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Risk of hepatitis C infection among injection drug users in Mizoram, India.

Background & objectives: Prevalence of injection drug users (IDUs) is high in the northeastern region of India. This coupled with unsafe injecting practices as well as practice of tattooing in remote tribal areas call for baseline data on the prevalence of parentally transmitted viral diseases. In the present study we aimed to measure the risk behaviours and seroprevalence of hepatitis C virus (HCV) antibodies amongst IDUs of Mizoram, a State of the northeast India.

Methods: A cross-sectional study was conducted in 2004-2005 amongst IDUs (including female sex workers) who had injected in the past six months and were unaware of their HCV/HIV status. They were recruited from various drop-in centers from Aizawl, Mizoram, and screened for anti-HCV antibodies using 3rd generation HCV EIA and recombinant immunoblot assay (RIBA).

Results: The prevalence of HCV antibodies was 71.2 per cent among the active IDUs. On univariate analysis increasing duration of injection, syringe sharing and heroin (diacetylmorphine) injectors were at a significantly higher risk of acquiring HCV antibodies (P<0.001). On multivariate analysis, HCV antibody prevalence showed a strong association with the type of drugs injected (P=0.001), frequency of injecting (P=0.013), multiplicity of drugs abused (P=0.004), and needle syringe sharing (P=0.003).

Interpretation & conclusions: Unsafe injecting practices were found to be associated with a higher risk of acquiring hepatitis C infection. Our findings showed that syringe and needle exchange programme alone was not sufficient as a preventive strategy for control of hepatitis C infection among IDUs of Aizawl.

Key words HCV--Hepatitis C--injection drug user--Mizoram--risk factors

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Hepatitis C virus (IICV) infections have reached epidemic proportions in many parts of the world especially among injection drug users (IDUs). With an estimated 170 million people worldwide with chronic HCV infection (1,2). Hepatitis C is a major cause of chronic liver disease. There is a high frequency of progressive chronic hepatitis, ranging from 50 to 80 per cent, which leads to cirrhosis in 20-50 per cent of patients after 10-20 yr (3).

Though the seroprevalence of HCV antibodies in general population in studies from India is around 1 per cent or less (4,5), HCV antibodies prevalence ranges from 50 to 95 per cent among IDUs in surveys conducted worldwide (6). Risk of exposure to HCV in IDUs increases as the number of lifetime injecting episodes increases (6-9). Unsafe injecting practices such as indirect sharing of injecting paraphernalia i.e., drug preparation equipments usually, cookers or spoons, cotton filter and water used for cleaning syringes; recipient syringe sharing, backloading (involves the preparation of the drug in one syringe and subsequent transfer of half the contents to a different syringe) help in the spread of this virus (6,10-15).

The present study was undertaken to measure the risk behaviours and seroprevalence of HCV antibodies in IDUs of Mizoram, a State of the northeast India. In neighbouring State of Manipur, various studies have shown a very high prevalence (90.4-98%) of HCV in IDUs (16-18). We hypothesized that the IDUs of Mizoram are equally at high risk for HCV infection. With the introduction of syringe exchange programme (SEPs) through out the world (19) to reduce the incidence of HIV, a need was felt to evaluate its impact on HCV infection. As the various drop-in centers run by non government organizations (NGOs) have come under resistance from local youth organization for propagating the SEPs in Mizoram, there was a need to prove the impact of safe injecting practices. We also hypothesized that SEPs may not alone be sufficient to reduce the prevalence of HCV.

Baseline data on the prevalence of HCV in Mizoram State, is needed to plan preventive strategies. Given the economic and health costs of hepatitis C infection and the ongoing transmission within the injecting drug user population, an understanding of HCV epidemiology within this risk group was necessary to develop and evaluate prevention efforts.

Material & Methods

Study area: This study was carried out from September 2004 to August 2005, among the injecting drug users of Aizawl, the capital town of Mizoram situated at an altitude of 1200 meters (4000 ft) above sea level. Mizoram, literally the "the land of highlanders" is one of the smallest States of India, with an area of 21,087 sq km, and a population of around one million. The State has about ten thousand IDUs, roughly 1 per cent of its total population. The State was known as the Lushai Hills under British rule. It is the 2nd State in India with highest literacy rate next to Kerala. The State shares two long international borders, one with Myanmar (273 km) in the east and south and another with Bangladesh (214 km) in the west. The geographical location of the State and socio-cultural and ethnic similarity between the population of Myanmar, results in harmonious intermixing of the populations between two countries and cross-border drug trafficking.

