Prevalence and risk factors of hepatitis B and C in Bahawalpur: a hospital-based studyAbstract
Hepatitis causes inflammation of the liver. The World Health Organization set a goal to eliminate viral hepatitis by 2030 due to an increase in the number of deaths from liver cirrhosis and hepatocellular carcinoma. The present study aimed to determine the prevalence of hepatitis B and C among the general population of Bahawalpur, along with various recognized risk factors. Samples were collected from December 2021 to May 2022. In total, 263 blood samples were collected from the patients who visited Bahawalpur Victoria Hospital, Bahawalpur Pakistan. A rapid diagnostic test (ICT) was used to diagnose Hepatitis B surface antigen and anti-HCV, followed by an enzyme-linked immunosorbent assay (ELISA). The data were analyzed using IBM SPSS version 22. In total, 263 samples were tested; 5.3% (14/263) tested positive for HBV, 25.4% (67/263) tested positive for HCV, and 0.76% (2/263) were co-infected. The study found a significant association between illiteracy 24% (63/263) and literacy 7.6% (20/263) (P = 0.001), age (31-40 years) 11% (29/263) (P = 0.027), hospitalization 38% (100/263) versus non-hospitalization 62% (163/263) (P = 0.008), and patients who had received any dental treatment 20.9% (55/263) versus those who had not 79.1% (208/263) (P = 0.057). According to the study, people who frequently visited hospitals received no medical care and were unaware of the causes of disease transmission, made them more susceptible to infection. The study will help formulate policies and adopt precautionary measures to control the increasing incidence of hepatitis B and C in Pakistan.
Keywords:
prevalence; hepatitis B; hepatitis C; co-infection; risk factors
Resumo
A hepatite causa inflamação do fígado. A Organização Mundial da Saúde estabeleceu a meta de eliminar as hepatites virais até 2030, devido ao aumento do número de mortes por cirrose hepática e carcinoma hepatocelular. O presente estudo teve como objetivo determinar a prevalência de hepatite B e C na população geral de Bahawalpur, juntamente com vários fatores de risco reconhecidos. As amostras foram coletadas de dezembro de 2021 a maio de 2022. No total, 263 amostras de sangue foram coletadas de pacientes que visitaram o Hospital Victoria de Bahawalpur, no Paquistão. Um teste de diagnóstico rápido (TIC) foi utilizado para diagnosticar o antígeno de superfície da hepatite B e o anti-HCV, seguido por um ensaio imunoenzimático (ELISA). Os dados foram analisados no IBM SPSS versão 22. No total, foram testadas 263 amostras; 5,3% (14/263) testaram positivo para HBV, 25,4% (67/263) testaram positivo para HCV e 0,76% (2/263) estavam coinfectados. O estudo encontrou associação significativa entre analfabetismo 24% (63/263) e alfabetização 7,6% (20/263) (P = 0,001), idade (31-40 anos) 11% (29/263) (P = 0,027), internação 38% (100/263) versus não internação 62% (163/263) (P = 0,008), e pacientes que receberam algum tratamento odontológico 20,9% (55/263) versus aqueles que não receberam 79,1% (208/263). 263) (P = 0,057). Segundo o estudo, as pessoas que visitavam hospitais com frequência não recebiam cuidados médicos e não tinham conhecimento das causas da transmissão da doença, o que as tornava mais suscetíveis à infecção. O estudo ajudará a formular políticas e a adotar medidas preventivas para controlar a crescente incidência da hepatite B e C no Paquistão.
Palavras-chave:
prevalência; hepatite B; hepatite C; coinfecção; fatores de risco
1. Introduction
The Greek words “hepar” (liver) and “itis” (infection) are combined to form the word hepatitis (Shahzeb et al., 2019). Hepatitis is a disease that affects the liver tissue. Viral hepatitis is classified into five types: A, B, C, D, and E (Bosan et al., 2010).
