research article open access high coverage needle/syringe programs

Des Jarlais et al. BMC Public Health 2013, 13:53http://www.biomedcentral.com/1471-2458/13/53

RESEARCH ARTICLE Open Access

High coverage needle/syringe programs forpeople who inject drugs in low and middleincome countries: a systematic reviewDon C Des Jarlais1*, Jonathan P Feelemyer1, Shilpa N Modi1, Abu Abdul-Quader2 and Holly Hagan3

Abstract

Background: Persons who inject drugs (PWID) are at an elevated risk for human immunodeficiency virus (HIV) andhepatitis C virus (HCV) infection. In many high-income countries, needle and syringe exchange programs (NSP)have been associated with reductions in blood-borne infections. However, we do not have a good understandingof the effectiveness of NSP in low/middle-income and transitional-economy countries.

Methods: A systematic literature review based on PRISMA guidelines was utilized to collect primary study data oncoverage of NSP programs and changes in HIV and HCV infection over time among PWID in low-and middle-income and transitional countries (LMICs). Included studies reported laboratory measures of either HIV or HCV andat least 50% coverage of the local injecting population (through direct use or through secondary exchange). Wealso included national reports on newly reported HIV cases for countries that had national level data for PWID inconjunction with NSP scale-up and implementation.

Results: Studies of 11 NSPs with high-coverage from Bangladesh, Brazil, China, Estonia, Iran, Lithuania, Taiwan,Thailand and Vietnam were included in the review. In five studies HIV prevalence decreased (range −3% to −15%)and in three studies HCV prevalence decreased (range −4.2% to −10.2%). In two studies HIV prevalence increased(range +5.6% to +14.8%). HCV incidence remained stable in one study. Of the four national reports of newlyreported HIV cases, three reported decreases during NSP expansion, ranging from −30% to −93.3%, while onenational report documented an increase in cases (+37.6%). Estimated incidence among new injectors decreased inthree studies, with reductions ranging from −11/100 person years at risk to −16/100 person years at risk.

Conclusions: While not fully consistent, the data generally support the effectiveness of NSP in reducing HIV andHCV infection in low/middle-income and transitional-economy countries. If high coverage is achieved, NSP appearto be as effective in LMICs as in high-income countries. Additional monitoring and evaluation research is neededfor NSPs where reductions in HIV/HCV infection among PWID are not occurring in order to identify and correctcontributing problems.

Keywords: HIV, Hepatitis C, Needle and syringe programs, Syringe exchange programs, People who inject drugs,Injecting drug use

* Correspondence: [email protected] Baron Edmond de Rothschild Chemical Dependency Institute, BethIsrael Medical Center, New York City, USAFull list of author information is available at the end of the article

© 2013 Des Jarlais et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of theCreative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use,distribution, and reproduction in any medium, provided the original work is properly cited.

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Des Jarlais et al. BMC Public Health 2013, 13:53 of 13http://www.biomedcentral.com/1471-2458/13/53

BackgroundHuman immunodeficiency virus (HIV) and hepatitis C(HCV) are relatively efficiently transmitted through themulti-person use (sharing) of needles and syringes usedfor injecting illicit psychoactive drugs [1,2]. There are anestimated 16 million people who inject drugs (PWID) inthe world, of whom 13 million live in low and middle-income countries (LMIC) [3]. PWID who live in LMICare generally at very high risk for infection with HIV andHCV. High rates of HIV prevalence (>20%) have beenreported among PWID in Eastern Europe, Asia andAfrica [3].Programs to provide PWID with access to sterile nee-

dles and syringes (NSPs) are generally considered to beamong the most effective means of reducing HIV andHCV transmission among PWID [4,5]. There is a con-siderable body of research on NSP, and syringe exchangeprograms in particular. There is general consensus thatthese programs reduce risk behavior [6] (sharing of nee-dles and syringes) and large-scale implementation ofNSP has been associated with reductions in transmissionof HIV [7]. The great majority of studies of syringe ex-change programs, however, have been conducted inhigh-income countries. For example, in a Palmateeret al. review [8], 144 of the 152 included studies wereconducted in high-income countries.There are a number of reasons why NSP may not be

as effective in low/middle-income countries as in high-income countries. First, LMIC may not have the financialresources or the public health and non-governmentalorganizational infrastructure for successful large-scale im-plementation of NSP. Second, PWID in LMIC may facegreater stigmatization, leading to less utilization of theprograms in LMIC [9]. Third, there may be greater lawenforcement interference with PWID utilizing syringe ex-change programs in LMIC, particularly in locations wherePWID may be incarcerated in “detention” centers or inlocations where they may suffer extortion or brutalityfrom the police [10]. Finally, NSP in high-income settingsmay be implemented in the context of other large scaleevidence-based HIV/HCV-related prevention programssuch as opiate substitution therapy/medication-assistedtreatment [11]. The NSPs in high-income countries maythus benefit from the synergistic effects of “combined”prevention programming [12,13]. In contrast, NSP inLMIC are often implemented either by themselves or inthe presence of other prevention programs that exist onlyon a pilot project scale [14].Given the great need to reduce HIV transmission

among PWID in many LMIC, and the potential barriersto the effectiveness of programs in these countries,understanding what has happened with the programsthat have been implemented is likely to be critical forefforts in halting ongoing HIV epidemic among PWID.

In this review, we examine structural level NSP in dif-ferent LMIC around the world to determine if imple-mentation and scale up of NSP are associated withlongitudinal changes in blood borne infection amongPWID populations. By focusing on locations where NSPhave been implemented and scaled compared with loca-tions in which NSP have already been established, thisreview can help to elucidate the association betweenNSP implementation and changes in HIV/HCV preva-lence and/or incidence among the PWID populationserved by the NSP.

