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Risk behaviours related to hepatitis B virus infection among adults in Malaysia: A cross-sectional household survey

  • Yogambigai Rajamoorthy
    Correspondence
    Corresponding author. Department of Economics, Faculty of Accountancy and Management, Universiti Tunku Abdul Rahman, Sungai Long Campus, Jalan Sungai Long, Cheras, 43000, Kajang, Selangor, Malaysia.
    Affiliations
    Department of Economics, Universiti Tunku Abdul Rahman, Selangor, Malaysia

    Department of Economics, Universiti Putra Malaysia, Serdang, Selangor, Malaysia
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  • Niazlin Mohd Taib
    Affiliations
    Department of Medical Microbiology and Parasitology, Universiti Putra Malaysia, Selangor, Malaysia
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  • Mudatsir Mudatsir
    Correspondence
    Corresponding author. Medical Research Unit, School of Medicine, Universitas Syiah Kuala, Jl. T. Tanoeh Abe, Darussalam, Banda Aceh, 23111, Indonesia.
    Affiliations
    Medical Research Unit, School of Medicine, Universitas Syiah Kuala, Banda Aceh, Indonesia

    Department of Microbiology, School of Medicine, Universitas Syiah Kuala Syiah Kuala, Banda Aceh, Indonesia
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  • Harapan Harapan
    Correspondence
    Corresponding author. Medical Research Unit, School of Medicine, Universitas Syiah Kuala, Jl. T. Tanoeh Abe, Darussalam, Banda Aceh, 23111, Indonesia.
    Affiliations
    Medical Research Unit, School of Medicine, Universitas Syiah Kuala, Banda Aceh, Indonesia

    Department of Microbiology, School of Medicine, Universitas Syiah Kuala Syiah Kuala, Banda Aceh, Indonesia
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  • Abram Luther Wagner
    Affiliations
    Department of Epidemiology, University of Michigan, Michigan, USA
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  • Subramaniam Munusamy
    Affiliations
    Department of Economics, Universiti Putra Malaysia, Serdang, Selangor, Malaysia

    Centre for Language and Foundation Studies, Manipal International University, Negeri Sembilan, Malaysia
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  • Khalid Abdul Rahim
    Affiliations
    Department of Economics, Universiti Putra Malaysia, Serdang, Selangor, Malaysia
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  • Alias Radam
    Affiliations
    Department of Economics, Universiti Putra Malaysia, Serdang, Selangor, Malaysia
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      Abstract

      Background

      The objective of this study was to identify the magnitude of various risk behaviours related to Hepatitis B (HepB) and to characterize the relationship between socio-demographic determinants and these risk factors among adults in Malaysia.

      Methods

      We conducted a cross-sectional study in nine districts in the state of Selangor in 2016. A two-stage cluster sampling design was used and adults aged 20 years or above who were living in the selected living quarters were interviewed face-to-face. A multivariable linear regression model analysed the association between sociodemographic predictors and eleven outcomes (different HepB risk behaviours).

      Results

      A total of 728 respondents were included in the final analysis. Sharing nail cutters, body-piercing, and alcohol use were the most prevalent risk behaviours among respondents. Males, married couples, adult respondents (between 27 and 40 years old), and individuals with low educational attainment were more likely to be exposed to HepB risk behaviours.

      Conclusion

      HepB risk behaviours are relatively high among Malaysians and particularly among certain groups. Therefore, specific programs such as forums, seminars and continuous education on preventive measures for HepB should be tailored to these groups. These programs could be conducted by government authorities such as the Ministry of Women, Family and Community of Malaysia.

      Keywords

      1. Introduction

      The World Health Organisation (WHO) has estimated that 257 million people are chronically infected with hepatitis B virus (HBV) globally and in 2015, 887,000 individuals died due to HBV complications.

      WHO: Hepatitis B. Available from: http://wwwwhoint/mediacentre/factsheets/fs204/en/(Accessed: 8 Feb 2018).