Hepatitis B virus was discovered in 1965. HBV is classified as a representative of the hepadnaviridae group and is approximately 42 nm in diameter (Zhao et al., 2020). HBV consists of 3200 nucleotides (Zhao et al., 2020). Vaccines against HBV are extremely efficient. HBV is 10 times more infectious than HCV and 50-100 times more transmissible than HIV, known as the silent killer (Samuel et al., 2004). The virus has been detected in various areas and secretions of the body, such as the skin, spleen, kidney, breast milk, urine, semen, saliva, vaginal fluid, and tears (Athalye et al., 2023). Hepatitis B virus is blood-borne and is caused by sexual contact and vertical transmission (Inoue and Tanaka, 2016). The disease has no symptoms at an early stage but can be recognized by yellowing of the skin, loss of appetite, and malaise. Hepatitis B vaccines can eliminate infection from the blood in 99% of cases. HBV was first made available in 1982. However, HBV causes chronic liver disease in 350 million people, resulting in 600,000 deaths per year (WHO, 2022).
Hepatitis C virus was identified in 1989 (Manns and Maasoumy, 2022). Hepatitis C is a single-strand RNA virus with a genome length of 9.6 kb. HCV is a major burden of disease prevalence in Pakistan (Farhat et al., 2014). HCV comprises 9600 nucleotides (Manns and Maasoumy, 2022). HCV is classified into a large group of viruses in the family Flaviviridae with 11 genotypes worldwide. HCV is an RNA virus 50 nm in size (Athar et al., 2015). HCV affects liver cells but can also proliferate in blood lymphocytes, gut cells, and cells of the nervous system (Mathew et al., 2016). HCV often remains asymptomatic but, once developed, may lead to liver cirrhosis or fibrosis (Umar et al., 2010). HCV progresses in 14-180 days (Gupta et al., 2014). The modes of transmission of HCV are blood, the sex of the individual affected by HCV, and vertical transmission (Yeung et al., 2014). Hepatitis C virus infects one out of every twenty people in Pakistan (Haqqi et al., 2019). Every year, HCV infects between 62 and 79 million people worldwide (Roudot-Thoraval, 2021). Both HBV and HCV are chronically transmitted by percutaneous means such as the reuse of needles, serum, and other body fluids (Coppola et al., 2016).
The global health sector strategy has set a goal of eliminating viral hepatitis by 2030, reducing chronic infection by 90%, and hepatitis-related mortality by 65% (WHO, 2021). Hepatitis B and C accounted for 94% of all deaths in 1990, but this number increased to 97% in 2017, resulting in 1.38 million deaths Worldwide. Among these deaths, hepatitis B accounts for 58% and hepatitis C for 42%. Over the past few decades, significant efforts have been made to eradicate viral hepatitis by introducing the hepatitis B vaccine and antiviral drugs for hepatitis C virus infection. According to the WHO, it was estimated that 257 million, or almost 3.5% of individuals, were affected by HBV, and 71 million, or almost 1% of people, were suffering from HCV globally in 2017 (Liu et al., 2020). According to the World Health Organization, Somalia and Sudan are highly endemic to HBV, whereas Pakistan and Egypt are highly endemic to HCV. Egypt and Pakistan bear 80% of the disease burden. Each year, 150,000 new cases are reported in Pakistan. Overall, 12 million people are infected with hepatitis B and C in Pakistan (WHO, 2017). According to the Pakistan Medical Research Council (PMRC), it is estimated that 12 million people, approximately 7.4% of the population, are infected with HBV and HCV. Among them, 2.4% were affected by HBV, and 4.9% were affected by HCV (Farhat et al., 2014).
This study aimed to determine the prevalence of hepatitis B, hepatitis C, and co-infection along with various risk factors to determine the actual cause of disease prevalence in the Bahawalpur region, Pakistan.
2. Material and Methods
2.1. Study area
The Bahawalpur district covers an area of 24,830 square kilometers and has a population of 0.92 million in 2023 (Macrotrends, 2024). Bahawalpur is located in South Punjab and was ranked as the 12th largest city in Pakistan after the 2017 census. The weather is hot and dry. The main challenges include poverty, dirty water, unsanitary conditions in public and private institutions, and illiteracy. The economy depends on agriculture, livestock, and small- and large-scale businesses.
2.2. Study duration
A survey was planned by the Department of Zoology at Cholistan University of Veterinary and Animal Sciences, Bahawalpur, in collaboration with the Bahawalpur Victoria Hospital to estimate the prevalence of hepatitis in Bahawalpur. The period of the study was six months from December 2021 to May 2022.