MethodsUnit of analysis and eligibility criteriaThe unit of analysis for this review was a NSP in a spe-cific location. In our search for eligible programs, weattempted to collect as much information as possible,including published and unpublished articles, conferencepresentations, and “gray” literature. This differs fromthe usual systematic review where individual researchreports or individual research studies are the standardunit of analysis. To be included in this review, the NSPhad to have reached a coverage level of 50% or more ofthe PWID in the local population (through either directservice provision or secondary exchange, in which PWIDreceive syringes from NSP and distribute to their PWIDpeers) and provide at least 10 syringes per injector peryear. This size criterion was used to distinguish betweenhigh coverage from programs that were “demonstrationprojects” or “pilot studies.” This level has also beenshown to be an adequate coverage level to influencepopulation level changes in rates of HIV and HCV infec-tion [15,16]. The amount of time that was needed foreach NSP to achieve structural level coverage varied;however, many of the studies achieved 50% coverageshortly after implementation, and by the follow-up bio-marker measurement, all NSP had achieved structurallevel coverage of their PWID.To include a specific program in the review, we

located data on when the program was implemented, in-cluding when it reached the minimum size requirement,and located data on either HIV/HCV prevalence or inci-dence from before and after implementation of the NSPprogram. We required that the HIV or HCV-related databe based on laboratory testing, not on self-reported ser-ostatus. Studies that used self-reported behavior changeas their outcome measure were not included because ofconcerns for social desirability effects and the often im-precise association between behavior change and changein HIV/HCV infection rates [17].A wide variety of research designs were included: ran-

domized clinical trials, time series analyses, cohort stud-ies, comparisons of injecting populations that receivedNSP with “comparable” injecting populations that did

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Search String

Search (randomized controlled trial[pt, #108] OR controlled clinical trial[pt, #108] OR randomized controlled trials[mh, #813] OR random allocation[mh, #813] OR double-blind method[mh, #813]OR single-blind method[mh, #813] OR clinical trial[pt, #108] OR clinical trials[mh, #813] OR ("clinical trial"[tw]) OR ((singl*[tw] OR doubl*[tw] OR trebl*[tw] OR tripl*[tw]) AND (mask*[tw] OR blind*[tw])) OR placebos[mh, #813] OR placebo*[tw] OR random*[tw] OR non-randomi*[tw] OR before after study[tw] OR time series[tw] OR case control[tw] OR prospective cohort[tw] OR retrospective cohort[tw] OR cross-section*[tw] OR prospective[tw] OR retrospective[tw] OR research design [mh:noexp] OR comparative study[mh, #813] OR evaluation studies[mh, #813] OR follow-up studies[mh, #813] OR prospective studies[mh, #813] OR control*[tw] OR prospectiv*[tw] OR volunteer*[tw] OR longitud*[tw] OR descripti*[title/abstract] OR study[title/abstract] OR evaluat*[title/abstract]) AND

Search (HIV Infections/prevention and control[MeSH] OR HIV[MeSH] OR hiv[tw] OR hiv-1[tw] OR hiv-2*[tw] OR hiv1[tw] OR hiv2[tw] OR hiv infect*[tw] OR human immunodeficiency virus[tw] OR human immune deficiency virus[tw] OR human immuno-deficiency virus[tw] OR human immune-deficiency virus[tw] OR ((human immun*) AND (deficiency virus[tw])) OR acquired immunodeficiency syndromes[tw] OR acquired immune deficiency syndrome[tw] OR acquired immuno-deficiency syndrome[tw] OR acquired immune-deficiency syndrome[tw] OR ((acquired immun*) AND (deficiency syndrome[tw])) OR (Hepatitis C/prevention and control[Mesh] OR hepatitis C[tw] OR hepatitis[title/abstract] OR HCV[title/abstract]) AND

Search (needle-exchange[title/abstract] OR needle exchange[title/abstract] OR needle/syringe program[title/abstract] OR needle/syringe programs[title/abstract] OR needle syringe[title/abstract] OR (needle[title/abstract] AND syringe[title/abstract]) OR needle/syringe program*[title/abstract] OR syringe-exchange[title/abstract] OR syringe exchange*[title/abstract] OR (supervis*[title/abstract] AND injecti*[title/abstract]) OR Combined program*[title/abstract] OR Combined prevention[title/abstract]) OR (needle*[title/abstract] AND access[title/abstract]) OR (syringe*[title/abstract] AND access[title/abstract]) OR ((injection drug user*[title/abstract] OR injecting drug user*[title/abstract] OR IDU[title/abstract]) AND pharmacy[title/abstract] OR pharmacies[title/abstract] OR dispensar*[title/abstract] OR chemist[title/abstract] OR chemists[title/abstract] OR apothecar*[title/abstract]) AND

Search (Needle-Exchange Programs[Mesh] OR Needle-Exchange Programs/legislation and jurisprudence[Mesh] OR Community Health Services[Mesh] OR Substance Abuse, Intravenous/prevention and control[Mesh] OR Health Policy[Mesh] OR Harm reduction[Mesh] OR Public health administration[Mesh] OR Regional health planning[Mesh] OR Preventive Health Services[Mesh] OR Local Government[Mesh] OR Government Agencies[Mesh] OR Community Health Planning[Mesh] OR Community Health Centers[Mesh] OR Program Evaluation[Mesh] OR Socioeconomic factors[Mesh] OR Delivery of Health Care[Mesh] OR Community Pharmacy Services/legislation and jurisprudence[Mesh] OR Legislation, Pharmacy[Mesh] OR structural intervention*[tw] OR politic*[title/abstract] OR community[title/abstract] OR region*[title/abstract] OR government[title/abstract] OR legislat*[title/abstract] OR law[title/abstract] OR policy[title/abstract] OR (structural[tw] AND intervention[tw]) OR (structural[title/abstract] AND intervention[title/abstract]))

