Low Prevalence of HEV Infection and No Associated Risk of HEV Transmission from Mother to Child among Pregnant Women in Vietnam
Abstract
:1. Introduction
2. Results
2.1. Baseline Characteristics of the Study Population
2.2. Anti-HEV IgM and IgG Seroprevalence in Pregnant Women
2.3. Genotype and Phylogenetic Analysis
2.4. Correlation of Serological and Genomic Results
3. Discussion
4. Materials and Methods
4.1. Ethics Statement
4.2. Study Design
4.3. Serological Assays
4.4. HEV Nucleic Acid Testing from Sera and Stool Samples
4.5. HEV Phylogenetic Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Pallerla, S.R.; Harms, D.; Johne, R.; Todt, D.; Steinmann, E.; Schemmerer, M.; Wenzel, J.J.; Hofmann, J.; Shih, J.W.K.; Wedemeyer, H.; et al. Hepatitis E Virus Infection: Circulation, Molecular Epidemiology, and Impact on Global Health. Pathogens 2020, 9, 856. [Google Scholar] [CrossRef]
- Velavan, T.P.; Pallerla, S.R.; Johne, R.; Todt, D.; Steinmann, E.; Schemmerer, M.; Wenzel, J.J.; Hofmann, J.; Shih, J.W.K.; Wedemeyer, H.; et al. Hepatitis E: An update on One Health and clinical medicine. Liver Int. 2021, 41, 1462–1473. [Google Scholar] [CrossRef]
- Rein, D.B.; Stevens, G.A.; Theaker, J.; Wittenborn, J.S.; Wiersma, S.T. The global burden of hepatitis E virus genotypes 1 and 2 in 2005. Hepatology 2012, 55, 988–997. [Google Scholar] [CrossRef]
- Hoan, N.X.; Huy, P.X.; Sy, B.T.; Meyer, C.G.; Son, T.V.; Binh, M.T.; Giang, D.P.; Tu Anh, D.; Bock, C.T.; Wang, B.; et al. High Hepatitis E virus (HEV) Positivity Among Domestic Pigs and Risk of HEV Infection of Individuals Occupationally Exposed to Pigs and Pork Meat in Hanoi, Vietnam. Open Forum Infect. Dis. 2019, 6, ofz306. [Google Scholar] [CrossRef] [Green Version]
- Li, M.; Bu, Q.; Gong, W.; Li, H.; Wang, L.; Li, S.; Sridhar, S.; Cy Woo, P.; Wang, L. Hepatitis E virus infection and its associated adverse feto-maternal outcomes among pregnant women in Qinhuangdao, China. J. Matern. -Fetal Neonatal Med. 2020, 33, 3647–3651. [Google Scholar] [CrossRef]
- Chauhan, A.; Webb, G.; Ferguson, J. Clinical presentations of Hepatitis E: A clinical review with representative case histories. Clin. Res. Hepatol. Gastroenterol. 2019, 43, 649–657. [Google Scholar] [CrossRef]
- van Tong, H.; Hoan, N.X.; Wang, B.; Wedemeyer, H.; Bock, C.T.; Velavan, T.P. Hepatitis E Virus Mutations: Functional and Clinical Relevance. EBioMedicine 2016, 11, 31–42. [Google Scholar] [CrossRef] [Green Version]
- Nimgaonkar, I.; Ding, Q.; Schwartz, R.E.; Ploss, A. Hepatitis E virus: Advances and challenges. Nat. Rev. Gastroenterol. Hepatol. 2018, 15, 96–110. [Google Scholar] [CrossRef]
- Wu, C.; Wu, X.; Xia, J. Hepatitis E virus infection during pregnancy. Virol. J. 2020, 17, 73. [Google Scholar] [CrossRef]
- Perez-Gracia, M.T.; Suay-Garcia, B.; Mateos-Lindemann, M.L. Hepatitis E and pregnancy: Current state. Rev. Med. Virol. 2017, 27, e1929. [Google Scholar] [CrossRef]
