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A Systematic Review of Risk Factors for Hepatitis C Virus Infection Among Low-Risk Population in India

      Background

      Identification of risk factors for hepatitis C virus (HCV) transmission will help in targeted screening of people who are at risk for HCV.

      Method

      Indian studies, published between January 1989 and June 2020, were systematically reviewed to identify the relevant studies. We searched electronic databases including PubMed/Medline, Embase, Scopus, and Google scholar to identify the original data published in English language. The full-text studies, published in any form, which reported data on risk factors for HCV transmission among low-risk population were selected. The studies which exclusively included high-risk groups were excluded.

      Results

      Data were extracted from 31,176 participants included in 25 studies (median [range] 40 [7–20,113). The participants were HCV infected patients who visited the hospital (n = 10), community population (n = 6), pregnant women (n = 5), blood donors (n = 2), people with diabetes mellitus (n = 1), army recruits (n = 1), or slum dwellers (n = 1). These studies provided data on blood transfusion, use of unsafe injections, minor or major surgery, unsafe dental procedures, tattooing, body piercing, obstetrical procedures, unsafe shaving, intravenous drug use, and unsafe sexual practices as risk factors for HCV transmission.

      Conclusion

      Unsafe injections, body piercing, unsafe dental procedure, unsafe shaving, and tattooing were identified as major risk factors for reported by HCV population participants.More data are needed to identify the risk factors for HCV in Indian population. Risk-factor-targeted screening may increase the yield and reduce the cost of HCV screening in India.

      Keywords

      Abbreviations:

      DAA (Direct-acting antivirals), HCV (Hepatitis C virus), MHD (Maintenance hemodialysis), NVHCP (National viral hepatitis control program), PLHIV (People living with HIV), PWID (People who inject drugs), WHO (World Health Organization)
      Hepatitis C virus (HCV) infection is a treatable cause for chronic hepatitis, cirrhosis and hepatocellular carcinoma. Globally, ∼1% population is infected with HCV, more than 71 million need anti-HCV treatment,
      Polaris Observatory
      Global prevalence and genotype distribution of hepatitis C virus infection in 2015: a modelling study.
      and more than 399,000 die every year due to HCV-related complication.
      India along with China, Pakistan, Nigeria, Egypt, and Russia account for more than half of total HCV infections in the world.
      • Gower E.
      • Estes C.
      • Blach S.
      • Razavi-Shearer K.
      • Razavi H.
      Global epidemiology and genotype distribution of the hepatitis C virus infection.
      In India, weighted anti-HCV seroprevalence in low-risk population is close to 0.49%, and the burden is estimated at ∼5 million.
      • Goel A.
      • Seguy N.
      • Aggarwal R.