Figure 1 Search terms and terminology used for retrieval of eligible citations and reports. This figure displays the terminology used to searchfor relevant studies. Keyword and subject terms were retrieved from previous research of systematic reviews on similar HIV/HCV topics among PWID.


not receive NSP, and pre-post comparisons. A wide var-iety of research designs, including many that do notpermit strong inferences about causation, were includedin order to capture as many studies as possible. Pro-grams for which we were able to locate data only afterfull NSP implementation were not included in thereview.Finally, the studies included had to come from loca-

tions defined by the World Bank as low/middle-incomecountries or transitional-economy countries [18]. Studiesfrom high-income locations were screened by research-ers, but not included in this review.

Search methodologySelection of studies for this review was based on a struc-tured literature review and analysis utilizing PreferredReporting items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines [19,20]. Systematic litera-ture searches were conducted to identify potentiallyeligible articles from journals and government/country

reports. Figure 1 describes in detail the search terms thatwere utilized for this review; the same search terminologywas used for each of the databases searched, whichincluded PubMed, EMBASE, Web of Science, and NLMGateway. In addition, we also searched conferenceabstracts from International AIDS Conferences (IAC)from 2000 through 2011 and International Harm Reduc-tion conferences (IHRA) from 2000 through 2011 [21],along with published reviews of needle and syringe ex-change programs throughout the world. For locations inwhich HIV or HCV information was available butcoverage information was not consistent (such as inBangladesh and Vietnam), we contacted researchersvia email with knowledge of the programs in each lo-cation to obtain the necessary coverage information ifavailable, including the number of PWID that visitthe NSP, the number of needles/syringes distributed,and the number of PWID that are covered by theNSP. The search included all studies published be-tween January 1st 1980 and November 30th 2011.

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Data abstraction and codingA standardized coding form was developed to documentpertinent information for each program. Informationcollected included demographics of the injecting popula-tion covered under the NSP, characteristics of the NSPincluding coverage and distribution information, and in-formation related to changes in HIV or HCV infectionsover time. If analysis of HIV or HCV infection data wasconducted on specific subgroups (such as by age, race,gender, etc.) these data were collected as well. Inaddition, we reported measures of changes in subgroupsor from multivariate modeling if studies reported effectswith adjustment for participant characteristics in relationto changes in HIV or HCV infection information overtime.Studies were independently coded by two research

associates (JF and SM). All coding forms were reviewedfor quality by the co-principal investigator (HH) beforefinalization, with disagreements in coding reviewed bythe principal investigator (DDJ).In locations where multiple studies described the same

NSP intervention, we compiled data across studies, fo-cusing on the most complete measures of exposure tothe NSP intervention with the most comprehensive re-view of HIV/HCV information including effect modi-fiers, adjustment for confounders, and length of theevaluation. We also combined data from multiple studiesof the same intervention if different aspects of the datawe needed were in different reports, e.g., number ofPWID in one report and numbers of syringes exchangedin a different report.

Types of interventionsWe were prepared to include both syringe exchange pro-grams and increased pharmacy sales programs as NSPs.However, all of the programs for which we were able toobtain the necessary data (see inclusion criteria above)were needle and syringe exchange programs.

Types of outcome measuresThe primary outcomes of interest in this review includechanges in prevalence or incidence of HIV, HCV, HIV/HCV co-infection or changes over time in newlyreported HIV or HCV cases of infection. For studies thatreported these measures for a specific subgroup, such asnew injectors vs. older injectors, race, age, ethnicity, lo-cation, or length of injecting career, these data wererecorded as well. For studies that included multivariatemodeling, adjusted effect sizes were presented if theywere based on changes in HIV or HCV infection dataamong PWID over time. Several studies used HIVprevalence among new injectors to estimate HIV inci-dence among new injectors, and we also included thosedata.

Analysis of included studiesWe performed a systematic review of the effects of ex-posure to NSP on incidence or prevalence of HIV andHCV infections among PWID in selected locations. Aquantitative synthesis was not conducted due to theconsiderable variations in time period of analyses, mea-sures of effect size, non-comparable study designs, thespecific operating characteristics of the programs, anduncertain bias across and between studies due to lack ofrandomization. A narrative analysis permits reviewing ofselected issues, cases, or events in depth identifiedthrough the systematic review [22], allowing for a morecomplete and detailed analyses not constrained by pre-determined categories.

ResultsDescription of search resultsFigure 2 displays the systematic search of the literature.Four domains were included in the search terms, includ-ing NSP terminology, pharmacy terminology, biomarkerterminology (HIV, HCV), and finally study design ter-minology. The original search comprised 1,291 citationsfrom a systematic search reviewed by two reviewers in-dependently (JF and SM) after removal of duplicaterecords not identified through the systematic import-ation of eligible studies from each database (NLMGateway, PubMed, Web of Science, and EMBASE). Add-itionally, we performed a secondary search of needle andsyringe exchange program papers utilizing reference listsfrom systematic review of NSP programs [8,23,24] andthrough collaboration with experts in the field of injec-tion drug use in low/middle and transitional incomelocations. An additional 570 articles/reports were obtainedand reviewed, and we identified an additional nine studiesfrom this secondary search after removal of duplicates fromthe secondary search. A total of 66 full text articles wereexamined, and 11 qualitative studies and reports wereobtained from this full text search.

