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    Sample chart showing study selection criteria of enrollment of participants in the study.

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Prevalence and Risk Factors Associated with Hepatitis B and C in Nawabshah, Sindh, Pakistan

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  • 1 Department of Physiology, University of Sindh, Jamshoro, Pakistan

ABSTRACT

In Pakistan, viral hepatitis is a serious public health problem affecting millions of people. Both hepatitis B and hepatitis C infections are spreading rapidly in all provinces of Pakistan, including Sindh, because of lack of knowledge about routes of transmission, low literacy rate, reuse of syringes, piercing, and other factors. However, information about the prevalence and risk factors is inadequate. So, a general population-based study was conducted to determine the prevalence rate and risk factors of hepatitis B and hepatitis C in Nawabshah. Healthy individuals were screened for hepatitis B and hepatitis C using an immunochromatographic rapid test followed by confirmation through ELISA and PCR. Information about sociodemographic and risk factors was obtained through a pretested questionnaire. Descriptive frequencies, odds ratio, and CI were calculated using SPSS software version 23 (IBM Corp, Armonk, NY). In total, 523 participants were screened for hepatitis B and hepatitis C, among whom 232 were females and 291 were males. The overall prevalence of hepatitis C and hepatitis B was 14.3% and 6.7%, respectively. In a bivariate analysis, hepatitis B infection was significantly associated with risk factors such as hospitalization, blood transfusion, needle injury, multiple sex partners, reused syringe, dental extraction, surgery, injectable drug abuse, and shaving at barbershops. Hepatitis C infection was associated with factors including surgery, needle injury, blood transfusion, reused syringes, dental extraction, and shaving at barbershops. The increasing prevalence of hepatitis B surface antigen and hepatitis C virus in Nawabshah is a public health concern. There is dire need to implement preventive measures.

INTRODUCTION

Infectious diseases including HIV, tuberculosis (TB), and viral hepatitis are great global public health concerns. Hepatitis is the inflammation of the liver, caused by virus types including A, B, C, D, and E. Hepatitis B virus (HBV) and hepatitis C virus (HCV) are commonly prevalent forms of viral hepatitis. The common factors associated with transmission of both HBV and HCV infections are the same including exposure to infective blood, injection drug use, and reuse of syringe, except that HBV infection can also be caused by sexual contact and mother-to-child transmission at prenatal stage.1,2 According to a recently published report of the WHO, more than a million people died of viral hepatitis in 2015, which is considered to be greater than mortalities caused by HIV and TB together in the same year. Although the mortality rate due to viral hepatitis is increasing, HIV- and TB-associated mortality rates are decreasing globally. In the year 2015, 720,000 people died of chronic liver disease and 470,000 people died of hepatocellular carcinoma due to viral hepatitis. In 2015, 328 million people were living with chronic HBV infection (257 million) and chronic HCV infection (71 million). The HBV more frequently affects the African region and the Western Pacific region; however, HBV also affects countries of other regions, including Asia. The HCV is frequent between and within countries all around the world.3,4

South Asian countries share a substantial global burden of HBV and HCV infections. According to reports, 18 million people are living with HCV and 37 million people are living with HBV infection in India. Eight million people are living with HBV, and more than a million people are living with HCV in Bangladesh. In Pakistan, 4.55 million people are affected by HBV and 8.74 million people are affected by HCV.5,6 Despite the hepatitis control and prevention programs run by the government of Pakistan, the prevalence of HBV and HCV is increasing in the country. It may be because of large pool of HBV- and HCV-infected people, who are multiplying and infecting the normal population. This might be because of lack of awareness about routes of transmission and prevention measures. The self-evident public health urgency is compelling to identify the national, provincial, and local situation of HCV and HBV infection dynamics. Such reporting would be helpful to study the changing clinical, social, and epidemiological aspects of HBV and HCV infections and to control the diverse regional risk factors, which are responsible for the increase in the burden of viral hepatitis including HBV and HCV.