      Burden of hepatitis C virus infection in India: a systematic review and meta-analysis.
      ,
      • Goel A.
      • Rewari B.B.
      • Sharma M.
      • Konath N.M.
      • Aggarwal R.
      Seroprevalence and burden of hepatitis C virus infection in WHO South-East Asia Region: a systematic review.
      The direct-acting antiviral (DAA) agents has made a paradigm change in HCV treatment.
      • Muir A.J.
      The rapid evolution of treatment strategies for hepatitis C.
      High safety profile, high (∼95%) cure rate, ease of administration, widespread availability, cost-effectiveness of HCV treatment,
      • Aggarwal R.
      • Chen Q.
      • Goel A.
      • et al.
      Cost-effectiveness of hepatitis C treatment using generic direct-acting antivirals available in India.
      ,
      • Goel A.
      • Chen Q.
      • Chhatwal J.
      • Aggarwal R.
      Cost-effectiveness of generic pan-genotypic sofosbuvir/velpatasvir versus genotype-dependent direct-acting antivirals for hepatitis C treatment.
      and affordable price of DAAs has led the World Health Organization (WHO) to set the goal to eliminate viral hepatitis by 2030.
      WHO
      Combating Hepatitis B and C to Reach Elimination by 2030.
      The Government of India has recently launched National Viral Hepatitis Control Program (NVHCP).
      HCV is transmitted through parenteral routes following exposure to contaminated blood/blood products, unsafe needles, unprotected sex, and in utero transmission from mother to child. Specific groups of people, such as those living with HIV (PLHIV), patients on maintenance hemodialysis (MHD), and people who inject drugs (PWID), are known to be at high risk for acquiring HCV infection.
      Larger proportion (∼88%) of total HCV burden in India are hidden in low-risk general population.
      • Goel A.
      • Rewari B.B.
      • Sharma M.
      • Konath N.M.
      • Aggarwal R.
      Seroprevalence and burden of hepatitis C virus infection in WHO South-East Asia Region: a systematic review.
      The benefit of NVHCP can only be maximized by identification of HCV infection in low-risk population at a preclinical stage. Beyond the universally accepted risk factors for HCV, there could be additional risk factors which might be prevailing in low-risk population. International studies have identified certain unique risk factors in low-risk population, and their identification has shown to improve the yield of HCV screening.
      • Mallette C.
      • Flynn M.A.
      • Promrat K.
      Outcome of screening for hepatitis C virus infection based on risk factors.
      ,
      • McGinn T.
      • O'Connor-Moore N.
      • Alfandre D.
      • Gardenier D.
      • Wisnivesky J.
      Validation of a hepatitis C screening tool in primary care.
      The cost of universal screening of low-risk population for HCV can be substantially reduced if we could also identify the risk factors for HCV infection among low-risk population in India.
      We report the results of our systematic review conducted to identify the risk factors for HCV infection in low-risk population in India.

