High Seroprevalence of Hepatitis C Virus Among Cisgender Women Who Exchange Sex in the Seattle,Washington Area

Abstract

Background:

Injection drug use (IDU) is a risk factor for hepatitis C virus (HCV) acquisition and occurs disproportionately among women who exchange sex (WES). However, little is known about HCV epidemiology in this population. We estimated HCV seroprevalence, identified correlates of HCV seropositivity, and characterized social networks by HCV serostatus and IDU history among WES in the Seattle, Washington, area.

Methods:

This was a secondary analysis of data from the 2016 National HIV Behavioral Surveillance survey in the Seattle, Washington area, a cross-sectional survey that used respondent-driven sampling (RDS) to enroll WES for money or drugs (N = 291). All participants were offered rapid HCV-antibody testing. We estimated HCV seropositivity and used log regression methods to estimate crude and adjusted prevalence ratios (PRs) for correlates of HCV seropositivity among WES. Using RDS recruitment chain data, we computed homophily indices to estimate the extent to which participants were likely to recruit another participant with the same HCV serostatus and IDU history.

Results:

In the study sample of WES in the Seattle, Washington area, 79% reported lifetime IDU and 60% were HCV seropositive. HCV seropositivity was strongly associated with ever injecting drugs (PR_adj: 7.7 [3.3, 18.0]). The RDS homophily scores for HCV seropositivity (0.07) and ever injecting drugs (0.02) suggested that participants did not tend to recruit others with the same characteristics beyond what would be expected by chance.

Conclusion:

Among this sample of WES in Seattle, Washington area, HCV seroprevalence was high and strongly associated with a history of IDU. The high burden of HCV among WES suggests this marginalized group would benefit from additional harm reduction services and targeted HCV treatment campaigns to reduce forward transmission. We saw little evidence of preferential recruitment among WES who were HCV seropositive or reported a history of IDU, suggesting the potential futility of peer-based referrals for HCV treatment.

Keywords

women who exchange sex hepatitis C injection drug use sex workers sex exchange

Introduction

Injection drug use (IDU) is common among women who exchange sex (WES) globally.^1
–4 Research in Russia found that 22% of WES report lifetime IDU,³ while more recent research in Iran⁴ and Kenya¹ found that over 47% and 70% prevalence of lifetime use, respectively. Studies from international settings have also documented that sex exchange is associated with hepatitis C virus (HCV) acquisition,^5
–7 likely driven by high rates of co-occurring IDU. However, sexual exposure facilitated by the presence of sexually transmitted infections and multiple sexual partners, as well as non-injection drug-related risks, also contributes to HCV risk.^5
–7 Among people who inject drugs (PWID), women are more likely than men to engage in risky injection behaviors such as sharing injection equipment and having drugs prepared by another person,^8,9 and are less likely to be treated for HCV.¹⁰ Such findings, taken with multiple recent HIV outbreaks among PWID in the United States,^11
–15 highlight the vulnerability of WES who inject drugs to bloodborne pathogens, including HCV. While there is recent work on the epidemiology of HCV among LGBTQ+ populations in the United States (eg, those that share an increased risk of bloodborne pathogens),^16,17 we know of no such work focusing on WES. Most research on the epidemiology of HCV among WES has been conducted among populations outside of the United States.

Direct-acting antivirals (DAAs) have revolutionized the HCV landscape, allowing for shorter, safer, and more effective treatment than interferon therapy.^18
–20 DAAs not only provide an opportunity to durably cure HCV but also prevent transmission among WES and other groups at risk through a treatment as prevention approach.^21,22 To ensure that HCV treatment and prevention strategies are successful among WES in the United States, additional work is needed to better understand the interplay between IDU, sex exchange, and HCV risk, as well as strategies for linkage to care in this population.^5,6,23 Previous studies among PWID have found peer referral to be an effective means of linking PWID with HCV care,^24,25 but most of this research has been conducted outside of the United States, and to our knowledge, none has focused on WES.

To address these knowledge gaps, we used data from a cross-sectional survey of WES in the Seattle, Washington area to (1) estimate the prevalence of HCV seropositivity, (2) identify correlates of HCV seropositivity, and (3) characterize social networks among WES by analyzing participant recruitment trees and measuring whether and to what extent individuals were likely to recruit others with the same HCV serostatus or IDU history.

Methods

Study Sample

The present study used cross-sectional data from the 2016 National HIV Behavioral Surveillance (NHBS) survey in the Seattle area conducted by Public Health—Seattle & King County (PHSKC). The survey was conducted during the NHBS-HET cycle, which focuses on low-income people at higher risk for HIV through heterosexual sex. In 2016, 5 NHBS sites (including Seattle) were selected to participate in a demonstration project that focused on WES. The survey eligibility criteria were similar to the parent NHBS-HET survey but differed in 2 ways: low-income status was not an eligibility criterion and only cisgender women were eligible. Specifically, potential participants were eligible if they (1) had a valid survey coupon, (2) had not already participated in the 2016 NHBS survey, (3) lived in King County, Washington or Snohomish County, Washington, (4) were 18 to 60 years old at the time of their study visit, (5) reported having vaginal or anal sex with a person of the opposite sex in the past 12 months, (6) were cisgender women, and (7) were able to complete the NHBS survey in English or Spanish. Women who did not report exchanging sex for money or drugs were eligible for the survey. However, we only included the subset of women who reported exchanging sex in this analysis.

Between June and December 2016, staff interviewed participants at a field site located close to downtown Seattle, Washington and at a homeless service center in North Seattle. Project leadership suspended the latter site after a short time due to limited recruitment success. PHSKC staff recruited participants using respondent-driven sampling (RDS),²⁶ a recruitment method designed to study small, marginalized populations. In accordance with RDS methods,²⁶ project staff selected initial “seed” participants. Eligible participants received $50 for completing the survey and having a rapid HIV test, plus $10 for each additional participant they referred (adjusted to $20 midway through the recruitment process). To focus recruitment on WES, respondents who completed the survey and reported exchanging sex for money or drugs could recruit up to 5 other individuals. Participants were linked to their recruiter by a unique identifier associated with the recruitment coupon. Participants who did not report exchanging sex in the last 12 months could complete the survey and receive testing but could not recruit other participants.