Results of the searchA total of 11 studies/reports examining nine low/mid-dle-income or transitional-economy countries were eli-gible for inclusion in this NSP review based onlaboratory HIV or HCV results and greater than 50%coverage of the NSP within the respective community.These 11 studies described 12 distinct locations involv-ing NSP evaluated from 1990 through 2010. If multiplelocations in a single country were examined the data arepresented by location and by time period. Studiesincluded in this review cover locations in Bangladesh,Brazil, China, Estonia, Iran, Lithuania, Taiwan, Thailand,and Vietnam.

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T2

2045 Records identified through database searching

1861 Records after duplicates removed

66 Full-text articles assessed for eligibility

11 Studies included in qualitative synthesis

9 Records identified from National Reports

1861 Records screened

55 Full-text articles excluded due to:

•Did not describe structural intervention•Biomarker data not presented•Longitudinal data not available•Sample is not all PWID•Study did not come from a low or middle Income country

Figure 2 PRISMA diagram of eligible studies included in review. This figure displays the methodology of review of literature from databasesincluded in the review. The PRISMA diagram outlines how the research team arrived at the eligible study list utilized in this review.


Review of studies, summary of resultsThere were six studies that documented population levelchanges in HIV prevalence over time and three studiesthat documented population level changes in HCV in-fection prevalence or incidence over time. Of the sixstudies reporting on HIV prevalence, four studies reportedpopulation level decreases in prevalence ranging from−3% to −15% while two studies reported population levelincreases ranging from +6% to +16%. Of the three studiesreporting on population level HCV infection prevalenceor incidence, all reported decreases in prevalence rangingfrom −4.2% to −10.1%, while one study reported a stablepopulation level incidence of 1.2-1.3/100 person years(PY). Estimated HIV incidence among new PWID(defined as less than three years of injecting history)decreased in three studies ranging from −16/100 PY to−11/100PY. Table 1 summarizes the HIV and HCV infec-tion prevalence/incidence studies included in the review.National surveillance reports were evaluated for

changes in newly reported HIV cases during NSP expan-sion in Iran, Taiwan, Lithuania and Vietnam. Reports

from Iran, Taiwan and Vietnam reported decreases innewly reported HIV cases, ranging from −30% to −93.3%.Lithuania reported an increase of +37.6% in newly reportedHIV cases among PWID. Table 2 summarizes the changesin newly reported HIV cases among PWID during imple-mentation of NSP services.

Included studiesThere were nine primary research articles included in thisreview: Azim 2008 [28], Azim 2009 [29], Caiaffa 2003 [26],Wu 2007 [27], Hammett 2006 [36], Des Jarlais 2007 [37]and Hammett 2012 [31], Uuskula 2011 [30], and Gray1998 [25]. Additionally, there were four national surveil-lance reports included: Iranian MOH 2007 [32], Astraus-kiene 2010 (Lithuania) [33], CDC 2010 (Taiwan) [34], andHammett 2012 (Vietnam) [35].

Primary study interventionsDhaka BangladeshIn Bangladesh, NSP were expanded significantly startingin 1998 with full implementation occurring in 2000. By

Table 1 Summary of primary studies with HIV/HCV biomarkers

Study Information Coverage Pre-Implementation and Expansion Post-Implementation and Expansion

Investigator Location Study Design Syringes perPWID/Year1

Year (n) HIVprev.

HCVprev.

EstimatedHIVinc.2

HCV inc. Year (n) HIV prev.3 HCVprev.3

EstimatedHIVinc.2

HCVinc.

Gray 1998 [25] Chiang Rai,Thailand

Time Series CrossSectional

150-160 1993 46 33% 1996 132 18% (15%)

Caiaffa 2003 [26] Porto Alegre, Brazil Pre-Post StudyComparison

6-20 1998 137 49% 2001 255 64.3%(+16%)

Wu 2007 [27] Dagou, China Pre-Post StudyComparison

290-300 2002 235 40% 99% 2003 226 34% (6%) 89% (10%)

Luzhai, China Pre-Post StudyComparison

140-150 2002 194 56% 89% 2003 219 53% (3%) 85% (4%)

Azim 2008 [28] Dhaka, Bangladesh Time Series CrossSectional

285-344 1990 418 2% 67% 2006 1092 7% (+5%) 57% (10%)

Azim 2009 [29] Dhaka, Bangladesh Time Series CrossSectional

285-344 1999 418 1.2/100PY

2007 1045 1.3/100PY

Uuskula 2011 [30] Tallinn, Estonia Time Series CrossSectional

23-78 2005 350 54% 20.9/100PY

2009 327 50% (4%) 9/100 PY

Hammett 2012[31]

Ning Ming, China Time Series CrossSectional

20-30 2002 290 17% 12/100 PY 2008 187 11% (6%) 11/100 PY

Lang Son, Vietnam Time Series CrossSectional

20-30 2002 342 46% 22/100 PY 2009 185 23% (23%) 3/100 PY

1. Syringes per PWID/Year are given as a range based on the first and last date of data collection in each primary study location.2. Among new PWID (persons who had begun injecting in the previous 3 years, assumed to be HIV negative when they began injecting).3. Post Implementation columns include follow-up biomarker information in addition to the difference from baseline to follow-up.

