HIV, Hepatitis C, and Hepatitis B Infections and Associated Risk Behavior in Inj

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EMERGING INFECTIOUS DISEASES

Volume 13, Number 9–September 2007

Research

HIV, Hepatitis C, and Hepatitis B Infections and Associated Risk Behavior in

Injection Drug Users, Kabul, Afghanistan

S. Todd,* Abdullah M.S. Abed,† Steffanie A. Strathdee,* T.

,‡ Boulos A. Botros,§ Naqibullah Safi,† and C. Earhart§

*University of California, San Diego, La Jolla, California, USA; †Ministry

of Public Health, Kabul, Afghanistan; ‡Walter Army Institute of

Research, Rockville, land, USA; and §United States Naval Medical

Research Unit 3, Cairo, Egypt

Abstract

Limited prevalence data for HIV, hepatitis B surface antigen (HBsAg), and

hepatitis C virus (HCV) exist for Afghanistan. We studied a cross-sectional

sample of adult injection drug users (IDUs) in Kabul, Afghanistan, from June

2005 through June 2006. Study participants completed

interviewer-administered questionnaires and underwent testing for HIV,

antibody to HCV, and HBsAg. Overall prevalences of HIV, HCV, and HBsAg were

3.0% (95% confidence interval [CI] 1.7%–5.1%), 36.6% (95% CI 32.2%–41.0%),

and 6.5% (95% CI 4.2%–8.7%), respectively (N = 464). Among male IDUs (n =

463), risky behavior, including sharing syringes (50.4%), paying women for

sex (76.2%), and having sex with men or boys (28.3%), were common. Needle

sharing, injecting for >3 years, and receiving injections from nonmedical

providers were independently associated with increased risk for HCV

infection. The high prevalence of risky behavior indicate that Kabul is at

risk for an HIV epidemic. Scale-up of harm-reducing interventions is

urgently needed.

Injection drug use has become increasingly common in Central and South Asia,

fostered by readily available opium and heroin (1,2). Many countries in this

region are experiencing HIV epidemics driven by injection drug use that is

extending to other populations (3,4). Four countries bordering Afghanistan

(Pakistan, Tajikistan, Uzbekistan, and Iran), which provided refuge to many

Afghans during the extended period of civil war, are experiencing HIV

epidemics among injection drug users (IDUs) (1,3,5,6). The population of

Kabul, the capital of Afghanistan, has increased to & #8776;3 million since

2001 because of returning refugees (7,8). Refugees may have acquired

high-risk bebavior, such as injection drug use, that may place communities

at risk upon their return.

Afghanistan provided 88% of the world's opium supply in 2005 (9). Although

noninjection use of opium (smoking, vaporization, or oral ingestion) is

traditional in Afghanistan, injecting likely represents a new behavior (10).

This behavior may be learned in countries of refuge during times of

political unrest, as indicated by the participants in a United Nations

Office on Drugs and Crime study in 2003, in which 50% (n = 34) of

participants had started using heroin in either Pakistan or Iran (11). A

prior study in the border city of Quetta, Pakistan, reported that Afghan

IDUs were more likely than their Pakistani counterparts to engage in risky

behavior (12). These observations raised concern that injection drug use and

accompanying high-risk behavior are increasing in Afghanistan and that a

concentrated HIV epidemic may soon ensue (13).

There were an estimated 470 IDUs in Kabul in 2003, although the United

Nations Office on Drugs and Crime Afghanistan survey in 2005 estimated that

there were 50,000 heroin users in Afghanistan, of whom 14% reported

injecting drugs (10,11). The same study also estimated that most IDUs reside

in Kabul and, of all heroin-using IDUs interviewed, 70% stated they had

shared needles (10). Of IDUs interviewed, all were men, but anecdotal

evidence from harm-reduction programs indicated that a few IDUs in Kabul

were female (10). Although drug use is illegal in Afghanistan and warrants

either rehabilitation for a first offense or imprisonment for recurrent

offenses (14) the motivating factor stated for initiating injection was

constant pain that was not relieved by smoking (10). However, little is

currently known about other aspects of injection drug use in Kabul, such as

syringe sources or harm-reducing programs.

