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Khatib et al.

BMC Public Health (2017) 17:917


DOI 10.1186/s12889-017-4933-0

RESEARCH ARTICLE Open Access

HIV and hepatitis B and C co-infection


among people who inject drugs in
Zanzibar
Ahmed Khatib1*, Eva Matiko2, Farhat Khalid1, Susie Welty3, Ameir Ali1, Asha Othman1, Shaaban Haji1,
Mohammed Dahoma4 and George Rutherford3

Abstract
Background: People who inject drugs are at high risk of acquiring hepatitis B (HBV), hepatitis C (HCV), and human
immunodeficiency virus (HIV) due to risky injection and sexual practices. The objective of this study is to investigate
the epidemiology of HIV, hepatitis B, and hepatitis C, and co-infection of these viruses among people who inject
drugs in Zanzibar, Tanzania.
Methods: We used respondent-driven sampling to identify 408 participants, from whom we collected demographic
data, information on sexual behaviours and injection drug practices, and blood samples for biological testing.
Results: Prevalence of hepatitis B surface antigenaemia, HCV, and HIV infection were 5.9, 25.4, and 11.3%, respectively.
Of the participants who were hepatitis B surface antigen (HBsAg) positive, 33.5% were infected with HCV and 18.8%
were infected with HIV. Of the HCV-infected participants, 29.3% were infected with HIV. Of the participants who were
infected with HIV, 9.0% were HBsAg positive, 66.6% had HCV and 8.5% had both. None of the potential risk factors we
measured were associated with HBsAg positivity. In contrast, older age and longer duration of injection drug use were
independently associated with HCV infection. HCV infection among people who inject drugs is lower in Zanzibar than
in other countries, but could rise without proper interventions.
Conclusions: These findings underscore the importance of screening people who inject drugs for HIV, HBsAg, and
HCV; providing HBV vaccination to those who are eligible; initiating antiretroviral therapy for those who are co-infected
with HIV/HBV and HIV/HCV; and introducing interventions that have high impact on reducing needle sharing.
Keywords: Co-infection, Hepatitis B, Hepatitis C, Human immunodeficiency virus, Injecting drug users, Respondent-
driven sampling, Zanzibar, Tanzania

Background [5]. Like HIV, HBV and HCV can be spread by unsafe in-
An estimated 16 million people injected drugs world- jection practices [6], increasing the chances of PWID ac-
wide in 2007 (range 11–21 million) [1]. People who in- quiring both viral hepatitis and HIV. It is estimated that
ject drugs (PWID) have an elevated risk of acquiring between 5 and 25% of the HIV-infected persons also
parenterally transmitted infectious diseases, as the prac- have HBV and/or HCV [7–9].
tice of sharing needles and other injection equipment There are approximately 3000 PWID in Zanzibar
can result in microtransfusions of blood and/or serum. [10]. Injection drug use is facilitated by its location on
There are an estimated 1.2 million PWID chronically in- the Indian Ocean coast of Africa along drug trafficking
fected with hepatitis B virus (HBV), 6.4 million with routes [11]. Like in other East African coastal cities, in-
hepatitis C virus (HCV) [2–4], and 3 million with HIV vestigators in Zanzibar have started reporting outbreaks
of HIV infection associated with injection drug use [12].
* Correspondence: ahmedbenga@yahoo.com
In Zanzibar, the prevalence of HIV, HBV, and HCV
1
Zanzibar AIDS Control Program, Ministry of Health, Zanzibar, United among PWID has previously been reported as 16, 6.5,
Republic of Tanzania and 26.9%, respectively [13]. However, little is known
Full list of author information is available at the end of the article