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Table 2 Summary of National Surveillance Data of HIV Biomarkers

Country Report Information Coverage Pre Implementation and Expansion Post Implementation and Expansion

Investigators Location Surveillance Method Syringes per PWID/Year1 Year Baseline HIV cases (n) Year Follow-up2 HIV cases (n) (Percent Change)

CDC 2007 [32] Iran National Surveillance Data 4-41 2003 2332 2007 426 (82%)

Astrauskiene 2010 [33] Lithuania National Surveillance Data 56-98 2005 85 2009 117 (+38%)

CDC 2010 [34] Taiwan National Surveillance Data 7-67 2006 1693 2010 114 (93%)

Hammett 2010 [35] Vietnam National Surveillance Data 9-52 2005 11358 2009 7947 (30%)

1. Syringes per PWID/Year are given as a range based on the first and last date of data collection in respective study.2. Post Implementation columns include follow-up biomarker information in addition to the difference from baseline to follow-up.

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1999, the NSP served a population of 3,500 PWID, cov-ered 89-93% of the PWID in Dhaka, and distributed upto three syringes and six needles per injector per weekwith an average needle and syringe exchange rate of 73%among program participants [28].Azim 2008 [28] and Azim 2009 [29] recruited male

PWID from NSP, detoxification centers, and clinics inDhaka, Bangladesh to analyze prevalence and incidenceof HIV and HCV infection. Azim 2008 [28] examined3,759 male PWID from 1999–2006 and documented anHIV prevalence increase from 1.4% (1999–2000) to 7%(2006). HCV infection prevalence decreased from 66.5%(1999–2000) to 56.4% (2006).Azim 2009 [29] analyzed PWID HIV incidence from

1998–2007. The HIV incidence among PWID remainedstable at 1.16/100 PY (1998–1999) to 1.29/100 PY (2007)while HCV infection incidence among PWID decreasedfrom 37.50/100 PY (1998–1999) to 11.58/100 PY (2007).Azim 2009 reported decreases in several injection

related behaviors; borrowing of needles/syringes decreased10.6% while lending of needles/syringes decreased 29.8%.Additionally, long term PWID were more likely to utilizethe NSP; those who had at least a 10 year history of injec-tion drug use were nearly three times more likely to utilizethe NSP compared to PWID who had been injecting forless than 10 years.

Porto Alegre BrazilNSP programs in Porto Alegre were started in 1996 withcooperation from the public health system in conjunc-tion with municipal and state authorities. In 1998, theNSP program distributed approximately 48,000 needles/syringes, increasing to over 150,000 in 2002 with an ex-change rate of nearly 50%; the NSP serve a population ofapproximately 7,000 to 8,000 PWID.Caiaffa 2003 [26] recruited PWID from non-institutio-

nalized locations in Porto Alegre in 1998 (when NSPwas still in its scale up and expansion period), and againin 2000–2001 (when NSP had become fully establishedin the city). PWID in both samples were predominatelyyoung (average age: 28–31 years old), male (81-84%),and injected mainly cocaine (74-87%). Both samples hadmoderate to high levels of sharing in the last six months(36-59%), and 60% had ever visited the NSP at leastonce. HIV prevalence among PWID in Porto Alegreduring NSP implementation increased from 48.5%(1998) to 64.3% (2000–2001). No explanation was givenby authors related to the changes in HIV infectionprevalence seen among locations without NSP in place.

Dagou & Luzhai ChinaIn 1998 the Ministry of Health of China promoted socialmarketing of safe injection as part of their HIV/AIDSprevention strategy. The first NSP were started in Dagou

and Luzhai with ramp up beginning in 2002. The num-ber of NSP locations in China increased from 93 sites inMarch 2006 to 729 by December 2006.Wu 2007 [27] analyzed the impact of NSP on HIV

prevalence in Dagou and Luzhai and compared resultsto two cities in China that did not have NSP programsin place, Yu’nan and Yongning. PWID were recruitedinto the study from several locations including detoxifi-cation centers and community outreach. In all four loca-tions in which PWID were recruited (Dagou, Luzhai,Yu’nan, and Yongning), PWID were predominantly maleand between 20 and 39 years of age.Both locations that had NSP documented decreases in

HIV and HCV infection prevalence. In Dagou, HIVprevalence decreased from 40% (2002) to 33.6% (2003)(p = 0.16), while HCV infection prevalence decreasedfrom 98.7% (2002) to 88.5% (2003) (p < 0.01). In Luzhai,HIV prevalence decreased from 56.2% (2002) to 53.2%(2003) (p = 0.54), while HCV infection prevalencedecreased from 88.7% (2002) to 84.5% (2003) (p = 0.22).In the cities that did not have NSP in place, changes in

HIV and HCV infection prevalence varied. In Yu’nan,HIV prevalence remained stable at 17.6% (2002–2003)(p = 0.99), while HCV prevalence decreased from 88.1%(2002) to 58.5% (2003) (p < 0.01). In Yongning HIVprevalence increased from 22.4% (2002) to 24.1% (2004)(p = 0.68) while HCV infection prevalence increasedfrom 81.6% (2002) to 88.2% (2004) (p = 0.07). No ex-planation was given by authors related to the changesseen in HIV and HCV infection prevalence seen amonglocations without NSP in place.