      There are two routes to HBV transmission: vertical transmission and horizontal transmission.
      • WHO
      Hepatitis B vaccines.
      Vertical transmission of hepatitis B (HepB) occurs mainly in highly endemic areas, while horizontal transmission is the main cause of infection in low endemic areas.
      • Alter M.J.
      • Hadler S.C.
      • Margolis H.S.
      • et al.
      The changing epidemiology of hepatitis-B in the united-states - need for alternative vaccination strategies.
      Several risk factors for horizontal transmission have been identified such as history of dental procedures
      • Piot P.
      • Goilav C.
      • Kegels E.
      Hepatitis B: transmission by sexual contact and needle sharing.
      • Ali M.
      • Idrees M.
      • Ali L.
      • et al.
      Hepatitis B virus in Pakistan: a systematic review of prevalence, risk factors, awareness status and genotypes.
      • Paez Jimenez A.
      • El-Din N.S.
      • El-Hoseiny M.
      • et al.
      Community transmission of hepatitis B virus in Egypt: results from a case-control study in Greater Cairo.
      • Palmateer N.E.
      • Hutchinson S.J.
      • Innes H.
      • et al.
      Review and meta-analysis of the association between self-reported sharing of needles/syringes and hepatitis C virus prevalence and incidence among people who inject drugs in Europe.
      or surgical interventions,
      • Piot P.
      • Goilav C.
      • Kegels E.
      Hepatitis B: transmission by sexual contact and needle sharing.
      ,
      • Ali M.
      • Idrees M.
      • Ali L.
      • et al.
      Hepatitis B virus in Pakistan: a systematic review of prevalence, risk factors, awareness status and genotypes.
      ,
      • Kay M.
      Hepatitis outbreak is traced to contaminated needles and barber shop razors, study shows.
      ,
      • Phoon W.O.
      • Fong N.P.
      • Lee J.
      History of blood-transfusion, tattooing, acupuncture and risk of hepatitis-B surface antigenemia among Chinese men in Singapore.
      blood transfusions,
      • Piot P.
      • Goilav C.
      • Kegels E.
      Hepatitis B: transmission by sexual contact and needle sharing.
      ,
      • Kay M.
      Hepatitis outbreak is traced to contaminated needles and barber shop razors, study shows.
      ,
      • Mathei C.
      • Shkedy Z.
      • Denis B.
      • et al.
      Evidence for a substantial role of sharing of injecting paraphernalia other than syringes/needles to the spread of hepatitis C among injecting drug users.
      hemodialysis,
      • Vassilev Z.P.
      • Hagan H.
      • Lyubenova A.
      • 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.
      and history of abrasions during haircuts.
      • Atkins M.
      • Nolan M.
      Sexual transmission of hepatitis B.
      Certain groups also have a higher risk of HepB for example men who have sex with men,
      • Rajamoorthy Y.
      • Radam A.
      • Taib N.
      • et al.
      Willingness to Pay for Self-Paid Hepatitis B Vaccination in Selangor.
      ,
      • Hagan H.
      • Pouget E.R.
      • Des Jarlais D.C.
      A systematic review and meta-analysis of interventions to prevent hepatitis C virus infection in people who inject drugs.
      drug and alcohol users,
      • Piot P.
      • Goilav C.
      • Kegels E.
      Hepatitis B: transmission by sexual contact and needle sharing.
      ,
      • Samuel M.C.
      • Doherty P.M.
      • Bulterys M.
      • Jenison S.A.
      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.
      • Shapatava E.
      • Nelson K.E.
      • Tsertsvadze T.
      • del Rio C.
      Risk behaviors and HIV hepatitis B, and hepatitis C seroprevalence among injection drug users in Georgia.
      • Hagan H.
      • Jarlais D.C.D.
      • Friedman S.R.
      • Purchase D.
      • Alter M.J.
      Reduced risk of hepatitis-B and hepatitis-C among injection-drug users in the tacoma syringe exchange program.
      • Koester S.
      • Glanz J.
      • Baron A.
      Drug sharing among heroin networks: implications for HIV and hepatitis B and C prevention.
      • 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.
      • Xu C.J.
      • Zhang C.P.
      • Luo B.F.
      • et al.
      Prevalence and characterization of hepatitis B and C virus infections in a needle-sharing population in Northern China.
      healthcare workers,
      • Talaat M.
      • Kandeel A.
      • El-Shoubary W.
      • et al.
      Occupational exposure to needlestick injuries and hepatitis B vaccination coverage among health care workers in Egypt.
      • Pruss-Ustun A.
      • Rapiti E.
      • Hutin Y.
      Estimation of the global burden of disease attributable to contaminated sharps injuries among health-care workers.
      • Gorgos L.
      Sexual transmission of viral hepatitis.
      • Beasley R.P.
      • Hwang L.Y.
      • Lin C.C.
      • Ko Y.C.
      • Twu S.J.
      Incidence of hepatitis among students at a university in taiwan.
      • Trepo C.
      • Chan H.L.Y.
      • Lok A.
      Hepatitis B virus infection.
      • Ozer A.
      • Yakupogullari Y.
      • Beytur A.
      • et al.
      Risk factors of hepatitis B virus infection in Turkey: a population-based, case-control study.
      household members who live with a HepB carrier,
      • Vassilev Z.P.
      • Hagan H.
      • Lyubenova A.
      • 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.
      ,
      • Goldstein S.T.
      • Alter M.J.
      • Williams I.T.
      • et al.
      Incidence and risk factors for acute hepatitis B in the United States, 1982-1998: implications for vaccination programs.
      ,
      • Pereira L.M.M.B.
      • Martelli C.M.T.
      • Merchan-Hamann E.
      • et al.
      Population-based multicentric survey of hepatitis B infection and risk factor differences among three regions in Brazil.
      and individuals with multiple sexual partners.
      • Beasley R.P.
      • Hwang L.Y.
      • Lin C.C.
      • Ko Y.C.
      • Twu S.J.
      Incidence of hepatitis among students at a university in taiwan.
      ,
      • Des Jarlais D.C.
      • Sloboda Z.
      • Friedman S.R.
      • Tempalski B.
      • McKnight C.
      • Braine N.
      Diffusion of the D.A.R.E and syringe exchange programs.
      In addition, HepB prevalence is higher among people who having been tattooed,
      • Piot P.
      • Goilav C.
      • Kegels E.
      Hepatitis B: transmission by sexual contact and needle sharing.
      ,
      • Phoon W.O.
      • Fong N.P.
      • Lee J.
      History of blood-transfusion, tattooing, acupuncture and risk of hepatitis-B surface antigenemia among Chinese men in Singapore.
      ,
      • Xu C.J.
      • Zhang C.P.
      • Luo B.F.
      • et al.
      Prevalence and characterization of hepatitis B and C virus infections in a needle-sharing population in Northern China.
      ,
      • Lichtenhan J.B.
      Sexual activity and recommendations for the hepatitis B vaccine.
      who have piercings
      • Kay M.
      Hepatitis outbreak is traced to contaminated needles and barber shop razors, study shows.
      and who share household tools such as toothbrushes, razor blades and nail cutters.
      • Ali M.
      • Idrees M.
      • Ali L.
      • et al.
      Hepatitis B virus in Pakistan: a systematic review of prevalence, risk factors, awareness status and genotypes.
      • Paez Jimenez A.
      • El-Din N.S.
      • El-Hoseiny M.
      • et al.
      Community transmission of hepatitis B virus in Egypt: results from a case-control study in Greater Cairo.
      • Palmateer N.E.
      • Hutchinson S.J.
      • Innes H.
      • et al.
      Review and meta-analysis of the association between self-reported sharing of needles/syringes and hepatitis C virus prevalence and incidence among people who inject drugs in Europe.
      • Kay M.
      Hepatitis outbreak is traced to contaminated needles and barber shop razors, study shows.
      ,
      • Trepo C.
      • Chan H.L.Y.
      • Lok A.
      Hepatitis B virus infection.
      ,
      • Ramadori P.
      • Cubero F.J.
      • Liedtke C.
      • Trautwein C.
      • Nevzorova Y.A.
      Alcohol and hepatocellular carcinoma: adding fuel to the flame.
      • Duraisamy G.
      Blood transfusion in Malaysia.
      • Van Herck K.
      • Vorsters A.
      • Van Damme P.
      Prevention of viral hepatitis (B and C) reassessed.
      • Yang J.
      • Hall K.
      • Nuriddin A.
      • Woolard D.
      Risk for hepatitis B and C virus transmission in nail salons and barbershops and state regulatory requirements to prevent such transmission in the United States.
      Hepatitis B is very common in Asia
      • Maynard J.E.
      Hepatitis B: global importance and need for control.
      • Romano L.
      • Paladini S.
      • Van Damme P.
      • Zanetti A.R.
      The worldwide impact of vaccination on the control and protection of viral hepatitis B.
      • Sung J.L.
      Hepatitis-B virus eradication strategy for Asia.
      and is recognized as an upcoming public health problem in middle-income countries like Malaysia.
      • Qua C.S.
      • Goh K.L.
      Liver cirrhosis in Malaysia: peculiar epidemiology in a multiracial Asian country.
      Before the national universal HepB vaccination of all newborn infants was implemented in 1989, the prevalence of HBV surface antigen (HBsAg) in Malaysia was 5%–7%.
      • Sulaiman H.A.
      • Sie J.A.
      • Rustam M.
      • Melani W.
      • Corwin A.
      • Jennings G.B.
      Prevalence of hepatitis-B and hepatitis-C viruses in healthy Indonesian blood-donors.
      After the implementation of the universal HepB vaccination program, a survey among 190,077 school children, who born between 1985 and 1996, found that the overall prevalence of HBsAg was 0.6%.
      • Jafari S.
      • Buxton J.A.
      • Afshar K.
      • Copes R.
      • Baharlou S.
      Tattooing and risk of hepatitis B: a systematic review and meta-analysis.