Little data are available on HIV, hepatitis B surface antigen (HBsAg), or

hepatitis C virus (HCV) prevalence and associated risk behavior in

Afghanistan. As of October, 2005, only 41 cases of HIV had been reported,

although this is believed to underestimate the potential problem (15). We

assessed prevalence of HIV, HCV, HBsAg, and associated risk behavior among

IDUs in Kabul.

Methods

Study Design and Participants

We conducted a cross-sectional study of IDUs in Kabul, Afghanistan, from

June 2005 through June 2006, through the Voluntary Counseling and Testing

(VCT) Center at the Central Polyclinic, an Afghan Ministry of Public Health

facility. At the time of this study, there were 3 harm-reduction programs in

Kabul, of which 1 had on-site syringe exchange.

Eligible participants were those >18 years of age who reported having

injected drugs within the past 6 months (confirmed through injection marks)

and were able to provide informed consent. Before data collection, this

study was reviewed and approved by the investigational review boards of the

University of California, San Diego; the US Naval Medical Research Unit No.

3; the Walter Army Institute of Research; and the Ministry of Public

Health of Afghanistan.

Procedures

Potential participants were approached by an experienced outreach worker

known to them. If participants were interested in entering the study, they

accompanied the outreach worker to the VCT Center. At the VCT, a study

representative explained the study in a confidential setting and obtained

informed consent. The participant was assigned a unique study number, the

sole identifier, which was required for receiving test results as needed.

Participants were interviewed by a trained study representative matched to

the participant's sex. The questionnaire included sociodemographics, travel

and medical histories, past and current drug use and sexual behavior, and

knowledge of bloodborne and sexually transmitted infections. No data were

recorded from those declining participation or ineligible to enter the

study.

Pretest and posttest counseling were given, and rapid antibody testing was

performed by using the Abbott Determine HIV 1/2 test, the Abbott Determine

HBsAg test (both from Abbott Diagnostics Japan, Tokyo, Japan), and the

Standard Diagnostics HCV test (Standard Diagnostics Laboratories, Yongin-si

Gyeonggi-do, Republic of Korea) for HCV. Participants with a positive HIV

test result underwent sequential testing with the OraSure OraQuick HIV 1/2

test (OraSure Technologies, Bethlehem, PA, USA). Repeatedly positive rapid

HIV test results were confirmed by Western blot (HIV BLOT 2.2; GeneLabs

Diagnostics, Singapore). Hepatitis B was confirmed with a second,

serum-based rapid test (Standard Diagnostics HBV; Standard Diagnostics

Laboratories) because nucleic acid testing was not available in Kabul. The

Abbott and Standard Diagnostics HBsAg rapid tests had sensitivities of 99.0%

and 99.0% and specificities of 99.0% and 100.0%, respectively, and a

positive predictive value of 99.9%, assuming a baseline HBsAg prevalence of

5.0% (16,17). The presence of antibody to HCV was confirmed with a

recombinant immunoblot assay (RIBA) test (RIBA 3.0 SIA; Chiron Corporation,

Emeryville, CA, USA).

All confirmatory testing was performed at the VCT Center in Kabul by trained

laboratory personnel. All participants received a small nonmonetary gift and

risk-reduction counseling, with referrals for detoxification and needle and

syringe programs upon request.

Statistical Analysis

Prevalence of infection was calculated with confidence intervals (CIs) based

on Poisson distribution for HIV and binomial distribution for HBsAg and HCV.