Data Collection

After obtaining informed consent, PHSKC staff conducted face-to-face structured surveys with participants using portable computers. Project coordinators trained staff to administer surveys in a standardized manner, and question logic was applied automatically by the survey computer interface. Staff members administered both Core and Local surveys. The Core survey was common to all NHBS sites and consisted of demographic, behavioral, and health questions. The Local survey was administered after completion of the Core survey and addressed partner violence, sexual practices, condom use, intentions to get pregnant, and interactions with local service agencies. Core and Local survey questions used for the present study are detailed in the “Measures” subsection. Staff offered OraQuick^® (OraSure Technologies, Inc., Bethlehem, PA, USA) rapid HIV and HCV testing upon completing surveys and uploaded test results to a secure data transfer portal. Interview staff collected dried blood spot specimens from participants with positive rapid HIV tests for confirmatory Western Blot testing at a partner laboratory. At the time of testing, participants received pre- and post-test counseling, with referrals as needed. Including the interview and optional testing, visits lasted 60 to 90 minutes.

Measures

Reported sex exchange in the last 12 months was determined in the Core NHBS survey with the question, “in the past 12 months, did [a casual sex partner] give you money or drugs to have sex with him?” Participants who did not report ≥1 casual sex exchange partner in the Core survey were asked in the Local survey, “in the past 12 months, did one or more men give you money or drugs to have vaginal, oral or anal sex with them?” Participants who answered “yes” to either question were included in the present analysis.

The primary outcome of interest was HCV seropositivity, measured by rapid HCV-antibody test result. Study staff also collected survey data on history of HCV infection (i.e., “Has a doctor, nurse or other healthcare provider ever told you that you had hepatitis C?”) and treatment (i.e., “Have you ever taken medicine to treat your hepatitis C infection?”).

The NHBS Core and Local surveys included measures of several exposures of interest. We organized these into demographic, behavioral, health, and experiential characteristics (Supplemental Table S1). Unless otherwise noted, we treated exposure variables in analyses as they were collected by PHSKC staff (ie, analyses used data exactly as they were originally coded) and were specific to the 12-month period preceding a study visit.

Analysis

Our analytic sample included women who reported exchanging sex for money or drugs in the last 12 months, determined by the data collected in the Local NHBS survey. We conducted statistical analyses in the RStudio environment.²⁷ Using the EpiR package,²⁸ we estimated HCV seroprevalence among WES. We used bivariate log binomial regression models to estimate prevalence ratios (PRs) for HCV seropositivity comparing individuals by demographic, behavioral, health, and experiential characteristics previously described. These variables were selected from the available dataset because they aligned with Social Determinants of Health defined by the US Department of Health and Human Services²⁹ and/or were found to be potentially associated with HCV following a literature review.^1
–6 We included correlates found to be significantly associated with HCV seropositivity in bivariate analyses (α ≤ .05) in a multivariate model to estimate adjusted PRs (PR_adj), but omitted those that were either only available for participants who injected drugs or had >5% missingness. We planned to use log binomial regression for the multivariate model. However, this model did not converge, so we opted for Poisson regression, a method to estimate PRs that is appropriate in this case.³⁰ Using RDS Analysis Tool³¹ we analyzed participant recruitment trees by calculating homophily indices.³² Using RDS Analyst,³³ we visualized these recruitment trees.

RDS analytic methods can include an adjustment for the recruitment method,³⁴ an approach that is useful when attempting to generalize to the population of interest. However, based on the high frequency of reported histories of IDU in the sample, we determined that it was unlikely that the sample was representative of all WES in the Seattle area. Therefore, we analyzed the data as a convenience sample, as has been done previously.¹⁰

Results

In total, 383 participants completed the 2016 NHBS Seattle, Washington area survey, 298 of whom were cisgender women and reported exchanging sex for money or drugs in the past 12 months. Of these 298 WES, 7 were excluded because they did not complete HCV serologic testing. This yielded an analytic sample of 291 WES. RDS referral began with 21 seeds, 8 of which resulted in at least 1 referral and were considered productive. Excluding the seed participants, among the productive seeds, the median number of participants in a referral chain was 9 (Interquartile range [IQR]: 7, 40). There were 16 waves of referral.

Most participants were White (65%), at least 40 years old (65%), and born in the United States (96%, Tables 1 and 2). Street-based sex exchange was the most common means of meeting clients (61%), followed by public places (51%), through a drug dealer or drug house (50%), and through family or friends (50%). Ten (3%) participants were living with HIV; 7 self-reported positive HIV status, and 3 had a new HIV diagnosis through NHBS. Challenging socioeconomic circumstances were common; half (50%) of participants were unstably housed or experiencing homelessness, 67% attained a high school degree/general education degree (GED) at most, and 79% reported an annual income of under $20 000.

Table 1.

Demographic Characteristics With Log Binomial Regression Prevalence Ratio Estimates for Hepatitis C Seropositivity Among Cisgender Women Who Exchange Sex, Seattle, Washington Area (National HIV Behavioral Surveillance, HET4, 2016) N = 291.