      Methods

      Electronic databases including PubMed/Medline, Embase, Scopus, and Google scholar were searched to identify the original data published between January 1989 and June 2020. Detailed search strategy is given as Supplementary file 1. Our search strategy included the various terms used for HCV, name of states, and major cities of the country. Cross-references from the published articles were manullay searched to identify the additional studies, if any.

      Inclusion and Exclusion Criteria

      We included Indian studies which reported original data on risk factors for HCV transmission among low-risk population, and were published as full-texts in any form such as original article, brief communication, and brief reports. Studies published as abstracts were excluded. We also excluded the studies that exclusively included the participants who are traditionally considered to be at high risk for acquiring HCV such as PLHIV, PWID, men having sex with men, people on MHD, thalassemic or hemophiliac, or high-risk sexual behavior.

      Data Extraction

      The literature search was performed by AG. Two independent reviewer groups (SP, BB, and AA; and AE and HG) screened the title/abstract to identify the relevant citations. Full-text articles were obtained for the relevant studies satisfying the inclusion criteria. The data were extracted independently by the two groups. Any disagreement between the authors was resolved after discussion with S and AG. Data were extracted from selected studies in a predesigned data extraction form.

      Results

      Data were extracted from 25 selected studies,
      • Khuroo M.S.
      • Dar M.Y.
      • Zargar S.A.
      • Khan B.A.
      • Boda M.I.
      • Yattoo G.N.
      Hepatitis C virus antibodies in acute and chronic liver disease in India.
      • Sood A.
      • Midha V.
      • Sood N.
      • Awasthi G.
      Prevalence of anti-HCV antibodies among family contacts of hepatitis C virus-infected patients.
      • Chowdhury A.
      • Santra A.
      • Chaudhuri S.
      • et al.
      Hepatitis C virus infection in the general population: a community-based study in West Bengal, India.
      • Marx M.A.
      • Murugavel K.G.
      • Tarwater P.M.
      • et al.
      Association of hepatitis C virus infection with sexual exposure in southern India.
      • Thakral B.
      • Marwaha N.
      • Chawla Y.K.
      • et al.
      Prevalence & significance of hepatitis C virus (HCV) seropositivity in blood donors.
      • Kumar A.
      • Sharma K.A.
      • Gupta R.K.
      • Kar P.
      • Chakravarti A.
      Prevalence & risk factors for hepatitis C virus among pregnant women.
      • Sharma R.
      • Sinha P.
      • Bachiwal R.
      • Rishi S.
      Seroprevalence of anti-hepatitis C virus antibody in a hospital-based population of Jaipur, Rajasthan.
      • Parthiban R.
      • Shanmugam S.
      • Velu V.
      • et al.
      Transmission of hepatitis C virus infection from asymptomatic mother to child in southern India.
      • Gill P.K.
      • Devi P.
      • Arora S.
      Seroprevalence of hepatitis B, hepatitis C, and human immunodeficiency viruses in asymptomatic pregnant women.
      • Singh M.
      • Kotwal A.
      • Gupta R.M.
      • Adhya S.
      • Chatterjee K.
      • Jayaram J.
      Sero-epidemiological and behavioural survey of HIV, HBV and HCV amongst Indian armed forces trainees.
      • Medhi S.
      • Goswami B.
      • Das A.K.
      • et al.
      New insights into hepatitis C virus infection in the tribal-dominant part of Northeast India.
      • Sood A.
      • Midha V.
      • Bansal M.
      • Sood N.
      • Puri S.
      • Thara A.
      Perinatal transmission of hepatitis C virus in northern India.
      • Sood A.
      • Sarin S.K.
      • Midha V.
      • et al.
      Prevalence of hepatitis C virus in a selected geographical area of northern India: a population based survey.
      • Goyal L.D.
      • Kaur S.
      • Jindal N.
      • Kaur H.
      HCV and pregnancy: prevalence, risk factors, and pregnancy outcome in north Indian population: a case-control study.
      • Sharma A.
      • Kaur S.
      Seropostivity of hepatitis C infection among voluntary and replacement blood donors in a tertiary care hospital in Punjab.
