https://doi.org/10.5812/archcid.15531

Reduction in Prevalence of Hepatitis B Surface Antigen Among Intravenous Drug Users in Tehran Drop-in-Centers

authors:

avatar Tahmineh kandelouei 1 , avatar Seyed Masoud Hosseini 1 , avatar Latif Gachkar 2 , avatar Hossein Keyvani 3 , avatar Foad Davoodbeglou 4 , avatar Maryam Vaezjalali 5 , *

Department of Microbiology, Faculty of Biological Sciences, Shahid Beheshti University of Medical Sciences, Tehran, IR Iran
Infectious Diseases and Tropical Medicine Research Center, Shahid Beheshti University of Medical Sciences, Tehran, IR Iran
Department of Virology, Faculty of Medicine, Iran University of Medical Sciences, Tehran, IR Iran
Department of Immunology, Faculty of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, IR Iran
Department of Microbiology, Faculty of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, IR Iran
Archives of Clinical Infectious Diseases: Vol.8, issue 2; e15531
published online: April 17, 2013
article type: Research Article
received: January 5, 2013
revised: March 2, 2013
accepted: March 29, 2013

how to cite: kandelouei T, Hosseini S M, Gachkar L, Keyvani H, Davoodbeglou F, et al. Reduction in Prevalence of Hepatitis B Surface Antigen Among Intravenous Drug Users in Tehran Drop-in-Centers. Arch Clin Infect Dis. 2013;8(2):e15531. https://doi.org/10.5812/archcid.15531.

Abstract

Background:

Despite the availability of an effective vaccine for more than three decades, HBV (hepatitis B virus) continues to infect many people worldwide, particularly in developing countries of Asia. In older people at higher risk of infection, high prevalence of HBV may exist, particularly among intravenous drug users (IDUs). This group is among groups at higher risk of infection as they share needles for drug injection.

Objectives:

The current study aimed to determine the prevalence of HBsAg (hepatitis B antigen) among intravenous drug users in drop-in-centers (DICs) of Tehran in 2013.

Patients and Methods:

This cross sectional study included 129 intravenous drug users recruited from DICs in Tehran in 2013. Socio-demographic characteristics and associated risk factors were recorded during the sample collection. Their serum samples were tested for the presence of HBsAg by enzyme-linked immunosorbent assay (ELISA).

Results:

HBsAg was detected in 4 of 129 subjects, giving an overall prevalence of 3.1%. No significant correlation was observed between HBsAg positivity and socio-demographic and associated risk factors.

Conclusions:

Undoubtedly, IDUs are one of the most high-risk groups exposed to infection; so the priority of preventive and educational programs would be beneficial for this high-risk group. Screening IDUs at the national level and statistical analysis for HBV in the larger sample size is recommended.

1. Background

Intravenous drug users (IDUs) are at increased risk for acquiring blood-borne infectious diseases, particularly hepatitis B virus (HBV) (1). Hazardous behaviors of these addicts such as sharing syringes, using the same syringe several times, or using infected syringes are the main routes for infection with human immunodeficiency virus (HIV), hepatitis B, C and various lung and cerebral abscesses. Infection with these types of diseases at family and society levels can be the result of sexual hazardous behaviors of this infected group (2). To the best of our knowledge, up to 90% of DIUs suffer from one of the viral diseases. There is a direct relationship between the number of cases infected by these viruses and duration of injection drug usage (3). Long duration of drug injection may lead to more sharing of needles and other instruments, resulting in a greater likelihood of transmission (4).

Other studies demonstrated that long-term imprisonment, with drug injection behavior is independently associated with HBV infection (5, 6). Incorporation of routine HBV screening, vaccination, long-term treatment, improved jail health system, detoxification clinics and harm reduction programs like DICs, are among important steps to reduce further transmission and the future burden of blood-borne diseases (7). Iran has one of the highest per capita number of opioid users in the world, with a substantial and potentially growing population of IDUs (8). According to a report by the Iranian welfare organization, among 1.8 million drug users in Iran, 9% to 16% are IDUs, while half of them share needles. It could be estimated that the IDU population in Iran ranges between 200000 and 300000 IDUs. As the number of IDUs is increasing in Iran, there could be potential danger for the national health system (9).