Since the published data on the prevalence of HCV infection among IDUs at Mizoram are not available, similar data available from the neighbouring State of Manipur (16) was considered for sample size calculation.

Study population: The study subjects were drawn in from various drop-in centers and treatment and counselling settings of nine local NGOs. Nine NGOs of Aizawl town (TNT, Jeriko Khualbuk, RTC, Jesus Army, World Vision, Volcmch, Protective Home, Danma Inn, Blessing Home and AMRO) participated in the study. The cases (both male and female) were enrolled into the study if they had a history of injecting in the previous six months. IDUs with known HCV/ HIV status were excluded from the study. One hundred and forty three subjects were enrolled randomly after due informed and written consent and approval from the Institution's ethics committee of the Regional Medical Research Centre, Dibrugarh. A detailed and structured questionnaire was prepared to include all socio-demographic and risk behaviour factors including unsafe injecting variables. The questionnaire was pre-tested in field condition and validated after interviewing 30 IDUs. A trained social worker and a medical officer carried out the detailed interview. The interview format included the duration of injecting career, frequency of unsafe injecting behaviours, use of SEPs (drop-in centers) etc. Recipient syringe sharing was explored specially across the range of categories of social relationships, including unknown sexual partner, friends, usual sexual partner, etc. Type of injecting drugs (heroin, brown sugar, dextropropoxyphene/dicylomine, etc.), frequency, and group size were also noted.

Laboratory tests: After taking written and informed consent for HCV testing, 5ml of blood sample was collected in a sterile vial and allowed to clot and the serum separated on the same day. One hundred and forty three current IDUs consented for the study. HCV antibody was detected by using 3rd generation enzyme linked immunosorbent assay (Genedia HCV ELISA 3.0, South Korea). Due to cost constraints, recombinant immunoblot assay (RIBA, Chiron, CA, USA) was performed on 60 samples only (50 HCV ELISA positive and 10 HCV ELISA negative samples with optical densities near cut-off point). Only those samples with two or more bands showing more than 1+ contrast in the RIBA test were taken as anti-HCV positive. However, samples were not processed for HCV RNA testing, as it was not included in the study protocol.

Statistical analysis: The statistical significance of the seroprevalence of anti-HCV was obtained using Karl Pearson's chi-square test. Associations between categorical variable and HCV status were examined. Odds ratios and their 95 per cent confidence intervals were documented to indicate magnitude and direction of associations. P<0.05 was considered as significant. Association tables were constructed for the purpose of data presentation and statistical analysis. Rows were combined wherever necessary for adequate representation of samples in each cell in order to minimize sampling error. Analysis was performed using SPSS 10.0 and MedCalc Statistical software (20,21). All variables examined by univariate analysis were entered into multivariate logistic regression by both forward and backward selection techniques for final regression equation.

Results

The study participants were between 14 to 56 yr with median age of participants at 24.72 yr (interquartile range 20-28 yr) and the median time since commencement of injecting drugs was 5.65 yr (interquartile range 2.9-9.8 yr). There was a significant increase in prevalence of HCV antibodies in IUSs>21 yr of age (P=0.01). Only 44.9 per cent of the IDUs reported regular use of the syringe and needle exchange programme of the drop-in centers. The prevalence of HCV antibodies in current injecting drug users of Aizawl was found to be 71.3 per cent (102 of 143). Dextropropoxyphene/dicylomine (Proxyvon) and diacetylmorphine (heroin) were the commonest drugs injected (81 and 73.5% respectively). A total of 26 IDUs were female sex workers (FSWS) and 50 per cent of them were anti-HCV positive. Only one (10%) of the 10 occasional IDUs but preferentially oral drug users was anti-HCV positive.

In the IDU group, males accounted for 73.4 per cent (105/143) and females 26.6 per cent (38/143), of which 75.2 (79/105) and 60.5 per cent (23/38) were anti-HCV positive respectively. Majority of the cases were high school dropouts. On univariate analysis it was observed that IDUs having education above primary school have a significantly higher anti-HCV prevalence rate than the illiterates or with minimal education (P=0.003). No other socio-demographic variables were significantly associated with anti-HCV positive status (Table I). More than 72 per cent of the IDUs were unemployed. Prevalence of anti-HCV was higher among those with tattoos (76.7 %) than without (65.7 %), but it was not statistically significant.