Characteristic	HCV seropositive^# (N = 176, 60%)	HCV seronegative^# (N = 115, 40%)	Total	Prevalence ratio (95% CI)	P-value
Characteristic	N (column %)			Prevalence ratio (95% CI)	P-value
Age
18-29	10 (6%)	17 (15%)	27 (9%)	Referent
30-39	41 (23%)	35 (30%)	76 (26%)	1.46 (0.85, 2.48)	.163
≥40	125 (71%)	63 (55%)	188 (65%)	1.80 (1.09, 2.97)	.022
Race and ethnicity^†
American Indian and Alaska Native	43 (24%)	22 (19%)	65 (22%)	1.12 (0.92, 1.38)	.264
Asian	4 (2%)	5 (4%)	9 (3%)	0.73 (0.35, 1.52)	.400
Black and African American	36 (20%)	42 (37%)	78 (27%)	0.70 (0.54, 0.91)	.007
Hispanic or Latinx	18 (10%)	13 (11%)	31 (11%)	0.96 (0.70, 1.31)	.777
Native Hawaiian and Pacific Islander	6 (3%)	0	6 (2%)	NA
White	122 (69%)	67 (58%)	189 (65%)	1.22 (0.99, 1.51)	.066
Country of birth
United States	168 (95%)	110 (96%)	278 (96%)	Referent
Another country	8 (5%)	4 (3%)	12 (4%)	1.10 (0.63, 1.66)	.640
Primary language
English	147 (84%)	106 (92%)	253 (87%)	Referent
Spanish	29 (16%)	9 (8%)	38 (13%)	1.31 (1.07, 1.61)	.009
Housing status
Stable	88 (50%)	56 (49%)	144 (49%)	Referent
Unstable or homeless	88 (50%)	59 (41%)	147 (51%)	0.98 (0.81, 1.18)	.828
Relationship status
Not married or no live-in partner	157 (89%)	100 (87%)	257 (88%)	Referent
Married or with live-in partner	19 (11%)	15 (13%)	34 (12%)	0.91 (0.67, 1.25)	.578
Highest level of education
High school, GED or less	126 (72%)	69 (60%)	195 (67%)	Referent
Two-year college, technical school, some college	47 (27%)	40 (35%)	87 (30%)	0.84 (0.67, 1.04)	.111
Four-year college and beyond	3 (2%)	6 (5%)	9 (3%)	0.52 (0.20, 1.31)	.163
Income (annual)
Less than $20 000	136 (77%)	94 (82%)	230 (79%)	Referent
$20 000-$39 999	26 (15%)	12 (10%)	38 (13%)	1.16 (0.91, 1.47)	.236
$40 000 and higher	14 (8%)	9 (8%)	23 (8%)	1.03 (0.73, 1.45)	.869
Neighborhood/suburb
Seattle	164 (93%)	105 (91%)	269 (92%)	Referent
South King Co. Communities	6 (4%)	5 (3%)	11 (4%)	0.89 (0.52, 1.55)	.691
North King Co. and East Side King Co. Communities	2 (1%)	3 (3%)	5 (2%)	0.66 (0.22, 1.93)	.443
Snohomish County	2 (1%)	2 (2%)	4 (1%)	0.82 (0.31, 2.20)	.693

Abbreviations: Co., County; GED, general education degree; HCV, hepatitis C virus; HET4, 4^th cycle of NHBS that focused on persons at increased risk of HIV through heterosexual contact; PR, prevalence ratio.

HCV serostatus determined by HCV-antibody test result or self-report of HCV seropositivity; ^†Individual participants could indicate multiple categories. Participants who reported each category are included in each of the corresponding groups; some individuals appear in multiple cells and PR estimates. For each group, the referent is all other participants who are not part of that group.

Table 2.

Substance Use, Sex Exchange, and Health Characteristics With Log Binomial Regression Prevalence Ratio Estimates for Hepatitis C Seropositivity Among Cisgender Women Who Exchange Sex, Seattle, Washington Area (National HIV Behavioral Surveillance, HET4, 2016) N = 291.

