019; Walters et al., 2023; Wilder et al., 2016; Williams et al., 2019). Social determinants of health are considered social and physical environments that make individuals more vulnerable to engaging in unsafe behaviors (Rourke et al., 2011; Walters et al., 2023; Williams et al., 2019). Social determinants such as poverty, race, and ethnicity, among others, affect health outcomes and increase a person’s chances of becoming infected with an infectious disease such as HCV (Edwards et al., 2014; United States Department of Health and Human Services Office of Minority Health, 2022.; Walters et al., 2023; Wilder et al., 2016; Williams et al., 2019). For instance, in the USA, HCV is more prevalent among Latinx and Blacks than Whites (Kim et al., 2019; Wilder et al., 2016). Among Latinx in the USA, Puerto Ricans have a higher rate of HCV prevalence and HCV-related mortality than other Latinx subgroups (Kim et al., 2019). Importantly, findings from this study also suggest that Black Puerto Ricans may be at higher risk of developing chronic HCV. Research is needed to understand the impact of race on HCV exposure.

Arguably, the elevated prevalence of HCV infections could be indicative of the low coverage of harm reduction and treatment services in Puerto Rico. Research studies have shown a positive association between the availability and coverage of harm reduction programs and HCV prevalence (Abdul-Quader et al., 2013; Platt et al., 2018). Countries that have invested in treatment programs for PWID and provide sustainable access to SSPs and opioid agonist therapy have been effective in reducing the prevalence of HCV (Abdul-Quader et al., 2013; Dhiman, et al.2021; Platt et al., 2018). Showcasing the scarcity of prevention in Puerto Rico, harm reduction programs such as SSPs are primarily funded by private foundations and donors, not by the government (Stone & Shirley-Beaven, 2018). Additionally, highly effective antiviral medicines can cure HCV in Puerto Rico, but access to treatment and diagnosis is low among HCV-infected PWID (Aponte-Meléndez et al., 2023), despite well-documented worldwide evidence that this population can be successfully treated (Dhiman et al., 2021; Eckhardt et al., 2022; Grebely et al., 2018; Janjua et al., 2019). The evidence indicates that negative experiences in healthcare settings; financial limitations, transportation, and insurance problems; lack of knowledge regarding treatment availability; low HCV risk perception; and fear of treatment side effects are barriers to seeking treatment in Puerto Rico (Aponte-Meléndez et al., 2023). Greater efforts are needed to enhance surveillance, prevention, testing, diagnosis, and treatment.

To date, most data on HCV prevalence among Puerto Rican PWID are the results of a few epidemiological studies, such as this one, conducted by independent scientists, and have mainly focused on a few municipalities. To develop effective prevention and treatment programs, a better understanding of the trends of HCV infections among people who use drugs countrywide is necessary. Additionally, the lack of financial investment in HCV prevention programs and PWID-centered treatment in Puerto Rico remains a major barrier to reducing HCV prevalence and saving the lives of many people who use drugs and are infected with HCV. The HCV epidemic among PWIDs in Puerto Rico has long been neglected, and little funding is available for HCV education and prevention programs. Although Puerto Rico lifted substance use abstinence requirements for HCV treatment (Center for Health Law and Policy Innovation, 2020), HCV elimination will not be possible without the efficient and sustainable allocation of funds to screen, diagnose, treat, and prevent new infections among PWID. A key to HCV elimination is funding community-based organizations, such as SSPs, that are closely connected to and have trusting relationships with this highly stigmatized community. However, in Puerto Rico, there is a need to implement appropriate funding mechanisms (National Minority AIDS Council, 2012; White House Office of National AIDS Policy, 2010). For decades, government funding for HIV- and drug-related services has relied on the deliverable-based approach, where community-based organizations are required to provide services first (i.e., meet deliverables) before being reimbursed (National Minority AIDS Council, 2012). Because community-based organizations are notoriously underfunded, this deliverable-based mechanism is a barrier to expanding community-based models of HCV care, especially to PWID in rural communities. Additionally, payment delays are normative, and this poses an added barrier to access to HIV (National Minority AIDS Council, 2012) and HCV care in Puerto Rico. Recent policy changes loosening restrictions on substance use and prescriber requirements offer a new opportunity for treating PWID (Administración de Seguros de Salud, 2023). However, these policies may not be sufficient to increase access to HCV treatment, as drug-related stigma is a major disincentive to pursuing treatment (Aponte-Meléndez et al., 2023).

Investing in HCV micro-elimination programs and offering PWID co-located HCV testing and treatment at SSPs is critical for minimizing transmission and HCV-related morbidity and mortality. A core principle of SSPs is to meet people where they are in their drug-use experience. Expanding access to HCV care for PWID in Puerto Rico within this framework may allow for more effective engagement and retention in HCV care. SPP-based HCV care has been proven to be more effective for increasing engagement and treatment among people in active injection use than clinic-based HCV care in high-income countries (Eckhardt et al., 2022; Kapadia et al., 2023; Muncan et al., 2021). The provision of non-stigmatizing, low-threshold, and PWID-centered services by SSPs may be the key to increasing HCV treatment for this population (Eckhardt et al., 2022; Kapadia et al., 2023). Providing access to HCV care for people who use drugs beyond traditional healthcare settings and opioid antagonist therapy programs (OPT) will be essential given the low enrollment and attrition in OPT on the island, especially in rural areas. Additionally, contextual and culturally appropriate HCV services tailored to the needs of high-risk populations such as PWID and the incarcerated population will be essential to achieving HCV elimination. Innovative and flexible interventions, such as the delivery of HCV care via telemedicine and SSPs mobile units, may be crucial to reaching isolated and marginalized PWID in rural communities. Research efforts will be crucial to assessing the effectiveness and sustainability of these alternative models of care.

This study has several notable strengths and limitations. This study is the first to examine risk factors associated with HCV RNA among PWID in Puerto Rico. This study, however, is limited in its sample size and geographic region, limiting its generalizability. Additionally, drug use and risk behaviors data relied on self-reports, which are known to suffer from social-desirability bias. We trained our research staff to be non-judgmental and provide a comfortable environment, so the participants would be more likely to give honest responses.

5. Conclusions

Our study suggests that incarceration, age, helping other people to inject, more years of injection, being Black, and belief in the syringe air blowing activity increase HCV risks among PWID in Puerto Rico. The combination of increasing access to medical care and developing interventions that reduce individual risks as well as risk environments will help decrease HCV among PWID. Efficient, sustainable, low-threshold and destigmatized access to HCV treatment is crucial to reduce deaths and the disproportionate high rates of HCV among PWID in Puerto Rico.

Highlights.

• Hepatitis C Antibody and RNA are prevalent among people who inject drugs in Puerto Rico.

• HCV was associated with injecting others, being Black, older age, and years of injection.

• Incarceration was significantly associated with HCV antibody and RNA.

• Syringe air-blowing appears to increase risk of HCV exposure.

• Community-based and PWID-centered models of care are crucial to reduce HCV prevalence in Puerto Rico.