© The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

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Khatib et al. BMC Public Health (2017) 17:917 Page 2 of 6

about their burden of co-infection. Given that PWID are and this was assumed to be equivalent to their duration
more vulnerable to blood-borne infections due to their of injection drug use.
risky injection practices, data on co-infection among this We based power and sample size estimates on achiev-
population is especially important. We used the oppor- ing desired precision around point estimates for HIV in-
tunity of a recent HIV integrated bio-behavioural survey fection in PWID. We based the HIV prevalence at 16%,
in Zanzibar to understand the epidemiology of HIV and with a 95% confidence interval of 11.6–21.6% leading to
HBV and HCV co-infection among PWID. To our a sample size of 407, after correction for an expected de-
knowledge, no studies have been conducted on this sub- sign effect of 1.8, based on the literature available at the
ject in Zanzibar. time of planning the study [16].
We tested blood serum for HIV antibodies using a ser-
Methods ial algorithm in accordance with the national testing
We conducted a cross-sectional survey to assess the guidelines for HIV. We screened all specimens using
prevalence of hepatitis B surface antigen (HBsAg) car- Determine HIV1/2 test (Abbott Diagnostic Division,
riage and HCV seropositivity and associated risk be- Hoofddorp, The Netherlands) and retested reactive spec-
haviours among PWID on Zanzibar Island in 2012. imens using Unigold (Trinity Biotech, Bray, Ireland). To
Zanzibar Island is the main island of the Zanzibar archi- ensure data quality, we conducted an external quality as-
pelago, a semiautonomous region of the United Republic sessment and retested 10% of the non-reactive samples
of Tanzania. Study methods have been described in de- and all of the HIV reactive samples. We also retested the
tail elsewhere [10]; to summarize, we recruited male and last test used in the field, followed by a series of ELISA
female PWID aged 15 years and above, who had lived in tests, which were performed at the National Health La-
Zanzibar the prior 3 months and who had injected illicit boratory Quality Assurance and Training Center, the na-
drugs in the prior 3 months. We used respondent-driven tional reference laboratory in Dar es Salaam.
sampling (RDS), a social network-based recruitment We tested blood serum for HBsAg using ACON
methodology that allows weighted adjustment of key HBsAg (ACON Laboratories, Inc., Hangzhou, China), a
variables to produce unbiased representative results for qualitative, lateral flow immunoassay for detection of
difficult-to-reach and hidden populations [14, 15], to HBsAg in serum or plasma. We measured antibody to
identify prospective study participants. We recruited six HCV using ACON Hepatitis C (ACON Laboratories, Inc.,
seeds, or initial participants identified through existing Hangzhou, China) virus test strip, a qualitative, membrane-
peer groups or organizations that work with PWID, to based immunoassay for the detection of antibody to HCV
begin initial recruitment and added an additional three in serum or plasma. The Centers for Disease Control and
seeds in the fourth study week to increase recruitment Prevention’s Hepatitis Laboratory in Atlanta, USA, con-
rates; of the nine seeds, two were female and seven were ducted external quality assurance (EQA) for HBsAg and
male. We distributed 1235 coupons and recruited 518 HCV testing.
potential participants. The longest chain in this survey After all samples had been collected and tested locally,
was 21 waves. One hundred and nine individuals (21%) we stored all reactive and 10% of non-reactive samples
did not meet the eligibility criteria, and one (< 1%) did at Mnazi Mmoja Laboratory at −20 °C prior to transpor-
not consent to participate, resulting in a study popula- tation to Atlanta. We conducted an external quality as-
tion of 408 eligible PWID. All participants received sessment once all samples had been collected and tested.
$3.90 for completing the survey and providing a blood We used the Respondent-Driven Sampling Analysis
specimen and $1.30 for each successful recruit regardless Tool (RDSAT) 6.0.1, an open-source software package
of sex. Trained project staff assessed candidates’ eligi- (www.respondentdrivensampling.org), to analyse data on
bility for enrolment and collected demographic infor- the prevalence of HBsAg, HCV, and HIV; sexual and
mation and self-reported sexual and injection risk drug-related risk behaviours; demographic characteris-
behaviour data through structured in-person interviews tics; and other variables, with adjustments for social net-
conducted by gender-matched interviewers. The net- work sizes and recruitment patterns. We calculated
work size was assessed by asking, “How many PWID do estimators and 95% confidence intervals for sexual and
you know personally (i.e., who are living in Unguja, are other risk factors associated with HBV and HCV trans-
aged 15 years and above, you know their name, you mission using partition and then prevalence analysis. We
know who they are, and they know you)?” This was also used RDSAT to produce weights for the dependent
followed by a question asking how many of those they variable used in multivariate analyses and exported these
had seen in the past month, so the network size was to STATA 12 (STATA Corporation, College Station, TX,
based on the number they had seen in the past month. USA) for bivariate and multivariate analysis using logis-
Time from first injection was calculated by subtracting tic regression. We selected variables that were associated
age at first injection from the participant’s current age, with Hepatitis B or Hepatitis C infection in bivariate