Lang Son Province Vietnam & Ning Ming County ChinaThe “Cross-Border” intervention took place in the regionsof Lang Son Province, Vietnam and Ning Ming County inthe Guangxi province in China. The intervention involvedpackaged harm reduction services, including a pharmacy-based voucher program for acquiring clean needles/syr-inges along with clean injecting equipment and condoms.On average, 7,000 to 10,000 needles/syringes were distrib-uted per month at each location, serving a population ofapproximately 3,000 PWID in each region. Three studiesreported on changes in HIV prevalence in these locations,Hammett 2006 [36], Des Jarlais 2007 [37] and Hammett2012 [31]; this review includes the more complete analysisutilizing a longer follow-up period from Hammett 2012.Hammett 2012 [31] documented changes in HIV preva-

lence and HIV incidence among new PWID over an eightyear period in conjunction with NSP expansion in bothlocations beginning in 2002 of which six years of data wasavailable for Ning Ming while seven years of data wasavailable for Lang Son. 2125 PWID were included in theNing Ming sample and 2677 PWID were included in theLang Son sample.


In Ning Ming, HIV prevalence decreased from 17% to14% after 12 months, and then stabilized at 11% after72 months (p = 0.003). In Lang Son, HIV prevalencedecreased to 43% after 12 months and decreased furtherto 23% after 84 months (p < 0.001). When examining onlynew PWID, defined as injectors that had injected for threeyears or less, HIV incidence in Ning Ming decreased from12/100 PY to 9/100 PY after 12 months and stabilizedat 11/100 PY after 72 months. Among new PWID in LangSon the HIV incidence decreased from 22/100 PY to16/100 PY after 12 months and decreased further to 3/100PY after 84 months (p < 0.001).

Tallinn EstoniaNSP was implemented in Estonia in 2003 with the ma-jority of services provided in the capital city of Tallinn,where nearly 75% of the PWID in Estonia are located.The NSP serve a population of approximately 10,000PWID and have increased needle/syringe distributiongreatly since implementation, from 18,000 needles/syr-inges distributed in 2003 to over 770,000 by 2009.Uusküla 2011 [30] recruited 1,027 PWID between

2005 and 2009, of which 168 were new injectors (definedas having injecting histories of three years or less). Thesample was predominately male (80%), Russian (80%),and young (mean ages: 24 to 27 years old). Among newinjectors, subjects were predominately male (74-82%),Russian ethnicity (78-89%), and mainly injected fentanyl(48-61%) or amphetamine (32-47%). High levels of re-ceptive needle/syringe sharing were documented amongnew PWID, with rates ranging from 74-79%.HIV prevalence in the entire sample decreased slightly

from 54% (2005) to 50% (2009). However, when examin-ing only new injectors, HIV prevalence decreased from34.2% (2005) to 15.8% (2009) (p = 0.046); after control-ling for age, gender, injection frequency and NSP use,the change in overall HIV prevalence among new injec-tors remained statistically significant (χ2 = 8.31, p =0.016). Estimated HIV incidence among new injectorsdecreased from 20.9/100 PY (2005) to 9/100 PY (2009)(p = 0.026).Several injection-related behaviors were measured in

the study among the PWID sample; during the studyperiod, receptive sharing of needles/syringes decreased5% and the percentage of injectors that utilized NSPincreased from 44% in 2005 to 76% in 2009.

Chiang Rai ThailandThe NSP in Chiang Rai Province Thailand originallybegan in 1992 in three of the nine Akha hill tribe villagesin northern Thailand. Five thousand needle and syringekits were provided by the government for vaccinationand were subsequently distributed among 46 PWID in

three villages from 1992 to May 1994. During the periodof evaluation, needles were not allowed to be distributedfor the purposes of needle exchange; however, there wasan agreement made that allowed for this small village toreceive needles and syringes in response to the elevatednumber of new infections among PWID in the hill tribevillages. In 1995 a grant from the Australian governmentallowed implementation of NSP in all nine villages. TheNSP served approximately 132 PWID and allowed up to12 needles/syringes to be acquired per month for eachPWID.Gray 1998 [25] analyzed the impact of the NSP on

HIV prevalence among PWID in Akha hill tribe villagesin Chiang Rai Province Thailand from 1993–1996. AllPWID in this location were included in the study; 46were part of the 1993–1994 sample while 132 were partof the follow-up 1995–96 sample. The samples were typ-ically male (85%) and injected primarily heroin.Over the course of the study, the HIV prevalence

among PWID decreased from 33% (1993) to 18% (1995–1996).

National surveillance report interventionsIslamic Republic of IranThe first NSP in the Islamic Republic of Iran was estab-lished in 2003 [32]. Programs slowly increased after2003 as laws were reformed so PWID were not arrestedif they were covered by prevention and care services in-cluding drop-in centers which offer NSP [38]. In 2007there were 4,665,512 needles/syringes distributed, withan average of 41 needles/syringes distributed per PWIDper year; during the same time period NSP sitesincreased from 170 in 2008 to 637 by 2010 [21].The Center for Disease Management at the Iranian

Ministry of Health reported national surveillance dataon annual newly reported cases of HIV among PWIDundergoing testing at surveillance sites from 1986 to2007. The number of newly reported cases among PWIDcontinued to increase through the late 1990s and early2000s with 2332 cases in 2003, and a peak of 3145 newcases in 2004. However, with the implementation andscale-up of NSP services, the number of newly reportedcases among PWID began to drop to 2,293 cases in2005, 1,658 cases in 2006, and 426 cases in 2007.