Sindh is the second largest populated province of Pakistan. Information about the prevalence of HBV and HCV infections among the general population is inadequate. Most of the previous studies were conducted on selected high-risk groups. These groups include blood donors; patients with diseases including dental abnormalities, hemodialysis, thalassemia, and HIV; drug addicts; sex workers; and hospitalized people.2,710 This conclusion was further supported by literature search analysis of last 5 years, 2014–2019, performed in PubMed search engine using Medical Subject Headings (MeSH) ([“Hepatitis B” {Mesh}] AND “Hepatitis C” [Mesh]) AND “Pakistan” (Mesh) (Supplemental Annexure 1).

The prevalence of HCV and HBV varies with geographical distribution. In India, the prevalence rate of HBV and HCV confection ranges from 0.2% to 16%.11 In Cambodia, the prevalence rate for HCV ranges between 2.8% and 14.7%. In Bangladesh, the prevalence of HBV ranges from 4.9% to 8.7%.12 In Pakistan, the prevalence rates of HCV ranges from 1.2% to 15.9%.13 The factors associated with HBV and HCV spread in Pakistani setting have been reported by several studies conducted in high-risk groups. The trend regarding age and hepatitis spread shows that HCV and HBV infections tend to increase along with age with predominant prevalence in the age-group above 30 years. The studies have also associated HBV and HCV infections with gender and marital status. A number of studies suggest that being male is more likely to be infected with HBV and HCV. Moreover, being married has also been found as a risk factor for HBV and HCV infections. The association of hepatitis with education and the area of residence shows that people who are living in rural areas and illiterate are more likely to be exposed to HBV and HCV.1317 Several factors that play a role in its spread are interlinked. Here, we targeted Nawabshah (urban area) of Sindh to assess the prevalence and risk factors associated with HBV and HCV spread in the general population.

METHODS

Study site.

Nawabshah city is the one among the medium-size cities of Sindh Province, Pakistan. According to the latest census report 2017, the population of Nawabshah Tehsil is 413,913.18 The population is ethnically diverse with Sindhi-, Urdu-, and Punjabi-speaking people with different religious affiliations. The economy of the district mainly depends on service sectors, small shops, livestock, and poultry. The agriculture sector depends on cultivation of bananas, sugarcane, cotton, and wheat. The city dwellers are facing problems including, poverty, unhygienic conditions, contaminated water, health-related problems, and unhygienic public and private healthcare centers.

Sample size calculation.

The sample size was calculated using epidemiological software “Open EPI” version 3 (Emory University, Atlanta, GA).19 The total population of the Nawabhshah tahsil was 413,913,18 and the expected frequency of outcome was set on 50%, with 5% of desired precision. The level of confidence was set to 95% to maximize the sample size. A sample size of 384 was enough to show the precision.

Study setting.

Screening camps were organized by the Department of Physiology, University of Sindh, Jamshoro, at Nawabshah to screen the general population. During the month of March 2019, healthy adults older than 18 years who were residents of Nawabshah were included in study. First, the field data collectors briefed the participants about the aim of the screening camp. Second, the participants were provided a written informed consent form. On agreement, the informed consent form was signed by participants. Then, a predesigned questionnaire comprising sections about sociodemography, medical history, and routes of transmission of hepatitis including injury, drug abuse, tattooing, piercing, sex, and visiting saloons for shaving; and other relevant questions was administered in participants who were literate, whereas illiterate participants were able answer the questionnaire with help of the field data collectors.

Blood sampling and hepatitis B surface antigen (HBsAg) and HCV screening.

Blood was drawn by a trained phlebotomist. Ten milliliters of blood was drawn in a serum separator tube. After 2 hours, the blood was centrifuged at 3,000 rounds/minute till 15 minutes to obtain the serum. The serologic test for HBsAg and HCV was performed using a commercially available rapid immunochromatographic test (ICT) kit (Accurate Diagnostic Canada, South Plainfield, NJ). The results of the ICT were further confirmed using ELISA and PCR performed by Cobas Roche Diagnostics using electrochemiluminescence immunological assay. Data of study participants with HBV and HCV who were diagnosed positive with all three methods including ICT, ELISA, and PCR were included in analysis (Figure 1). Results were communicated to the participants of study, and those participants who were HBsAg negative were suggested for vaccination, and those participants who were HBsAg positive and HCV positive were suggested to contact with the physicians for treatment.

Figure 1.
Figure 1.

Sample chart showing study selection criteria of enrollment of participants in the study.