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Khatib et al. BMC Public Health (2017) 17:917 Page 3 of 6

Table 1 Sociodemographic characteristics, risk behaviours, and Table 1 Sociodemographic characteristics, risk behaviours, and
Hepatitis Co-Infection among PWID in Zanzibar, 2012 Hepatitis Co-Infection among PWID in Zanzibar, 2012
Crude N %a [95% CI] (Continued)
Age Crude N %a [95% CI]

15–19 years 1 3.0 [0.0–10.0] Median number of past month


non-paid sex partners 1 partner
20–24 years 38 11.0 [7.1–15.7] (IQR 1–1) Min. 1 – Max. 5
25–29 years 100 28.9 [22.7–35.5] Frequency of condom use with
non-paid partners in past month
30–34 years 103 23.9 [18.8–30.4]
among those who had a
≥ 35 years 166 35.8 [28.9–41.7] non-paid partner
Median age in years (IQR) 32 years Always 18 15.9 [8.3–23.0]
(IQR 28–38) Min. 18 – Max. 54
Inconsistently 34 13.1 [7.4–20.3]
Sex
Never 144 71.0 [62.4–80.0]
Male 401 98.5 [97.6–99.8]
HBV 25 5.9 [3.5–8.8]
Female 7 1.5 [2.0–2.4]
HBV and HCV (of those with HBV) 13 33.5 [16.2–56.9]
Income TZS among those who
HBV and HIV (of those with HIV) 7 18.8 [7.3–40.4]
know their income
HCV 128 25.4 [19.1–32.0]
< 50,000 1 0.6 [0.0–2.0]
HCV and HIV (of those with HIV) 47 29.3 [21.1–39.1]
50,000–120,000 17 12.4 [7.1–18.3]
HIV 67 11.3 [7.7–15.2]
120,001–200,000 18 10.6 [6.1–16.7]
HIV and HBV (of those with HBV) 7 9.0 [2.3–19.3]
≥ 200,001 187 76.5 [67.8–83.5]
HIV and HCV (of those with HCV) 47 66.6 [52.3–83.0]
Median income 450,000 TZS
(IQR 300,000–600,000) Min. 3500 HBV and HCV and HIV 6 8.5 [1.8–18.6]
– Max. 12,000,000 (of those with HIV)
Duration of injection drug use CI confidence interval, IQR interquartile range, TZS Tanzanian shillings
a
RDSAT weighted
3 years or less 167 48.0 [41.7–53.8]
4–6 years 76 15.1 [11.9–19.0]
7 years or more 165 36.9 [31.5–42.5] analysis at the level of p < 0.2. We then used backwards
stepwise regression to find the best fit model as the one
Median duration 5 Years (IQR 2–
9) that included variables associated with HIV at or near
Median age at first injection 26 years
the p < 0.05 level.
(IQR 21–30) Min. 12 – Max. 51
Ever shared a needle 224 54.8 [48.5–61.0] Results
The sample was overwhelmingly male N = 401 (98%)
Injected in the last month with a 122 29.1 [23.6–36.2]
needle previously used by someone and had a median age of 32 years. Overall, participants
else among all respondents had a median duration of injection drug use of 5 years,
Injected blood from someone who 19 4.8 [2.4–7.6] 48% had injected for 3 years or less, and the median age
had taken drugs in the past 1 month at first injection was 26 years. Needle sharing was com-
(flashblood)
mon; 54.8% had ever shared a needle, and 29% had
Condom use at last sex with a 68 14.4 [10.2–18.2] shared a needle in the past month (Table 1).
non-paying partner among those
who had a non-paying partner An estimated 5.9% of participants were HBsAg positive,
(n = 212) 25.4% were infected with HCV, and 11.3% were infected
Number of non-paid partners in past with HIV. Of the participants who were HBsAg positive,
month among those who had a 33.5% were co-infected with HCV and 9.0% were co-
non-paid partner infected with HIV. Of HCV-infected participants, 29.3%
1 partner 117 86.4 [74.6–92.7] were co-infected with HIV. Of the participants who were
2 or more partners 29 13.6 [7.3–25.4] infected with HIV, 9.0% were co-infected with HBV, 66.6%
with HCV and 8.5% with both (Fig. 1). None of the poten-
tial injection risk factors measured were associated with
HBsAg positivity (Table 2). In contrast, older age (above
the median) and longer duration of injection drug use
(above the median) were independently associated with
HCV infection (Table 3).