LithuaniaIn early 1997 NSP was first introduced in Lithuania viamobile and illegal underground needle/syringe distribu-tion. In 2006 NSP was legalized in Lithuania, and by2009, there were 12 NSP sites in Lithuania serving ap-proximately 3,200 PWID. The number of needles/syr-inges distributed increased starting in 2006 and by 2008313,000 needle/syringes were distributed to PWID, de-creasing to 188,000 in 2009. No explanation was given


by the report as to the reason for the decrease in distri-bution in the last year of data analysis.Astrauskiene 2010 [33] reported national newly

reported HIV cases among PWID, collected by the Min-istry of Health of Lithuania. The number of newlyreported HIV infections among PWID decreased from85 cases in 2005 to 62 cases in 2006, 59 cases in 2007,and 42 cases in 2008. However, in 2009, there was an in-crease with 117 newly reported cases among PWID. Theincrease in cases in 2009 coincided with a significant de-crease (40%) in needle/syringe distribution.

TaiwanIn 2005, Taiwan instituted NSP on a trial basis through-out the country. By 2006 NSP in Taiwan had ramped upto full-scale operation with a 900% increase in coverageof PWID during the first two years of operation. A totalof 450,000 needles/syringes were distributed in the firstyear, expanding to nearly four million in 2007, servingapproximately 60,000 PWID.A 2010 Taiwan Center for Disease Control (CDC) [34]

document reported national surveillance data of newlyreported HIV cases among PWID. Surveillance data cap-tured in this analysis include all HIV incident PWIDcases registered with CDC Taiwan between 2006 and2010. The number of newly reported HIV cases amongPWID decreased from 1,693 cases in 2006 to 114 casesin 2010.

VietnamNSP programs in Vietnam were started as pilot projectsin 1993, with major scale-up occurring in 2005 as a re-sult of the HIV Prevention Project implemented by theWorld Bank. In 2006, HIV/AIDS law mandated harm re-duction activities that included NSP, leading to expan-sion from 21 provinces in 2005 to over 60 provinces by2009. During this same time period, the number of nee-dles/syringes distributed increased from two million in2006 to over 11 million in 2007, serving approximately215,000 PWID.Vietnam surveillance data among at risk groups col-

lected newly reported HIV cases from 2005 through2009, coinciding with the period of expanding NSP inthe country [35]. During this time period, the number ofHIV cases among PWID decreased from 11,358 in 2005to 7,947 cases in 2009.

DiscussionBefore considering the substantive findings, it will beuseful to consider limitations on the quantity and qualityof the data on NSPs in low-and middle-income coun-tries. As noted in the introduction, previous systematicreviews of NSPs in LMICs included only two programs,while we were able to locate data from 11 programs,

despite stricter eligibility criteria such as biological mea-sures of HIV or HCV as outcomes. Still, that we wereable to obtain the needed information for only a modestnumber of NSP in LMICs raises concerns. Given ourdifficulties in finding data on NSPs in LMICs, we haveto conclude that that the NSPs included in our system-atic review probably do not reflect typical operations ofNSPs in low/middle-income countries. As programswith better implementation are probably more likelyto report data, it is likely that the data included inour review probably reflect NSPs with better reportingmechanisms, supportive policies, or program operationsthan “average.”The data for the programs included in this study often

had considerable imprecision and variability. Coveragein terms of the percentage of PWID who were reachedor the numbers of syringes exchanged per PWID peryear was often quite imprecise, as the estimates of PWIDin the local area often had very wide ranges, and thenumbers of syringes exchanged was sometimes reportedas a range rather than a simple count.Another aspect of imprecision in the data comes from

using changes in HIV and/or HCV infection prevalenceand newly reported HIV cases among PWID as outcomemeasures. Changes in HIV or HCV infection incidencewould be the most desirable outcome measure, but arequite difficult to measure for both practical and ethicalreasons. An ethically conducted cohort study would needto provide good access to sterile injection equipment tosubjects and thus may not reflect HIV or HCV infectionincidence in the local PWID population. Estimating HIVincidence from HIV prevalence among new injectorsrequires the assumption new injectors were HIV seronega-tive when they began injecting, which is may not be validif there is substantial sexual transmission in the local area.Changes in HIV/HCV co-infection prevalence reflect bothchanges in the rate of new infections and differential lossof HIV/HCV-infected versus HIV/HCV-uninfected per-sons in the local population. (It is likely that more HIVseropositives will be lost from the active injecting popula-tion than HIV-negatives due to HIV-related morbidity andmortality). Changes in the numbers of newly-diagnosedHIV infections among PWID also have limitations as anoutcome measures. They may reflect changes in surveil-lance methods and even if the surveillance methods donot change, the time between when a new HIV infectionoccurs and when it is reported may be substantial and thereporting lag may itself change over time. We did not for-mally grade the quality of the data in the different studies,as there typically was not sufficient detail reported in thestudies for differentiating data quality among these studies.It is our impression, however, that there was no relation-ship between the quality of the data and the size of the de-cline in HIV or HCV prevalence across the studies.


Additionally, most of the changes in HIV/HCV infec-tion incidence or prevalence in the studies reported herealso suffer from the lack of any comparison group.All of these methodological limitations are likely to

persist in assessing the effectiveness of large-scale NSP forHIV prevention among PWID. Communities are the ap-propriate unit of analysis for assessing implementation ofhigh coverage NSP programs, so any studies with compari-son groups would have to be very large and would likely belogistically complex. Also, given the current data on the ef-fectiveness of NSPs, it would be unethical to fail to provideNSPs to PWID simply for the sake of conducting research.