2.3. Sample size and settings
In this survey, 263 blood samples of individuals across all age groups were collected. The collected samples included 81 males and 182 females. Samples were collected from patients who visited the district headquarters (Bahawalpur Victoria Hospital). Sampling was performed randomly. A questionnaire sheet was filled with direct interviews with the patients. The patients were asked about 13 questions, which included direct and indirect variables. Direct variables included marital status, age, gender, education, economic status, and occupation, which were directly associated with the patient’s health, and indirect variables included hospitalization, surgery, dental treatment, barber, nose or ear piercing, needle injury, blood transfusion, and previous disease history, which were related to person hygiene.
2.4. Blood sampling
Blood samples (5ml) were taken by an expert phlebotomist using 5-cc syringes from the medial ulnar vein and then transferred to clot activator vials. After collection, the samples were transferred to the pathology laboratory of Quaid-e-Azam Medical College, Bahawalpur. To avoid inconvenience, each sample was assigned a number. Samples were allowed to clot in a vial. Each vial was also numbered according to the sample number. Blood was separated by clotting and centrifuged at 3500 rpm for 15 min. The samples were initially analyzed using immunochromatographic kits (STANDARD DIAGNOSTICs, INC.) for HBsAg and anti-HCV detection. Positive samples were then analyzed using enzyme-linked immunosorbent assay (AUTOBIO DIAGNOSTICS CO., LTD) kits. The cut-off value for HBsAg was 0.102 and that for anti-HCV was 0.109. If the absorbance value of the samples was greater than the cut-off value, it was considered positive. If the absorbance value was less than the cut-off value, it was considered negative.
2.5. Statistical analysis
The collected data were evaluated using SPSS IBM version 22. The chi-square test was used to analyze sociodemographic components and risk factors. The percentage and P values were determined to show a significant and non-significant association of the elements with disease test results. The level of significance was α=0.05.
2.6. Ethical consideration
The ethical committee of Cholistan University of Veterinary and Animal Sciences, Bahawalpur signed an ethical consideration letter.
3. Results
A total of 263 individuals were screened for HBsAg and anti-HCV. Out of 263, (31.5%) 83/263 tested positive for hepatitis, including (5.3%) 14/263 tested positive for HBV, HCV accounted for (25.4%) 67/263 and (0.76%) 2/263 were co-infected (Figure 1).
According to age, different age groups have different incidence rates. People over the age of 30 years had the highest incidence rate. The prevalence was 9.1% in the age group 3-30, 11% in the age group 31-40, 5% in the age group 41-50, 4.1% in the age group 51-60, and 1.1% among people aged 61-70 and 71-80 (Figure 2). According to the gender distribution, the prevalence of HBsAg in females was 3.8% (10/182), HCV in females was 17.5% (46/182), and the incidence of coinfection was 0.76% (2/263). The prevalence of HBsAg in males was 1.5% (4/81), HCV in males was 8% (21/81), and no coinfection-positive cases were observed in males (Figure 2). The marital status distribution showed 4.1% prevalence among unmarried people (11/263), with 1.1% infected with HBsAg and 3.0% infected with HCV. In married people, the prevalence was 27.3% (72/263), 4.2% of people were infected with HBsAg, 22.4% were infected with HCV, and 0.760% were co-infected (Figure 2). This shows that married individuals were more likely to contract viral hepatitis.
Small-scale business owners and laborers had the highest occupational prevalence. Labor had a 19.76% prevalence (52/263); farmers had a 1.9% (5/263); people doing private jobs had a 1.1% (3/263); people having small-scale businesses had a 4.1% (11/263); people doing government jobs had a 4.5% (12/263); and large-scale business owners, students, and landlords had no or 0% prevalence (Figure 2). Economic status was divided into three categories: poor, middle class, and good. The poor had the highest prevalence, 17.1% (45/263). People in the middle class had a prevalence rate of 10.6% (28/263), whereas those in good economic status had a prevalence rate of 3.8% (10/263). Prevalence was also observed in individuals from various educational backgrounds (Figure 2). The educational status was classified into two categories: literate and illiterate. Uneducated people were infected with HBsAg, HCV, and co-infection at a higher rate of 24% (63/263) than literate people (7.6% (20/263) (Figure 2).