      On a national scale, an estimation one million Malaysian are chronically infected with HBV,
      • Van Herck K.
      • Vorsters A.
      • Van Damme P.
      Prevention of viral hepatitis (B and C) reassessed.
      ,
      • Khairullah N.S.
      • Merican D.I.
      Hepatitis disease management programs in Malaysia.
      and it is the main cause of liver cirrhosis and liver cancer in the country.
      • Yang J.
      • Hall K.
      • Nuriddin A.
      • Woolard D.
      Risk for hepatitis B and C virus transmission in nail salons and barbershops and state regulatory requirements to prevent such transmission in the United States.
      ,
      • Qua C.S.
      • Goh K.L.
      Liver cirrhosis in Malaysia: peculiar epidemiology in a multiracial Asian country.
      With a total population of 29.9 million in Malaysia in 2013, the prevalence of HepB in the country is approximately 3%.
      Globally, studies have been conducted to address risk behaviours related to HBV infection and some variables have been confirmed. Risk factors in these studies include socioeconomic factors,
      • Pereira L.M.M.B.
      • Martelli C.M.T.
      • Merchan-Hamann E.
      • et al.
      Population-based multicentric survey of hepatitis B infection and risk factor differences among three regions in Brazil.
      ,
      • Gogos C.A.
      • Fouka K.P.
      • Nikiforidis G.
      • et al.
      Prevalence of hepatitis B and C virus infection in the general population and selected groups in South-Western Greece.
      • Lee D.H.
      • Kim J.H.
      • Nam J.J.
      • Kim H.R.
      • Shin H.R.
      Epidemiological findings of hepatitis B infection based on 1998 national health and nutrition survey in korea.
      • Liang X.F.
      • Bi S.L.
      • Yang W.Z.
      • et al.
      Reprint of: epidemiological serosurvey of Hepatitis B in China-Declining HBV prevalence due to Hepatitis B vaccination.
      medical history,
      • Piot P.
      • Goilav C.
      • Kegels E.
      Hepatitis B: transmission by sexual contact and needle sharing.
      • Ali M.
      • Idrees M.
      • Ali L.
      • et al.
      Hepatitis B virus in Pakistan: a systematic review of prevalence, risk factors, awareness status and genotypes.
      • Paez Jimenez A.
      • El-Din N.S.
      • El-Hoseiny M.
      • et al.
      Community transmission of hepatitis B virus in Egypt: results from a case-control study in Greater Cairo.
      • Palmateer N.E.
      • Hutchinson S.J.
      • Innes H.
      • et al.
      Review and meta-analysis of the association between self-reported sharing of needles/syringes and hepatitis C virus prevalence and incidence among people who inject drugs in Europe.
      • Kay M.
      Hepatitis outbreak is traced to contaminated needles and barber shop razors, study shows.
      • Phoon W.O.
      • Fong N.P.
      • Lee J.
      History of blood-transfusion, tattooing, acupuncture and risk of hepatitis-B surface antigenemia among Chinese men in Singapore.
      • Mathei C.
      • Shkedy Z.
      • Denis B.
      • et al.
      Evidence for a substantial role of sharing of injecting paraphernalia other than syringes/needles to the spread of hepatitis C among injecting drug users.
      • Vassilev Z.P.
      • Hagan H.
      • Lyubenova A.
      • 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.
      ,
      • Talaat M.
      • Kandeel A.
      • El-Shoubary W.
      • et al.
      Occupational exposure to needlestick injuries and hepatitis B vaccination coverage among health care workers in Egypt.
      • Pruss-Ustun A.
      • Rapiti E.
      • Hutin Y.
      Estimation of the global burden of disease attributable to contaminated sharps injuries among health-care workers.
      • Gorgos L.
      Sexual transmission of viral hepatitis.
      • Beasley R.P.
      • Hwang L.Y.
      • Lin C.C.
      • Ko Y.C.
      • Twu S.J.
      Incidence of hepatitis among students at a university in taiwan.
      • Trepo C.
      • Chan H.L.Y.
      • Lok A.
      Hepatitis B virus infection.
      • Ozer A.
      • Yakupogullari Y.
      • Beytur A.
      • et al.
      Risk factors of hepatitis B virus infection in Turkey: a population-based, case-control study.
      occupational risk behaviours,
      • Talaat M.
      • Kandeel A.
      • El-Shoubary W.
      • et al.
      Occupational exposure to needlestick injuries and hepatitis B vaccination coverage among health care workers in Egypt.
      • Pruss-Ustun A.
      • Rapiti E.
      • Hutin Y.
      Estimation of the global burden of disease attributable to contaminated sharps injuries among health-care workers.
      • Gorgos L.
      Sexual transmission of viral hepatitis.
      • Beasley R.P.
      • Hwang L.Y.
      • Lin C.C.
      • Ko Y.C.
      • Twu S.J.
      Incidence of hepatitis among students at a university in taiwan.
      • Trepo C.
      • Chan H.L.Y.
      • Lok A.
      Hepatitis B virus infection.
      • Ozer A.
      • Yakupogullari Y.
      • Beytur A.
      • et al.
      Risk factors of hepatitis B virus infection in Turkey: a population-based, case-control study.
      and lifestyle-related behaviour risk factors. Lifestyle-related behaviour risk factors for HepB include living with a chronic HepB infection,
      • Vassilev Z.P.
      • Hagan H.
      • Lyubenova A.
      • 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.
      ,
      • Goldstein S.T.
      • Alter M.J.
      • Williams I.T.
      • et al.
      Incidence and risk factors for acute hepatitis B in the United States, 1982-1998: implications for vaccination programs.
      ,
      • Pereira L.M.M.B.
      • Martelli C.M.T.
      • Merchan-Hamann E.
      • et al.
      Population-based multicentric survey of hepatitis B infection and risk factor differences among three regions in Brazil.
      unsafe sexual activity and having multiple sexual partners,
      • Beasley R.P.
      • Hwang L.Y.
      • Lin C.C.
      • Ko Y.C.
      • Twu S.J.
      Incidence of hepatitis among students at a university in taiwan.
      ,
      • Des Jarlais D.C.
      • Sloboda Z.
      • Friedman S.R.
      • Tempalski B.
      • McKnight C.
      • Braine N.
      Diffusion of the D.A.R.E and syringe exchange programs.
      having tattoos and body piercing,
      • Piot P.
      • Goilav C.
      • Kegels E.
      Hepatitis B: transmission by sexual contact and needle sharing.
      ,
      • Kay M.
      Hepatitis outbreak is traced to contaminated needles and barber shop razors, study shows.
      ,
      • Phoon W.O.
      • Fong N.P.
      • Lee J.
      History of blood-transfusion, tattooing, acupuncture and risk of hepatitis-B surface antigenemia among Chinese men in Singapore.
      ,
      • Xu C.J.
      • Zhang C.P.
      • Luo B.F.
      • et al.
      Prevalence and characterization of hepatitis B and C virus infections in a needle-sharing population in Northern China.
      ,
      • Lichtenhan J.B.
      Sexual activity and recommendations for the hepatitis B vaccine.
      sharing household tools such as toothbrushes, razor blades and nail cutters,
      • Ali M.
      • Idrees M.
      • Ali L.
      • et al.
      Hepatitis B virus in Pakistan: a systematic review of prevalence, risk factors, awareness status and genotypes.
      • Paez Jimenez A.
      • El-Din N.S.
      • El-Hoseiny M.
      • et al.
      Community transmission of hepatitis B virus in Egypt: results from a case-control study in Greater Cairo.
      • Palmateer N.E.
      • Hutchinson S.J.
      • Innes H.
      • et al.
      Review and meta-analysis of the association between self-reported sharing of needles/syringes and hepatitis C virus prevalence and incidence among people who inject drugs in Europe.
      • Kay M.
      Hepatitis outbreak is traced to contaminated needles and barber shop razors, study shows.
      ,
      • Trepo C.
      • Chan H.L.Y.
      • Lok A.
      Hepatitis B virus infection.
      ,
      • Ramadori P.
      • Cubero F.J.
      • Liedtke C.
      • Trautwein C.
      • Nevzorova Y.A.
      Alcohol and hepatocellular carcinoma: adding fuel to the flame.
      • Duraisamy G.
      Blood transfusion in Malaysia.
      • Van Herck K.
      • Vorsters A.
      • Van Damme P.
      Prevention of viral hepatitis (B and C) reassessed.
      • Yang J.
      • Hall K.
      • Nuriddin A.
      • Woolard D.
      Risk for hepatitis B and C virus transmission in nail salons and barbershops and state regulatory requirements to prevent such transmission in the United States.
      and drug and alcohol use.
      • Piot P.
      • Goilav C.
      • Kegels E.
      Hepatitis B: transmission by sexual contact and needle sharing.
      ,
      • Samuel M.C.
      • Doherty P.M.
      • Bulterys M.
      • Jenison S.A.
      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.
      • Shapatava E.
      • Nelson K.E.
      • Tsertsvadze T.
      • del Rio C.
      Risk behaviors and HIV hepatitis B, and hepatitis C seroprevalence among injection drug users in Georgia.
      • Hagan H.
      • Jarlais D.C.D.
      • Friedman S.R.
      • Purchase D.
      • Alter M.J.
      Reduced risk of hepatitis-B and hepatitis-C among injection-drug users in the tacoma syringe exchange program.
      • Koester S.
      • Glanz J.
      • Baron A.
      Drug sharing among heroin networks: implications for HIV and hepatitis B and C prevention.
      • 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.
      • Xu C.J.
      • Zhang C.P.
      • Luo B.F.
      • et al.
      Prevalence and characterization of hepatitis B and C virus infections in a needle-sharing population in Northern China.
      The aim of this study was to identify the magnitude of HepB lifestyle-related behaviour risk factors and to characterize the relationship between socio-demographic determinants and these risk factors among adults in Selangor, Malaysia.