Injection drug usage has been the most major route of drug abuse in Iran during the past decade (3). In this regard, the high rates of HCV and HBV infection among IDUs have been reported in Iran (10-12). The reports showed controversial results about the association between injecting drug behavior and the high rate of HBV & HCV (13-16). In 2002, a harm reduction policy was adopted in Iran; expansion of harm reduction policy started after the design of the national five-year program (2002-2007). Around 1400000 needles and syringes were distributed to IDUs through 120 DICs, over a six-month period in 2007 (17). Another program was opioid substitution treatment among 22000 drug users in mid-2007 (17). Educational programs on hepatitis B risk factors, increasing easy and affordable access to HBV-testing and free vaccination for IDUs are important to reduce the prevalence of HBV infection in this group (18).

2. Objectives

This study examined the characteristics, risk behaviors and risk factors of HBV infection among IDUs in Tehran. The results of this study were associated with the prevalence of HBsAg and the correlating factors in this group, and services provided for IDUs in DICs such as needle and syringe program (NSP) in Tehran.

3. Patients and Methods

3.1. Sample Selection and Study Population

A cross-sectional study was performed on 129 volunteers (128 males and 1 female), current IDUs selected from three DICs located in different well-known areas with high rates of drug-related risk behaviors between April and June 2013 in Tehran. Face-to-face interviews were done using questionnaires that elicited personal data containing demographic data such as age, gender, employment status, marital status, history and duration of addiction, history of imprisonment, kind and route of drug use, hepatitis B vaccination, and some high-risk behaviors like sharing syringes, sexual behaviors and tattooing. Five milliliter peripheral blood was taken from each individual and transported to the laboratory for storage. IDUs were able to receive the results of their tests based on their own code number.

3.2. Detection of Serology Markers

Sera were collected and stored in aliquots at -20 °C for further testing. The samples were examined using enzyme-linked immunosorbent assay (ELISA) to detect HBsAg. HBsAg was checked using highly specific enzyme immune assays (DIA. Pro, ITALY, specificity > 99%). All positive samples for HBsAg were tested twice using the same method to confirm the results.

3.3. Statistical Analysis

Data were extracted from questionnaires, and summarized. The standard Chi-square test was used to assess the correlation of demographic and behavioral variables and HBsAg positivity. All analyses were performed using SPSS for windows (version 19: SPSS Inc, USA). Results were regarded as significant when P < 0.05.

4. Results

A total of 129 IDUs participated in this study; note that some of them were DIC workers who had a history of injection drug usage. Regarding the age of the participants, 17.1% of subjects were between 20-30 years old, 34.1% were between 30-40, 29.5% were between 40-50 and the rest were above 50 years old (Table 1).

Table 1.

Socio-demographic Characteristics of IDUs in Tehran 2013

CharacteristicsFrequencyIntravenous drug users, %
Age, n a = 129
20 - 302217.3
30 - 404434.6
40 - 503829.9
> 502318.1
Employment status, n = 129
Unemployed9674.4
Employed3325.6
Marital status, n = 126
Married and living with a partner9474.6
Single or separated3225.4
Duration of drug usage, n =125
< 1, y21.6
1 - 5, y1915.2
5 - 10, y2620.8
> 10, y7862.4
History of imprisonment, n = 1238468.3
Frequency of injection in a day, n = 70
1 - 34158.6
3 - 62130.0
> 6811.4
History of sharing needle equipment, n = 641625
Type of drug, n = 126
Heroin3124.6
Other b4434.9
Heroin + other5140.5
History of tattooing, n = 1214738.8
History of blood transfusion, n = 571729.8
History of surgery, n = 1175123.6
History of sexual behavior, n = 743435.9
History of dentistry, n = 876979.3
HBV vaccination, n = 98578.25

aNumber of injection of drug users who answered each question, n = 129.

bOther drugs including opium, crack, crystal, etc.

Socio-demographic profiles of participants with regard to the number of subjects, who answered each question, are presented in Table 1. Among the 129 cases in this study the prevalence of HBsAg was 3.1%. No statistically significant association was observed between HBsAg positivity and sharing needle equipment, duration of drug use, history of imprisonment, frequency of injection per day, type of drug, tattooing, history of surgery and high risk sexual behaviors, P > 0.05 (Table 2). The highest rate of HBsAg positivity was among cases with more than 10 years duration of drug usage, and history of imprisonment (Table 3).