Injecting duration was also significantly associated with anti-HCV positive status (P=0.0004). Prevalence of anti-HCV was 31.2 per cent within the first year of injecting duration. Frequency of injecting correlated directly to a significantly higher risk of anti-HCV positive status (P=0.001). There was a significant increase in prevalence of HCV antibodies with increasing numbers of drug use (P =0.002). Respondents claimed to have used pre-used syringe, syringe sharing among friends, more than two syringe sharing partners, syringe sharing or sharing containers during injection in the previous one month of their interview had a higher risk of acquiring HCV (P=0.04, 0.03, 0.047, 0.0003, and 0.046 respectively). Injecting heroin users were at the highest risk of acquiring positive anti-HCV status than any other group (P=0.0002) (Table II).

There was no association of anti-HCV seroprevalence with numbers of sexual partners or age at first sex or the type of sexual partners in the study (data not shown).

On multivariate logistic regression using backward (Wald) step-wise elimination method (Table III), only the frequency of injecting drugs (P=0.013), type of injecting drugs (P=0.001), number of substance abuse (P=0.004) and syringe sharing (P=0.003) were strongly associated with positive anti-HCV status.

The prevalence of anti-HCV was higher (76.5%) among the respondents reporting regularly for SEPs facilities as compared to 67.5 per cent among the respondents not utilizing SEPs facilities regularly.

Discussion

The present study showed a high risk of acquiring hepatitis C infection among the injection drug users of Mizoram. The prevalence of HCV antibodies in 71.3 per cent IDUs was alarmingly high and this finding was expected as the median age of injectors was >5 yr. A very high prevalence of HCV antibodies (90.4-98%) amongst the IDUs from neighbouring State of Manipur has been recorded (16-18), so the present findings were not unexpected. In studies from Kolkata and Delhi, anti-HCV prevalence in IDUs was also found to be quite high (42.96 and 36.45% respectively) (22,23).

High anti-HCV seroprevalence of 80 per cent has been reported among a cohort of IDUs from Kolkata, India (24), and also among IDUs from Nepal (25). Recent studies in Georgian and Bulgarian injectors also reported anti-HCV prevalence of 68.8 and 73.9 per cent respectively (26,27). Studies from Sydney Dublin and San Francisco reported a prevalence of 45, 61 and 45 per cent respectively of HCV antibodies among injecting drug users (7,9,12). Another study from Victoria, Australia, reported a prevalence of HCV antibodies at 68 per cent amongst the IDUs (28). In our study, 31.2 per cent IDUs tested positive for anti-HCV were within the first year of injecting duration. One study had reported 50-80 per cent of new injectors tested positive for anti-HCV within the first 6 to 12 months (29). The high prevalence and more rapid acquisition of HCV among the IDUs is probably the result of the extraordinarily high rate of persistent HCV infection, which has created a large reservoir of potentially infectious persons in the community, providing multiple opportunities for transmission to occur (30).

We found that injection heroin users, duration and frequency of injecting, numbers of drug abused, use of pre-used syringes, sharing of syringes in previous 1 month, sharing injection containers in previous 1 month, increasing numbers of injecting partners were significantly associated with positive anti-HCV status. However, some of the specific unsafe injecting practices like pre-used syringes or sharing of containers or number of injecting partners though initially revealed significance under univariate analysis, did not show a strong association with anti-HCV status after adjusting all factors under regression analysis. There may be inadvertent, unnoticed or accidental sharing of injecting equipment which may have not been reported by the respondents (9). HCV may be transmitted between injecting drug users on equipment other than needles and syringes such as by indirect sharing of injecting paraphernalia (swabs, spoons, containers, filter, water, tourniquets) (8,9,15).

As many as 85.2 per cent of the participants reporting only injecting heroin had HCV positive status compared to only 41.9 per cent among the dextropropoxphene/dicylomine (proxyvon) users. The chances of backloading or sharing of the drug from the same container is most likely with heroin users. This is not perceived as unsafe injecting practice by the IDUs as each of the users is injecting with the personal syringe. Studies have reported higher risk of HCV in heroin injectors than amphetamines or other drugs (28). A recent study has elucidated that heroin/morphine inhibits intrahepatic Interferon-[alpha] expression and enhances complete HCV replication (31). This might be a reason for high HCV prevalence amongst heroin abusers than in proxyvon abusers. The high prevalence of HCV (>90%) amongst IDUs of Manipur (16-18), in fact may be due to the predominant heroin users in that State compared to the present study in Mizoram. Moreover, it was seen that seroprevalence of HCV among IDUs of neighbouring Nagaland is around 30 per cent (authors' unpublished data), where the IDUs inject predominantly proxyvon or spasmoproxyvon (dicylomine).