The only female participant was excluded from remaining analyses. Correlates

of HIV, HBsAg, and HCV infection were assessed with univariate and

multivariate logistic regression analyses. Variables were entered into a

multivariate model if they were significantly associated with HIV, HBsAg, or

HCV infection at the 5% level in univariate analysis or showed epidemiologic

relationships. A multivariate model was generated to identify factors

independently associated with HIV, HBsAg, and HCV infections by using the

likelihood ratio test to determine which variables were retained.

Results

Sociodemographic Data and Prevalence of Infection

A total of 464 participants were enrolled; 463 were male. Fourteen

participants (3.0%, 95% CI 1.7%–5.1%) were infected with HIV, 30 (6.5%, 95%

CI 4.2%–8.7%) were positive for HBsAg, 170 (36.6%, 95% CI 32.2%–41.0%) were

infected with HCV, and 7 (1.5%, 95% CI 0.6%–3.1%) were coinfected with HIV

and HCV.

Among male participants, most were Afghan, had traveled outside Afghanistan

in the previous 10 years, and reported heroin as their most frequently used

drug in the past 6 months, either alone (42.4%) or with pheniramine maleate

(56.0%) (Appendix Table).

Risk Behavior

High-risk injection and sexual behavior were common. Sharing needles or

syringes (50.4%) and difficulty obtaining new syringes (43.6%) were

frequently reported. Patronizing female sex workers and having sexual

relations with men or boys were also common. More than half the participants

had been incarcerated; of these, nearly one third injected drugs while in

prison. A total of 23.1% had received a therapeutic injection in the past 6

months, and 5.2% had sold or donated blood (Appendix Table).

Correlates of HIV, HBsAg, and HCV Infection

No sociodemographic variables were significantly associated with HIV or

HBsAg infection. Sharing needles and injecting drugs while in prison were

associated with HBsAg by univariate logistic regression analysis (Appendix

Table). Multivariate analysis showed that HBsAg remained associated with

injecting drugs in prison (adjusted odds ratio 3.23, 95% CI 1.16–9.00).

Univariate analysis showed that those with HIV infections were more likely

to report needle or syringe sharing and injecting drugs for >3 years

(Appendix Table). No variables were independently associated with HIV

infection by multivariate logistic regression analysis (results not shown).

Participants with HCV infection were less likely to be educated or married

and had higher incomes (Appendix Table). HCV infection was associated with

needle or syringe sharing, injecting drugs for >3 years, having sex with men

or boys, and receiving injections from a nonmedical provider (Appendix

Table). Adjustment by demographic factors did not appreciably change these

relationships. Multivariate logistic regression showed that needle or

syringe sharing, injecting drugs for >3 years, and receiving injections from

a nonmedical provider were independently associated with HCV infection, and

inverse associations persisted for higher education level and for being

married (Table).

Discussion

This report is among the first to describe HIV, HBsAg, and HCV prevalence

and risk behavior in Afghanistan. The low HIV prevalence among IDUs in Kabul

is not surprising given the short median duration of injection drug use.

Although opium has been used for centuries in Afghanistan, our data are

consistent with the suggestion that injection drug use is a relatively new

behavior in this setting (10). Although HIV prevalence was low, 37% were HCV

infected, a finding that potentially foreshadows an HIV epidemic caused by

risk factors shared by these infections.

Injecting drugs in prison was related to HBsAg and marginally to HIV by

univariate analysis, which are similar to findings in Iran and other

settings (3,18,19). In Iran, Zamani et al. reported that that multiple

incarcerations increased likelihood of HIV infection (20). We did not

observe this relationship, but this result may be due to low statistical

power. However, 47% of the Iranian prison population is incarcerated because

of drug-related offenses (18). Afghan law allows an addict, as diagnosed by

a medical professional, to enter a detoxification facility, which may reduce

the number and exposure of IDUs to prison settings. Because one third of

Afghan IDUs who had been incarcerated reported drug injection in prisons,

prisons should remain a priority site for needle and syringe programs.