      2. Methods

      2.1 Study design and setting

      A cross-sectional study was conducted in nine districts (Gombak, Klang, Kuala Langat, Kuala Selangor, Petaling, Sabak Bernam, Sepang, Ulu Langat and Ulu Selangor) of Selangor state between 18 January and 14 May 2016. This study was part of the Malaysian Hepatitis B Project.
      • Rajamoorthy Y.
      • Radam A.
      • Taib N.
      • et al.
      Willingness to pay for self-paid hepatitis B vaccination in Selangor, Malaysia.
      • Rajamoorthy Y.
      • Taib N.M.
      • Munusamy S.
      • et al.
      Knowledge and awareness of hepatitis B among households in Malaysia: a community-based cross-sectional survey.
      • Rajamoorthy Y.
      • Radam A.
      • Taib N.M.
      • et al.
      The relationship between perceptions and self-paid hepatitis B vaccination: a structural equation modeling approach.
      Selangor was chosen because it is the most populated state in Malaysia and has the highest number of households (Department of Statistic Malaysia, 2015). The protocol used in this study was approved by Universiti Putra Malaysia, Selangor, Malaysia. All informed consent was obtained from all participants prior to enrolment. The work was carried out in accordance with the Code of Ethics of the World Medical Association for experiments involving humans.