Characteristic	HCV seropositive^# (N = 176, 60%)	HCV seronegative^# (N = 115, 40%)	Total	Prevalence ratio (95% CI)	P-value
Characteristic	N (column %)			Prevalence ratio (95% CI)	P-value
Substance use
Injection drug use, ever	170 (97%)	60 (52%)	230 (79%)	7.51 (3.50, 16.13)	<.000001
Age at injection debut (years)^‡
<18	61 (36%)	14 (23%)	75 (33%)	1.31 (1.01, 1.71)	.040
19-29	77 (45%)	27 (45%)	104 (45%)	1.20 (0.92, 1.56)	.183
>30	26 (15%)	16 (27%)	42 (18%)	Referent
Drugs injected most often^{‡ ¶}
Heroin/opioids	70 (41%)	14 (27%)	84 (37%)	1.67 (1.01, 2.73)	.045
Methamphetamine	8 (5%)	8 (13%)	16 (7%)	Referent
Both	53 (31%)	16 (27%)	69 (30%)	1.54 (0.93, 2.55)	.097
Neither	39 (23%)	22 (37%)	61 (27%)	1.28 (0.76, 2.16)	.359
Drugs used but not injected^¶
Heroin/opioids	41 (23%)	16 (14%)	57 (20%)	1.16 (0.84, 1.61)	.378
Methamphetamine	28 (16%)	18 (16%)	46 (16%)	0.98 (0.68, 1.42)	.917
Both	69 (39%)	39 (34%)	108 (37%)	1.03 (0.75, 1.41)	.859
Neither; other drugs only	19 (11%)	31 (27%)	50 (17%)	0.61 (0.39, 0.96)	.034
No drug use in the past 12 months	18 (10%)	11 (10%)	29 (10%)	Referent
Shared syringes^‡,¶	74 (44%)	20 (33%)	94 (31%)	1.12 (0.96, 1.30)	.157
Shared other injection equipment^{‡ ¶}	99 (58%)	27 (45%)	126 (55%)	1.15 (0.98, 1.35)	.084
Sex exchange
Vaginal sex with client(s)^¶	171 (97%)	112 (97%)	293 (97%)	1.06 (0.55, 2.02)	.866
Anal sex with client(s)^¶	80 (45%)	35 (30%)	115 (40%)	1.28 (1.07, 1.54)	.008
Condomless sex^¶	144 (82%)	99 (86%)	243 (84%)	0.97 (0.69, 1.37)	.879
Violence from a client^¶	19 (11%)	13 (11%)	32 (11%)	0.98 (0.72, 1.33)	.893
Sexual coercion^¶	35 (20%)	15 (13%)	50 (17%)	1.25 (1.00, 1.56)	.054
How sex clients were met^†,¶
Walking on the street	122 (69%)	73 (63%)	195 (67%)	1.10 (0.89, 1.35)	.377
Public places	97 (55%)	66 (57%)	163 (56%)	0.97 (0.80, 1.17)	.741
Online	42 (24%)	35 (30%)	77 (26%)	0.87 (0.69, 1.10)	.247
Strip club	8 (5%)	8 (7%)	16 (5%)	0.82 (0.50, 1.35)	.437
Through a drug dealer/drug house	98 (56%)	62 (54%)	160 (55%)	1.02 (0.84, 1.23)	.850
Massage parlor/brothel	4 (2%)	2 (2%)	6 (2%)	1.11 (0.62, 1.96)	.728
Escort service	23 (13%)	11 (10%)	34 (12%)	1.14 (0.88, 1.47)	.313
Manager/pimp/madame	12 (7%)	9 (8%)	21 (7%)	0.94 (0.64, 1.37)	.735
Through boyfriend/husband	31 (18%)	27 (23%)	58 (20%)	0.86 (0.66, 1.12)	.260
Through family/friend	95 (54%)	69 (60%)	164 (56%)	0.91 (0.76, 1.10)	.333
Health
HIV status^§
Negative	170 (97%)	111 (97%)	281 (97%)	Referent
Positive	6 (3%)	4 (3%)	10 (3%)	0.99 (0.59, 1.66)	.975
Saw a healthcare provider^¶	165 (94%)	105 (91%)	27 (93%)	1.17 (0.77, 1.77)	.471
Self-reported sexually-transmitted infection diagnosis^¶	17 (10%)	13 (11%)	30 (10%)	0.93 (0.67, 1.29)	.676
Ever told that they have HCV^₩
No	40 (23%)	76 (66%)	116 (40%)	Referent
Yes	118 (67%)	6 (5%)	124 (43%)	2.76 (1.93, 3.95)	<.000001
Never tested for HCV (not asked)	18 (10%)	33 (29%)	51 (18%)	NA
History of HCV treatment^¥	23 (13%)	NA
Incarceration^¶	59 (34%)	34 (30%)	93 (32%)	1.02 (0.84, 1.24)	.815

Abbreviations: HCV, hepatitis C virus; HIV, Human Immunodeficiency Virus; PR, prevalence ratio.

HCV serostatus determined by HCV-antibody test result or self-report of HCV seropositivity; ^†Individual participants could indicate multiple categories for these variables. Participants who reported categories are included in each of those groups; some individuals appear in multiple cells and PR estimates. For each group, the referent is all other participants who are not part of that group; ^‡Among those with a lifetime history of injection drug use (N = 230); ^¶Indicates that participants were asked about only the past 12 months; ^§HIV status inferred through rapid test result when available, otherwise self-report; ^₩Only participants who reported ever being tested for HCV were asked if they were ever told by a clinician that they had HCV; ^¥Among those who were HCV seropositive and provided HCV treatment history data (N = 174).

Most participants (79%) reported ever injecting drugs. Overall, 65% report injecting drugs in the past 12 months, among whom 57% reported that heroin/opioids were the primary drug they used. Of those who injected drugs, 60% reported sharing injection equipment of any kind in the past 12 months. A total of 32% of participants had been incarcerated in the past 12 months, 11% reported physical violence from a client, and 17% reported sexual coercion by any partner in the past 12 months. Healthcare use was high with 93% of participants reporting any healthcare provider visit in the past 12 months, including routine care, emergency department, or urgent care.

We estimated an overall HCV seroprevalence of 60% (95% CI: 55, 66) among WES in the Seattle, Washington area. HCV seroprevalence was 74% (95% CI: 68, 79) among those who reported ever injecting drugs and 10% (95% CI: 4, 20) among those who had never injected drugs. Among HCV-positive participants, only 13% reported prior HCV treatment.

In bivariate analyses, participants who were HCV seropositive were more likely than those who were HCV seronegative to report ever injecting drugs (PR: 7.51 [95% CI: 3.33, 16.96], Tables 1 and 2), to be at least 40 years old (PR: 1.80 [1.09, 2.97]), to speak primarily Spanish (PR: 1.31 [1.07, 1.61]), to report having anal sex with client(s) in the last 12 months (PR: 1.28 [1.07, 1.54]), to report meeting a client through an escort service in the last 12 months (PR: 1.25 [1.00, 1.55]), and to have ever been told by a clinician that they had HCV (PR: 2.76 [1.93, 3.95]). Those who were HCV seropositive were less likely to be Black or African American (PR: 0.70 [0.52, 0.91]).

Among participants who reported a history of IDU (N = 230), those who were HCV seropositive were more likely to start injecting before the age of 19 (PR: 1.31 [1.01, 1.71]). Using participants who indicated that methamphetamine was the most frequently injected drug as the referent, heroin as the most frequently injected drug was associated with higher HCV seroprevalence (PR: 1.67 [1.01, 2.73]). In the multivariate model, the only correlate that remained strongly associated with HCV seropositivity was history of IDU (PR_adj: 7.66 [3.26, 18.01], Table 3).

Table 3.