Table 2.

Risk Factors Associated With HBV Infection in IDUs

Risk Factor HBsAg Positive, No. (%) HBsAg Negative, No. (%) Total P value
Sharing syringe
Yes0 (0)1616> 0.05
No2 (4.1)4648> 0.05
Duration of drug use, y
< 10 (0)22> 0.05
1 - 51 (5.2)1819> 0.05
5 - 100 (0)2626> 0.05
> 103 (3.8)7578> 0.05
History of imprisonment
Yes3 (3.5)8184> 0.05
No1 (2.5)3839> 0.05
Frequency of injection
1 - 33 (7.3)3841> 0.05
3 - 60 (0)2121> 0.05
> 60 (0)88> 0.05
Type of drug
Heroin2 (6.4)2931> 0.05
Other a1 (2.2)4344> 0.05
Heroin + other1 (1.9)5051> 0.05
Tattoo
Yes2 (4.2)4547> 0.05
No2 (2.7)7173> 0.05
History of surgery
Yes1 (1.9)5051> 0.05
No3 (4.5)6366> 0.05
High risk sexual behaviors
Yes1 (2.9)3334> 0.05
No2 (5)3840> 0.05

aOther drugs such as opium, crack, crystal, etc.

Table 3.

Statues of HBsAg Among Studied Population Cross Tab With History of Imprisonment and Duration of Drug Usage

D. Drug.U a H. IMPR a Total
No Yes
< 1, y
Negative1NA a1
Total1NA1
1 - 5, y
Negative61218
Positive011
Total61319
5 - 10, y
Negative111526
Total111526
> 10, y
Negative195473
Positive123
Total205676
Total
Negative3781118
Positive134
Total3884122

aAbbreviations: D. Drug.U, drug duration usage; H. IMPR, history of imprisonment; NA, not available.

Due to the low number of female cases, the statistical analysis of data between different sexes was ignored. Results showed that immunization strategies in DICs targeting IDUs have been instrumental in reducing overall prevalence of HBsAg. Continuous surveillance and repeated studies are needed to monitor trends, and effects of large scale harm reduction intervention.

5. Discussion

In this study, of 129 IDUs, four subjects were HBsAg positive (3.1%). In Khodadadizade et al. (2005), of 180 subjects five were HBV infected from whom three subjects were IDUs (19). In Nikkhooy et al. study in Ahvaz, South-west of Iran conducted in 2004, 1.5% of 258 IDUs who were hospitalized in Razi Hospital were positive for HBsAg (20). In another study, 970 IDU male prisoners were examined by Daneshmand et al. in 2009 in Esfahan, central Iran, and 32 subjects (3.3%) were positive for HBsAg. Daneshmand et al. study concluded that the longer duration of being incarcerated is associated with higher prevalence of HBV infection (18). In another descriptive analytical study on 133 IDUs, 8 (6.2%) were HBV positive cases; a strong correlation between the use of shared needle and HBV infection was demonstrated (P < 0.05) (21). Also, in the research by Nokhodian et al. (2012) on female prisoners in Esfahan, results showed that there is no association between the number of arrests and serological HBV markers; their study was limited on one hand by the number of cases that was only 163 and on the other hand it was only conducted on females (22). Another study on females with illegal social behaviors in Esfahan showed the same results, that demonstrated no association between having prison history and HBV infection (23). In a study in Shahrekord, located in West of Iran, by Khosravani et al. (2012) of 158 IDUs, 3.2% were HBsAg positive (24). The prevalence of HBsAg among male IDUs in Tehran was reported to be 5.8%, whereas in Zahedan, South-east of Iran, it was 19.3% among hospitalized IDUs (25). In another study, in Ahvaz, South-west of Iran, HBsAg prevalence was 3.6% among hospitalized drug users (26). In Amin-Esmaeili et al. (2012) study on IDUs, in Tehran, the prevalence of past or current HBV infection had a high rate (46.1%), that was mainly correlated with history of imprisonment and drug use of more than 10 years (17). In some reports from Iran (27) and other countries regarding imprisonment (28, 29), the frequency (30) and duration of drug injection (28, 31) are demonstrated as risk factors for HBV infection. Mir-Nasseri et al. (2011) study in Tehran, showed that the prevalence of HBsAg was 3.7% among 518 IDUs (27), they showed that incarceration increased the risk of co-infection by 7.5 folds. This result was confirmed by a similar study by Zamani et al. (2005) (32) on IDUs, and showed that infection was strongly associated with a history of shared drug injection inside prison, whereas it was not significantly related to shared drug injection outside the prison.

