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Respondent-Driven Sampling of Injection Drug Users in Two U.S.–Mexico Border Cities: Recruitment Dynamics and Impact on Estimates of HIV and Syphilis Prevalence

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Respondent-driven sampling (RDS), a chain referral sampling approach, is increasingly used to recruit participants from hard-to-reach populations, such as injection drug users (IDUs). Using RDS, we recruited IDUs in Tijuana and Ciudad (Cd.) Juárez,
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   Journal of Urban Health: Bulletin of the New York Academy of Medicine, Vol. 83, No. 7doi:10.1007/s11524-006-9104-z  *  2006 The New York Academy of Medicine Respondent-DrivenSamplingofInjectionDrugUsersin Two U.S.–Mexico Border Cities: Recruitment Dynamicsand Impact on Estimates of HIV and Syphilis Prevalence Simon D. W. Frost, Kimberly C. Brouwer, Michelle A. Firestone Cruz,Rebeca Ramos, Maria Elena Ramos, Remedios M. Lozada,Carlos Magis-Rodriguez, and Steffanie A. Strathdee ABSTRACT  Respondent-driven sampling (RDS), a chain referral sampling approach, isincreasingly used to recruit participants from hard-to-reach populations, such asinjection drug users (IDUs). Using RDS, we recruited IDUs in Tijuana and Ciudad (Cd.) Jua´rez, two Mexican cities bordering San Diego, CA and El Paso, TX,respectively, and compared recruitment dynamics, reported network size, and estimatesof HIV and syphilis prevalence. Between February and April 2005, we used RDS torecruit IDUs in Tijuana (15 seeds, 207 recruits) and Cd. Jua´ rez (9 seeds, 197 recruits),Mexico for a cross-sectional study of behavioral and contextual factors associated withHIV, HCV and syphilis infections. All subjects provided informed consent, ananonymous interview, and a venous blood sample for serologic testing of HIV, HCV,HBV (Cd. Jua´ rez only) and syphilis antibody. Log-linear models were used to analyzethe association between the state of the recruiter and that of the recruitee in the referral chains, and population estimates of the presence of syphilis antibody were obtained,correcting for biased sampling using RDS-based estimators. Sampling of the targeted 200 recruits per city was achieved rapidly (2 months in Tijuana, 2 weeks in Cd. Jua´ rez).After excluding seeds and missing data, the sample prevalence of HCV, HIV and syphilis were 96.6, 1.9 and 13.5% respectively in Tijuana, and 95.3, 4.1, and 2.7%respectively in Cd. Jua´ rez (where HBV prevalence was 84.7%). Syphilis cases wereclustered in recruitment trees. RDS-corrected estimates of syphilis antibody prevalenceranged from 12.8 to 26.8% in Tijuana and from 2.9 to 15.6% in Ciudad Jua´ rez,depending on how recruitment patterns were modeled, and assumptions about hownetwork size affected an individual  _ s probability of being included in the sample. RDSwas an effective method to rapidly recruit IDUs in these cities. Although the frequencyof HIV was low, syphilis prevalence was high, particularly in Tijuana. RDS-corrected estimates of syphilis prevalence were sensitive to model assumptions, suggesting that further validation of RDS is necessary. KEYWORDS  HIV and syphilis prevalence, Injection drug users, Respondent drivensampling. Frost is with the Department of Pathology and Antiviral Research Center, University of California, SanDiego, CA, USA; Brouwer, Firestone Cruz, and Strathdee are with the Division of International Healthand Cross Cultural Medicine, Department of Family and Preventive Medicine, University of California,San Diego, CA, USA; R. Ramos is with the United States–Mexico Border Health Association, El Paso,TX, USA; M. E. Ramos is with Programa Compan ˜ eros, Ciudad Jua ´rez, Chihuahua, Mexico; Lozada iswith Patronato COMUSIDA, Tijuana, Baja California, Mexico; Magis-Rodriguez is with the CentroNacional para la Prevencio ´n y el Control del VIH/SIDA (CENSIDA), Me ´xico City, Me ´xico.Correspondence: Simon D. W. Frost, UCSD Antiviral Research Center, 150 W. Washington St., Suite100, San Diego, CA 92103, USA. (E-mail: sdfrost@ucsd.edu) i83  INTRODUCTION InjectiondruguseisagrowingproblemincitieslocatedalongtheU.S.–Mexicoborder.Approximately 70%ofU.S. cocaine srcinatinginSouthAmerica passes through theCentral America–Mexico corridor. 1 Cities and towns positioned on drug trafficking routesoftenexperienceepidemicsofinjectiondruguse. 