Multivariate Poisson Regression Prevalence Ratio Estimates for Hepatitis C Seropositivity Among Cisgender Women Who Exchange Sex, Seattle, Washingtion Area (National HIV Behavioral Surveillance, HET4, 2016) N = 289.^†

Characteristic	PR_adj (95% CI)	P-value
Age
18-29	Referent
30-39	1.28 (0.63, 2.57)	.494
≥40	1.75 (0.91, 3.36)	.091
Black or African American race	0.87 (0.59, 1.29)	.502
Spanish is primary language	1.16 (0.77, 1.75)	.473
Injection drug use, ever	7.66 (2.36, 18.01)	<.00001
Drugs used but not injected
Heroin/opioids	Referent
Methamphetamine	0.90 (0.54, 1.48)	.739
Both	0.83 (0.55, 1.25)	.373
Neither; other drugs only	1.00 (0.56, 1.79)	.996
No drug use in the past 12 months	0.85 (0.48, 1.49)	.567
Report of anal sex with client(s)	1.09 (0.80, 1.48)	.589

The multivariate model included only the variables included in this table.

Abbreviations: PR_adj: adjusted prevalence ratios.

†

Two observations were omitted due to missing data.

We present recruitment trees of participants, color coded by their HCV status (Figure 1) and IDU history (Figure 2). The RDS homophily scores revealed that (1) participants who were HCV seropositive recruited other HCV-seropositive participants preferentially 7% of the time, (2) HCV-seronegative participants recruited other HCV-seronegative participants preferentially 24% of the time, (3) participants with a history of IDU recruited others with a history of IDU preferentially 3% of the time, and (4) participants with no reported history of IDU recruited others with no history of IDU, preferentially 26% of the time. Affiliation matrices and associated homophily indices are presented in Tables 4 and 5.

Figure 1.

Recruitment tree of HCV status among women who exchange sex in Seattle, Washington (NHBS HET4, 2016).

Figure 2.

Recruitment tree of IDU history among women who exchange sex in Seattle, Washington (NHBS HET4, 2016).

Table 4.

Affiliation Matrix and Associated Homophily Scores for HCV Status Among Cisgender Women Who Exchange Sex, Seattle, Washington Area (National HIV Behavioral Surveillance, HET4, 2016).

Recruiter HCV status	Participant HCV status
Recruiter HCV status	Positive	Negative
Positive	119 (0.07)	55 (−0.07)
Negative	46 (−0.24)	46 (0.24)

Abbreviations: HCV, hepatitis C virus.

Table 5.

Affiliation Matrix and Associated Homophily Scores for IDU History Among Cisgender Women Who Exchange Sex, Seattle, Washington Area (National HIV Behavioral Surveillance, HET4, 2016).

Recruiter IDU history	Participant IDU history
Recruiter IDU history	Ever injected	Never injected
Ever injected	187 (0.03)	40 (−0.03)
Never injected	26 (−0.26)	17 (0.26)

Abbreviations: IDU, injection drug use.

Discussion

The majority (nearly 80%) of individuals in our survey of WES in the Seattle, Washington area—most of whom engaged in street-based sex exchange—reported ever injecting drugs, explaining the high HCV seroprevalence (60%) in this sample. Notably, approximately half were unstably housed or experiencing homelessness, and few reported ever receiving HCV treatment. The sociodemographic makeup of this sample also bears similarities to that of individuals who were part of an HIV outbreak in Seattle, Washington,³⁵ which PHSKC identified 2 years after these data were collected. While this survey sample is likely not a representative sample of all WES in the Seattle, Washington area, our findings highlight that there is a subgroup of WES who have substantial healthcare needs. It is important that injection-related risk factors are not overlooked in this population where prevention and screening efforts are often focused on sexual risk factors alone.

The finding that younger age at initiation of injection was associated with HCV seroprevalence is not surprising, as those who began injecting at an earlier age have likely spent more time injecting and therefore had greater opportunity to acquire HCV. We also found that those whose most frequently injected drug was heroin were more likely to be HCV seropositive than those whose most frequently injected drug was methamphetamine. This finding—that HCV seropositivity is associated with the use of specific substances among PWID—is consistent with recent work from other areas in the United States,^36,37 suggesting that HCV transmission among WES may be linked to drug use networks. Future work should be explore this phenomenon among WES.

The high prevalence of lifetime IDU in our sample of WES highlights the need for targeted HCV services and interventions for this population. WES—as well as other women who have HCV—are likely to encounter barriers and stigma when accessing health care.^38,39 One strategy for reaching stigmatized communities is through peer referral. For example, a team from the University of British Columbia found that peer referrals to drug treatment were effective for WES.⁴⁰ Based on this and other work among populations with a high HCV burden,^24,25 we hypothesized that HCV treatment interventions involving peer referral of networks may be beneficial to WES. Given the RDS recruitment strategy employed in this survey, we were able to evaluate if participants who have HCV were more or less likely to recruit (eg, be networked with) other women with HCV who exchange sex. Unfortunately, we did not see compelling evidence of this. Results of the homophily index calculations suggest that WES who are HCV seropositive and those who had a history of IDU were only marginally more likely to recruit others who shared these qualities. It is possible that this is because we did not specifically ask respondents to recruit other WES known to have HCV. These findings suggest that WES may build social links on their shared experience of engagement in sex exchange or other relationships, rather than along the lines of drug use behaviors or health experience.

With a treatment course as short as 8 weeks, DAAs present an opportunity to cure HCV durably and expeditiously. Although our findings suggest that peer referral to treatment may be ineffective, several potential alternative models exist. An incentivized walk-in care model, such as that of the Max Clinic at PHSKC⁴¹ has proven effective in improving HIV viral suppression levels among patients with complex needs.⁴² Similar to the sample of WES in our study, housing instability and IDU are common among Max Clinic patients. An expanded HCV care model for WES may also mirror the SHE Clinic, a partnership between Harborview Medical Center and Aurora Commons, an established, community-based agency serving homeless people in North Seattle.⁴³ SHE Clinic provides comprehensive healthcare services to women, including HCV treatment, and may present a scalable model for other locales. An additional potential model of care includes pharmacy-based or pharmacist-driven HCV treatment provision, which has been shown to be feasible and acceptable for PWID.^44,45

This study has several important limitations. First, we did not have access to HCV RNA laboratory results, so we were limited to estimating associations between ever having had HCV as opposed to having a chronic or current infection, which likely has more public health significance. Second, we cannot be sure that our sample is representative of WES in the Seattle, Washington area. Third, these data were collected in 2016. Considering the displacement experienced by many people because of the COVID-19 pandemic, it is conceivable that the profile of this small and potentially transient population has shifted since that time. Fourth, while concerns regarding the statistical reliability of RDS recruitment and analysis methods are well documented,^46
–48 we elected to analyze our data as a convenience sample to avoid potentially inducing bias with RDS weighted analysis. Lastly, self-reported data—particularly that concerned with sexual and drug use behaviors—always carry a risk of misclassification. Additionally, as we used cross-sectional data, we were limited in our ability to make risk inferences and could only identify associations between participants’ characteristics and HCV serostatus.