      • Vasudevan S.
      • Kavimandan A.
      • Kalra N.
      • et al.
      Demographic profile, host, disease & viral predictive factors of response in patients with chronic hepatitis C virus infection at a tertiary care hospital in north India.
      • Khatoon R.
      • Jahan N.
      Assessment of seroprevalence of hepatitis C virus-specific antibodies among patients attending hospital of semi-urban North India using rapid qualitative in vitro diagnostic test.
      • Grewal U.S.
      • Walia G.
      • Bakshi R.
      • Chopra S.
      Hepatitis B and C viruses, their coinfection and correlations in chronic liver disease patients: a tertiary care hospital study.
      • Gupta S.
      • Sodhi S.P.S.
      • Brar G.K.
      • Bansal R.N.
      Risk factors for hepatitis C: a clinical study.
      • Mahajan R.
      • Midha V.
      • Goyal O.
      • et al.
      Clinical profile of hepatitis C virus infection in a developing country: India.
      • Ramya E.
      • Daniel J.C.
      • Ramalakshmi S.
      • Usha R.
      Prevalence and risk factors of hepatitis C virus in irula tribal community, Tamilnadu, India.
      • Dhiman R.K.
      • Grover G.S.
      • Premkumar M.
      • et al.
      Decentralized care with generic direct-acting antivirals in the management of chronic hepatitis C in a public health care setting.
      • Juttada U.
      • Smina T.P.
      • Kumpatla S.
      • Viswanathan V.
      Seroprevalence and risk factors associated with HBV and HCV infection among subjects with type 2 diabetes from South India.
      • Kar S.K.
      • Sabat J.
      • Ho L.M.
      • Arora R.
      • Dwibedi B.
      High prevalence of hepatitis C virus infection in primitive tribes of eastern India and associated sociobehavioral risks for transmission: a retrospective analysis.
      • Sood A.K.
      • Manrai M.
      • Thareja S.
      • Shukla R.
      • Patel A.
      Epidemiology of hepatitis C virus infection in a tertiary care hospital.
      which provided information from a total of 31,176 participants (Figure 1). Characteristics of the studies included in analysis are summarized in Table 1. The participants, included in selected studies, were either known HCV-positive patients (n = 10), community population (n = 6), pregnant women (n = 5), or few other small groups. Only 2 studies had representation of multiple states, 10 studies were from the state of Punjab, remaining 13 studies were from nine states. Of the 37 states/union territories (UTs) in India, only 10 states/UTs were represented in data. The median number of study participant in each study was 40, with minimum being seven and maximum being 20,113.
      Figure 1
      Figure 1The PRISMA flow diagram for literature search and study selection.
      Table 1Characteristics of the Studies Selected for Analysis.
      NoAuthor, yearState in which study was conductedStudy settingStudy participants (n)Risk factors studied
      1Khuroo, 1993
      • Khuroo M.S.
      • Dar M.Y.
      • Zargar S.A.
      • Khan B.A.
      • Boda M.I.
      • Yattoo G.N.
      Hepatitis C virus antibodies in acute and chronic liver disease in India.
      KashmirHospital basedHCV positive patients (n = 7)Unsafe or multiple injections, blood transfusion
      2Sood, 2002
      • Sood A.
      • Midha V.
      • Sood N.
      • Awasthi G.
      Prevalence of anti-HCV antibodies among family contacts of hepatitis C virus-infected patients.
      PunjabHospital basedHCV positive patients (n = 20)Unsafe or multiple injections, blood transfusion, major surgery, body piercing
      3Chowdhury, 2003
      • Chowdhury A.
      • Santra A.
      • Chaudhuri S.
      • et al.
      Hepatitis C virus infection in the general population: a community-based study in West Bengal, India.
      West BengalCommunityCommunity population (n = 26)Unsafe or multiple injections, dental procedure, tattooing, unsafe shaving
      4Marx, 2003
      • Marx M.A.
      • Murugavel K.G.
      • Tarwater P.M.
      • et al.
      Association of hepatitis C virus infection with sexual exposure in southern India.
      Tamil NaduCommunitySlum dwellers (n = 39)Minor surgery, tattooing
      5Thakral, 2006
      • Thakral B.
      • Marwaha N.