The participants had varying percentages of risk factors. (100/263) 38% of those who participated in the study remained hospitalized, while (163/263) 62% had never been hospitalized. Other risk factors showed different percentages, showing that 95/263 (36.1%) were those who were exposed to surgery, 168/263 (63.9%) were those who did not seek any surgical procedure, and 55/263 (20.9%) were those who received dental treatment versus those who did not receive any dental treatment. 208/263 (79.1%), 120/263 (45.6%) individuals received barber service or participated in nose and ear piercing and exchanged their jewelry without noticing the possibility of bleeding from infection in females compared to those who did not participate in any such practice. 143/263 (54.4%), 36/263 (13.7%) individuals were injured by needles compared to those who did not, 227/263 (86.3%) actively participated in blood transfusion versus 180/263 (68.4%) who did not, 9/263 (3.4%) were drug addicts, 254/263 (96.6%) were those who refused to take any drug, and 59/263 (22.4%) did not have any previous disease history of hepatitis B and C (Figure 3).
The findings revealed that HCV has a significant association with age (P = 0.001), marital status (P = 0.025), economic status (P = 0.051), and education (P = 0.001), whereas HBV and co-infection have a non-significant association with sociodemographic factors. The findings revealed a significant association between the combined results of hepatitis B, hepatitis C, and HBV and HCV with age (P = 0.027) and education (P = 0.01) as shown in Table 1.
The findings showed that HBsAg is associated with dental treatment (P = 0.038) and previous disease history (P = 0.0001), whereas anti-HCV is associated with hospitalization (P = 0.013) and previous disease history (P < 0.0001), and co-infection was associated with hospitalization (P = 0.070), surgery (P = 0.059), and previous disease history (P = 0.008). The total positive direct variable results showed a significant association with hospitalization (P = 0.008), dental treatment (P = 0.057), and a history of disease (P < 0.0001) as shown in Table 2.
4. Discussion
The overall prevalence of HBsAg and HCV antibodies was 5.3% and 25.4%, respectively. The study found the highest prevalence of hepatitis B and C. However, the prevalence rate varied by area, with an overall prevalence range of 8-42% across the country. The results are consistent with those of a study published in 2023 (Jamali et al., 2023). The international health community has devised a strategy to eradicate viral hepatitis by 2030 (WHO, 2021). The study found that hepatitis C was more common than hepatitis B, which is similar to previous studies conducted in various regions of Pakistan, including Faisalabad, Lahore, and Mirpur Khas (Khalid et al., 2015; Junaid et al., 2020; Arain et al., 2020). Hepatitis B and C were associated with age (P = 0.027), education (P = 0.001), hospitalization (P = 0.008), and dental treatment (P = 0.057). It was observed that the highest prevalence with an increase in age was due to a decrease in immunity and the chance of infection with external risk factors. The results are consistent as previously stated by (Khan et al., 2014; Shamim et al., 2022; Mehmood et al., 2020; Samo et al., 2020).
The study showed a higher prevalence in women than in men. The same trend has been reported by (Bigna et al., 2019) from Africa in 2019. Another potential factor may be the larger sample size of females (n = 182) than males (n = 81). The highest prevalence in females was observed in pregnant women, as previously reported from Abbottabad, Pakistan in 2017 (Jadoon et al., 2018). However, the study target was the general population.
Married people had the highest prevalence compared with unmarried people. The same trend has been previously reported by studies from Nigeria and Bahawalpur, Pakistan in 2022 (Shamim et al., 2022; Odukoya et al., 2022). The other sociodemographic factors discussed in this study include economic status, education, and occupation. According to the findings, illiterate people had the highest prevalence of the disease. Other researchers from various regions of Pakistan (Junaid et al., 2020; Arain et al., 2020) have also addressed and reported the same trend. The greatest prevalence in these groups may be due to a lack of awareness and the practice of unsanitary conditions. Many risk factors were also considered to identify the true cause of disease spread. Patients who were admitted to hospitals and underwent surgery, frequently visited barbers for shaving, underwent blood transfusions, needle injuries, body piercings, or received dental treatment were more likely to have Hepatitis B and C. These factors were also addressed in other studies that showed a significant association with age, education, and marital status. Our results are compatible with those of these studies (Khan et al., 2017; Shamim et al., 2022).