We acknowledge that seroprevalence does not reflect the true burden of active disease. Based on prior work,^49,50 we estimate that up to 75% of those who are HCV seropositive may have an active, chronic infection. We used data collected in 2016, and since that time, HCV incidence among PWID has increased nationally.⁵¹ Concurrently, HCV treatment for PWID has been increasing locally in the era of DAAs.⁵² Notably, Washington State has enacted policies which have removed Medicaid restrictions to HCV treatment for persons who are actively using drugs⁵³ and it encourages providers to offer HCV testing and treatment to people who use drugs.⁵⁴ HCV treatment scale-up has taken place locally since these data were collected, thus it is possible that many study participants who had a chronic HCV infection have since been treated. Yet, prior research suggests that policy changes in WA has not rapidly translated into increased numbers of treated patients, pointing to implementation gaps.⁵⁵ Furthermore, WES who inject drugs experience intersectional stigma and it is conceivable that members of such a marginalized population do not access the consistent healthcare needed for HCV treatment success. Indeed, work from members of this authorship group that used 2018 NHBS data found that women who inject drugs were less likely than men to be treated for HCV.¹⁰

As the opioid epidemic and concurrent stimulant use epidemic persist, populations of WES may continue to carry high burdens of HCV due to frequent IDU, and further study is warranted to mitigate these potential public health crises for this highly marginalized group. In the context of widely available DAA treatment, public health agencies and medical providers are equipped to intervene in the spread of HCV among WES, and future studies should explore the best way to approach and address this public health problem.

Supplemental Material

sj-docx-1-saj-10.1177_29767342231208936 – Supplemental material for High Seroprevalence of Hepatitis C Virus Among Cisgender Women Who Exchange Sex in the Seattle, Washington Area

Supplemental material, sj-docx-1-saj-10.1177_29767342231208936 for High Seroprevalence of Hepatitis C Virus Among Cisgender Women Who Exchange Sex in the Seattle, Washington Area by Michael P. Barry, Maria A. Corcorran, Judith I. Tsui, Courtney Moreno, Susan E. Buskin, Brandon L. Guthrie and Sara N. Glick in Substance Abuse

Footnotes

Acknowledgements

The authors wish to thank the NHBS interview staff at Public Health—Seattle & King County. Without their work, the present study would not have been possible.

Author Contributions

MPB and SNG conceived of the study. MPB, CM, and SNG conducted statistical analyses. All authors provided subject matter expertise and contributed to the development of the article.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The project was supported by cooperative agreement with the Centers for Disease Control and Prevention (6 NU62PS005094-01).

Compliance,Ethical Standards,and Ethical Approval

The Washington State Institutional Review Board approved all data collection activities. The University of Washington Human Subjects Division approved the present analysis.

ORCID iD

Michael P. Barry

Supplemental Material

Supplemental material for this article is available online at the SAJ website

References

Syvertsen

Agot

Ohaga

Bazzi

AR.

You can’t do this job when you are sober: heroin use among female sex workers and the need for comprehensive drug treatment programming in Kenya. Drug Alcohol Depend. 2019;194:495-499. doi:10.1016/j.drugalcdep.2018.10.019

Hail-Jares

Choi

Duo

Luo

Huang

ZJ.

Occupational and demographic factors associated with drug use among female sex workers at the China–Myanmar border. Drug Alcohol Depend. 2016;161:42-49. doi:10.1016/j.drugalcdep.2016.01.026

Wirtz

Peryshkina

Mogilniy

Beyrer

Decker

MR.

Current and recent drug use intensifies sexual and structural HIV risk outcomes among female sex workers in the Russian Federation. Int J Drug Policy. 2015;26(8):755-763. doi:10.1016/j.drugpo.2015.04.017

Roshanfekr

Khezri

Karimi

, et al. Lifetime and past-month substance use and injection among street-based female sex workers in Iran. Harm Reduct J. 2021;18(1):33. doi:10.1186/s12954-021-00477-5

Goldenberg

Montaner

Braschel

Socias

Guillemi

Shannon

Dual sexual and drug-related predictors of hepatitis C incidence among sex workers in a Canadian setting: gaps and opportunities for scale-up of hepatitis C virus prevention, treatment, and care. Int J Infect Dis. 2017;55:31-37. doi:10.1016/j.ijid.2016.12.019

Zhang

Liu

, et al. Human immunodeficiency virus, syphilis and hepatitis C virus prevalence trends among cross-border migrant Vietnamese female sex workers in Guangxi, China. BMC Public Health. 2015;15:1223. doi:10.1186/s12889-015-2561-0

Jacka

Roy

Høj

, et al. Sexual behaviour as a risk factor for hepatitis C virus infection among people who inject drugs in Montreal, Canada. J Viral Hepat. 2019;26(12):1413-1422. doi:10.1111/jvh.13194

Karlsson

Santacatterina

Käll

, et al. Risk behaviour determinants among people who inject drugs in Stockholm, Sweden over a 10-year period, from 2002 to 2012. Harm Reduct J. 2017;14(1):57. doi:10.1186/s12954-017-0184-8

Evans

JL.