      2.2 Sampling procedure and sample size

      The sampling procedure was conducted with assistance from the Department of Statistics Malaysia and used population data from the National Population and Housing Census 2010. Based on the conservative assumption that 50% of participants would be at high risk for HepB, a 5% margin of error with a confidence interval of 95% and Selangor's population of 5.79 million people,
      • DSM
      Population Distribution and Basic Demographic Characteristics Report 2010.
      385 respondents were required for this study. However, because this study was part of Malaysian Hepatitis B Project
      • Rajamoorthy Y.
      • Radam A.
      • Taib N.
      • et al.
      Willingness to pay for self-paid hepatitis B vaccination in Selangor, Malaysia.
      • Rajamoorthy Y.
      • Taib N.M.
      • Munusamy S.
      • et al.
      Knowledge and awareness of hepatitis B among households in Malaysia: a community-based cross-sectional survey.
      • Rajamoorthy Y.
      • Radam A.
      • Taib N.M.
      • et al.
      The relationship between perceptions and self-paid hepatitis B vaccination: a structural equation modeling approach.
      whose main objective was to assess the willingness-to-pay (WTP) for HepB vaccine,
      • Rajamoorthy Y.
      • Radam A.
      • Taib N.
      • et al.
      Willingness to pay for self-paid hepatitis B vaccination in Selangor, Malaysia.
      the sample size was calculated to answer the main project's objective. Based on a formula from the literature,
      • Prince R.
      Using surveys to value public-goods - the contingent valuation method.
      the minimum sample size required was 683. This is based on an assumption that the relative error of the true WTP (V) was 2.0, the deviation of the estimated WTP from the true value (Δ) was 15%, with a 5% margin of error and a confidence interval of 95%. This sample size was acceptable for the aim of the study presented in this article. To avoid repetitive field visits and to obtain a more robust estimate,
      • Harapan H.
      • Mudatsir M.
      • Yufika A.
      • et al.
      Community acceptance and willingness-to-pay for a hypothetical Zika vaccine: a cross-sectional study in Indonesia.
      ,
      • Harapan H.
      • Rajamoorthy Y.
      • Anwar S.
      • et al.
      Knowledge, attitude, and practice regarding dengue virus infection among inhabitants of Aceh, Indonesia: a cross-sectional study.
      85 additional participants were added for a final sample size 768. A stratified two-stage cluster sampling design with proportional allocation was employed to recruit the participants (Fig. 1). Briefly, 1,575,200 households in Selangor were divided into 16,562 Enumeration Blocks (EB) in nine districts and each EB consisted of 80 and 120 living quarters (LQ). Sixty-four out of 16,562 EBs (59 EBs for urban areas and 5 EBs for rural areas) and 12 LQs within each EB were randomly selected. In total, 768 LQs were sampled (708 LQs for urban and 60 LQs for rural areas) and one individual, who was Malaysian and a minimum of 20 years old, was selected from each LQ.
      Fig. 1
      Fig. 1Flow chart of sampling methods used in the study.

      2.3 Data collection

      Face-to-face interviews were conducted at selected households by trained enumerators. The interviews were conducted in Malay or English. Participants who were unable to understand English and Malay were attended by translators who were able to communicate and translate the questionnaire into their preferred language. If the participants were absent over multiple days, a neighbour who adhered to the eligibility criteria (Malaysian and a minimum of 20 years old), with a similar race as the previously selected participant was selected instead. Prior to the interview, an overview of the aims and benefits were given the participants, and, for those who agreed to participate, verbal or written informed consent was obtained. Prior to asking the participant questions, interviewers gave the participants a brochure from the Ministry of Health Malaysia which contained photographs, symptoms of HepB, information on the transmission of HBV, and prevention methods for HBV.

      2.4 Instruments

      Questions were adopted from a previous study.
      • Gheorghe L.
      • Csiki I.E.
      • Iacob S.
      • Gheorghe C.
      • Smira G.
      • Regep L.
      The prevalence and risk factors of hepatitis C virus infection in adult population in Romania: a nationwide survey 2006-2008.
      The English version of the questionnaire was developed based on the existing literature and translated into the Malay language. Both versions of the questionnaire were evaluated by a panel of three medical experts in which wording and structure of some of the questions were revised. The revised versions of both versions of questionnaire were initially tested among 121 respondents. This pilot study revealed that questions related to risk behaviour had good internal consistency (Cronbach's alpha value of 0.7). During this pilot test, the respondents were also asked to provide feedback, which was considered for the final version of the questionnaire. The questionnaire used in this study is available in Supplementary data.

      2.5 Study variables

      The main outcome variable in this study was a set of risk behaviours for HepB that was related to household members' lifestyle. Eleven lifestyle-related behaviour risk factors were selected as outcome variable in this study which were the most relevant to Malaysia: sharing needles, sharing razor blades, sharing a toothbrush, sharing a nail cutter, tattoos, body-piercing, acupuncture, sex with an unknown person, >10 sexual partners, alcohol use and prison experience. The questions related to risk behaviours were all on a seven-point Likert scale (1 for ‘never’ and 7 for ‘every time’).
      Explanatory variables for this study included gender, ethnicity, education, and age. During the interview, the ethnicity of the participants was recorded and then grouped into Malay, Chinese, Indian and others. Educational attainment was defined as the highest level of formal education completed and was classified into the following categories: illiterate, primary school, secondary school, diploma, degree and postgraduate. The date of birth was recorded during the interview, converted into actual age and divided in to three groups (20–26, 27–40, and 41–54 years old).

      2.6 Statistical analysis

      A linear regression modelled the association between demographic factors and risk behaviours for HBV infection. Separate models were constructed for all 11 risk behaviours considered. Before conducting the regression analysis, several diagnostic checks were performed on how well the data met assumptions of a linear regression model, including a multicollinearity test (variance inflation factor, <5), a heteroscedasticity test (White test, p-value >0.05), a serial autocorrelation test (Lagrange multiplier, p-value >0.05), and a normality test (Jarque-Bera test, p-value >0.05). Our diagnostic results revealed no violation in linear regression assumptions. All analyses were conducted using the IBM SPSS statistics version 22.0.

      3. Results

      3.1 Participant characteristics

      We interviewed 768 households and 40 responses were excluded due to incomplete information. A total of 728 (94.7%) participants were included in the final analysis. Characteristics of the participants are provided in Table 1. More than half (54.5%) of participants were male and the mean age of respondents was 40 years (SD ± 11.0). Most respondents were Malay, followed by Chinese and Indians. Approximately 29% participants were working in the private sector, approximately 24% of participants were entrepreneurs and about 20% were unemployed. Less than 2% participants were illiterate and the mean monthly income was RM 4421.21 (USD 1132).
      Table 1Demographic characteristics of participants (n = 728).
      VariableFrequency (%)
      Age in years (mean ± SD)40 ± 11.0
      Sex
       Male397 (54.5)
       Female331 (45.5)
      Ethnicity
       Malay439 (60.3)
       Chinese170 (23.4)
       Indian116 (19.9)
       Others3 (0.4)
      Occupation
       Private employee214 (29.4)
       Self-employment175 (24.0)
       Civil servant96 (13.2)
       Retired53 (7.3)
       Student26 (3.6)
       Others19 (2.6)
       Unemployed145 (19.9)
      Marital status
       Single139 (19.1)
       Married574 (78.8)
       Widowed9 (1.2)
       Divorced6 (0.8)
      Literation
       Illiterate (never been to school)13 (1.7)
       Literate715 (98.3)
      Education
       Primary36 (5)
       Secondary342 (37)
       Diploma188 (25.8)
       Degree123 (16.9)
       Postgraduate26 (3.6)
      Monthly income (mean ± SD) (RM)4421.21 ± 3856
      RM: Malaysian ringgit, SD: Standard deviation

      3.2 Hepatitis B risk behaviour

      The frequencies of risk behaviours of HepB among participants are presented in Table 2. The most common high risk behaviours were sharing nail cutters (82.4% did rarely or more often), body piercing (34.9% reported a value of rarely or more often), alcohol use (20.1% did rarely or more often), and undergoing acupuncture (15.7% did rarely or more often). The prevalence of risk behaviours (% of those engaging in a behaviour rarely or more often) varied by gender (Fig. 2). Among males, the two most common risk behaviours were sharing nail cutters and alcohol use, whereas the two most common risk behaviours were sharing nail cutters and body piercing for females.
      Table 2Descriptive statistic of hepatitis B risk behaviour (n = 728).
      Risk BehaviourNeverRarelyOccasionallySometimesFrequentlyUsuallyEvery time
      n (%)n (%)n (%)n (%)n (%)n (%)n (%)
      Sharing needles718 (98.6)7 (1.0)0 (0.0)3 (0.4)0 (0.0)0 (0.0)0 (0.0)
      Sharing razors658 (90.4)38 (5.2)7 (1.0)5 (0.7)6 (0.8)7 (1.0)7 (1.0)
      Sharing toothbrushes629 (86.4)46 (6.3)20 (2.7)5 (0.7)4 (0.5)18 (2.5)6 (0.8)
      Sharing nail cutters128 (17.6)31 (4.3)47 (6.5)63 (8.7)69 (9.5)90 (12.4)300 (41.2)
      Tattooed671 (92.3)28 (3.9)8 (1.1)1 (0.1)8 (1.1)4 (0.6)7 (1.0)
      Body piercing473 (65.1)104 (14.3)38 (5.2)28 (3.9)25 (3.4)20 (2.8)39 (5.4)
      Undergoing acupuncture614 (84.3)34 (4.7)20 (2.7)15 (2.1)19 (2.6)20 (2.7)6 (0.8)
      Sex with unknown partner697 (95.7)16 (2.2)7 (1.0)3 (0.4)1 (0.1)2 (0.3)2 (0.3)
      >10 lifetime sexual partners695 (95.6)8 (1.1)2 (0.3)1 (0.1)3 (0.4)6 (0.8)12 (1.7)
      Prisoners723 (99.3)2 (0.3)1 (0.1)0 (0.0)1 (0.1)1 (0.1)0 (0.0)
      Alcohol use576 (79.1)23 (3.2)37 (5.1)35 (4.8)20 (2.7)22 (3.0)15 (2.1)
      Fig. 2
      Fig. 2Prevalence of risk behaviours for hepatitis B for males (A) and females (B).