The high level of HCV antibodies among IDUs of Mizoram implies a well-established prevalence of HCV infection in this group of population. The reason for this is not clear. It is difficult to come to any conclusion without a detailed phylogenetic study of the strains of the virus circulating in the region and a seroprevalence study among the general population and in other risk groups.

Though SEPs are critical component of strategies for controlling the spread of blood-borne infectious diseases, the findings of the present study pointed towards an ineffective interruption of transmission by SEPs alone especially for controlling HCV infection. Probably interventions that reduce injecting habit are more likely to have an impact on lowering HCV prevalence than the interventions designed to make injection safer. It is also imperative to persuade those who do not quit injecting to use new syringes for every injection and to stop indirect sharing of injecting paraphernalia, which is critical for preventing transmission of HCV among the IDUs.

Acknowledgment

Authors acknowledge the Indian Council of Medical Research (ICMR), New Delhi for financial support, and thank the Directorate of Health services, Mizoram; the NGOs that participated in the study (TNT, Jeriko Khualbuk, RTC, Jesus Army, World vision, Volcmch, Protective home, Damna Inn, Blessing Home and AMRO); and Shriyut D.C. Boruah, U. Sharma, C. Saikia, Lanie, Mamie and Dr Josef for their co-operation in carrying out the study.

Received May 24, 2007

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Reprint requests: Dr J. Mahanta, Scientist G & Director, Regional Medical Research Centre, Northeast Region (ICMR) PO Box 105, Dibrugarh 786 001, India e-mail: icmrrcdi@hub.nic.in

P.K. Chelleng, B.J. Borkakoty, M. Chetia, H.K. Das & J. Mahanta

Regional Medical Research Centre, Northeast Region (Indian Council of Medical Research), Dibrugarh, India
Table I. Characteristics of injection drug users who have
seroprevalence for antibodies to hepatitis C virus (n=143;
univariate analysis)

Variables n anti-HCV %
 positive
1. Age (yr):
21 41 23 56
>21 102 79 77.4
2. Gender:
 Male 105 79 75.2
 Female 38 23 60.5
3. Education:
Up to primary/middle school 44 24 54.5
Up to secondary/graduation and above 99 78 78.8
4. Tattooing:
Yes 73 56 76.7
No 70 46 65.7
5. Marital status:
Unmarried 79 55 69.6
Married 16 13 81.2
Divorced or separated 48 34 70.8
h. Alcohol:
Yes 94 69 73.4
No 48 32 66.6
7. Type of family:
Staying alone 3 2 66.6
Nuclear family 58 39 67.2
Joint Family 82 61 74.4
8. Employment:
Unemployed 106 77 72.6
Employed 21 14 66.6
Student 16 11 68.7

Variables odds Ratio 95% C.I. of OR

1. Age (yr):
21 1.0
>21 2.69 1.242 to 5.817
2. Gender:
 Male 1.0
 Female 0.5 0.22 to 1.10
3. Education:
Up to primary/middle school 1.0
Up to secondary/graduation and above 3.09 1.441 to 6.647
4. Tattooing:
Yes 1.0
No 0.58 0.279 to 1.211
5. Marital status:
Unmarried 1.0
Married 1.9 0.493 to 7.249
Divorced or separated 1.05 0.483 to 2.325
h. Alcohol:
Yes 1.0
No 0.72 0.340 to 1.541
7. Type of family:
Staying alone 1.0
Nuclear family 1.02 0.087 to 12.04
Joint Family 1.45 0.125 to 16.85
8. Employment:
Unemployed
Employed 0.75 0.273 to 2.053
Student 0.83 0.265 to 2.591

Variables P

1. Age (yr):
21
>21 0.01
2. Gender:
 Male
 Female 0.08
3. Education:
Up to primary/middle school
Up to secondary/graduation and above 0.003
4. Tattooing:
Yes
No 0.14
5. Marital status:
Unmarried
Married
Divorced or separated 0.64
h. Alcohol:
Yes
No 0.40
7. Type of family:
Staying alone
Nuclear family
Joint Family 0.64
8. Employment:
Unemployed
Employed
Student 0.83