Gender differences in sexual and injection risk behavior among active young injection drug users in San Francisco (the UFO study). J Urban Health. 2003;80(1):137-146. doi:10.1093/jurban/jtg137

10.

Corcorran

Tsui

Scott

Dombrowski

Glick

SN.

Age and gender-specific hepatitis C continuum of care and predictors of direct acting antiviral treatment among persons who inject drugs in Seattle, Washington. Drug Alcohol Depend. 2021;220:108525. doi:10.1016/j.drugalcdep.2021.108525

11.

Alpren

Dawson

John

, et al. Opioid use fueling HIV transmission in an urban setting: an outbreak of HIV infection among people who inject drugs—Massachusetts, 2015–2018. Am J Public Health. 2020;110(1):37-44. doi:10.2105/AJPH.2019.305366

12.

Lyss

Buchacz

McClung

Asher

Oster

AM.

Responding to outbreaks of human immunodeficiency virus among persons who inject drugs—United States, 2016–2019: perspectives on recent experience and lessons learned. J Infect Dis. 2020;222(Supplement_5):S239-S249. doi:10.1093/infdis/jiaa112

13.

Peters

Pontones

Hoover

, et al. HIV infection linked to injection use of oxymorphone in Indiana, 2014–2015. N Engl J Med. 2016;375(3):229-239. doi:10.1056/NEJMoa1515195

14.

Tookes

Bartholomew

Geary

, et al. Rapid identification and investigation of an HIV risk network among people who inject drugs –Miami, FL, 2018. AIDS Behav. 2020;24(1):246-256. doi:10.1007/s10461-019-02680-9

15.

McClung

Atkins

Kilkenny

, et al. Response to a large HIV outbreak, cabell county, West Virginia, 2018–2019. Am J Prev Med. 2021;61(5):S143-S150. doi:10.1016/j.amepre.2021.05.039

16.

Grov

Westmoreland

Carrico

Nash

Are we on the precipice of a new epidemic? Risk for hepatitis C among HIV-negative men-, trans women-, and trans men- who have sex with men in the United States. AIDS Care. 2020;32(sup2):74-82. doi:10.1080/09540121.2020.1739204

17.

Wolfe

Hughto

JMW

Quint

Hashemi

Hughes

LD.

Hepatitis C virus testing and care cascade among transgender and gender diverse individuals. Am J Prev Med. 2023;64(5):695-703. doi:10.1016/j.amepre.2023.01.005

18.

Nagaoki

Imamura

Nishida

, et al. The impact of interferon-free direct-acting antivirals on clinical outcome after curative treatment for hepatitis C virus-associated hepatocellular carcinoma: comparison with interferon-based therapy. J Med Virol. 2019;91(4):650-658. doi:10.1002/jmv.25352

19.

Cortez

Kottilil

Beyond interferon: rationale and prospects for newer treatment paradigms for chronic hepatitis C. Ther Adv Chronic Dis. 2015;6(1):4-14. doi:10.1177/2040622314551934

20.

Schmidt

Nelson

Pawlotsky

Sherman

Thomas

Chung

RT.

Direct-acting antiviral agents and the path to interferon independence. Clin Gastroenterol Hepatol. 2014;12(5):728-737. doi:10.1016/j.cgh.2013.06.024

21.

Lok

Chung

Vargas

Kim

Naggie

Powderly

WG.

Benefits of direct-acting antivirals for hepatitis C. Ann Intern Med. 2017;167(11):812. doi:10.7326/M17-1876

22.

Rodger

Cambiano

Bruun

, et al. Sexual activity without condoms and risk of HIV transmission in serodifferent couples when the HIV-positive partner is using suppressive antiretroviral therapy. JAMA. 2016;316(2):171. doi:10.1001/jama.2016.5148

23.

Cepeda

Vickerman

Bruneau

, et al. Estimating the contribution of stimulant injection to HIV and HCV epidemics among people who inject drugs and implications for harm reduction: a modeling analysis. Drug Alcohol Depend. 2020;213:108135. doi:10.1016/j.drugalcdep.2020.108135

24.

Surey

Menezes

Francis

, et al. From peer-based to peer-led: redefining the role of peers across the hepatitis C care pathway: HepCare Europe. J Antimicrob Chemother. 2019;74(Supplement_5):v17-v23. doi:10.1093/jac/dkz452

25.

Broad

Mason

Guyton

Lettner

Matelski

Powis

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:10.1016/j.drugpo.2020.102755

26.

Heckathorn

DD.

Respondent-driven sampling: a new approach to the study of hidden populations. Soc Probl. 1997;44(2):174-199. doi:10.2307/3096941

27.

R Studio Team. RStudio: integrated development for R. 2020. Accessed November 10, 2021. http://www.rstudio.com/

28.

Stevenson

Nunes

Sanchez

, et al. EpiR: an R package for the analysis of epidemiological data. 2021. Accessed November 10, 2021. https://fvas.unimelb.edu.au/research/groups/veterinary-epidemiology-melbourne

29.

US Department of Health and Human Services, Office of Disease Prevention and Health Promotion. Social determinants of health. Healthy People 2030. 2020. Accessed February 8, 2021. https://health.gov/healthypeople/priority-areas/social-determinants-health

30.

Spiegelman

Hertzmark

Easy SAS calculations for risk or prevalence ratios and differences. Am J Epidemiol. 2005;162(3):199-200. doi:10.1093/aje/kwi188

31.

Volz

Wejnert

Cameron

, et al. Respondent-Driven Sampling Analysis Tool (RDSAT). Version 7.1. Ithaca, NY: Cornell University.

32.

Heckathorn

DD.

Respondent-driven sampling II: deriving valid population estimates from chain-referral samples of hidden populations. Soc Probl. 2002;49(1):11-34. doi:10.1525/sp.2002.49.1.11

33.