      • Chawla Y.K.
      • et al.
      Prevalence & significance of hepatitis C virus (HCV) seropositivity in blood donors.
      ChandigarhHospital basedBlood donors (n = 31)Unsafe or multiple injection, major surgery, unsafe shaving, unsafe sex, intravenous drug use
      6Kumar, 2007
      • Kumar A.
      • Sharma K.A.
      • Gupta R.K.
      • Kar P.
      • Chakravarti A.
      Prevalence & risk factors for hepatitis C virus among pregnant women.
      New DelhiHospital basedPregnant women (n = 84)Blood transfusion, major surgery, body piercing, obstetrical procedure
      7Sharma, 2007
      • Sharma R.
      • Sinha P.
      • Bachiwal R.
      • Rishi S.
      Seroprevalence of anti-hepatitis C virus antibody in a hospital-based population of Jaipur, Rajasthan.
      RajasthanHospital basedHCV positive patients (n = 72)Blood transfusion
      8Parthiban, 2009
      • Parthiban R.
      • Shanmugam S.
      • Velu V.
      • et al.
      Transmission of hepatitis C virus infection from asymptomatic mother to child in southern India.
      Tamil NaduHospital basedPregnant women (n = 18)Blood transfusion, unsafe injection or multiple injection
      9Gill, 2010
      • Gill P.K.
      • Devi P.
      • Arora S.
      Seroprevalence of hepatitis B, hepatitis C, and human immunodeficiency viruses in asymptomatic pregnant women.
      PunjabHospital basedPregnant women (n = 16)Blood transfusion, unsafe injection or multiple injection,
      10Singh, 2010
      • Singh M.
      • Kotwal A.
      • Gupta R.M.
      • Adhya S.
      • Chatterjee K.
      • Jayaram J.
      Sero-epidemiological and behavioural survey of HIV, HBV and HCV amongst Indian armed forces trainees.
      Multi-statesHospital basedArmy Recruit (n = 101)Intravenous drug use, unsafe sex
      11Medhi, 2012
      • Medhi S.
      • Goswami B.
      • Das A.K.
      • et al.
      New insights into hepatitis C virus infection in the tribal-dominant part of Northeast India.
      Assam, ManipurHospital basedHCV positive patients (n = 75)Blood transfusion, intravenous drug use, acupuncture, unsafe sex, unsafe shaving
      12Sood, 2012
      • Sood A.
      • Midha V.
      • Bansal M.
      • Sood N.
      • Puri S.
      • Thara A.
      Perinatal transmission of hepatitis C virus in northern India.
      PunjabHospital basedPregnant women (n = 7)Dental procedure
      13Sood, 2012
      • Sood A.
      • Sarin S.K.
      • Midha V.
      • et al.
      Prevalence of hepatitis C virus in a selected geographical area of northern India: a population based survey.
      PunjabCommunityCommunity population (n = 272)Blood transfusion, unsafe injection, minor surgery, major surgery, dental procedure, tattooing, body piercing, unsafe sex, intravenous drug use
      14Goyal, 2014
      • Goyal L.D.
      • Kaur S.
      • Jindal N.
      • Kaur H.
      HCV and pregnancy: prevalence, risk factors, and pregnancy outcome in north Indian population: a case-control study.
      PunjabHospital basedPregnant women (n = 40)Blood transfusion, major surgery, dental procedure, obstetrical procedures
      15Sharma, 2014
      • Sharma A.
      • Kaur S.
      Seropostivity of hepatitis C infection among voluntary and replacement blood donors in a tertiary care hospital in Punjab.
      PunjabHospital basedBlood donors (n = 49)Blood transfusion, unsafe injection, major surgery, body piercing, tattooing, intravenous drug use, unsafe sex, unsafe saving practices
      16Vasudevan, 2016
      • Vasudevan S.
      • Kavimandan A.
      • Kalra N.
      • et al.
      Demographic profile, host, disease & viral predictive factors of response in patients with chronic hepatitis C virus infection at a tertiary care hospital in north India.
      New DelhiHospital basedHCV positive patients (n = 211)Blood transfusion, previous surgery, dental extraction, intravenous drug use, needle stick injury
      17Khatoon, 2017
      • Khatoon R.
      • Jahan N.
      Assessment of seroprevalence of hepatitis C virus-specific antibodies among patients attending hospital of semi-urban North India using rapid qualitative in vitro diagnostic test.
      Uttar PradeshHospital basedHCV positive patients (n = 15)Blood transfusion, body piercing, intravenous drug use, razor sharing, unsafe sexual activity, major surgery, tattooing