Citation: The American Journal of Tropical Medicine and Hygiene 104, 3; 10.4269/ajtmh.20-1228

Statistical analysis.

Data analysis was performed using Statistical Package for the Social Sciences software version 23. Data were analyzed on descriptive and bivariate levels. Distribution of sociodemographic factors was calculated using the chi-square test. Mean and SD were computed for quantifiable variables. Association among categorical variables was determined by using odds ratio (OR), with 95% of CI.

Ethical consideration.

The project was approved by the Institutional Review Board of the Department of Physiology, Faculty of Natural Sciences, University of Sindh, Jamshoro.

RESULTS

Baseline characteristic of study participants.

In total, 523 participants were screened for HBsAg and HCV. The prevalence rate for HCV was 14.3%, and for HBsAg, the prevalence rate was 6.7%. The baseline characteristics of the participants of the study were as follows: age-wise distribution shows that prevalence of HBsAg in age-groups < 30 years was 7% (n = 10/138), in the age-group ranging between 31 and 40 years, the prevalence was 5% (n = 10/195), in the age-group ranging between 41 and 50 years, the prevalence was 13% (n = 15/116), and in the age-group ranging between 51 and 60, the prevalence was 13% (n = 10/75). The age-wise distribution of HCV shows that the prevalence of HCV in age-groups < 30 years was 13.7% (n = 20/146), in the age-group ranging between 31 and 40 years, the prevalence was 10% (n = 20/195), in the age-group ranging between 41 and 50 years, the prevalence was 18.7% (n = 20/106), and in the age-group ranging between 51 and 60 years, the prevalence was 18.5% (n = 15/81). The gender-wise distribution shows that the prevalence of HBsAg in female participants was 6.5% (n = 15/232), and in male participants, the prevalence was 6.9% (n = 20/291). The prevalence of HCV in female participants was 12.9% (n = 30/232), whereas in male participants, the prevalence of HCV was 15.5% (n = 45/291). The marital status–wise distribution shows that the prevalence of HBsAg in married and unmarried participants was 7% (n = 27/384) and 5.8% (n = 8/139), respectively. The prevalence of HCV in married and unmarried participants was 15.6% (n = 60/384) and 10.8% (n = 15/139), respectively. The religion-wise distribution shows in Hindu community, the prevalence of HBsAg was 9.8% (n = 5/51) and prevalence in Muslim community was 6.4% (n = 30/472). The prevalence of HCV in Hindu participants was 18% (n = 9/50) and that in participants in Muslim community was 14% (n = 66/473). Sex partner–wise distribution shows that prevalence of HBsAg among participants who had only one sex partner was 5.4% (n = 20/371), in participants with multiple sex partners, the prevalence of HBsAg was 4% (n = 5/25), and the HBsAg prevalence rate in participants with no sex partner was 7.9% (n = 10/127). The prevalence of HCV was 12% (n = 45/371), 60% (n = 15/25), 12% (15/127) among participants with single sex partner, multiple sex partners, and no sex partner, respectively. Drug abuse–wise distribution shows that the prevalence of HBsAg among drug abusers was 50% (5/10), whereas the prevalence of HCV among drug abusers was 45% (5/11) (Table 1).

Table 1

Association between sociodemographic factors and prevalence of HBsAg and HCV in the general population of Nawabshah, Sindh, Pakistan

FactorHBsAg-positive cases (n = 35)HBsAg-negative cases (n = 488)χ2/P-valueHCV-positive cases (n = 75)HCV-positive cases (n = 448)Statistical test/P-value
Age (years)
 < 3010 (7%)13720 (13.7%)126
 31–4010 (5%)18520 (10%)175
 41–505 (4.8%)1016.720 (18.9%)866.3
 51–6010 (13%)65P = 0.0815 (19.8%)61P = 0.099
Gender
 Female15 (6.5%)2172.130 (9%)2020.7
 Male20 (6.9%)271P = 0.145 (15.5%)246P = 0.4
Marital status
 Married27 (7%)3570.2760 (15.6%)3241.94
 Unmarried8 (5.8%)131P = 0.715 (10.8)124P = 0.2
Education
 Illiterate30 (8.9%)20824.5430 (12.6%)2081.07
 Literate5 (1.8%)280P < 0.0000145 (15.8%)240P = 0.3
Religion
 Hindu5 (9.8%)460.99 (18%)410.6
 Muslim30 (6%)442P = 0.366 (14%)407P = 0.5
Sex partners
 120 (5.4%)35145 (12%)326
 > 15 (20%)208.415 (60%)1044.5
 Nil10 (7.9%)117P = 0.0115 (11.8%)112P < 0.00001
Drug abuse
 Yes5 (50%)530.65 (45.5%)68.8
 No30 (5.8%)483P < 0.0000170 (13.7%)442P = 0.002

HBsAg = hepatitis B surface antigen; HCV = hepatitis C virus.