In Tofigi et al. study on cadaver of 400 intravenous drug users in Tehran, seroprevalence of HBsAg was 27.5% (3). Merat et al. (2000) (33), Farhat et al. (2003) (34) and Sharif et al. (2009) (35) reported a rate of 1.3%-4%; hepatitis virus infection in IDUs population was associated with sharing injection instruments and a long duration of prison stay and drug usage. Studies from other parts of the world, such as Brazil by Stief et al. (2010) (36) and Berlin showed similar results, as they concluded that positive history of imprisonment is associated with 1.9 fold and 1.5 fold increase in the risk of HBV seropositivity, respectively. Their studies showed that history of syringe sharing in prison was associated with HBV, HCV and HIV infections. A research done by Nguyen et al. (2006), estimated the prevalence of HBV among IDUs in Australia to be 2% - 3%, in this study long term injection, having been to prison, and injecting in prison were independently associated with HBV infection (37). There are also reports of greater than 50% prevalence of HBV among IDUs in other countries around the world such as Germany, Georgia and Bulgaria (28, 38, 39).

Different studies showed that the prevalence of HBV in Europe and America is respectively more than those of Asia and the Middle East. According to previous studies, the prevalence of HBV among IDUs in Kopenhak drug users, Mexican and Denmark prisoners as well as Spain drug users was 64%, 61.1%, 64% and 67.3% (40-42), respectively, while the prevalence of HBsAg was reported to be 6.2% in Bangladesh (43) and the rate of HBsAg positivity among IDUs in Kabul was demonstrated to be 6.5% (44) and for Karachi,7.5% (45). In Mirahmadzade et al. (2004) study on IDUs in Shiraz, South of Iran, HBV prevalence was reported to be 3% among the subjects (46). In another study by Javadi et al. (2006) among IDU prisoners in central parts of Iran, the prevalence of HBsAg was 3.5% (47). Rahimi-Movaghar study (2010) on 899 IDUs recruited in Tehran from treatment and harm reduction facilities and from drug users hangouts in public areas in 2007, showed 30.9% HBsAg positivity among these subjects (48). As mentioned before, in the current study the prevalence of HBsAg among IDUs was 3.1% which is slightly lower than those reported from Tehran, Ahvaz, Shahrekord or other parts of Iran (3, 20, 24, 26) (Table 4).

Table 4.

Studies on the Prevalence of HBsAg in IDUs in Iran

CityYearNumber of Blood SamplesHBsAg+, %Reference
Ahvaz20042581.5(20)
Esfahan20099703.3(18)
Kohgeloyeh and Boyeahmad20091583.2(24)
Tehran200686424.7(17)
Tehran20064995.8(7)
Tehran20015183.7(27)
Zanjan20013463.8(49)
Tehran200940027.5(3)
Tehran2007706(50)
Ahvaz20093333.6(26)
Tehran200790430.9(48)
Esfahan20081061.8(51)
Shahrekord20041336.2(21)
Tehran200753176.7(52)
Present study20131293.1NA a

aAbbreviation: NA, not available.

Low rate of HBsAg positivity in this study might be reflected by HBV vaccination; in this study of 98 subjects, 58.2% had a history of HBV vaccination. The study of Khosravani et al. (2012) (24), showed a similar low prevalence for HBsAg positivity among high risk groups, same as IDUs in South-west of Iran studied by Khosravani et al. (2012), where it was concluded that this result may be due to HBV vaccination in that area. It is interesting to note that national levels of 1st (HBV1), 2nd (HBV2) and 3rd (HBV3) dose coverage in Iran have been reported to be 98.9%, 98.8% and 98.4%, respectively (53). After employment of the HBV vaccination in the Iranian national program of Immunization, and the expanded Program of Immunization (EPI) since 1993, the prevalence of HBV has decreased throughout the country (33, 54). Another possibility for reduction in prevalence of HBsAg in our study can be due to harm reduction programs that are provided in DICs, since 2005 there have been continuous attempts to raise coverage of harm reduction intervention in Iran (17). These findings can be a result of the scaling-up of harm reduction facilities such as NSP and MMT that started from 2002 and have been expanded since 2005 in Tehran. A considerable number of IDUs are covered under harm-reduction programs, either in DICs or in prison (55). These results present a good opportunity to receive services for HBV patients to decrease exposure to contaminated blood, as well as risk reduction in high risk behaviors. Drug use is often a hidden behavior in society, and drug users are a kind of hard-to-reach group; therefore, selecting a representative sample of drug users in a geographical area is difficult. Additionally in this study, only IDUs in Tehran were involved, and the results may not be generalized to the entire Iranian IDU population. Due to difficulty in approaching IDUs as a hard-to-reach group,