      18Grewal, 2018
      • Grewal U.S.
      • Walia G.
      • Bakshi R.
      • Chopra S.
      Hepatitis B and C viruses, their coinfection and correlations in chronic liver disease patients: a tertiary care hospital study.
      PunjabHospital basedHCV positive patients (n = 40)Blood transfusion, unsafe sex, drug addiction, intravenous drug use
      19Gupta, 2018
      • Gupta S.
      • Sodhi S.P.S.
      • Brar G.K.
      • Bansal R.N.
      Risk factors for hepatitis C: a clinical study.
      PunjabHospital basedHCV positive patients (n = 740)Blood transfusion, body piercing, intravenous drug abuse, tattooing, dental procedure, major surgery
      20Mahajan, 2018
      • Mahajan R.
      • Midha V.
      • Goyal O.
      • et al.
      Clinical profile of hepatitis C virus infection in a developing country: India.
      PunjabHospital basedHCV positive patients (n = 8,035)Dental procedure, unsafe injections, major surgery, blood transfusion, body piercing, intravenous drug use
      21Ramya, 2018
      • Ramya E.
      • Daniel J.C.
      • Ramalakshmi S.
      • Usha R.
      Prevalence and risk factors of hepatitis C virus in irula tribal community, Tamilnadu, India.
      Tamil NaduCommunityTribal community (n = 19)Tattooing, major surgery, unsafe injection, unsafe sex
      22Dhiman, 2019
      • Dhiman R.K.
      • Grover G.S.
      • Premkumar M.
      • et al.
      Decentralized care with generic direct-acting antivirals in the management of chronic hepatitis C in a public health care setting.
      PunjabCommunityCommunity population(n = 20,113)Dental procedure, unsafe injections, major surgery, unprotected sex, tattooing, barber shaving, razor sharing, intravenous drug use
      23Juttada, 2019
      • Juttada U.
      • Smina T.P.
      • Kumpatla S.
      • Viswanathan V.
      Seroprevalence and risk factors associated with HBV and HCV infection among subjects with type 2 diabetes from South India.
      Tamil NaduHospital basedPeople with DM (n = 11)Major surgery
      24Kar,2019
      • Kar S.K.
      • Sabat J.
      • Ho L.M.
      • Arora R.
      • Dwibedi B.
      High prevalence of hepatitis C virus infection in primitive tribes of eastern India and associated sociobehavioral risks for transmission: a retrospective analysis.
      OdishaCommunityTribal community (n = 127)Tattooing, razor sharing, body piercing, unsafe injections, barber shaving,
      25Sood, 2020
      • Sood A.K.
      • Manrai M.
      • Thareja S.
      • Shukla R.
      • Patel A.
      Epidemiology of hepatitis C virus infection in a tertiary care hospital.
      Multi-state; 90% participants were from Punjab or HaryanaHospital basedHCV positive patients (n-1012)Blood transfusion, Major surgery, Intravenous drug use, Tattooing
      DM, Diabetes Mellitus; HCV, Hepatitis C virus
      These studies provided data on blood transfusion, use of unsafe injections, minor or major surgery, unsafe dental procedures, tattooing, body piercing, obstetrical procedures, unsafe shaving, intravenous drug use, and unsafe sexual practices as risk factors for HCV transmission.
      The risk factors assessed by different investigators are summarized in Table 2. Among the factors studied, unsafe injections, obstetrical procedures, body piercing, unsafe dental procedure, unsafe shaving, and tattooing were identified as major risk factors reported by HCV population participants.
      Table 2Risk Factor Studies for Hepatitis C Virus Transmission in India.
      Risk factorsNo. of studies reported a particular risk factorTotal number of study participants included in studies (N)Number of participants with a particular risk factor (n)Proportion of participants with a particular risk factor (%)
      Blood transfusion1910,7783963.7
      Unsafe or multiple injections or needle stick injury1429,01515,76154.3
      Minor surgery231172.3
      Major surgery1430,648321110.5
      Unsafe dental procedures829,440552218.8
      Tattooing1430,582349611.4
      Body piercing99373239325.5
      Obstetric procedure21243830.6
      Unsafe shaving720,436301514.7
      Intravenous drug user or drug addiction1310,6477957.5
      Unsafe sexual practices1020,7842091.0