Risk factors associated with HBsAg and HCV.

In bivariate analysis, HBsAg prevalence was significantly associated with several factors such as hospitalization (OR = 3.50; CI: 1.72–7.12), surgery (OR = 3.35; CI: 1.34–8.35), blood transfusion (OR = 7.03; CI: 3.37–14.66), needle injury (OR = 4.48; CI: 1.17–17.09), reused syringe (OR = 8.52; CI: 4.15–17.48), shaving at saloons (OR = 131.7; CI: 7.90–2,194), and dental extraction (OR = 3.72; CI: 1.61–6.63). Moreover, analysis shows that HCV prevalence was significantly associated with several factors such as hospitalization (OR = 10.50; CI: 16.11–18.02), surgery (OR = 7.25; CI: 3.91–13.48), blood transfusion (OR = 14.88; CI: 8.14–27.16), needle injury (OR = 17.08; CI: 5.20–56.06), reused syringe (OR = 68.31; CI: 34.25–136.3), drug abuse (OR = 6.26; CI: 1.22–32.05), shaving at barbershops (OR = 120.3; CI = 7.32–1977), and dental extraction (OR = 14 CI: 8.03–24.41) (Table 2).

Table 2

Association between risk factors and prevalence of HBsAg and HCV in the general population of Nawabshah, Sindh, Pakistan

FactorHBsAg-positive cases (n = 35)HBsAg-negative cases (n = 488)ORHCV-positive cases (n = 75)HCV-negative cases (n = 448)OR
95% CI95% CI
P-valueP-value
HospitalizedOR = 3.50OR = 10.50
 Yes15 (14.9%)86CI = 1.72–7.1245 (44.6%)56CI = 6.11–18.02
 No20 (4.7%)402P = 0.000730 (7%)392P < 0.0001
SurgeryOR = 3.35OR = 7.25
 Yes7 (13%)46CI = 1.34–8.3525 (48%)27CI = 3.91–13.48
 No28 (6%)442P = 0.0150 (10.6%)421P < 0.0001
Blood transfusionOR = 7.03OR = 14.88
 Yes15 (23.8%)47CI = 3.37–14.6635 (57.4%)26CI = 8.14–27.16
 No20 (4.3%)441P < 0.000140 (8.7%)422P < 0.0001
Needle injuryOR = 4.48OR = 17.08
 Yes3 (23%)10CI = 1.17–17.0910 (71.4%)4CI = 5.20–56.06
 No32 (6.3%)478P = 0.0465 (12.8%)444P < 0.0001
Reused syringeOR = 8.52OR = 68.31
 Yes20 (23.3%)66CI = 4.15–17.4860 (69.8%)26CI = 34.25–136.3
 No15 (3.4%)422P < 0.000115 (3.4%)422P < 0.0001
Shaving at barbershops (males)OR = 131.7OR = 120.3
 Yes20 (13.2%)131CI = 7.90–2,19445 (30%)105CI = 7.32–1977
 No0140P < 0.00010139P < 0.0001
Dental extractionOR = 3.72OR = 14
 Yes15 (14%)91CI = 1.61–6.6350 (47.2%)56CI = 8.03–24.41
 No20 (4.8%)397P = 0.00125 (6%)392P < 0.0001

HBsAg = hepatitis B surface antigen; HCV = hepatitis C virus; OR = odds ratio.