      3.3 Association of sociodemographic factors and hepatitis B risk behaviour

      A linear regression model examined the relationship between sociodemographic factors and HepB risk behaviours (Table 3). Being male was significantly associated with a number of exposures, including sharing needles, sharing razor blades, sharing toothbrushes, tattoos, unhealthy sex behaviours, prison experience and alcohol use. Being married was significantly associated with two exposures: sharing toothbrushes and sharing nail cutters. Compared to respondents 55 and older, respondents aged 20 and 26 were more likely to share nail cutters, have body piercings and have sex with an unknown person, while respondents aged 27 and 40 were more likely to share razor blades, share toothbrushes, share nail cutters, have tattoos and have body piercings. Respondents aged 41 and 54 had similar exposures to those older, but were also more likely to share nail cutters. Compared to those with a university degree, respondents with a lower educational background had greater risk behaviours of sharing nail cutters and using alcohol.
      Table 3Association between sociodemographic variables and hepatitis B risk behaviours (n = 728).
      VariablesSharing needlesSharing razor bladesSharing toothbrushSharing nail cutterTattoosBody-piercingAcupunctureSex with unknown person>10 sex partnersPrison experienceAlcohol use
      Male0.076***0.100***0.071*0.0180.079***−0.404***0.0570.114***0.070*0.072*0.196***
      Ethnicity
       Chinese0.018−0.535***0.1240.044−0.105−0.051−0.2030.1030.0880.0120.249
       Malay0.022−0.572***0.2070.131−0.330−0.168−0.3990.0730.1130.043−0.280
       Indian0.100−0.454***0.1150.014−0.1130.059−0.3360.0890.0520.044−0.020
       Other (R)
      Married vs. not−0.021−0.0300.098***0.127***0.0310.0520.0410.0090.079*0.0100.047
      Age
       20-26−0.0520.0480.0680.185***0.0550.074**−0.0180.095*0.0520.0060.035
       27-40−0.0240.128***0.148***0.310***0.167***0.133***0.0190.0850.0340.0420.082
       41-54−0.0060.0530.0380.172***0.0860.0520.0810.0910.0730.0610.058
       >55 (R)
      University degree vs. not0.0150.0550.0190.121***0.024−0.015−0.0500.0570.0100.0180.066*
      R21.4%2.7%2.7%6.6%4.9%22.1%4.3%2.1%1.4%0.8%26.7%
      *P < 0.05.
      **P < 0.01.
      ***P < 0.001.