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Khatib et al. BMC Public Health (2017) 17:917 Page 4 of 6

Fig. 1 Rates of HIV, HCV, and HBV co-infection. Rates of HIV, HCV, and HBV co-infection among PWID in Zanzibar, Tanzania

Discussion elsewhere. It is likely that we have intervened in a mo-


We found that approximately one-fourth of PWID in ment where a larger HCV epidemic can be prevented.
Zanzibar were infected with HCV, which is moderately PWID may be a relatively new phenomenon in Zanzibar,
low compared to the same populations in other parts of or Zanzibari PWID may be more isolated from other
the world [17–19]. HIV prevalence among PWID in countries’ networks. Prevention of HCV is difficult, and
Zanzibar was on the low end of the range for HIV vaccine trials currently underway in other parts of the
prevalence in these same studies (4.6 to 59.6%). Chronic world may eventually benefit PWID in Zanzibar. The
HBV infection (as measured by hepatitis B surface anti- relatively low level of chronic HBV infection was ex-
genaemia) was substantially less common among PWID pected and consistent with rates of perinatal trans-
in Zanzibar (5.9%). We also found that co-infection of mission, understood through the recent introduction of
HIV with HCV was substantial (66.6%). In addition, we prenatal screening for HBsAg and infant HBV
found that infection with HCV was associated with age immunization in Zanzibar. The background rate of
and duration of injection drug use, but were unable to HBsAg positivity in general African populations is esti-
associate standard risk factors for parenteral and sexual mated to be between 9 and 20% [20]; however, HBsAg
transmission with HBsAg positivity. prevalence in antenatal clinic surveillance (ANC) in
HCV among PWID has been widely described, but less Zanzibar was 1.3% [21]. Although this is low compared
so in Africa. In studies conducted in India, Iran, and to the general population in other parts of Africa, given
Australia, investigators found HCV prevalence ranges the relatively low HBV prevalence in the general popula-
from 34.5 to 90.4% [16–18]. Given their risky injection tion, the figure among PWID is high for Zanzibar
practices, it is surprising that PWID in Zanzibar have a though given that only surface antigen can be detected
relatively low prevalence of HCV compared to PWID immunization coverage could account for this higher

Table 2 Predictors of Hepatitis B surface antigenaemia among people who inject drugs in Zanzibar, 2012
Crude N OR P Value 95% CI
Age categories (above and below median age of 32) 204 1.33 0.24 0.83–2.12
Duration (above and below median of 5 year duration) 201 1.07 0.09 0.99–1.16
Income (Above and below 50,00 TShillings) 204 1.11 0.72 0.63–1.95
Ever shared a needle (No/Yes) 224 1.41 0.51 0.50–3.96
Shared a needle in last month (No/Yes) 112 1.47 0.53 0.44–4.92
Flash blood (No/Yes) 19 0.41 0.29 0.08–2.13
Had a paid partner in the last month (No/Yes) 93 0.46 0.15 0.16–1.33
Used a condom at last sex with paid partner (No/Yes) 97 1.03 0.95 0.47–2.24
Number of non-paying partners (above and below median number of 1) 117 0.31 0.30 0.03–3.74
Condom use with non-paid partner (No/Yes) 23 1.39 0.52 0.51–3.74

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Khatib et al. BMC Public Health (2017) 17:917 Page 5 of 6