DISCUSSION

This is the first ever study carried out to screen HBsAg and HCV prevalence and risk factors associated with them in the general population of Nawabshah, Sindh. The overall prevalence of HCV was 14.4%, and for HBsAg, the prevalence rate was 6.7%. Previous reports from cities of Sindh Province such as Larkana, Thatta, Nousheroferoz, and Karachi showed that HCV prevalence ranges from 3.2% to 25.1%, and our prevalence result falls in this range.13 Our finding about HCV prevalence is consistent with reports from other cities of Pakistan, such as in Peshawar where the HCV prevalence was 12.9% and in Mardan, where the HCV prevalence was 11.7%,13 and other South Asian cities.11,12 Our result of HBsAg prevalence is consistent with that in studies on HBsAg conducted among high-risk groups such as hemodialysis,8 pregnant women,20 and barbers.21 These reports have shown that the HBsAg prevalence rate ranges from 2% to 7.5%. The rising prevalence rate of HBsAg and HCV can be attributed to the lack of public awareness about routes of transmission.22 In our study, we noticed that HBsAg and HCV are frequently prevalent in participants aged > 30 years; a large sample size–based study from Punjab about HCV has also reported that HCV is common in people aged > 30 years.23 The higher frequency in elderly participants may be due to their frequent visits to unsafe barbershops for haircut and shaving, and beauty parlors.24 The gender-wise classification of data showed that the prevalence of HBsAg and HCV in male and female participants was nearly equal. A few studies from Pakistan have suggested that being male is a risk factor for HBsAg and HCV exposure. However, this needs to be confirmed in large cohorts.13

In our data, HBsAg was frequent in illiterate participants compared with literate participants. However, HCV was mildly frequent in literate participants, with a mild difference of 3.1%. Illiteracy or unawareness about risk factors and routes of transmission of HBsAg and HCV is one major barrier in controlling and preventing disease spread.22,25 Hepatitis B surface antigen and HCV were prevalent in Hindu and Muslim participants with insignificant difference, and mildly high prevalence of HCV in Hindu participants can be due to tattooing practice.

Several risk factors were selected to understand the dynamics of disease spread; these factors include blood transfusion. The participants who went for blood transfusion or donation, who had needle injury, who used reused syringes, who went for shaving at barbershops, who went for dental extraction, who went for piercing, who went to seek hospital care, and who underwent surgical procedure and injection drug use were more likely to have been infected by HBsAg and HCV than participants who never went for the aforementioned factors (Table 2). This shows that nosocomial infections significantly contribute to disease spread.26 This includes unhygienic public and private hospitals, unavailability of auto-lock injections, unsafe surgical practices during minor and major surgical operations, unsafe dental extraction, root canal therapy, and gum treatment.27,28 It was observed during discussion with participants that nursing staff involved in minor surgery do not use gloves. The patients of various diseases ask physicians and quacks for prescription of injection use to get quick relief. The desire for saving money by reusing the syringes by physicians and quacks was also observed as a factor for infectious disease outbreaks.

CONCLUSION

The high prevalence of hepatitis B and hepatitis C indicates that the general population in Nawabshah is continuously exposed to risk of infection. There is dire need to launch effective community-based health education programs to create awareness among the public about routes of transmission and prevention from viral hepatitis. The curriculum can play an effective role in the awareness of routes of transmission of viral hepatitis. We recommend that Sindh TextBook Board should include a lesson about the awareness of infectious diseases in general science and biology subjects. It is recommended that teams of hepatitis control program should also visit the public and private schools and residential areas to vaccinate the school children and general public against HBsAg. The awareness of routes of transmission, complete ban of quakes, and prevention of hospital-associated infection of HBsAg and HCC can also be achieved through public health awareness and strict health governance.

Supplemental annexure

ACKNOWLEDGMENTS

We are thankful to participants of the study who cooperated in the study. The American Society of Tropical Medicine and Hygiene (ASTMH) assisted with publication expenses.

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Author Notes

Address correspondence to Ayaz Ali Samo, Department of Physiology, University of Sindh, Jamshoro, 76090 Sindh, Pakistan. E-mail: ayazsamo@usindh.edu.pk

Authors’ addresses: Ayaz Ali Samo, Zulfiqar Ali Laghari, Nimra Masood Baig, and Ghulam Murtaza Khoso, Department of Physiology, University of Sindh, Jamshoro, Pakistan, E-mails: ayazsamo@usindh.edu.pk, zulfiqar.laghari@usindh.edu.pk, nimrabaig32@gmail.com, and gm.khoso@usindh.edu.pk.

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