The study showed a significant association between the hepatitis B virus and risk factors such as dental treatment (P = 0.038), as previously reported by a study from Yemen and Pakistan in 2020 (Arain et al., 2020; Alnwany, 2020). The current study showed the highest prevalence of hepatitis C virus and showed significant associations with demographic factors like age (P = 0.001), education (P = 0.001), marital status (P = 0.025), and economic status (P = 0.051). These results showed similarity to a study conducted in India in 2021 and in Pakistan in 2018 (Jindal et al., 2021; Al Kanaani et al., 2018). The results showed a significant association between HCV and hospitalization (P = 0.013), which is consistent with a study conducted in Italy (Cammarota et al., 2019).
This shows the highest disease prevalence in low-income and illiterate people, with a particularly high prevalence of HCV, which needs to be addressed on an immediate basis. The study revealed an alarming situation in an area, prompting many researchers to conduct additional studies in the area.
5. Conclusion
The study showed the highest prevalence of hepatitis B and C in Bahawalpur compared with other cities in Pakistan. Hepatitis C was more prevalent than hepatitis B. The highest prevalence shows alarming conditions that require an immediate effective control strategy. It seems that either the hospital administration is unable to apply the recommendations or visitors to BVH are not following the hospital administration norms for limiting infectious diseases in hospitals. According to the study, people who visited hospitals frequently, received any medical care, including dental treatment, and were unaware of the causes of disease transmission were more susceptible to infection.
Acknowledgements
The present study was financed by project MECESUP UCT 0804, May 2023. We thank the Head of the Pathology Department, Quaid e Azam Medical College, Bahawalpur, for their help and cooperation.
References
-
AL KANAANI, Z., MAHMUD, S., KOUYOUMJIAN, S.P. and ABU-RADDAD, L.J., 2018. The epidemiology of hepatitis C virus in Pakistan: systematic review and meta-analyses. Royal Society Open Science, vol. 5, no. 4, pp. 180257. http://doi.org/10.1098/rsos.180257 PMid:29765698.
» http://doi.org/10.1098/rsos.180257 - ALNWANY, N., 2020. Prevalence Of hepatitis b virus Infection and associated factors Among Blood Donors In 48 Hospital Sana’a City- Yemen During 2016. Journal of Medical and Pharmaceutical Sciences, vol. 1, no. 4, pp. 111-126.
- ARAIN, M.A., LAGHARI, Z.A., SAMO, A.A., MEMON, S.F., SHAIKH, S.A. and WARSI, J., 2020. Prevalence and risk factors associated with Hepatitis B and Hepatitis C infection in Mirpurkhas, Sindh, Pakistan. Rawal Medical Journal, vol. 45, no. 4, pp. 750-754.
-
ATHALYE, S., KHARGEKAR, N., SHINDE, S., PARMAR, T., CHAVAN, S., SWAMIDURAI, G., PUJARI, V., PANALE, P., KOLI, P., SHANKARKUMAR, A. and BANERJEE, A., 2023. Exploring risk factors and transmission dynamics of Hepatitis B infection among Indian families: implications and perspective. Journal of Infection and Public Health, vol. 16, no. 7, pp. 1109-1114. http://doi.org/10.1016/j.jiph.2023.05.003 PMid:37224621.
» http://doi.org/10.1016/j.jiph.2023.05.003 -
ATHAR, M.A., XU, Y., XIE, X., XU, Z., AHMAD, V., HAYDER, Z., HUSSAIN, S.S., LIAO, Y. and LI, Q., 2015. Rapid detection of HCV genotyping 1a, 1b, 2a, 3a, 3b and 6a in a single reaction using two-melting temperature codes by a real-time PCR-based assay. Journal of Virological Methods, vol. 222, pp. 85-90. http://doi.org/10.1016/j.jviromet.2015.05.013 PMid:26068393.
» http://doi.org/10.1016/j.jviromet.2015.05.013 -
BIGNA, J.J., KENNE, A.M., HAMROUN, A., NDANGANG, M.S., FOKA, A.J., TOUNOUGA, D.N., LENAIN, R., AMOUGOU, M.A. and NANSSEU, J.R., 2019. Gender development and hepatitis B and C infections among pregnant women in Africa: a systematic review and meta-analysis. Infectious Diseases of Poverty, vol. 8, no. 1, pp. 16. http://doi.org/10.1186/s40249-019-0526-8 PMid:30827278.