Table 3 Predictors of Hepatitis C among people who inject drugs in Zanzibar, 2012
Crude N OR P-Value 95% CI aOR P- Value 95% CI
Age categories (above and below median age of 32) 204 2.52 0.00 1.44–4.39 2.06 0.02 1.14–3.73
Duration (above and below median of 5 year duration) 201 3.37 0.00 1.86–6.10 2.79 0.00 1.49–5.20
Income (Above and below 50,00 TShillings) 204 1.02 0.92 0.73–1.42
Ever shared a needle (No/Yes) 224 1.66 0.07 0.96–2.89 1.63 0.09 0.93–2.84
Shared a needle in last month (No/Yes) 112 1.00 0.99 0.49–2.05
Flash blood (No/Yes) 19 0.76 0.70 0.18–3.23
Had a paid partner in the last month (No/Yes) 93 1.58 0.21 0.77–3.23
Used a condom at last sex with paid partner (No/Yes) 97 1.21 0.36 0.81–1.80
Number of non-paying partners (above and below median number of 1) 117 0.95 0.93 0.28–3.19
Condom use with non-paid partner (No/Yes) 23 0.86 0.66 0.44–1.69

prevalence among PWID. Future studies would benefit decline. HBV prevalence among PWID is also low com-
from assessing the prevalence of hepatitis B core pared to PWID in other settings. This underscores the
(HBcAb) and surface (HBsAb) antibody to understand importance of screening PWID for HIV, HBV, and HCV;
the burden of disease and HBV immunization coverage. providing HBV vaccination to those eligible; initiating
Our study has some limitations. First, we measured antiretroviral therapy early for those with HIV/HBV or
HBsAg rather than HBV antibodies; therefore it is im- HIV/HCV co-infection; introducing interventions that
possible to distinguish chronic HBV infection from acute have high impact on reducing needle sharing; and con-
HBV infection. In addition, self-reported behavior, recall tinued monitoring to understand the impact of preven-
bias, and social-desirability bias may have influenced tion programs.
participant’s responses. Underreporting of these risks
Abbreviations
may have biased results toward the null with consequent CI: Confidence interval; HBsAg: Hepatitis B surface antigen; HBV: Hepatitis B
Type II error. Secondly, we used RDS to generate our virus; HCV: Hepatitis C virus; HIV: Human immunodeficiency virus;
study population, which is highly dependent on accurate IQR: Interquartile range; PWID: People who inject drugs; RDS: Respondent-
driven sampling; TZS: Tanzanian shillings
estimates of participants’ network sizes [14]. Inaccuracies
in estimating network sizes can lead to overestimation or Acknowledgements
underestimation of outcome variables. However, a particu- We thank the numerous members of the research design and data collection
team as well as the men and women who participated in this study. This
lar strength of RDS is its ability to enroll a diverse range research has been supported by the President’s Emergency Plan for AIDS Relief
of participants from different social networks [13, 14]. (PEPFAR) through the Centers for Disease Control and Prevention (CDC) under
How well these social networks intersect by the end of the the terms of cooperative agreement 5UGPS002039-02. The findings and
conclusions in this report are those of the authors and do not necessarily
survey is among the more important determinants of the represent the official position of the CDC.
accuracy of the estimates produced.
Interestingly, despite having two female seeds, very Funding
This research has been supported by the President’s Emergency Plan for
few female PWID were enrolled in the survey. Other AIDS Relief (PEPFAR) through the Centers for Disease Control and Prevention
similar studies have had difficulty enrolling female (CDC) under the terms of cooperative agreement 5UGPS002039–02. The
PWID using RDS [22], though studies have been suc- findings and conclusions in this report are those of the authors and do not
necessarily represent the official position of the CDC. The funders had no
cessful at recruiting female PWID using convenience- role in study design, data collection and analysis, decision to publish, or
based sampling techniques at HIV counseling and test- preparation of the manuscript.
ing centers [23]. It may be the case the female PWID are
Availability of data and materials
not as accessible through peer referral as male PWID All data underlying the findings are fully available without restriction. The
and they may need to be sought out in order to partici- relevant dataset can be accessed on Figshare: https://figshare.com/articles/
pate in surveys. It is also possible that there are fewer fe- IDU_ZNZ_xlsx/4563922.
male PWID. Authors’ contributions
GR, SW, FK, AK, EM, MD, and MK designed the study, FK, AK, SW, AA, AO, SH,
Conclusions MD implemented the study and collected the data, SH, FK, AK, SW, AA, AO,
SH analyzed the data, GR, SW, FK, AK, and EM developed the manuscript. All
Despite these potential limitations, we conclude that authors read and approved the final manuscript.
HCV infection is common among PWID in Zanzibar, al-
though at a much lower prevalence than in PWID in Ethics approval and consent to participate
All participants provided written informed consent prior to enrolment in the
more mature epidemics. With improved access to pre- study. Adolescents aged 15–17 whose circumstances allowed them to
vention, HCV prevalence may stabilize and eventually consent for themselves were considered liberated minors and included in