2,3 Injectiondrugusers(IDUs)areathighriskofblood-borneinfections,suchashepatitisCvirus(HCV)andhumanimmunodeficiency virus type-1 (HIV-1) infection, and of acquiring HIV-1 and othersexually transmitted infections (STIs) through high rates of unprotected sex. 4–10 Mexico is currently considered a country of low HIV/AIDS prevalence 11 (180,000 adult cases in 2005, a seroprevalence in the general population of 0.3% 12 ),and the HIV epidemic has been mainly confined to men who have sex with men. 13 Although injection drug use appears to have played only a minor role in theepidemic on a country-wide level, 14 injection drug use appears to be increasinglyimportant as a risk factor for HIV infection in some Mexican cities bordering theU.S. Viani et al. 15 noted that the prevalence of HIV among pregnant women givingbirth at Tijuana General Hospital rose from 0.29% in 1998 to 1.02% in 2001 and,in a subsequent study, showed that pregnant HIV-infected women were more likelyto either inject drugs or to have a spouse/partner who injected drugs. 16 In 2002,Valdez et al. 17 reported that 21% of female sex workers in Ciudad (Cd.) Jua ´rezinjected illicit drugs, whereas a study by Patterson et al. 18 in 2005 showed that overhalf of female sex workers in Cd. Jua ´rez injected drugs, suggesting increasingoverlap between sexual and IDU networks.Overlap between injection drug use and the trade of sex for money or drugsmay contribute to elevated risk of STIs other than HIV, such as syphilis. Syphilis hasbeen associated with higher HIV seroprevalence in a number of populations and isconsidered a cofactor of HIV transmission. 19–22 In contrast to HIV, syphilis hasbeen present in Mexico since at least the time of the Spanish invasion; however, thenumber of reported cases has decreased from 40,607 in 1945 (190.5 per 100,000)to 2,608 in 1990 (3.2 per 100,0000). 23 Aggregate figures for syphilis prevalence belie the sub-epidemics occurringwithin specific risk groups. Several studies have been conducted with female sexworkers in Mexico and have found varying syphilis prevalence levels. In 1990,23.7% of 1,386 sex workers in four Mexican states had a reactive syphilis test. 24 In1993, testing of 826 sex workers in Mexico City showed an overall prevalence of 6.4%, with different syphilis rates associated with different patterns of sex work:1.3% for massage parlor workers, 4.4% for bar girls, and 9.6% for streetwalkers. 25 The prevalence of syphilis among 3,100 female sex workers tested at an AIDS clinicduring 1992 and 1993 was 8.2%. 26 Incontrast,syphilisprevalencewaslow(2.3and1.1%) among gynecological outpatients in two Mexican cities between the years1994 and 1995. 27 However, little is known about syphilis prevalence in IDUpopulations in Mexico.In order to estimate the prevalence of HIV, HCV, and syphilis among IDUs, weconducted a cross-sectional study of IDUs in the border cities of Tijuana and Cd. Jua ´rez, Mexico. Both cities are located on major drug trafficking routes and havelarge IDU populations (c. 6,000), with a similar sex ratio among the IDUs (c. 80%male). 3 As stigma surrounding injection drug use makes it difficult to obtain arepresentative sample of injection drug users, we recruited individuals usingrespondent-driven sampling (RDS). 28,29 By collecting data on individuals _  personalnetwork sizes, RDS attempts to correct for biases in the sampling process, in order FROST ET AL.i84  to obtain unbiased estimates of parameters such as the prevalence of a disease. Inthis study, we report on patterns of recruitment and the prevalence of HIV, HCV,and syphilis (and hepatitis B infection, for Cd. Jua ´rez) in the context of sexual risk. MATERIALS AND METHODSStudy Population From February through April 2005, IDUs were enrolled in a cross-sectional study inTijuana and Cd. Jua ´rez, Mexico. Eligibility criteria for the study included: havinginjected illicit drugs within the past month, confirmed by inspection of injectionstigmata ( F track marks _ ); aged 18 years or older; willing and able to provideinformed consent; and not having been previously interviewed for the study.Subjects gave their written informed consent to participate in the study. Studymethods were approved by the Institutional Review Board of the University of California, San Diego and the Ethics Board of the Tijuana General Hospital, whichhas one of the few federal-wide assurances in Mexico. Recruitment RDS methods were used to recruit participants. 