      4. Discussion

      The outcomes in this study were a set of risk behaviours for HepB that were related to household members’ lifestyle. We selected well-known risk behaviours that are most relevant to Malaysia. Needling sharing has long been identified as risk factor
      • Piot P.
      • Goilav C.
      • Kegels E.
      Hepatitis B: transmission by sexual contact and needle sharing.
      ,
      • Palmateer N.E.
      • Hutchinson S.J.
      • Innes H.
      • et al.
      Review and meta-analysis of the association between self-reported sharing of needles/syringes and hepatitis C virus prevalence and incidence among people who inject drugs in Europe.
      ,
      • Mathei C.
      • Shkedy Z.
      • Denis B.
      • et al.
      Evidence for a substantial role of sharing of injecting paraphernalia other than syringes/needles to the spread of hepatitis C among injecting drug users.
      ,
      • Vassilev Z.P.
      • Hagan H.
      • Lyubenova A.
      • 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.
      ,
      • Samuel M.C.
      • Doherty P.M.
      • Bulterys M.
      • Jenison S.A.
      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.
      ,
      • Xu C.J.
      • Zhang C.P.
      • Luo B.F.
      • et al.
      Prevalence and characterization of hepatitis B and C virus infections in a needle-sharing population in Northern China.
      and due to its major role in HBV transmission, Needle Exchange Programs were proposed and adopted in 1983 to prevent HBV transmission in communities.
      • Des Jarlais D.C.
      • Sloboda Z.
      • Friedman S.R.
      • Tempalski B.
      • McKnight C.
      • Braine N.
      Diffusion of the D.A.R.E and syringe exchange programs.
      HBV can survive outside the body for at least 7 days, and, during this period, sharing contaminated razor blades, toothbrushes and nail cutters are significant risk factors in transmitting HBV among household members.
      • Ali M.
      • Idrees M.
      • Ali L.
      • et al.
      Hepatitis B virus in Pakistan: a systematic review of prevalence, risk factors, awareness status and genotypes.
      • Paez Jimenez A.
      • El-Din N.S.
      • El-Hoseiny M.
      • et al.
      Community transmission of hepatitis B virus in Egypt: results from a case-control study in Greater Cairo.
      • Palmateer N.E.
      • Hutchinson S.J.
      • Innes H.
      • et al.
      Review and meta-analysis of the association between self-reported sharing of needles/syringes and hepatitis C virus prevalence and incidence among people who inject drugs in Europe.
      ,
      • Trepo C.
      • Chan H.L.Y.
      • Lok A.
      Hepatitis B virus infection.
      ,
      • Ramadori P.
      • Cubero F.J.
      • Liedtke C.
      • Trautwein C.
      • Nevzorova Y.A.
      Alcohol and hepatocellular carcinoma: adding fuel to the flame.
      • Duraisamy G.
      Blood transfusion in Malaysia.
      • Van Herck K.
      • Vorsters A.
      • Van Damme P.
      Prevention of viral hepatitis (B and C) reassessed.
      • Yang J.
      • Hall K.
      • Nuriddin A.
      • Woolard D.
      Risk for hepatitis B and C virus transmission in nail salons and barbershops and state regulatory requirements to prevent such transmission in the United States.
      Studies also confirm that these tools are reservoirs of HBV DNA
      • Koroglu M.
      • T. D
      • Ozbek A.
      • et al.
      Nail scissors and fingernails as reservoirs of hepatitis B virus DNA: role of nail scissors in household transmission of hepatitis B virus.
      ,
      • Eroglu C.
      • Zivalioglu M.
      • Esen S.
      • Sunbul M.
      • Leblebicioglu H.
      Detection of hepatitis B virus in used razor blades by PCR.
      and they have been reported as a source of HBV transmission in a HepB outbreak.
      • Kay M.
      Hepatitis outbreak is traced to contaminated needles and barber shop razors, study shows.
      A meta-analysis also indicates that tattooing
      • Jafari S.
      • Buxton J.A.
      • Afshar K.
      • Copes R.
      • Baharlou S.
      Tattooing and risk of hepatitis B: a systematic review and meta-analysis.
      and body-piercing
      • Yang S.G.
      • Wang D.
      • Zhang Y.L.
      • et al.
      Transmission of hepatitis B and C virus infection through body piercing a systematic review and meta-analysis.
      are risk factors for HBV transmission, and in the past two decades, it has been asserted that acupuncture is an independent risk factor for HepB infection.
      • Phoon W.O.
      • Fong N.P.
      • Lee J.
      History of blood-transfusion, tattooing, acupuncture and risk of hepatitis-B surface antigenemia among Chinese men in Singapore.
      ,
      • Beasley R.P.
      • Hwang L.Y.
      • Lin C.C.
      • Ko Y.C.
      • Twu S.J.
      Incidence of hepatitis among students at a university in taiwan.
      ,
      • Sulaiman H.A.
      • Sie J.A.
      • Rustam M.
      • Melani W.
      • Corwin A.
      • Jennings G.B.
      Prevalence of hepatitis-B and hepatitis-C viruses in healthy Indonesian blood-donors.
      It is also well-known that HepB could be transmitted through sexual intercourse and therefore unsafe sexual practices are a risk factor for HepB infection. Such practices including sexual activities with multiple partners and with someone with unknown HepB status.
      • Piot P.
      • Goilav C.
      • Kegels E.
      Hepatitis B: transmission by sexual contact and needle sharing.
      ,
      • Atkins M.
      • Nolan M.
      Sexual transmission of hepatitis B.
      ,
      • Gorgos L.
      Sexual transmission of viral hepatitis.
      ,
      • Lichtenhan J.B.
      Sexual activity and recommendations for the hepatitis B vaccine.
      ,
      • Walling A.D.
      Role of semen in the sexual transfer of hepatitis viruses.
      • Everhart J.E.
      • Di Bisceglie A.M.
      • Murray L.M.
      • et al.
      Risk for non-A, non-B (type C) hepatitis through sexual or household contact with chronic carriers.
      • Peterkin M.A.
      • Crawford R.J.
      Hepatitis B: sexual contacts.
      • Lim K.S.
      • Wong V.T.
      • Fulford K.W.
      • Catterall R.D.
      • Briggs M.
      • Dane D.S.
      Role of sexual and non-sexual practices in the transmission of hepatitis B.
      • Fass R.J.
      Sexual transmission of viral hepatitis?.
      Although alcohol consumption is not associated with HBV transmission, it is associated with hepatocellular carcinoma,
      • Ramadori P.
      • Cubero F.J.
      • Liedtke C.
      • Trautwein C.
      • Nevzorova Y.A.
      Alcohol and hepatocellular carcinoma: adding fuel to the flame.
      ,
      • Chuang S.C.
      • Lee Y.C.
      • Wu G.J.
      • Straif K.
      • Hashibe M.
      Alcohol consumption and liver cancer risk: a meta-analysis.
      ,
      • Testino G.
      • Leone S.
      • Borro P.
      Alcohol and hepatocellular carcinoma: a review and a point of view.
      and therefore included in this study.
      The WHO has put forward a goal to eliminate HepB and C by 2030.
      However, due to a high prevalence of HepB chronic carrier status and a vaccination programme that is limited to infants, Malaysia is likely to remain highly endemic for HBV in the near future. A consideration of the distribution of risk behaviours related to HepB infection in the population can better inform efforts to target screening and vaccination programs. In this paper, we examined the sociodemographic, or individual-based, risk factors related to HepB infection. Link and Phelan
      • Link B.G.
      • Phelan J.
      Social conditions as fundamental causes of disease.
      have argued that individual-based risk factors should be given more attention to improve health conditions in general. In this study, we focus on gender, ethnicity, education, and age.
      Previous studies in other countries have also found a relationship between HepB risk behaviours and sociodemographic status. As early as 1990, Koblin et al.
      • Koblin B.A.
      • McCusker J.
      • Lewis B.F.
      • Sullivan J.L.
      Racial/ethnic differences in HIV-1 seroprevalence and risky behaviors among intravenous drug users in a multisite study.
      found that HB risk behaviour depended on ethnicity. In more recent years, a study indicated that males are more likely to be exposed to certain risk behaviours, such as multiple sexual partners and alcohol consumption.
      • Nanbur S.
      • Ajayi A.
      • Andy E.
      • et al.
      Prevalence of hepatitis B surface antiginaemia and risk behaviour among youths in kwanpe community of Lantang north, plateau state, nigeri.
      In other studies, sharing various household items,
      • Goh K.T.
      • Ding J.L.
      • Monteiro E.H.
      • Oon C.J.
      Hepatitis-B infection in households of acute cases.
      having tattoos,
      • Limentani A.E.
      • Elliott L.M.
      • Noah N.D.
      • Lamborn J.K.
      An outbreak of hepatitis B from tattooing.
      and having unsafe sexual intercourse were more likely in males,
      • Szmuness W.
      On the role of sexual behaviour in the spread of hepatitis B infection.
      and all these behaviours increased the risk of HBV infection. Martinson et al.’s study
      • Martinson F.E.A.
      • Weigle K.A.
      • Royce R.A.
      • Weber D.J.
      • Suchindran C.M.
      • Lemon S.M.
      Risk factors for horizontal transmission of hepatitis B virus in a rural district in Ghana.
      found that the distribution of risk behaviours varied across ages. Of course, the transmission patterns of HBV within a community vary widely between countries, which can influence the demographic distribution of risk behaviours. In the United States, HBV (along with other blood-borne infections like HIV and hepatitis C virus) is often transmitted through injection drug use, and injection drug use is more common among younger ages.
      • Murrill C.S.
      • Weeks H.
      • Castrucci B.C.
      • et al.
      Age-specific seroprevalence of HIV, hepatitis B virus, and hepatitis C virus infection among injection drug users admitted to drug treatment in 6 US cities.
      Our study reveals that the most common risk behaviours related to HepB were sharing nail cutters, having body piercings, using alcohol, and undergoing acupuncture. The risk behaviours examined in this study were based on theoretical concerns and have been investigated in previous epidemiological studies. One study reported that sharing various household items increased the risk of HBV infection.
      • Goh K.T.
      • Ding J.L.
      • Monteiro E.H.
      • Oon C.J.
      Hepatitis-B infection in households of acute cases.
      More specifically, a study conducted in Northern Brazil showed HBV transmission via a nail clipper.
      • Oliveira M.D.D.
      • Matos M.A.
      • Martins R.M.B.
      • Teles S.A.
      Tattooing and body piercing as lifestyle indicator of risk behaviors in Brazilian adolescents.
      However, another study conducted in Egypt found no evidence of sharing nail cutters being a substantial means of HBV transmission.
      • Jimenez A.P.
      • El-Din N.S.
      • El-Hoseiny M.
      • et al.
      Community transmission of hepatitis B virus in Egypt: results from a case-control study in Greater Cairo.
      Body piercing, a relatively common risk behaviour, especially among women in this study, has also been linked to HBV infection. In Bangkok, young children with ear piercings had a higher chance of HBV infection.
      • Luksamijarulkul P.
      • Maneesri P.
      • Kittigul L.
      Hepatitis B sero-prevalence and risk factors among school-age children in a low socioeconomic community, Bangkok.
      And a study in Brazilian adolescents found that body piercing was a source of HBV transmission.
      • Oliveira M.D.D.
      • Matos M.A.
      • Martins R.M.B.
      • Teles S.A.
      Tattooing and body piercing as lifestyle indicator of risk behaviors in Brazilian adolescents.
      Males and individuals of low educational attainment had greater occurrence of alcohol use in our study. The relationship between education and HBV infection is theoretically mediated by lower income and a less healthy lifestyle.
      • Gheorghe L.
      • Csiki I.E.
      • Iacob S.
      • Gheorghe C.
      • Smira G.
      • Regep L.
      The prevalence and risk factors of hepatitis C virus infection in adult population in Romania: a nationwide survey 2006-2008.
      One study in Egypt did find that individuals with greater levels of alcohol consumption had a higher incidence of acute HepB.
      • Jimenez A.P.
      • El-Din N.S.
      • El-Hoseiny M.
      • et al.
      Community transmission of hepatitis B virus in Egypt: results from a case-control study in Greater Cairo.
      Altogether, our findings indicate that risk behaviours of HepB are relatively high among Malaysians, and especially certain groups – particularly males, younger and middle-aged adults, and those with a lower education level (i.e., who did not have a university degree). To reduce risk behaviours among these groups, specific programmes such as forums, seminars and continuous education programs on preventive measures are needed. These prevention measures could be conducted by the authorities such as the Ministry of Women, Family and Community. The groups with the most risk behaviours were of reproductive age. Therefore, HepB prevention measures including HBV screening would reduce the rate of maternal transmission of HBV to newborns. Expanded screening and vaccination programmes in government hospitals should be dedicated to these risk groups. Hepatitis B vaccination to postnatal mothers with negative HBV immunity should be emphasized while their spouses and family members should be screened for HepB status if they are HBsAg reactive during antenatal screening. Further preventive actions can be incorporated into educational messaging to these groups such as avoidance of common risk factors and how to prevent transmission to others if they are chronic carriers of HBV.
      Adults aged 27 to 40 had greater exposure to HepB risk behaviours and thus could be specific targets for health programming. They are in the working age group and are often the primary generators for their family's income. Early illness and death associated with HepB in this group would severely impact national economic growth. Since many in this group have the purchasing power to buy the vaccine, awareness programmes can familiarize young and middle-aged adults with HepB screening and vaccination. For example, health campaigns could be implemented on World Hepatitis Day or as part of Corporate Social Responsibility programs.
      This study had several strengths and limitations. Risk behaviours were based on self-report and could be underreported due to participants forgetting or not wanting to express undesirable behaviours. We chose these risk behaviours based off of previous scientific literature, but this study did not directly assess actual exposure to HBV, and so we did not measure the contribution of each risk factor to HepB disease burden within the country. This study is a part of the Malaysian Hepatitis B Project in which other aspects of HepB were also assessed such as acceptance and WTP for HepB vaccine.
      • Rajamoorthy Y.
      • Radam A.
      • Taib N.
      • et al.
      Willingness to Pay for Self-Paid Hepatitis B Vaccination in Selangor.
      Therefore, the participant was provided with a brochure from the Ministry of Health Malaysia before the interview because not all of the population were well informed about the disease. It contained symptoms of HepB, information on the transmission and prevention methods of HBV, and photographs. This intervention might influence participants’ responses related to risk behaviours. A strength of this study is that we attempted a random selection from the population and, therefore, have high confidence in the ability of our results to generalize to the population of Selangor. Nonetheless, the population may differ significantly from others in Malaysia and in other countries of the world.