      Discussion

      In meta-analysis of risk factors for HCV transmission in India, we observed unsafe injections as the most common cause followed by obstetric procedures and body piercing. Our results have implications for the public health perspective and will be helpful in planning our national policy on HCV screening and case finding.
      The successful elimination of viral hepatitis by 2030, as set by WHO, require identification of 90% or more of HCV infected people. Only 20% of those with active HCV infection, progresses to cirrhosis over 20 years
      • Seeff L.B.
      Natural history of chronic hepatitis C.
      while it remains completely asymptomatic in a large proportion. The only measure to identify such subclinical HCV infection in low-risk community population is large-scale screening of the population.
      Large-scale screening and linkage with care is one of the major obstacles in HCV elimination. The WHO restricts the HCV screening to individuals who are part of a high-risk population or who have a history of HCV risk exposure or high-risk behavior.
      WHO
      Guidelines for the Screening, Acre and Treatment of Persons with Chronic Hepatitis C Infection.
      The opinion on HCV screening of low-risk community population are divided. The joint guideline of American Association for the Study of Liver Diseases (AASLD) and Infectious Disease Society of America (IDSA) recommend one-time HCV screening

      AASLD-IDSA. Recommendations for testing, managing, and treating hepatitis C. http://www.hcvguidelines.org. [22nd March 2022]..

      for all individuals with age >18 years, whereas European Association for the Study of the Liver (EASL) suggests that optimal regional or national screening approaches should be determined based on the local HCV epidemiology.
      EASL recommendations on treatment of hepatitis C: final update of the series.
      The estimated HCV burden in low-risk population in India is ∼5 million.
      • Goel A.
      • Rewari B.B.
      • Sharma M.
      • Konath N.M.
      • Aggarwal R.
      Seroprevalence and burden of hepatitis C virus infection in WHO South-East Asia Region: a systematic review.
      As of now, estimated low-risk adult population of India is ∼1 billion. Hence, India needs to curate its own HCV screening strategy to identify a large pool of HCV-infected population in a cost-efficient way. Screening of high-risk population alone will fail to identify 88% of the HCV burden. On the other hand, practice of universal screening will pose not only implementational problem but also a huge financial burden.
      Our country needs to adopt a middle way to minimize the cost and maximize the benefits. There could be quite a few screening strategies such as screening of blood and blood product recipients who had received transfusion before the year 2001, that is, before the blood bank screening for HCV was implemented in the country; adoption of passive screening with point of care devices at the time of routine health care; antenatal screening during antenatal visits; or practicing the pre-surgical screening for HCV.
      An alternate strategy could be identification of risk factors, associated with HCV transmission in the country, followed by questionnaire-based screening of the low-risk population for their exposures to such risk factors and prioritize their HCV screening. Our review identified blood transfusion, major or minor surgical procedures, dental and obstetric procedures, multiple injections, tattooing, body piercing, and unsafe shaving as risk factors associated with HCV.
      The factors reported in our review (multiple injections, obstetrical procedure, tattoo, and dental procedures) are not unique to India. Reports from adjacent countries such as Pakistan
      • Butt A.K.
      • Khan A.A.
      • Khan S.Y.
      • Sharea I.
      Dentistry as a possible route of hepatitis C transmission in Pakistan.
      • Hashmi A.
      • Saleem K.
      • Soomro J.A.
      Prevalence and factors associated with hepatitis C virus seropositivity in female individuals in Islamabad, Pakistan.
      • Trickey A.
      • May M.T.
      • Davies C.
      • et al.
      Importance and contribution of community, social, and healthcare risk factors for hepatitis C infection in Pakistan.
      and Bangladesh,
      • Mamun Al M.
      • Karim F.
      • Foster G.
      • Akbar S.F.
      • Rahman S.
      Prevalence and risk factors of asymptomatic hepatitis C virus infection in Bangladesh.
      have also identified these factors for HCV transmission. A recent systematic review of thirty studies, from both developed and developing countries, have reported the odd ratio of 1.83 for the risk of HCV transmission with body piercing.
      • Yang S.
      • Wang D.
      • Zhang Y.
      • et al.
      Transmission of hepatitis B and C virus infection through body piercing: a systematic review and meta-analysis.