we could not gain access to female groups; therefore, further studies are required to examine the studied high risk issue among females. In conclusion, fewer infected cases found in this study promises that in case of performing on-time detriment prevention and decreasing measures will cause future satisfying results in this case.

Acknowledgements

References

  • 1.

    Lugoboni F, Quaglio G, Civitelli P, Mezzelani P. Bloodborne viral hepatitis infections among drug users: the role of vaccination. Int J Environ Res Public Health. 2009;6(1):400-13. [PubMed ID: 19440291]. https://doi.org/10.3390/ijerph6010400.

  • 2.

    Schleicher S, Schieffer M, Jurgens S, Wehner HD, Flehmig B. Evidence of multiple hepatitis virus infections in autopsied materials of intravenous drug addicts. Ig Sanita Pubbl. 2005;61(5):435-50. [PubMed ID: 17214028].

  • 3.

    Tofigi H, Ghorbani M, Akhlaghi M, Yaghmaei A, Mostafazadeh B, Farzaneh E, et al. Incidence of hepatitis B and HIV virus at cadaver of IV drug abusers in Tehran. Acta Med Iran. 2011;49(1):59-63. [PubMed ID: 21425074].

  • 4.

    Levine OS, Vlahov D, Koehler J, Cohn S, Spronk AM, Nelson KE. Seroepidemiology of hepatitis B virus in a population of injecting drug users. Association with drug injection patterns. Am J Epidemiol. 1995;142(3):331-41. [PubMed ID: 7631637].

  • 5.

    Maher L, Chant K, Jalaludin B, Sargent P. Risk behaviors and antibody hepatitis B and C prevalence among injecting drug users in south-western Sydney, Australia. J Gastroenterol Hepatol. 2004;19(10):1114-20. [PubMed ID: 15377287]. https://doi.org/10.1111/j.1440-1746.2004.03438.x.

  • 6.

    Butler T, Boonwaat L, Hailstone S, Falconer T, Lems P, Ginley T, et al. The 2004 Australian prison entrants' blood-borne virus and risk behaviour survey. Aust N Z J Public Health. 2007;31(1):44-50. [PubMed ID: 17333608].

  • 7.

    Seyed Alinaghi SA, Kheirandish P, Karami N, Salem S, Shirzad H, Jahani MR, et al. High prevalence of chronic hepatitis B infection among injection drug users in Iran: the need to increase vaccination of adults at risk. Acta Med Iran. 2010;48(1):58-60. [PubMed ID: 21137671].

  • 8.

    Forouzanfar MH, Mohammad K, Majdzadeh R, Malekzadeh R, Abou AlhasaniF, Mohammadnejad M, et al. Effectiveness of adolescents'immunization against hepatitis B on burden of the disease in Iran. Hakim. 2006;9(2):1-1.

  • 9.

    Razzaghi EM, Movaghar AR, Green TC, Khoshnood K. Profiles of risk: a qualitative study of injecting drug users in Tehran, Iran. Harm Reduct J. 2006;3:12. [PubMed ID: 16545137]. https://doi.org/10.1186/1477-7517-3-12.

  • 10.

    Karimi A. P.483 Seroprevalence of HBV, HCV and HIV among intravenous drug users in Iran. J Clin Virol. 2006;36:S210-S1.

  • 11.

    Zamani S, Ichikawa S, Nassirimanesh B, Vazirian M, Ichikawa K, Gouya MM, et al. Prevalence and correlates of hepatitis C virus infection among injecting drug users in Tehran. Int J Drug Policy. 2007;18(5):359-63. [PubMed ID: 17854723]. https://doi.org/10.1016/j.drugpo.2007.02.007.