      5. Conclusions

      Our study reveals that the most common risk behaviours related to HepB were sharing nail cutters, having body piercings, using alcohol, and undergoing acupuncture. Being male, married, aged 27–40 years and not having a university degree were all significantly related to greater exposure to a range of HepB risk behaviours. These groups can represent targets for future governmental prevention programs, for example HepB screening or vaccination programs. As Malaysia seeks to control HepB, or eliminate it following a goal from the World Health Organisation to do so by 2030, it will need to develop cost-effective solutions to the large number of HBV carriers in the adult population.

      Conflicts of interest

      The authors declare that they have no competing interests.

      Acknowledgement

      This study was funded by the Putra Grant - Putra Graduate Initiative (IPS) , grant number GP-IPS/2013-939220 . ALW's salary was funded through a fellowship from the PhRMA Foundation .

      Appendix A. Supplementary data

      The following is the Supplementary data to this article:

      References

      1. WHO: Hepatitis B. Available from: http://wwwwhoint/mediacentre/factsheets/fs204/en/(Accessed: 8 Feb 2018).

        • WHO
        Hepatitis B vaccines.
        Wkly Epidemiol Rec. 2009; 84: 405-420
        • Alter M.J.
        • Hadler S.C.
        • Margolis H.S.
        • et al.
        The changing epidemiology of hepatitis-B in the united-states - need for alternative vaccination strategies.
        JAMA, J Am Med Assoc. 1990; 263: 1218-1222
        • Piot P.
        • Goilav C.
        • Kegels E.
        Hepatitis B: transmission by sexual contact and needle sharing.
        Vaccine. 1990; 8 (discussion S41-33): S37-S40
        • Ali M.
        • Idrees M.
        • Ali L.
        • et al.
        Hepatitis B virus in Pakistan: a systematic review of prevalence, risk factors, awareness status and genotypes.
        Virol J. 2011; 8: 102
        • Paez Jimenez A.
        • El-Din N.S.
        • El-Hoseiny M.
        • et al.
        Community transmission of hepatitis B virus in Egypt: results from a case-control study in Greater Cairo.
        Int J Epidemiol. 2009; 38: 757-765
        • Palmateer N.E.
        • Hutchinson S.J.
        • Innes H.
        • et al.
        Review and meta-analysis of the association between self-reported sharing of needles/syringes and hepatitis C virus prevalence and incidence among people who inject drugs in Europe.
        Int J Drug Policy. 2013; 24: 85-100
        • Kay M.
        Hepatitis outbreak is traced to contaminated needles and barber shop razors, study shows.
        Br Med J. 2012; 345
        • Phoon W.O.
        • Fong N.P.
        • Lee J.
        History of blood-transfusion, tattooing, acupuncture and risk of hepatitis-B surface antigenemia among Chinese men in Singapore.
        Am J Public Health. 1988; 78: 958-960
        • Mathei C.
        • Shkedy Z.
        • Denis B.
        • et al.
        Evidence for a substantial role of sharing of injecting paraphernalia other than syringes/needles to the spread of hepatitis C among injecting drug users.
        J Viral Hepat. 2006; 13: 560-570
        • Vassilev Z.P.
        • Hagan H.
        • Lyubenova A.
        • 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: 621-626
        • Atkins M.
        • Nolan M.
        Sexual transmission of hepatitis B.
        Curr Opin Infect Dis. 2005; 18: 67-72
        • Rajamoorthy Y.
        • Radam A.
        • Taib N.
        • et al.
        Willingness to Pay for Self-Paid Hepatitis B Vaccination in Selangor.
        (Malaysia)2018 ([Submitted to Vaccine] 2018)
        • Hagan H.
        • Pouget E.R.
        • Des Jarlais D.C.
        A systematic review and meta-analysis of interventions to prevent hepatitis C virus infection in people who inject drugs.
        J Infect Dis. 2011; 204: 74-83
        • Samuel M.C.
        • Doherty P.M.
        • Bulterys M.
        • Jenison S.A.
        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: 475-484
        • Shapatava E.
        • Nelson K.E.
        • 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: S35-S38
        • Hagan H.
        • Jarlais D.C.D.
        • Friedman S.R.
        • Purchase D.
        • Alter M.J.
        Reduced risk of hepatitis-B and hepatitis-C among injection-drug users in the tacoma syringe exchange program.
        Am J Public Health. 1995; 85: 1531-1537
        • Koester S.
        • Glanz J.
        • Baron A.
        Drug sharing among heroin networks: implications for HIV and hepatitis B and C prevention.
        AIDS Behav. 2005; 9: 27-39
        • 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: 1114-1120
        • Xu C.J.
        • Zhang C.P.
        • Luo B.F.
        • et al.
        Prevalence and characterization of hepatitis B and C virus infections in a needle-sharing population in Northern China.
        BMC Public Health. 2015; 15: 460
        • Talaat M.
        • Kandeel A.
        • El-Shoubary W.
        • et al.
        Occupational exposure to needlestick injuries and hepatitis B vaccination coverage among health care workers in Egypt.
        Am J Infect Contr. 2003; 31: 469-474
        • Pruss-Ustun A.
        • Rapiti E.
        • Hutin Y.
        Estimation of the global burden of disease attributable to contaminated sharps injuries among health-care workers.
        Am J Ind Med. 2005; 48: 482-490
        • Gorgos L.
        Sexual transmission of viral hepatitis.
        Infect Dis Clin N Am. 2013; 27: 811-836
        • Beasley R.P.
        • Hwang L.Y.
        • Lin C.C.
        • Ko Y.C.
        • Twu S.J.
        Incidence of hepatitis among students at a university in taiwan.
        Am J Epidemiol. 1983; 117: 213-222
        • Trepo C.
        • Chan H.L.Y.
        • Lok A.
        Hepatitis B virus infection.
        Lancet. 2014; 384: 2053-2063
        • Ozer A.
        • Yakupogullari Y.
        • Beytur A.
        • et al.
        Risk factors of hepatitis B virus infection in Turkey: a population-based, case-control study.
        Hepat Mon. 2011; 11: 263-268
        • Goldstein S.T.
        • Alter M.J.
        • Williams I.T.
        • et al.
        Incidence and risk factors for acute hepatitis B in the United States, 1982-1998: implications for vaccination programs.
        J Infect Dis. 2002; 185: 713-719
        • Pereira L.M.M.B.
        • Martelli C.M.T.
        • Merchan-Hamann E.
        • et al.
        Population-based multicentric survey of hepatitis B infection and risk factor differences among three regions in Brazil.
        Am J Trop Med Hyg. 2009; 81: 240-247
        • Des Jarlais D.C.
        • Sloboda Z.
        • Friedman S.R.
        • Tempalski B.
        • McKnight C.
        • Braine N.
        Diffusion of the D.A.R.E and syringe exchange programs.
        Am J Public Health. 2006; 96: 1354-1358
        • Lichtenhan J.B.
        Sexual activity and recommendations for the hepatitis B vaccine.
        Am Fam Physician. 1995; 52: 1277-1278
        • Ramadori P.
        • Cubero F.J.
        • Liedtke C.
        • Trautwein C.
        • Nevzorova Y.A.
        Alcohol and hepatocellular carcinoma: adding fuel to the flame.
        Cancers. 2017; 9
        • Duraisamy G.
        Blood transfusion in Malaysia.
        Jpn J Blood Transfus. 1994; 40: 776-778
        • Van Herck K.
        • Vorsters A.
        • Van Damme P.
        Prevention of viral hepatitis (B and C) reassessed.
        Best Pract Res Clin Gastroenterol. 2008; 22: 1009-1029
        • Yang J.
        • Hall K.
        • Nuriddin A.
        • Woolard D.
        Risk for hepatitis B and C virus transmission in nail salons and barbershops and state regulatory requirements to prevent such transmission in the United States.
        J Public Health Manag Pract. 2014; 20: E20-E30
        • Maynard J.E.
        Hepatitis B: global importance and need for control.
        Vaccine. 1990; 8 (discussion S21-13): S18-S20
        • Romano L.
        • Paladini S.
        • Van Damme P.
        • Zanetti A.R.
        The worldwide impact of vaccination on the control and protection of viral hepatitis B.
        Dig Liver Dis. 2011; 43: S2-S7
        • Sung J.L.
        Hepatitis-B virus eradication strategy for Asia.
        Vaccine. 1990; 8: S95-S99
        • Qua C.S.
        • Goh K.L.
        Liver cirrhosis in Malaysia: peculiar epidemiology in a multiracial Asian country.
        J Gastroenterol Hepatol. 2011; 26: 1333-1337
        • Sulaiman H.A.
        • Sie J.A.
        • Rustam M.
        • Melani W.
        • Corwin A.
        • Jennings G.B.
        Prevalence of hepatitis-B and hepatitis-C viruses in healthy Indonesian blood-donors.
        Trans R Soc Trop Med Hyg. 1995; 89: 167-170
        • Jafari S.
        • Buxton J.A.
        • Afshar K.
        • Copes R.
        • Baharlou S.
        Tattooing and risk of hepatitis B: a systematic review and meta-analysis.
        Can J Public Health. 2012; 103: 207-212
        • Khairullah N.S.
        • Merican D.I.
        Hepatitis disease management programs in Malaysia.
        J Gastroenterol Hepatol. 2004; 19: S13-S16
        • Gogos C.A.
        • Fouka K.P.
        • Nikiforidis G.
        • et al.
        Prevalence of hepatitis B and C virus infection in the general population and selected groups in South-Western Greece.
        Eur J Epidemiol. 2003; 18: 551-557
        • Lee D.H.
        • Kim J.H.
        • Nam J.J.
        • Kim H.R.
        • Shin H.R.
        Epidemiological findings of hepatitis B infection based on 1998 national health and nutrition survey in korea.
        J Korean Med Sci. 2002; 17: 457-462
        • Liang X.F.
        • Bi S.L.
        • Yang W.Z.
        • et al.
        Reprint of: epidemiological serosurvey of Hepatitis B in China-Declining HBV prevalence due to Hepatitis B vaccination.
        Vaccine. 2013; 31: J21-J28
        • Rajamoorthy Y.
        • Radam A.
        • Taib N.
        • et al.
        Willingness to pay for self-paid hepatitis B vaccination in Selangor, Malaysia.
        PLoS One. 2019; 14e0215125
        • Rajamoorthy Y.
        • Taib N.M.
        • Munusamy S.
        • et al.
        Knowledge and awareness of hepatitis B among households in Malaysia: a community-based cross-sectional survey.
        BMC Public Health. 2019; 19: 47
        • Rajamoorthy Y.
        • Radam A.
        • Taib N.M.
        • et al.
        The relationship between perceptions and self-paid hepatitis B vaccination: a structural equation modeling approach.
        PLoS One. 2018; 13e0208402
        • DSM
        Population Distribution and Basic Demographic Characteristics Report 2010.
        Department of Statistic Malaysia, Kuala Lumpur, Malaysia2011
        • Prince R.
        Using surveys to value public-goods - the contingent valuation method.
        Nat Resour J. 1989; 29: 900-902
        • Harapan H.
        • Mudatsir M.
        • Yufika A.
        • et al.
        Community acceptance and willingness-to-pay for a hypothetical Zika vaccine: a cross-sectional study in Indonesia.
        Vaccine. 2019; 37: 1398-1406
        • Harapan H.
        • Rajamoorthy Y.
        • Anwar S.
        • et al.
        Knowledge, attitude, and practice regarding dengue virus infection among inhabitants of Aceh, Indonesia: a cross-sectional study.
        BMC Infect Dis. 2018; 18: 96
        • Gheorghe L.
        • Csiki I.E.
        • Iacob S.
        • Gheorghe C.
        • Smira G.
        • Regep L.
        The prevalence and risk factors of hepatitis C virus infection in adult population in Romania: a nationwide survey 2006-2008.
        J Gastrointest Liver. 2010; 19: 373-379
        • Koroglu M.
        • T. D
        • Ozbek A.
        • et al.
        Nail scissors and fingernails as reservoirs of hepatitis B virus DNA: role of nail scissors in household transmission of hepatitis B virus.
        Am J Infect Contr. 2018; 46: 793-797
        • Eroglu C.
        • Zivalioglu M.
        • Esen S.
        • Sunbul M.
        • Leblebicioglu H.
        Detection of hepatitis B virus in used razor blades by PCR.
        Hepat Mon. 2010; 10: 22-25
        • Yang S.G.
        • Wang D.
        • Zhang Y.L.
        • et al.
        Transmission of hepatitis B and C virus infection through body piercing a systematic review and meta-analysis.
        Medicine. 2015; 94
        • Walling A.D.
        Role of semen in the sexual transfer of hepatitis viruses.
        Am Fam Physician. 1998; 58: 509
        • Everhart J.E.
        • Di Bisceglie A.M.
        • Murray L.M.
        • et al.
        Risk for non-A, non-B (type C) hepatitis through sexual or household contact with chronic carriers.
        Ann Intern Med. 1990; 112: 544-545
        • Peterkin M.A.
        • Crawford R.J.
        Hepatitis B: sexual contacts.
        Arch Intern Med. 1985; 145: 761-762
        • Lim K.S.
        • Wong V.T.
        • Fulford K.W.
        • Catterall R.D.
        • Briggs M.
        • Dane D.S.
        Role of sexual and non-sexual practices in the transmission of hepatitis B.
        Br J Vener Dis. 1977; 53: 190-192
        • Fass R.J.
        Sexual transmission of viral hepatitis?.
        J Am Med Assoc. 1974; 230: 861-862
        • Chuang S.C.
        • Lee Y.C.
        • Wu G.J.
        • Straif K.
        • Hashibe M.
        Alcohol consumption and liver cancer risk: a meta-analysis.
        Cancer Causes Control. 2015; 26: 1205-1231
        • Testino G.
        • Leone S.
        • Borro P.
        Alcohol and hepatocellular carcinoma: a review and a point of view.
        World J Gastroenterol. 2014; 20: 15943-15954
      2. WHO: Combatting Hepatitis B and C to Reach Elimination by 2030. WHO Press, Geneva, Switzerland2016
        • Link B.G.
        • Phelan J.
        Social conditions as fundamental causes of disease.
        J Health Soc Behav. 1995; 35: 80-94
        • Koblin B.A.
        • McCusker J.
        • Lewis B.F.
        • Sullivan J.L.
        Racial/ethnic differences in HIV-1 seroprevalence and risky behaviors among intravenous drug users in a multisite study.
        Am J Epidemiol. 1990; 132: 837-846
        • Nanbur S.
        • Ajayi A.
        • Andy E.
        • et al.
        Prevalence of hepatitis B surface antiginaemia and risk behaviour among youths in kwanpe community of Lantang north, plateau state, nigeri.
        Int J Public Health Res. 2015; 3: 239-242
        • Goh K.T.
        • Ding J.L.
        • Monteiro E.H.
        • Oon C.J.
        Hepatitis-B infection in households of acute cases.
        J Epidemiol Community Health. 1985; 39: 123-128
        • Limentani A.E.
        • Elliott L.M.
        • Noah N.D.
        • Lamborn J.K.
        An outbreak of hepatitis B from tattooing.
        Lancet. 1979; 2: 86-88
        • Szmuness W.
        On the role of sexual behaviour in the spread of hepatitis B infection.
        Ann Intern Med. 1975; 83: 489-495
        • Martinson F.E.A.
        • Weigle K.A.
        • Royce R.A.
        • Weber D.J.
        • Suchindran C.M.
        • Lemon S.M.
        Risk factors for horizontal transmission of hepatitis B virus in a rural district in Ghana.
        Am J Epidemiol. 1998; 147: 478-487
        • Murrill C.S.
        • Weeks H.
        • Castrucci B.C.
        • et al.
        Age-specific seroprevalence of HIV, hepatitis B virus, and hepatitis C virus infection among injection drug users admitted to drug treatment in 6 US cities.
        Am J Public Health. 2002; 92: 385-387
        • Oliveira M.D.D.
        • Matos M.A.
        • Martins R.M.B.
        • Teles S.A.
        Tattooing and body piercing as lifestyle indicator of risk behaviors in Brazilian adolescents.
        Eur J Epidemiol. 2006; 21: 559-560
        • Jimenez A.P.
        • El-Din N.S.
        • El-Hoseiny M.
        • et al.
        Community transmission of hepatitis B virus in Egypt: results from a case-control study in Greater Cairo.
        Int J Epidemiol. 2009; 38: 757-765
        • Luksamijarulkul P.
        • Maneesri P.
        • Kittigul L.
        Hepatitis B sero-prevalence and risk factors among school-age children in a low socioeconomic community, Bangkok.
        Asia Pac J Public Health. 1995; 8: 158-161