» http://doi.org/10.1186/s40249-019-0526-8 - BOSAN, A., QURESHI, H., BILE, K.M., AHMAD, I. and HAFIZ, R., 2010. A review of hepatitis viral infections in Pakistan. JPMA. The Journal of the Pakistan Medical Association, vol. 60, no. 12, pp. 1045-1058. PMid:21381562.
-
CAMMAROTA, S., CITARELLA, A., GUIDA, A., CONTI, V., IANNACCONE, T., FLACCO, M.E., BRAVI, F., NACCARATO, C., PISCITELLI, A., PISCITELLI, R., VALENTE, A., CALELLA, G., COPPOLA, N. and PARRUTI, G., 2019. The inpatient hospital burden of comorbidities in HCV-infected patients: a population-based study in two Italian regions with high HCV endemicity (The BaCH study). PLoS One, vol. 14, no. 7, e0219396. http://doi.org/10.1371/journal.pone.0219396 PMid:31291351.
» http://doi.org/10.1371/journal.pone.0219396 -
COPPOLA, N., DE PASCALIS, S., ONORATO, L., CALÒ, F., SAGNELLI, C. and SAGNELLI, E., 2016. Hepatitis B virus and hepatitis C virus infection in healthcare workers. World Journal of Hepatology, vol. 8, no. 5, pp. 273-281. http://doi.org/10.4254/wjh.v8.i5.273 PMid:26925201.
» http://doi.org/10.4254/wjh.v8.i5.273 - FARHAT, M., YASMEEN, A. and AHMAD, A., 2014. An overview of hepatitis B and C in Pakistan. International Journal of Medical and Applied Sciences., vol. 1, no. 2, pp. 98-102.
-
GUPTA, E., BAJPAI, M. and CHOUDHARY, A., 2014. Hepatitis C virus: screening, diagnosis, and interpretation of laboratory assays. Asian Journal of Transfusion Science, vol. 8, no. 1, pp. 19-25. http://doi.org/10.4103/0973-6247.126683 PMid:24678168.
» http://doi.org/10.4103/0973-6247.126683 -
HAQQI, A., MUNIR, R., KHALID, M., KHURRAM, M., ZAID, M., ALI, M., SHAH, Z.H., AHMED, H. and AFZAL, M.S., 2019. Prevalence of hepatitis C virus genotypes in Pakistan: current scenario and review of literature. Viral Immunology, vol. 32, no. 9, pp. 402-413. http://doi.org/10.1089/vim.2019.0058 PMid:31556811.
» http://doi.org/10.1089/vim.2019.0058 -
INOUE, T. and TANAKA, Y., 2016. Hepatitis B virus and its sexually transmitted infection-an update. Microbial Cell, vol. 3, no. 9, pp. 420-437. http://doi.org/10.15698/mic2016.09.527 PMid:28357379.
» http://doi.org/10.15698/mic2016.09.527 - JADOON, M., SARWAR, I., HABIB, S., GUL, S. and PARVEEN, Z., 2018. Viral hepatitis among pregnant women. The Professional Medical Journal, vol. 25, no. 4, pp. 480-483. PMid:28994560.
-
JAMALI, Y.A., NOONARI, A.G., KHUHRO, A.B., KALHORO, S., SHAH, H. and GAD, A.G., 2023. Prevalence of hepatitis B and C in Pakistan from 2001 to 2022: a systematic review. Journal of Health and Rehabilitation Research, vol. 3, no. 2, pp. 316-325. http://doi.org/10.61919/jhrr.v3i2.107
» http://doi.org/10.61919/jhrr.v3i2.107 -
JINDAL, N., GOYAL, L.D. and SINGH, C., 2021. Sociodemographic features associated with hepatitis C Virus (HCV) in pregnant females: A tertiary care centre study from Malwa region of Punjab (North India). Journal of Family Medicine and Primary Care, vol. 10, no. 7, pp. 2679-2683. http://doi.org/10.4103/jfmpc.jfmpc_2372_20 PMid:34568154.
» http://doi.org/10.4103/jfmpc.jfmpc_2372_20 - JUNAID, K., TAHIR, B., MUNIR, S. and UL MUSTAFA, A., 2020. Prevalence of hepatitis B and C among different cohorts of Lahore, Pakistan. Asian Journal of Allied Health Science, vol. 2, no. 1, pp. 3-7.