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Khatib et al. BMC Public Health (2017) 17:917 Page 6 of 6

this study. We defined a liberated minor as one not currently living under 14. Malekinejad M, Johnston LG, Kendall C, Kerr LR, Rifkin MR, Rutherford GW.
the direction or auspices of parent or guardian and not otherwise supported Using respondent-driven sampling methodology for HIV biological and
by a parent or guardian, based on self-report. The study received approval behavioral surveillance in international settings: a systematic review. AIDS
from the Zanzibar Medical Research Ethical Committee; the Committee on Behav. 2008; doi:10.1007/s10461-008-9421-1.
Human Research of the University of California, San Francisco; and the Office 15. Abdul-Quader AS, Heckathorn DD, McKnight C, Bramson H, Nemeth C,
of the Associate Director for Science of the United States Centers for Disease Sabin K, et al. Effectiveness of respondent-driven sampling for recruiting
Control and Prevention. drug users in new York City: findings from a pilot study. J Urban Health.
2006; doi:10.1007/s11524-006-9052-7.
Consent for publication 16. Salganik MJ. Variance estimation, design effects, and sample size calculations
Not applicable. for respondent-driven sampling. J Urban Health. 2006;83(6 Suppl):i98–112.
17. Rahimi-Movaghar A, Razaghi EM, Sahimi-Izadian E, Amin-Esmaeili M. HIV,
Competing interests hepatitis C virus, and hepatitis B virus co-infections among injecting drug
The authors declare that they have no competing interests. users in Tehran, Iran. Int J Infect Dis. 2010; doi:10.1016/j/ijid.2009.03.002.
18. Crofts N. Hepatitis C infection among injecting drug users: where do we go
from here? Drug Alcohol Rev. 1994; doi:10.1080/09595239400185321.
Publisher’s Note 19. Devi KS, Singh NB, Singh HL, Sing YM. Coinfection by human
Springer Nature remains neutral with regard to jurisdictional claims in immunodeficiency virus, hepatitis B virus and hepatitis C virus in injecting
published maps and institutional affiliations. drug users. J Commun Dis. 2005;37(1):73–7.
20. Kiire CF. The epidemiology and prophylaxis of hepatitis B in sub-Saharan
Author details Africa: a view from tropical and subtropical Africa. Gut. 1996;38(Suppl 2):S5–12.
1
Zanzibar AIDS Control Program, Ministry of Health, Zanzibar, United 21. Zanzibar AIDS Control Programme. HIV ANC surveillance report: Zanzibar
Republic of Tanzania. 2Division of Global HIV/AIDS, US Centers for Disease AIDS Control Programme; 2010. Zanzibar: Republic of Tanzania; 2010.
Control and Prevention, Dar es Salaam, United Republic of Tanzania. 3Global 22. Abramovitz D, Volz EM, Strathdee SA, Patterson TL, Vera A, Frost SD, et al.
Health Sciences, University of California, San Francisco, San Francisco, CA, Using respondent-driven sampling in a hidden population at risk of HIV
USA. 4Directorate of Preventive Services and Health Education, Ministry of infection: who do HIV-positive recruiters recruit? Sex Transm Dis. 2009;
Health, Zanzibar, United Republic of Tanzania. doi:10.1097/OLQ.0b013e3181b0f311.
23. McCurdy SA, Ross MW, Williams ML, Kilonzo GP, Leshabari MT. Flashblood:
Received: 7 June 2017 Accepted: 21 November 2017 blood sharing among female injecting drug users in Tanzania; 2010. doi:10.
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