- Yockey, L.J.; Lucas, C.; Iwasaki, A. Contributions of maternal and fetal antiviral immunity in congenital disease. Science 2020, 368, 608–612. [Google Scholar] [CrossRef]
- Talapko, J.; Mestrovic, T.; Pustijanac, E.; Skrlec, I. Towards the Improved Accuracy of Hepatitis E Diagnosis in Vulnerable and Target Groups: A Global Perspective on the Current State of Knowledge and the Implications for Practice. Healthcare 2021, 9, 133. [Google Scholar] [CrossRef] [PubMed]
- Vollmer, T.; Knabbe, C.; Dreier, J. Comparison of real-time PCR and antigen assays for detection of hepatitis E virus in blood donors. J. Clin. Microbiol. 2014, 52, 2150–2156. [Google Scholar] [CrossRef] [Green Version]
- Lee, H.S.; Dao, D.T.; Bui, V.N.; Bui, N.A.; Le, T.D.; Nguyen-Viet, H.; Grace, D.; Thakur, K.K.; Hagiwara, K. Prevalence and phylogenetic analysis of hepatitis E virus in pigs in Vietnam. BMC Vet. Res. 2020, 16, 333. [Google Scholar] [CrossRef]
- Hoan, N.X.; Tong, H.V.; Hecht, N.; Sy, B.T.; Marcinek, P.; Meyer, C.G.; Song, L.H.; Toan, N.L.; Kurreck, J.; Kremsner, P.G.; et al. Hepatitis E Virus Superinfection and Clinical Progression in Hepatitis B Patients. EBioMedicine 2015, 2, 2080–2086. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Raji, Y.E.; Toung, O.P.; Mohd Taib, N.; Sekawi, Z.B. A systematic review of the epidemiology of Hepatitis E virus infection in South—Eastern Asia. Virulence 2021, 12, 114–129. [Google Scholar] [CrossRef]
- Ahmad, T.; Hui, J.; Musa, T.H.; Behzadifar, M.; Baig, M. Seroprevalence of hepatitis E virus infection in pregnant women: A systematic review and meta-analysis. Ann. Saudi Med. 2020, 40, 136–146. [Google Scholar] [CrossRef] [Green Version]
- Lachish, T.; Erez, O.; Daudi, N.; Shouval, D.; Schwartz, E. Acute hepatitis E virus in pregnant women in Israel and in other industrialized countries. J. Clin. Virol. 2015, 73, 20–24. [Google Scholar] [CrossRef]
- Li, P.; Liu, J.; Li, Y.; Su, J.; Ma, Z.; Bramer, W.M.; Cao, W.; de Man, R.A.; Peppelenbosch, M.P.; Pan, Q. The global epidemiology of hepatitis E virus infection: A systematic review and meta-analysis. Liver Int. 2020, 40, 1516–1528. [Google Scholar] [CrossRef] [Green Version]
- Julin, C.H.; Hjortaas, K.; Dembinski, J.L.; Sandbu, S.; Øverbø, J.; Stene-Johansen, K.; Dudman, S. Hepatitis E in Pregnant Women and the Potential Use of HEV Vaccine to Prevent Maternal Infection and Mortality. Curr. Trop. Med. Rep. 2019, 6, 197–204. [Google Scholar] [CrossRef]
- Webb, G.W.; Dalton, H.R. Hepatitis E: An underestimated emerging threat. Ther. Adv. Infect. Dis. 2019, 6, 2049936119837162. [Google Scholar] [CrossRef] [Green Version]
- Bigna, J.J.; Modiyinji, A.F.; Nansseu, J.R.; Amougou, M.A.; Nola, M.; Kenmoe, S.; Temfack, E.; Njouom, R. Burden of hepatitis E virus infection in pregnancy and maternofoetal outcomes: A systematic review and meta-analysis. BMC Pregnancy Childbirth 2020, 20, 426. [Google Scholar] [CrossRef]
- Sharma, S.; Kumar, A.; Kar, P.; Agarwal, S.; Ramji, S.; Husain, S.A.; Prasad, S.; Sharma, S. Risk factors for vertical transmission of hepatitis E virus infection. J. Viral Hepat. 2017, 24, 1067–1075. [Google Scholar] [CrossRef]