      Various forms of body piercing, such as Godna, nose piercing, and ear piercing, are very common in Indian culture. These occult routes of transmission might be responsible for HCV transmission among those who lack the traditional risk factors. The identification and screening of these factors might help in self-screening or targeted screening to reduce the cost and increase the yield of investment. Nguyen et al showed in their self-reported 72-item questionnaire that people with two risk factors had a 10% chance of HCV infection, whereas those with ≥4 risk factors had a 50% chance for HCV infection.
      • Nguyen M.T.
      • Herrine S.K.
      • Laine C.A.
      • Ruth K.
      • Weinberg D.S.
      Description of a new hepatitis C risk assessment tool.
      Another study by Mallette et al reported 7.3% anti-HCV positivity among those who had ≥1 risk factor.
      • Mallette C.
      • Flynn M.A.
      • Promrat K.
      Outcome of screening for hepatitis C virus infection based on risk factors.
      In a study from New York tested a 27-item questionnaire in 1000 participants from primary care clinic and reported 8.3% HCV prevalence, which was more than four times the reported national prevalence rate.
      • McGinn T.
      • O'Connor-Moore N.
      • Alfandre D.
      • Gardenier D.
      • Wisnivesky J.
      Validation of a hepatitis C screening tool in primary care.
      The studies, included in our report, had few limitations; first, their results are likely to be influenced by recall bias of the participants because all the participants were aware of their HCV status; second, there were no control groups; third, lack of uniformity in definitions for the reported risk factors; the risk factors were completely based on information provided by the participants but not on documentary evidence; retrospective nature of studies; and identification of risk factors was not the primary objective for any of the studies. Further, we had data from only 10 of the 37 states and UTs in India, with 13 studies from the two states only Punjab
      WHO
      Combating Hepatitis B and C to Reach Elimination by 2030.
      and Tamil Nadu.
      • Goel A.
      • Seguy N.
      • Aggarwal R.
      Burden of hepatitis C virus infection in India: a systematic review and meta-analysis.
      This suggests a gross under representation of the country. The risk factors are likely to vary between the different states in the country.
      Although our data had several limitations, the results are important from a public health perspective for the policy makers and primary care physicians. We need to further explore the yield of risk-factor-based HCV screening in well-designed prospective studies, preferably in community setting. We can also take measures to reduce the exposure to those risk factors. We can advocate and practice judicious and minimal use of blood and blood products to reduce their unscrupulous use. Similarly, “unsafe shaving practice” shall also be discouraged without blaming any profession or livelihood because reuse of shaving blades and potash alum, a popular astringent in the Indian subcontinent, are presumed to transmit HCV.
      • Waheed Y.
      • Safi S.Z.
      • Qadri I.
      Role of Potash Alum in hepatitis C virus transmission at barber's shop.
      We shall also educate the health care workers, traditional healers, and traditional dais (lady in the village who provide obstetrical and gynecological services) who frequently perform minor/major surgeries, dental and obstetrical procedures, about the risk of HCV transmission, use of single-use syringes, and biomedical waste disposal.
      In conclusion, unsafe injections, dental and obstetrical procedures, previous blood transfusion or surgery, tattooing, body piercing, and unsafe shaving could be a risk factors for HCV transmission in our country, and these risk factors can be used to screen for HCV testing.

      Credit Authorship Contribution Statement

      Shalimar. Concept, Analysis, First draft; Critical editing, Sai Priya, Concept; Study search and selection; First draft, Hardik Gupta; Study search and selection; Data extraction; First draft, Bhavik Bansal; Study search and selection, Data extraction; Analysis, Anshuman Elhence; Study search and selection; Data extraction; First draft, Ravi V Krishna Kishore; Data extraction; Analysis; Yes, Amit Goel; Concept, Study search and selection, Analysis, Critical editing.

      Conflicts of interest

      All authors have none to declare.

      Acknowledgements

      None.

      Funding

      None.

      Authors’ declaration

      All the authors had full access to all the data in the study and approves the final version of the manuscript.

      Ethics approval

      Not applicable.

      Availability of data/material

      The data that support the findings of this study are available from the corresponding author, upon reasonable request.

      Code availability

      Not applicable.

      Supplementary data

      The following is the supplementary data to this article:

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