- KHALID, A., ZAHID, M., ASLAM, Z., BILAL, M. and HAIDER, A., 2015. Sero-epidemiology of hepatitis B and C virus in rural population of Tehsil Samundri, District Faisalabad, Pakistan. International Journal of Virology and Molecular Biology, vol. 4, no. 2, pp. 19-22.
-
KHAN, J., SHAFIQ, M., MUSHTAQ, S., AYAZ, S., ULLAH, R., ABDEI-SALAM, N.M., FOUAD, H. and WASIM, M.A., 2014. Seropositivity and coinfection of hepatitis B and C among patients seeking hospital care in Islamabad, Pakistan. BioMed Research International, vol. 2014, pp. 516859. http://doi.org/10.1155/2014/516859 PMid:25050357.
» http://doi.org/10.1155/2014/516859 -
KHAN, N., ALI, F., BAHADAR, S., RAHMAN, K., AZIZ, A., AKBAR, N., DAUD, M., HAYAT, A. and REHMAN, M., 2017. Prevalence of hepatitis B viral infection in Punjab province of Pakistan. Pakistan Journal of Zoology, vol. 49, no. 2, pp. 1511-1513. http://doi.org/10.17582/journal.pjz/2017.49.4.sc4
» http://doi.org/10.17582/journal.pjz/2017.49.4.sc4 -
LIU, Z., SHI, O., ZHANG, T., JIN, L. and CHEN, X., 2020. Disease burden of viral hepatitis A, B, C and E: a systematic analysis. Journal of Viral Hepatitis, vol. 27, no. 12, pp. 1284-1296. http://doi.org/10.1111/jvh.13371 PMid:32741034.
» http://doi.org/10.1111/jvh.13371 -
MACROTRENDS, 2024 [viewed 9 September 2024]. Bahawalpur, Pakistan Metro area population 1950-2024 [online]. Available from: https://www.macrotrends.net/cities/22035/bahawalpur/population
» https://www.macrotrends.net/cities/22035/bahawalpur/population -
MANNS, M.P. and MAASOUMY, B., 2022. Breakthroughs in hepatitis C research: from discovery to cure. Nature Reviews. Gastroenterology & Hepatology, vol. 19, no. 8, pp. 533-550. http://doi.org/10.1038/s41575-022-00608-8 PMid:35595834.
» http://doi.org/10.1038/s41575-022-00608-8 -
MATHEW, S., FAHEEM, M., IBRAHIM, S.M., IQBAL, W., RAUFF, B., FATIMA, K. and QADRI, I., 2016. Hepatitis C virus and neurological damage. World Journal of Hepatology, vol. 8, no. 12, pp. 545-556. http://doi.org/10.4254/wjh.v8.i12.545 PMid:27134702.
» http://doi.org/10.4254/wjh.v8.i12.545 -
MEHMOOD, S., RAZA, H., ABID, F., SAEED, N., REHMAN, H.M., JAVED, S. and KHAN, M.S., 2020. National prevalence rate of hepatitis B and C in Pakistan and its risk factors. Journal of Public Health, vol. 28, no. 4, pp. 751-764. http://doi.org/10.1007/s10389-019-01081-5
» http://doi.org/10.1007/s10389-019-01081-5 -
ODUKOYA, O.O., ODEYEMI, K.A., ODUBANJO, O.M., ISIKEKPEI, B.C., IGWILO, U.U., DISU, Y.M., ROBERTS, A.A., OLUFUNLAYO, T.F., KUYINU, Y., ARIYIBI, N., EZE, U.T., AWOYALE, T., IKPEEKHA, O., ODUSANYA, O.O. and ONAJOLE, A.T., 2022. Hepatitis B and C seroprevalence among residents in Lagos State, Nigeria: a population-based survey. The Nigerian Postgraduate Medical Journal, vol. 29, no. 2, pp. 75-81. http://doi.org/10.4103/npmj.npmj_776_21 PMid:35488573.
» http://doi.org/10.4103/npmj.npmj_776_21 -
ROUDOT-THORAVAL, F., 2021. Epidemiology of hepatitis C virus infection. Clinics and Research in Hepatology and Gastroenterology, vol. 45, no. 3, pp. 101596. http://doi.org/10.1016/j.clinre.2020.101596 PMid:33610022.