- Pallerla, S.R.; Schembecker, S.; Meyer, C.G.; Linh, L.T.K.; Johne, R.; Wedemeyer, H.; Bock, C.T.; Kremsner, P.G.; Velavan, T.P. Hepatitis E virus genome detection in commercial pork livers and pork meat products in Germany. J. Viral Hepat. 2021, 28, 196–204. [Google Scholar] [CrossRef] [PubMed]
- Al-Sadeq, D.W.; Majdalawieh, A.F.; Mesleh, A.G.; Abdalla, O.M.; Nasrallah, G.K. Laboratory challenges in the diagnosis of hepatitis E virus. J. Med. Microbiol. 2018, 67, 466–480. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Q.; Zong, X.; Li, D.; Lin, J.; Li, L. Performance Evaluation of Different Commercial Serological Kits for Diagnosis of Acute Hepatitis E Viral Infection. Pol. J. Microbiol. 2020, 69, 217–222. [Google Scholar] [CrossRef] [PubMed]
- Shrestha, A.C.; Flower, R.L.; Seed, C.R.; Stramer, S.L.; Faddy, H.M. A Comparative Study of Assay Performance of Commercial Hepatitis E Virus Enzyme-Linked Immunosorbent Assay Kits in Australian Blood Donor Samples. J. Blood Transfus. 2016, 2016, 9647675. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- El Sayed Zaki, M.; El Aal, A.A.; Badawy, A.; El-Deeb, D.R.; El-Kheir, N.Y. Clinicolaboratory study of mother-to-neonate transmission of hepatitis E virus in Egypt. Am. J. Clin. Pathol. 2013, 140, 721–726. [Google Scholar] [CrossRef] [Green Version]
- Kumar, R.M.; Uduman, S.; Rana, S.; Kochiyil, J.K.; Usmani, A.; Thomas, L. Sero-prevalence and mother-to-infant transmission of hepatitis E virus among pregnant women in the United Arab Emirates. Eur. J. Obstet. Gynecol. Reprod. Biol. 2001, 100, 9–15. [Google Scholar] [CrossRef]
- Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef]
Parameters | Pregnant Women; n = 183 (%) or (IQR) |
Age (years) | |
Median (IQR) | 27.9 (24–32) |
Accommodation | |
Rural | 160 (87) |
Suburban | 23 (13) |
Source of drinking water | |
Rain | 15 (8) |
Bore/Tap | 168 (92) |
Past pregnancies | |
None | 89 (49) |
One or more | 91 (49) |
Data missing | 3 (2) |
History of abortions | |
None | 164 (90) |
One or more | 17 (9) |
Data missing | 2 (1) |
History of miscarriages | |
None | 157 (86) |
One or more | 26 (14) |
History of blood transfusion | |
No | 175 (96) |
Yes | 8 (4) |
History of jaundice | |
No | 181 (99) |
Yes | 2 (1) |
Hepatitis B virus | |
No | 179 (98) |
Yes | 4 (2) |
Full-term birth (37–42 weeks) | |
No | 38 (21) |
Yes | 145 (79) |
Postpartum jaundice | |
No | 181 (99) |
Yes | 2 (1) |
AST (normal range ≤ 37 U/L) | |
Median (IQR) | 17.23 (13–20) |
ALT (normal range ≤ 40 U/L) | |
Median (IQR) | 12.54 (9–14) |
Platelet count | |
Median (IQR) | 229 (194–258) |
Parameters | anti-HEV-negative and RNA-negative n = 161 (%)/(IQR) | anti-HEV-IgG-positive n = 14 (%)/(IQR) | anti-HEV-IgM-positive n = 4 (%)/(IQR) | HEVRNA-positive n = 4 (%)/(IQR) |
Age (years) | 27 (24–32) | 29.5 (24–35) | 28 (26–29) | 27 (24–30) |
Median (IQR) | ||||
Accommodation | ||||
Rural | 139 (86) | 13 (93) | 4 (100) | 4(100) |