Handcock

Fellows

Gile

. RDS analyst: software for the analysis of respondent-driven sampling data. 2014. Accessed November 10, 2021. Hpmrg.org

34.

Heckathorn

DD.

Extensions of respondent-driven sampling: analyzing continuous variables and controlling for differential recruitment. Sociol Methodol. 2007;37(1):151-208. doi:10.1111/j.1467-9531.2007.00188.x

35.

Buskin

Erly

Glick

, et al. Detection and response to an HIV cluster: people living homeless and using drugs in Seattle, Washington. Am J Prev Med. 2021;61(5):S160-S169. doi:10.1016/j.amepre.2021.04.037

36.

Barranco

Rosenberg

Flanigan

, et al. A cross-sectional study of hepatitis C prevalence and correlates among persons who inject drugs in rural and non-rural communities. J Viral Hepat. 2022;29(11):994-1003. doi:10.1111/jvh.13735

37.

Wagner

Zhong

Teshale

, et al. Hepatitis C virus infection and polysubstance use among young adult people who inject drugs in a rural county of New Mexico. Drug Alcohol Depend. 2021;220:108527. doi:10.1016/j.drugalcdep.2021.108527

38.

Potter

Horwood

Feder

Access to healthcare for street sex workers in the UK: perspectives and best practice guidance from a national cross-sectional survey of frontline workers. BMC Health Serv Res. 2022;22(1):178. doi:10.1186/s12913-022-07581-7

39.

Austin

Tsui

Barry

, et al. Health care-seeking experiences for people who inject drugs with hepatitis C: qualitative explorations of stigma. J Subst Abuse Treat. 2022;137:108684. doi:10.1016/j.jsat.2021.108684

40.

Deering

Kerr

Tyndall

, et al. A peer-led mobile outreach program and increased utilization of detoxification and residential drug treatment among female sex workers who use drugs in a Canadian setting. Drug Alcohol Depend. 2011;113(1):46-54. doi:10.1016/j.drugalcdep.2010.07.007

41.

Dombrowski

Ramchandani

Dhanireddy

Harrington

Moore

Golden

MR.

The max clinic: medical care designed to engage the hardest-to-reach persons living with HIV in Seattle and King County, Washington. AIDS Patient Care STDs. 2018;32(4):149-156. doi:10.1089/apc.2017.0313

42.

Dombrowski

Galagan

Ramchandani

, et al. HIV care for patients with complex needs: a controlled evaluation of a walk-in, incentivized care model. Open Forum Infect Dis. 2019;6(7):ofz294. doi:10.1093/ofid/ofz294

43.

Stewart

Stadeli

Green

, et al. A co-located continuity clinic model to address healthcare needs of women living unhoused with opioid use disorder, who engage in transactional sex in North Seattle. Sex Transm Dis. 2020;47(1):e5-e7. doi:10.1097/OLQ.0000000000001064

44.

Tsui

Barry

Austin

, et al. ‘Treat my whole person, not just my condition’: qualitative explorations of hepatitis C care delivery preferences among people who inject drugs. Addict Sci Clin Pract. 2021;16(1):52. doi:10.1186/s13722-021-00260-8

45.

Austin

Gojic

Bhatraju

, et al. Barriers and facilitators to implementing a Pharmacist, Physician, and Patient Navigator-Collaborative Care Model (PPP-CCM) to treat hepatitis C among people who inject drugs. Int J Drug Policy. 2023;111:103924. doi:10.1016/j.drugpo.2022.103924

46.

Goel

Salganik

MJ.

Assessing respondent-driven sampling. Proc Natl Acad Sci USA. 2010;107(15):6743-6747. doi:10.1073/pnas.1000261107

47.

McCreesh

Frost

SDW

Seeley

, et al. Evaluation of respondent-driven sampling. Epidemiology. 2012;23(1):138-147. doi:10.1097/EDE.0b013e31823ac17c

48.

Rudolph

Fuller

Latkin

The importance of measuring and accounting for potential biases in respondent-driven samples. AIDS Behav. 2013;17(6):2244-2252. doi:10.1007/s10461-013-0451-y

49.

Soriano

Mocroft

Rockstroh

, et al. Spontaneous viral clearance, viral load, and genotype distribution of hepatitis C virus (HCV) in HIV-infected patients with anti-HCV antibodies in Europe. J Infect Dis. 2008;198(9):1337-1344. doi:10.1086/592171

50.

Hajarizadeh

Grebely

Dore

GJ.

Epidemiology and natural history of HCV infection. Nat Rev Gastroenterol Hepatol. 2013;10(9):553-562. doi:10.1038/nrgastro.2013.107

51.

Centers for Disease Control and Prevention. Division of viral hepatitis 2025 strategic plan. 2020. Accessed March 27, 2023. https://www.cdc.gov/hepatitis/pdfs/DVH-StrategicPlan2020-2025.pdf

52.

Tsui

Miller

Scott

Corcorran

Dombrowski

Glick

SN.

Hepatitis C continuum of care and utilization of healthcare and harm reduction services among persons who inject drugs in Seattle. Drug Alcohol Depend. 2019;195:114-120. doi:10.1016/j.drugalcdep.2018.11.026

53.

State of HepC. 2023 hep C: state of medicaid access report cards are in. 2023. Accessed August 17, 2023. https://stateofhepc.org/2023-hep-c-state-of-medicaid-access-report-cards-are-in/

54.

Washington State Department of Health, Washington State Healthcare Authority. Urgent: test and treat people who use drugs for hepatitis C. 2021. Accessed August 17, 2023. https://doh.wa.gov/sites/default/files/legacy/Documents/Pubs//150-146-HepC-cliniciantestingbrief.pdf

55.

Auty

Shafer

Griffith

KN.

Medicaid subscription-based payment models and implications for access to hepatitis C medications. JAMA Health Forum. 2021;2(8):e212291. doi:10.1001/jamahealthforum.2021.2291

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.01 MB