The established risk factors of needle sharing and duration of injection use

were strongly related to both HIV and HCV infections. The prevalence of

HBsAg was relatively low among the IDUs and close to that reported by

International Committee of the Red Cross/Crescent–supported blood banks in

2004. While only those with acute or active hepatitis B would have

circulating antigen, the prevalence of hepatitis B in this group still seems

comparatively low, given the prevalence of risky behavior. The prevalence of

HIV and hepatitis B infection may not have not reached sufficient levels to

result in a self-sustaining epidemic; further surveillance is warranted. The

prevalence of HBsAg likely underestimates the number of IDUs exposed to

hepatitis B. Because hepatitis B infection resolves after the acute phase in

90%–95% of those infected as adults, the actual proportion of IDUs infected

may approach or exceed 64.7% of participants (21). A more reliable number

might be accessed through testing for antibody to HbsAg, which might be used

to create a cost-effective vaccination program for this high-risk group.

Although donating blood was not associated with any of the 3 infections,

risk for bloodborne infection through iatrogenic routes deserves emphasis

because 8.3% of participants who reported donating or selling blood were

infected with HIV. A prior report estimated that only 30% of blood donations

were screened in Afghanistan (22). Furthermore, those infected with HCV were

more likely to have had injections from nonmedical providers, which has been

linked to a high prevalence of HCV and hepatitis B in neighboring Pakistan

(23).

Our study has some limitations. Respondent-driven sampling was not possible

because of concerns of compromising the identities of IDUs; participants

were enrolled by convenience sampling, which may not be representative of

IDUs in Kabul. Because risky behavior was assessed by self-reporting,

socially desirable responses may have been made. Analysis of factors

associated with HIV and HBsAg had low power because of low prevalence of

these infections, which potentially masks some associations. Additionally,

testing for surface antigen may have underestimated the true prevalence of

hepatitis B infection because only those with acute or chronic infections

would be detected. Another approach for future studies would be screening

for both surface antigen and antibody to HbsAg and offering vaccination to

IDUs negative for this antibody.

In summary, although prevalence of HIV and HBsAg is low among IDUs in Kabul,

the prevalence of HCV and high-risk behavior are alarmingly high. Political

instability, poverty, mobility, and low literacy may also increase

vulnerability of IDUs to HIV and other bloodborne or sexually transmitted

infections (13). During the study, 1 needle and syringe program and 3 drug

rehabilitation and counseling programs were operating in Kabul; opioid

substitution treatment was not available. Initiation or scale-up of

interventions, particularly needle and syringe programs and opioid

substitution therapy, are urgently needed to prevent an HIV epidemic among

Afghan IDUs. Attempts to prevent or control HIV and other bloodborne

infections among IDUs without adequate coverage of IDUs by harm-reduction

programs have been unsuccessful (24,25). However, settings with outreach

programs that linked VCT, needle and syringe programs, and opiate

substitution therapies have stabilized HIV prevalence among IDUs at low

levels (25,26). Political support for harm-reduction and HIV awareness

campaigns among the Ministries of Counter Narcotics, Public Health, and

Religious Affairs is present in Afghanistan; donor attention is urgently

needed to expand these efforts to avert an HIV epidemic.

Acknowledgments

We thank the Ministries of Public Health and Counter-Narcotics, the Kabul

Volunteer Counseling and Testing Center, and the Zindagi Nawin and Nejat

programs for their assistance, and the study participants for their time and

trust.

This study was supported by the Walter Army Institute of Research.

C.S.T. was supported by the Fogarty International Center of the National

Institutes of Health (K01TW007408).

Dr Todd is assistant professor in the Division of International Health and

Cross-Cultural Medicine at the University of California, San Diego. She is

currently based in Kabul, Afghanistan. Her research interests include the

epidemiology of HIV among high- and low-risk populations and the effect of

HIV on reproductive health.

References<CUT>

http://www.cdc.gov/eid/content/13/9/1327.htm?s_cid=eid1327_e

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