Suburban | 22 (14) | 1 (7) | 0 (0) | 0 (0) |
Source of drinking water | ||||
Rain | 14 (9) | 1 (7) | 0 (0) | 0 (0) |
Bore/Tap | 147 (92) | 13 (93) | 4 (100) | 4 (100) |
Past pregnancies | ||||
None | 80 (50) | 5 (36) | 2(50) | 2 (50) |
One or more | 78 (48) | 9 (64) | 2 (50) | 2 (50) |
Data missing | ||||
History of abortions | ||||
None | 144 (89) | 13 (93) | 3 (75) | 4 (100) |
One or more | 13 (11) | 1 (7) | 1 (25) | 0 (0) |
Data missing | ||||
History of miscarriages | ||||
None | 140 (87) | 10 (71) | 4(100) | 3 (75) |
One or more | 21 (13) | 4 (29) | 0 (0) | 1 (25) |
History of blood transfusion | ||||
No | 154 (96) | 13 (93) | 4 (100) | 4 (100) |
Yes | 7 (4) | 1 (7) | 0 (0) | 0 (0) |
History of jaundice | ||||
No | 160 (99) | 13 (93) | 4 (100) | 4 (100) |
Yes | 1 (1) | 1 (7) | 0 (0) | 0 (0) |
Hepatitis B virus | ||||
No | 155 (96) | 0 (0) | 0 (0) | 0 (0) |
Yes | 4 (3) | 0 (0) | 0 (0) | 0 (0) |
Full-term birth (37–42 weeks) | ||||
No | 33 (20) | 4 (29) | 1 (25) | 0 (0) |
Yes | 128 (80) | 10 (71) | 3 (75) | 4 (100) |
Postpartum jaundice | ||||
No | 159 (99) | 14 (100) | 4 (100) | 4 (100) |
Yes | 2 (1) | 0 (0) | 0 (0) | 0 (0) |
AST (normal range ≤ 37 U /l) | 15 (13–20) | 17 (14–19) | 15 (12–17) | 21 (18-23) |
Median (IQR) | ||||
ALT (normal range ≤ 40 U /l) | 11 (9–14) | 10 (9–12) | 9 (8–22) | 14 (10–18) |
Median (IQR) | ||||
Platelet count | 231 (197–260) | 230 (171–251) | 192 (171–222) | 194 (187–216) |
Median (IQR) |
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Huy, P.X.; Chung, D.T.; Linh, D.T.; Hang, N.T.; Rachakonda, S.; Pallerla, S.R.; Linh, L.T.K.; Tong, H.V.; Dung, L.M.; Mao, C.V.; et al. Low Prevalence of HEV Infection and No Associated Risk of HEV Transmission from Mother to Child among Pregnant Women in Vietnam. Pathogens 2021, 10, 1340. https://doi.org/10.3390/pathogens10101340
Huy PX, Chung DT, Linh DT, Hang NT, Rachakonda S, Pallerla SR, Linh LTK, Tong HV, Dung LM, Mao CV, et al. Low Prevalence of HEV Infection and No Associated Risk of HEV Transmission from Mother to Child among Pregnant Women in Vietnam. Pathogens. 2021; 10(10):1340. https://doi.org/10.3390/pathogens10101340
Chicago/Turabian StyleHuy, Pham Xuan, Dang Thanh Chung, Dang Thuy Linh, Ngo Thu Hang, Sivaramakrishna Rachakonda, Srinivas Reddy Pallerla, Le Thi Kieu Linh, Hoang Van Tong, Le Minh Dung, Can Van Mao, and et al. 2021. "Low Prevalence of HEV Infection and No Associated Risk of HEV Transmission from Mother to Child among Pregnant Women in Vietnam" Pathogens 10, no. 10: 1340. https://doi.org/10.3390/pathogens10101340
APA StyleHuy, P. X., Chung, D. T., Linh, D. T., Hang, N. T., Rachakonda, S., Pallerla, S. R., Linh, L. T. K., Tong, H. V., Dung, L. M., Mao, C. V., Wedemeyer, H., Bock, C.-T., Kremsner, P. G., Song, L. H., Sy, B. T., Toan, N. L., & Velavan, T. P. (2021). Low Prevalence of HEV Infection and No Associated Risk of HEV Transmission from Mother to Child among Pregnant Women in Vietnam. Pathogens, 10(10), 1340. https://doi.org/10.3390/pathogens10101340