28,29 A diverse group of   B seeds ^ (heterogeneous in age, gender, and geographic location) were selected to initiate theprocess. After providing informed consent, seeds underwent an interview, wereeducated on how to refer other eligible IDUs, and were given three uniquely codedcoupons to refer their peers. Coupons were given to participants until approxi-mately 150 participants were recruited in order to obtain a target sample size of approximately 200 per site.On each coupon, the study name, locations where they could participate, and abrief explanation was printed. In Cd. Jua ´rez, interviews were conducted at a clinicrun by Programa Compan ˜ eros, A.C., which is a trusted and well-respected non-governmental organization (NGO) that has been providing services to andconducting studies with IDUs in the city for decades. In Tijuana, staff from bothCOMUSIDA, the municipal HIV/AIDS program, and the Centro de Integracio ´n yRecuperacio ´n para Enfermos de Alcoholismo y Drogadiccio ´n  B Mario CamachoEspı ´ritu ^ , A.C. (CIRAD), an NGO that began working with drug users in 1991,made weekly trips to three geographically diverse  F colonias _  (i.e., neighborhoods) inthe city: Zona Norte, Grupo Me ´xico, and Sepanal, using a modified recreationalvehicle that operated as a mobile clinic (the  F Prevemovihl _ ).Monetary reimbursements were given to participants to cover transportationcosts and to compensate them for their time. The study staff in each site proposedthe incentive levels based on their experience with this population and the incentivesfor previous studies. Participants in Cd. Jua ´rez received $20 U.S. dollars (USD) forparticipation in the baseline visit and $5 USD when receiving laboratory test resultsat a one month follow-up visit. In Tijuana, $10 USD was given at baseline and $5 forthe follow-up visit. In addition, participants at both sites were given $5 for eacheligible person they recruited. These levels were not regarded as high. Data Collection Upon enrollment, trained staff administered quantitative surveys eliciting informa-tion on topics such as socio-economic and demographic profiles, drug use practices, RDS OF IDUS IN TWO U.S.–MEXICO BORDER CITIES i85  sterile syringe access, barriers to sterile syringe use, experience with drug abusetreatment and incarceration history, health status, and HIV knowledge and testinghistory. We also asked about sexual behaviors and condom use with regular, casualand client partners of the opposite and same sex. Questions pertained to lifetimerisk behaviors and those occurring in the prior six months.For RDS purposes, we measured network size using the question  B En losu ´ltimos 6 meses,  > cua ´ntas personas conoce de nombre o de apodo que se haninyectado drogas? ^  ( B In the past 6 months, how many people do you know byname or street name who have injected drugs? ^ ). To determine the relationshipbetween recruiter and recruitee, we asked  B> Cua ´l es su relacio ´n con la persona quele entrego ´ el cupo ´n? ^  ( B What is your relationship to the person who gave you thecoupon? ^ ). Participants were given the choice of:  B parientes ^  (relative);  B parejasexual ^  (sex partner/spouse);  B amigo(a) ^  (friend);  B conocido ^  (acquaintance); B desconocido ^  (stranger); and  B otro ^  (other). To determine the size of individuals _ networks with respect to injection drug use, we asked  B En los u ´ltimos 6 meses,  > concua ´ntas personas diferentes acostumbra inyectarse? ^  ( B In the last 6 months, onaverage how many different people did you usually inject with? ^ ). After theinterview, blood was drawn for antibody testing of HIV, HCV, HBV (Cd. Jua ´rezonly), and syphilis. Pre- and post-test counseling, and referral to treatment whereindicated, was provided to all participants. Laboratory Samples Blood samples were obtained by venipuncture and serum was stored at themunicipal health clinic in Tijuana or Cd. Jua ´rez before being shipped frozen to theSan Diego County public health laboratory or New Mexico State Laboratory,respectively. All participants were screened on-site in Mexico for HIV with theDetermine rapid test (Abbott Laboratories). For the Tijuana samples, in the event of an HIV-positive or indeterminate test, results were confirmed with a Western blot,HIV enzyme immunoassay (EIA), and HIV immunofluorescence assay. For samplesfrom Cd. Jua ´rez, the HIV EIA was conducted on all samples, and a confirmatoryWesternblotwasperformedonpositiveorindeterminatesample.Cd.Jua ´rezsampleswere also tested for hepatitis B antigen (Genetic Systems HBsAg EIA 3.0, Bio-RadLaboratories) and antibody (DiaSorin ETI-AB-COREK PLUS). All samples weretested for syphilis with the rapid plasma reagin (RPR) test (Macro-Vue, BectonDickenson) and if reactive, confirmed by a  Treponema pallidum  particle agglu-tination assay (TPPA; Fujirebio Diagnostics). Statistical Methods Obtaining estimates of population proportions of groups using RDS involvescombining three kinds of data: the sample proportion of each group, thecrosstabulation of groups between pairs of recruiters and recruitees, and differencesin network size between groups. To estimate equilibrium proportions of differentgroups, and to estimate the pattern of mixing between groups, we assumed that therecruitment process followed a first order Markov process. 