  • 12.

    Mir-Nasseri SM, Poustchi H, Nasseri-Moghadam S, Nouraie SM, Tahaghoghi S, Afshar P, et al. HCV in intravenous drug users. Govaresh. 2012;10(2):80-6.

  • 13.

    Alavian SM. Control of hepatitis C in Iran: vision and missions. Hepat Mon. 2007;7(2):57-8.

  • 14.

    Alavi SM, Etemadi A. HIV/HBV, HIV/HCV and HIV/HTLV-1 co infection among injecting drug user patients hospitalized at the infectious disease ward of a training hospital in Iran. Pakistan J Med Sci. 2007;23(4):510.

  • 15.

    Zali MR, Aghazadeh R, Nowroozi A, Amir-Rasouly H. Anti-HCV antibody among Iranian IV drug users: is it a serious problem. Arch Iran Med. 2001;4(3):115-9.

  • 16.

    Alizadeh AHM, Alavian SM, Jafari K, Yazdi N. Prevalence of hepatitis C virus infection and its related risk factors in drug abuser prisoners in Hamedan-Iran. World J Gastroenterol. 2005;11(26):4085.

  • 17.

    Amin-Esmaeili M, Rahimi-Movaghar A, Razaghi EM, Baghestani AR, Jafari S. Factors Correlated With Hepatitis C and B Virus Infections Among Injecting Drug Users in Tehran, IR Iran. Hepat Mon. 2012;12(1):23-31. [PubMed ID: 22451840]. https://doi.org/10.5812/kowsar.1735143X.806.

  • 18.

    Daneshmand D, Nokhodian Z, Adibi P, Ataei B. Risk prison and hepatitis B virus infection among inmates with history of drug injection in Isfahan, Iran. Sci World J. 2013;2013.

  • 19.

    Khodadadizadeh A, Esmaeili NA, Hossieni SH, Shabani Sharbabaki Z. The prevalence of HIV, HBV and HCV in narcotic addicted persons referred to the out patient clinic of rafsanjan university of medical sciences in 2003. J Rafsanjan Univ Med Sci. 2006;5(1):23-30.

  • 20.

    Nikkhooy A, Nikkhooy M, Saadati N. Determination of relative frequency of HBS Ag, HCV and HIV antibodies serum markers among admitted intravenous drug users in infectious disease wardof Razi Hospital in Ahvaz, 2004-2005. J Health Res. 2012;1(1):26-33.

  • 21.

    Imani R, karymi A, Kasaeeian N. The relevance of related-risk behaviors and seroprevalence of HBV, HCV and HIV infection in intravenous drug users from Shahrekord, Iran, 2004. Shahrekord U Med Sci J. 2006;8(1):58-62.

  • 22.

    Nokhodian Z, Yazdani MR, Yaran M, Shoaei P, Mirian M, Ataei B, et al. Prevalence and Risk Factors of HIV, Syphilis, Hepatitis B and C Among Female Prisoners in Isfahan, Iran. Hepat Mon. 2012;12(7):442-7. [PubMed ID: 23008724]. https://doi.org/10.5812/hepatmon.6144.

  • 23.

    Kassaian N, Ataei B, Yaran M, Babak A, Shoaei P. Hepatitis B and C among women with illegal social behavior in Isfahan, Iran: Seroprevalence and associated factors. Hepat Mon. 2011;11(5):368-71. [PubMed ID: 22087163].

  • 24.

    Khosravani A, Sarkari B, Negahban H, Sharifi A, Toori MA, Eilami O. Hepatitis B Infection among high risk population: a seroepidemiological survey in Southwest of Iran. BMC Infect Dis. 2012;12:378. [PubMed ID: 23270391]. https://doi.org/10.1186/1471-2334-12-378.

  • 25.

    Zali MR, Kazem M, Farhadi A, Masjedi MR, Zargar A, Nowroozi A. Epidemiology of hepatitis B in the Islamic Republic of Iran. Relation. 1996;2(2):290-8.

  • 26.

    Alavi SM, Behdad F. Seroprevalence study of hepatitis C and Hepatitis B virus among hospitalized intravenous drug users in Ahvaz, Iran (2002-2006). Hepat Mon. 2010;10(2):101-4. [PubMed ID: 22312381].

  • 27.