Table II. Association of anti-hepatitis C virus seroprevalence
by exposure group and injecting variables: (unadjusted estimates)

Variables n anti-HCV %
 positive

1. Duration of injecting career (yr)
[less than or equal to] 1 16 5 31.2
1 126 97 77
2. Frequency of injecting last
 one month
Once or more/day 102 81 79.4
Less than once e day 40 21 52.5
3. Ever injecting with used syringe
Yes 98 75 76.5
No 45 27 60
4. No. of substances abused
1 43 24 55.8
2 56 40 71.4
[greater than or equal to] 3 44 38 86.4
5. Syringe sharing last 1 month
No 41 20 48.8
Yes 102 82 80.4
6. No. of needle sharing partners
[less than or equal to] 2 79 51 64.5
2 64 51 79.7
7. Usual injecting partner last
 one month
Usual sexual partner 8 3 37.5
Unknown sexual partner 6 4 66.7
Friend 100 78 78
Not shared 29 17 58.6
8. Sharing injecting containers
 last 1 month
No 30 17 56.7
Yes 113 85 75.2
9. Use of SEPs in last 1 month
 (drop-in centers)
Yes 63 48 76.2
No 80 54 67.5
10. Types of drugs injected
Pure dextropropoxyphene /dicylomine 31 13 41.9
 (proxyvon) users
Both proxyvon and heroin users 85 66 77.6
Only heroin user 27 23 85.2
11. Study population
a) Past IDU/ODU 10 1 10
b) Injecting FSW 26 13 50
c) IDU (Not FSW) 117 89 76.1
Total IDU (b+c) 143 102 71.3
Total (a+b+c) 153 103 67.3

Variables [chi square] P
 (Chi-square)
 or [chi square] trend

1. Duration of injecting career (yr)
[less than or equal to] 1
1 12.502 0.0004
2. Frequency of injecting last
 one month
Once or more/day
Less than once e day 10.28 0.001
3. Ever injecting with used syringe
Yes
No 4.121 0.04
4. No. of substances abused
1
2
[greater than or equal to] 3 9.923 (trend) 0.002
5. Syringe sharing last 1 month
No
Yes 12.786 0.0003
6. No. of needle sharing partners
[less than or equal to] 2
2 3.95 0.047
7. Usual injecting partner last
 one month
Usual sexual partner
Unknown sexual partner
Friend
Not shared 9.00 0.03
8. Sharing injecting containers
 last 1 month
No
Yes 3.99 0.046
9. Use of SEPs in last 1 month
 (drop-in centers)
Yes
No 1.30 0.25
10. Types of drugs injected
Pure dextropropoxyphene /dicylomine
 (proxyvon) users
Both proxyvon and heroin users
Only heroin user 17.29 0.0002
11. Study population
a) Past IDU/ODU
b) Injecting FSW
c) IDU (Not FSW) 46.23 (trend) <0.0001
Total IDU (b+c)
Total (a+b+c)

Table III. Injecting risk factors significantly associated with
risk for hepatitis C (adjusted estimates after final regression
analysis) *

Risk factors Adjusted 95% CI of AOR P
 odds ratio
 (AOR)
1. Frequency of injecting
last one month
Less than once/ day 1.0
Once or more/day 3.711 1.324-10.404 0.013
2. No. of substances
abused
1 1.0
2 5.32 1.056-26.831 0.043
? 3 20.45 2.64- 158.44 0.004
3. Syringe sharing last
1 month
No 1.0
Yes 4.74 1.675-13.434 0.003
4. Types of drugs injected
Pure extropropoxyphene 1.0
/dicylomine (proxyvon)
users
Both proxyvon and 0.708 0.139- 3.606 0.671
heroin users
Only heroin user 13.011 2.692- 62.93 0.001

* Multiple logistic regressions applied using Wald backward
step-wise elimination method. Probability for step-wise entry
and removal calculation was taken at 0.05 and 0.1 per cent
respectively
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Author:Chelleng, P.K.; Borkakoty, B.J.; Chetia, M.; Das, H.K.; Mahanta, J.
Publication:Indian Journal of Medical Research
Article Type:Clinical report
Date:Nov 1, 2008
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