InterpretationDespite the limited quantity of data on NSPs in low-andmiddle-income countries, we do believe that the data pre-sented here can be used to address three critical questionsabout NSPs in LMICs.1. Is there a “critical coverage” level of syringe distri-

bution and PWID in NSP to affect change in HIV orHCV infection incidence or prevalence? The numbers ofsyringes distributed per PWID per year varied greatlyamong the studies reported here, and there are only amodest number of studies. Nevertheless, the data pre-sented in Table 1 suggest that 20–30 syringes per yearper PWID might be considered a minimum level ofcoverage that would lead to population-level effectsamong opiate-using populations [16]. Note that in thePorto Alegre study, only 20 syringes were distributed perPWID per year, and cocaine was the primary druginjected. As cocaine is often injected at very high fre-quencies, it is likely that more syringes per PWID peryear are needed to control HIV transmission amongcocaine-injecting populations.2. What is the “causal lag” time period before a high

coverage NSP will lead to changes in HIV incidence orprevalence in a population of PWID? With the exceptionof the Bangladesh studies, all of the studies reportedhere showed the changes in HIV or HCV infection inci-dence or prevalence occurring within relatively shorttime periods, typically 2 to 4 years. This does suggestthat implementation of high coverage of PWID and ster-ile injection equipment may have effects within veryshort time periods [39].3. Is high-coverage of sterile injection equipment and

PWID in NSP programs in LIMCs as effective as NSPsin high-income countries? A number of the studiesreported here do show rather substantial reductions inHIV infection associated with the implementation ofhigh coverage NSPs. These are most clearly seen in thestudies that measured HIV incidence or estimated HIVincidence (through prevalence among new injectors) orused newly reported HIV cases. In the Estonia study, esti-mated HIV incidence among new injectors fell by half

while in the Cross-Border studies (China and Vietnam),estimated HIV incidence among new injectors fell by ap-proximately three quarters or more. Even in the Bangla-desh study, where HIV incidence was stable over eightyears at slightly over 1/100 person-years at risk, keepingincidence this low over such an extended period can beconsidered a prevention success.For the NSP where newly reported HIV cases were used

as an outcome measure, the reductions ranged from 30%to 93%. The data from Lithuania, however, showed a sub-stantial increase in newly reported HIV cases in the lastyear of the study period, coincident with a reduction insyringes distributed during that year. There also has beena recent outbreak of HIV among PWID in Greece thatwas associated with low implementation of preventionservices [40,41].Overall, the data in Table 1 suggests that NSPs in

LMIC show similar rates of reduction in HIV incidenceand prevalence as NSPs in high-income countries [8].There are, however, examples from both high-incomeand LMICs where NSPs have not prevented outbreaksof HIV transmission among PWID [39,42].With the possible exceptions of the estimated HIV

prevalence in Guangxi province China [27] and the num-bers of newly reported HIV cases in Taiwan, the studiesreviewed here provide little evidence that the NSPs inthese locations are eliminating injecting-related HIVtransmission in the local population of PWID. Some ofthe estimated incidence rates are still unacceptably high,from 4/100 to 9/100 person-years at risk. Large-scale“combined” HIV prevention programming, with not onlyNSPs but also substance dependence treatment, HIVcounseling and testing and anti-retroviral treatment forHIV seropositives may be required to reduce HIV trans-mission to a level where zero new injecting-related infec-tions becomes a realistic public health goal.

ConclusionsWe conducted a systematic review of NSPs in low-andmiddle-income countries. The inclusion criteria includedhigh coverage of at least 50% of local PWID participatingin the program or a minimum of 10 syringes distributedper PWID per year, HIV and/or HCV biomarker outcomedata, and data for pre and post high-coverage implemen-tation of the NSP. We were able to locate the needed datafor only 11 such NSPs. (Previous reviews had includedonly two of these NSPs). The data suggest that a mini-mum of 20 to 30 syringes per PWID per year may beneeded to affect HIV and/or HCV transmission in a popu-lation of PWID. Reaching high coverage levels (between20–30 syringes per PWID per year and at least 50% of thePWID population) for NSP is very likely to be followed byreductions in HIV and/or HCV infection in the localpopulation of PWID [16]. Additional prevention and


treatment services for PWID may be needed, however, inorder to eliminate HIV among PWID in low and middleincome countries.

Competing interestsThe authors declare that they have no competing interests.

Authors’ contributionsJF and SM conducted the review of the literature, extracted the pertinentdata, and performed analysis of the individual study and nationalsurveillance data; DDJ, JPF and HH wrote the first draft of the manuscript;HH and DDJ provided strategic advice and assisted with editing of themanuscript; DDJ supervised the project, and all authors read and approvedthe final manuscript.The findings and conclusions in this report are those of the authors and donot necessarily represent the views of the organizations and/or agencies theauthors are affiliated with.

AcknowledgmentsThis study was funded by the National Institutes of Health (R01 AI 083035–02). The review is conducted in parallel with a Cochrane Systematic Reviewon high income countries utilizing different inclusion criteria, but benefitedfrom joint discussions between the two research teams. The views expressedin this publication do not necessarily represent the position of the NationalInstitutes of Health, Beth Israel Medical Center, the Centers for DiseaseControl and Prevention, or New York University.

Author details1The Baron Edmond de Rothschild Chemical Dependency Institute, BethIsrael Medical Center, New York City, USA. 2Centers for Disease Control andPrevention, Atlanta, USA. 3College of Nursing, New York University, New YorkCity, USA.

Received: 18 April 2012 Accepted: 7 January 2013Published: 19 January 2013

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doi:10.1186/1471-2458-13-53Cite this article as: Des Jarlais et al.: High coverage needle/syringeprograms for people who inject drugs in low and middle incomecountries: a systematic review. BMC Public Health 2013 13:53.

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