    Mir-Nasseri MM, Mohammadkhani A, Tavakkoli H, Ansari E, Poustchi H. Incarceration is a major risk factor for blood-borne infection among intravenous drug users: Incarceration and blood borne infection among intravenous drug users. Hepat Mon. 2011;11(1):19-22. [PubMed ID: 22087111].

  • 28.

    Backmund M, Meyer K, Schuetz C, Reimer J. Factors associated with exposure to hepatitis B virus in injection drug users. Drug Alcohol Depend. 2006;84(2):154-9. [PubMed ID: 16481128]. https://doi.org/10.1016/j.drugalcdep.2006.01.009.

  • 29.

    Mansson AS, Moestrup T, Nordenfelt E, Widell A. Continued transmission of hepatitis B and C viruses, but no transmission of human immunodeficiency virus among intravenous drug users participating in a syringe/needle exchange program. Scand J Infect Dis. 2000;32(3):253-8. [PubMed ID: 10879594].

  • 30.

    Ruan Y, Qin G, Yin L, Chen K, Qian HZ, Hao C, et al. Incidence of HIV, hepatitis C and hepatitis B viruses among injection drug users in southwestern China: a 3-year follow-up study. AIDS. 2007;21 Suppl 8:S39-46. [PubMed ID: 18172390]. https://doi.org/10.1097/01.aids.0000304695.54884.4f.

  • 31.

    Miller ER, Hellard ME, Bowden S, Bharadwaj M, Aitken CK. Markers and risk factors for HCV, HBV and HIV in a network of injecting drug users in Melbourne, Australia. J Infect. 2009;58(5):375-82. [PubMed ID: 19328555]. https://doi.org/10.1016/j.jinf.2009.02.014.

  • 32.

    Zamani S, Kihara M, Gouya MM, Vazirian M, Ono-Kihara M, Razzaghi EM, et al. Prevalence of and factors associated with HIV-1 infection among drug users visiting treatment centers in Tehran, Iran. AIDS. 2005;19(7):709-16. [PubMed ID: 15821397].

  • 33.

    Merat S, Malekzadeh R, Rezvan H, Khatibian M. Hepatitis B in Iran. Arch Iranian Med. 2000;3(4):192-201.

  • 34.

    Farhat A, Khademi G, Mazlouman SJ. The prevalence of hepatitis B carrier state in Khorassan province of Iran. Saudi Med J. 2003;24(5):549-51. [PubMed ID: 12847639].

  • 35.

    Sharif M, Sherif A, Sayyah M. Frequency of HBV, HCV and HIV infections among hospitalized injecting drug users in Kashan. Indian J Sex Transm Dis. 2009;30(1):28-30. [PubMed ID: 21938111]. https://doi.org/10.4103/0253-7184.55477.

  • 36.

    Stief AC, Martins RM, Andrade SM, Pompilio MA, Fernandes SM, Murat PG, et al. Seroprevalence of hepatitis B virus infection and associated factors among prison inmates in state of Mato Grosso do Sul, Brazil. Rev Soc Bras Med Trop. 2010;43(5):512-5. [PubMed ID: 21085860].

  • 37.

    Nguyen VTT, Dore GJ. Prevalence and epidemiology of hepatitis B. All You Wanted to Know About. 2001:13.

  • 38.

    Shapatava E, Nelson KE, Tsertsvadze T, del Rio C. Risk behaviors and HIV, hepatitis B, and hepatitis C seroprevalence among injection drug users in Georgia. Drug Alcohol Depend. 2006;82 Suppl 1:S35-8. [PubMed ID: 16769443].

  • 39.

    Vassilev ZP, Hagan H, Lyubenova A, Tomov N, Vasilev G, Krasteva D, et al. Needle exchange use, sexual risk behaviour, and the prevalence of HIV, hepatitis B virus, and hepatitis C virus infections among Bulgarian injection drug users. Int J STD AIDS. 2006;17(9):621-6. [PubMed ID: 16942654]. https://doi.org/10.1258/095646206778113041.

  • 40.

    Fuglsang T, Fouchard JR, Ege PP. [Prevalence of HIV and hepatitis B and C among drug addicts in the city of Copenhagen]. Ugeskr Laeger. 2000;162(27):3860-4. [PubMed ID: 10920701].

  • 41.