28,29 Under this model,the relationship between the state of the recruiter and recruitee can be modeledusing log-linear models applied to a two-way table of counts. 30,31 We classifiedindividuals by sex and syphilis seropositivity and fitted a series of hierarchical log-linear models of increasing complexity to the data to determine patterns of nonrandom mixing between groups along each recruitment tree, choosing the bestmodel as that which had the lowest value of Akaike _ s Information Criterion. 32 For FROST ET AL.i86  the purposes of analysis, we considered all individuals with positive syphilis testsbased upon RPR, and did not classify individuals further into those with TPPAtiters greater than or equal to 1:8 (who may represent infectious cases) and thosewith titers of 1:1 to 1:4 (who may represent past infection).To derive RDS-corrected estimates of syphilis seropositivity in men and womenin Tijuana and Ciudad Jua ´rez, we estimated recruitment weights for each group (asthe ratio of the equilibrium to sample proportions of each group). We estimated theequilibrium fraction as previously described. 29 We used both raw counts andpredicted counts based on the best fitting log-linear model. Degree weights wereestimated using linear least squares. 29 We used both unadjusted and adjustedestimates of personal network size. 33 An overall sampling weight was derived foreach group, from which population-level estimates were obtained.Pre-processing of the data was performed using Stata v. 8.2 (Stata Corporation,College Station, TX). Networks and trees were generated using scripts written inPython and visualized using GraphViz (AT&T Research, Florham Park, NJ).Statistical analyses and summary statistics of the recruitment network weregenerated in R, 34 and RDS based corrections were calculated using Maxima (http:// maxima.sourceforge.net). We chose to develop our own programs rather than useRDSAT (http://www.respondentdrivensampling.org) primarily to familiarize our-selves with the statistical theory underlying RDS-based corrections. All code isavailable from the first author on request. RESULTSStudy Population Table 1 summarizes some basic data relating to the Tijuana (15 seeds, 207 recruits)and Cd. Jua ´rez (9 seeds, 197 recruits) study populations. Both populations werepredominantly male, with participants in their early to mid-30s. Crude HCVseroprevalence was extremely high ( 9 95%) in both cities. Hepatitis B seropreva-lence was only determined for Cd. Jua ´rez, where it was high (85% overall); onlyone individual was positive for HBV antigen. Crude HIV seroprevalence was low,but the crude prevalence of syphilis was high, especially among women. Recruitment Dynamics RDS was an effective means of recruiting IDUs in both cities. The number of individuals recruited increased rapidly following the first interview, especially in Cd. Jua ´rez (Figure 1a), where many individuals interviewed the same day as theirrecruiter (Figure 1b). Apart from these differences in the tempo of recruitment,patterns of recruitment were very similar between the two cities; recruitment washighest in the fourth wave of recruitment, with some individuals being recruitedafter eight waves, suggesting that despite rapid recruitment, good sociometric depthwas obtained (Figure 1c). After excluding individuals who were not given coupons,the number of recruits per recruiter showed a bimodal distribution, with manyindividuals either recruiting zero or three recruits (Figure 1d), suggesting thepresence of a mixed population of ineffective and effective recruiters. In both cities,approximately one half of participants were recruited via referral trees srcinatingfrom two seeds (Figure 1e). The relationship between recruiter and recruit wasusually  F friend, _ F acquaintance, _  or another close relationship such as a family RDS OF IDUS IN TWO U.S.–MEXICO BORDER CITIES i87
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