» http://doi.org/10.1016/j.clinre.2020.101596 -
SAMO, A.A., LAGHARI, Z.A., BAIG, N.M. and KHOSO, G.M., 2020. Prevalence and risk factors associated with hepatitis B and C in Nawabshah, Sindh, Pakistan. The American Journal of Tropical Medicine and Hygiene, vol. 104, no. 3, pp. 1101-1105. http://doi.org/10.4269/ajtmh.20-1228 PMid:33350368.
» http://doi.org/10.4269/ajtmh.20-1228 - SAMUEL, D., MULLER, R. and ALEXANDE, G., 2004. Educational research, national hepatitis B virus programme. Infectious Diseases, vol. 234, no. 2, pp. 221-332.
-
SHAMIM, T., SUMREEN, L., SHAHEEN, G. and SHIRAZI, J.H., 2022. Incidence of hepatitis B & hepatitis C virus infections in potential blood donors In Bahawalpur Reigon, Pakistan. Plant Cell Biotechnology and Molecular Biology, vol. 23, no. 3-4, pp. 35-44. http://doi.org/10.56557/pcbmb/2022/v23i3-47403
» http://doi.org/10.56557/pcbmb/2022/v23i3-47403 -
SHAHZEB, K.S., NOOR, U. and RAFIQUE, I., 2019. Prevalence of hepatitis B and C in District Dir Upper, Khyber Pakhtunkhwa, Pakistan. Global Journal of Clinical Virology, vol. 4, no. 1, pp. 8-18. http://doi.org/10.17352/gjcv.000006
» http://doi.org/10.17352/gjcv.000006 - UMAR, M., BUSHRA, H.T., AHMAD, M., DATA, A., AHMAD, M., KHURRAM, M., USMAN, S., ARIF, M., ADAM, T., MINHAS, Z., ARIF, A., NAEEM, A., EJAZ, K., BUTT, Z. and BILAL, M., 2010. Hepatitis C in Pakistan: a review of available data. Hepatitis Monthly, vol. 10, no. 3, pp. 205-214. PMid:22308140.
-
WORLD HEALTH ORGANIZATION – WHO, 2017 [viewed 27 May 2021]. Global hepatitis report 2017 [online]. Geneve: WHO. Available from: https://www.who.int/publications-detail-redirect/9789241565455
» https://www.who.int/publications-detail-redirect/9789241565455 -
WORLD HEALTH ORGANIZATION – WHO, 2021 [viewed 27 May 2021]. Developing global health sector strategies on HIV, viral hepatitis and sexually transmitted infections for 2022-2030 [online]. Geneve: WHO. Available from: https://www.who.int/news/item/27-05-2021-developing-global-health-sector-strategies-on-hiv-viral-hepatitis-and-sexually-transmitted-infections-for-2022-2030
» https://www.who.int/news/item/27-05-2021-developing-global-health-sector-strategies-on-hiv-viral-hepatitis-and-sexually-transmitted-infections-for-2022-2030 -
WORLD HEALTH ORGANIZATION – WHO, 2022 [viewed 24 June 2022]. Hepatitis B [online]. Geneve: WHO. Available from: https://www.who.int/news-room/fact-sheets/detail/hepatitis-b
» https://www.who.int/news-room/fact-sheets/detail/hepatitis-b -
YEUNG, C.-Y., LEE, H.-C., CHAN, W.-T., JIANG, C.-B., CHANG, S.-W. and CHUANG, C.-K., 2014. Vertical transmission of hepatitis C virus: current knowledge and perspectives. World Journal of Hepatology, vol. 6, no. 9, pp. 643-651. http://doi.org/10.4254/wjh.v6.i9.643 PMid:25276280.
» http://doi.org/10.4254/wjh.v6.i9.643 -
ZHAO, K., LIU, A. and XIA, Y., 2020. Insights into hepatitis B virus DNA integration-55 years after virus discovery. The Innovation, vol. 1, no. 2, pp. 100034. http://doi.org/10.1016/j.xinn.2020.100034 PMid:34557710.
» http://doi.org/10.1016/j.xinn.2020.100034