    Samuel MC, Doherty PM, Bulterys M, Jenison SA. Association between heroin use, needle sharing and tattoos received in prison with hepatitis B and C positivity among street-recruited injecting drug users in New Mexico, USA. Epidemiol Infect. 2001;127(3):475-84. [PubMed ID: 11811881].

  • 42.

    Christensen PB, Krarup HB, Niesters HG, Norder H, Georgsen J. Prevalence and incidence of bloodborne viral infections among Danish prisoners. Eur J Epidemiol. 2000;16(11):1043-9. [PubMed ID: 11421474].

  • 43.

    Shirin T, Ahmed T, Iqbal A, Islam M, Islam MN. Prevalence and risk factors of hepatitis B virus, hepatitis C virus, and human immunodeficiency virus infections among drug addicts in Bangladesh. J Health Popul Nutr. 2000;18(3):145-50. [PubMed ID: 11262767].

  • 44.

    Todd CS, Abed AM, Strathdee SA, Scott PT, Botros BA, Safi N, et al. HIV, hepatitis C, and hepatitis B infections and associated risk behavior in injection drug users, Kabul, Afghanistan. Emerg Infect Dis. 2007;13(9):1327-31. [PubMed ID: 18252103]. https://doi.org/10.3201/eid1309.070036.

  • 45.

    Altaf A, Shah SA, Zaidi NA, Memon A, Nadeem ur R, Wray N. High risk behaviors of injection drug users registered with harm reduction programme in Karachi, Pakistan. Harm Reduct J. 2007;4:7. [PubMed ID: 17291354]. https://doi.org/10.1186/1477-7517-4-7.

  • 46.

    Mirahmadizadeh A, Kadivar M, Hemmati A, Javadi A. Infection with HIV and hepatitis C and B viruses among injecting drug users in Shiraz, Southern Iran. International Conference on AIDS; Shiraz. 2004.

  • 47.

    Javadi AA, Avijgan M, Hafizi M. Prevalence of HBV and HCV infections and associated risk factors in addict prisoners. Iranian J Public Health. 2006;35(4).

  • 48.

    Rahimi-Movaghar A, Razaghi EM, Sahimi-Izadian E, Amin-Esmaeili M. HIV, hepatitis C virus, and hepatitis B virus co-infections among injecting drug users in Tehran, Iran. Int J Infect Dis. 2010;14(1):e28-33. [PubMed ID: 19464218]. https://doi.org/10.1016/j.ijid.2009.03.002.

  • 49.

    Khani M, Vakili MM. Prevalence and risk factors of HIV, hepatitis B virus and hepatitis C virus infections in drug addicts among Zanjan prisoners. Arch Iranian Med. 2003;6(1):1-4.

  • 50.

    Aminzade Z, Aghazadeh Sarhangi Poor K. [Seroepidemiology of HIV,HBV, HCV and syphilis among intravenous drug user hospitilized in Loghman Hospital,Tehran, Iran]. J Iran Med Microbilogy. 2007;1(3):53-6.

  • 51.

    Taeri K, Kassaeian N, Fadaei Nobari R, Ataei B. [A survay on prevalence of HBV, HCV and main risk factors among HIV positive intravenous drug users in Esfahan]. Esfahan Med Sch J. 2009;26(90).

  • 52.

    Mohammad K, Asgari F, Gooya MM, Fotoohi A, Yoosefi A. [HBV in Iran prisons and it's correlation with addiction]. Payesh J. 2008;7(3):279-86.

  • 53.

    Esteghamati A, Keshtkar AA, Nadjafi L, Gouya MM, Salaramoli M, Roshandel G, et al. Hepatitis B vaccination coverage among Iranian children aged 15-26 months in 2006. East Mediterr Health J. 2011;17(2):93-100. [PubMed ID: 21735942].

  • 54.

    Zali MR, Mohammad K, Noorbala AA, Noorimayer B, Shahraz S. Rate of hepatitis B seropositivity following mass vaccination in the Islamic Republic of Iran. East Mediterr Health J. 2005;11(1-2):62-7. [PubMed ID: 16532672].

  • 55.

    Islamic republic of Iran country report on monitoring of the united nations, general assembly special session on HIV and AIDS. National AIDS Committee Secretariat. Ministry of Health and Medical Education; 2010. Available from: http://data.unaids.org/Pub/report/2010/iran_2010_country_progress_report_en.pdf.