Seroprevalence of Dromedary Camel HEV in Domestic and Imported Camels from Saudi Arabia
Abstract
1. Introduction
2. Materials and Methods
2.1. Samples
2.2. Methodology
2.3. Ethics Statement
2.4. Statistical Analysis
3. Results
4. Discussion
Author Contributions
Funding
Conflicts of Interest
References
- Balayan, M.S.; Andjaparidze, A.G.; Savinskaya, S.S.; Ketiladze, E.S.; Braginsky, D.M.; Savinov, A.P.; Poleschuk, V.F. Evidence for a virus in non-A, non-B hepatitis transmitted via the fecal-oral route. Intervirology 1983, 20, 23–31. [Google Scholar] [PubMed]
- Cai, Y.; Qin, S.-Y.; Qian, A.; Xu, P.; Xu, Y.-T.; Xie, L.-H.; Zhao, Q.; Zhang, X.-X. Seroprevalence and risk factors of hepatitis E virus infection among the Korean, Manchu, Mongol, and Han ethnic groups in Eastern and Northeastern China. J. Med. Virol. 2017, 89, 1988–1994. [Google Scholar] [CrossRef] [PubMed]
- Obaidat, M.M.; Roess, A.A. Seroprevalence and risk factors of Hepatitis E infection in Jordan’s population: First report. Int. J. Infect. Dis. 2018, 66, 121–125. [Google Scholar] [CrossRef] [PubMed]
- Bricks, G.; Senise, J.F.; Pott Junior, H.; Grandi, G.; Passarini, A.; Caldeira, D.B.; Carnaúba Junior, D.; Moraes, H.A.B.D.; Granato, C.F.H.; Castelo, A. Seroprevalence of hepatitis E virus in chronic hepatitis C in Brazil. Braz. J. Infect. Dis. 2018, 22, 85–91. [Google Scholar] [CrossRef]
- Grabarczyk, P.; Sulkowska, E.; Gdowska, J.; Kopacz, A.; Liszewski, G.; Kubicka-Russel, D.; Baylis, S.A.; Corman, V.M.; Noceń, E.; Piotrowski, D.; et al. Molecular and serological infection marker screening in blood donors indicates high endemicity of hepatitis E virus in Poland. Transfusion 2018, 58, 1245–1253. [Google Scholar] [CrossRef]
- Farshadpour, F.; Taherkhani, R.; Ravanbod, M.R.; Eghbali, S.S.; Taherkhani, S.; Mahdavi, E. Prevalence, risk factors and molecular evaluation of hepatitis E virus infection among pregnant women resident in the northern shores of Persian Gulf, Iran. PLoS ONE 2018, 13, e0191090. [Google Scholar] [CrossRef]
- Sridhar, S.; Lau, S.K.P.; Woo, P.C.Y. Hepatitis E: A disease of reemerging importance. J. Formos. Med. Assoc. 2015, 114, 681–690. [Google Scholar] [CrossRef]
- Miyoshi, M.; Kakinuma, S.; Tanabe, Y.; Ishii, K.; Li, T.-C.; Wakita, T.; Tsuura, Y.; Watanabe, H.; Asahina, Y.; Watanabe, M.; et al. Chronic Hepatitis E Infection in a Persistently Immunosuppressed Patient Unable to Be Eliminated after Ribavirin Therapy. Intern. Med. 2016, 55, 2811–2817. [Google Scholar] [CrossRef]
- Purcell, R.H.; Emerson, S.U. Hepatitis E: An emerging awareness of an old disease. J. Hepatol. 2008, 48, 494–503. [Google Scholar] [CrossRef]
- Dagnew, M.; Belachew, A.; Tiruneh, M.; Moges, F. Hepatitis E virus infection among pregnant women in Africa: Systematic review and meta-analysis. BMC Infect. Dis. 2019, 19, 519. [Google Scholar] [CrossRef]
- Pischke, S.; Behrendt, P.; Manns, M.P.; Wedemeyer, H. HEV-associated cryoglobulinaemia and extrahepatic manifestations of hepatitis E. Lancet Infect. Dis. 2014, 14, 678–679. [Google Scholar] [CrossRef]
- Deroux, A.; Brion, J.P.; Hyerle, L.; Belbezier, A.; Vaillant, M.; Mosnier, E.; Larrat, S.; Morand, P.; Pavese, P. Association between hepatitis E and neurological disorders: Two case studies and literature review. J. Clini. Virol. 2014, 60, 60–62. [Google Scholar] [CrossRef] [PubMed]
- Meng, X.J. Hepatitis E virus: Animal reservoirs and zoonotic risk. Vet. Microbiol. 2010, 140, 256–265. [Google Scholar] [CrossRef] [PubMed]
- Lin, J.; Norder, H.; Uhlhorn, H.; Belák, S.; Widén, F. Novel hepatitis E like virus found in Swedish moose. J. General Virol. 2014, 95, 557–570. [Google Scholar] [CrossRef]
- Woo, P.C.Y.; Lau, S.K.P.; Teng, J.L.L.; Tsang, A.K.L.; Joseph, M.; Wong, E.Y.M.; Tang, Y.; Sivakumar, S.; Xie, J.; Bai, R.; et al. New hepatitis E virus genotype in camels, the Middle East. Emerg. Infect. Dis. 2014, 20, 1044–1048. [Google Scholar] [CrossRef]
- Batts, W.; Yun, S.; Hedrick, R.; Winton, J. A novel member of the family Hepeviridae from cutthroat trout (Oncorhynchus clarkii). Virus Res. 2011, 158, 116–123. [Google Scholar] [CrossRef]
- Sridhar, S.; Teng, J.L.L.; Chiu, T.-H.; Lau, S.K.P.; Woo, P.C.Y. Hepatitis E Virus Genotypes and Evolution: Emergence of Camel Hepatitis E Variants. Int. J. Mol. Sci. 2017, 18, 869. [Google Scholar] [CrossRef]
- Smith, D.B.; Simmonds, P.; Members Of The International Committee On The Taxonomy Of Viruses Hepeviridae Study, G.; Jameel, S.; Emerson, S.U.; Harrison, T.J.; Meng, X.-J.; Okamoto, H.; Van der Poel, W.H.M.; Purdy, M.A. Consensus proposals for classification of the family Hepeviridae. J. General Virol. 2014, 95, 2223–2232. [Google Scholar] [CrossRef]
- Rasche, A.; Saqib, M.; Liljander, A.M.; Bornstein, S.; Zohaib, A.; Renneker, S.; Steinhagen, K.; Wernery, R.; Younan, M.; Gluecks, I.; et al. Hepatitis E Virus Infection in Dromedaries, North and East Africa, United Arab Emirates, and Pakistan, 1983-2015. Emerg. Infect. Dis. 2016, 22, 1249–1252. [Google Scholar] [CrossRef]
- Lee, G.H.; Tan, B.H.; Teo, E.C.; Lim, S.G.; Dan, Y.Y.; Wee, A.; Aw, P.P.; Zhu, Y.; Hibberd, M.L.; Tan, C.K.; et al. Chronic Infection With Camelid Hepatitis E Virus in a Liver Transplant Recipient Who Regularly Consumes Camel Meat and Milk. Gastroenterology 2016, 150, 355–357. [Google Scholar] [CrossRef]
- Yazbek, S.; Kreidieh, K.; Ramia, S. Hepatitis E virus in the countries of the Middle East and North Africa region: An awareness of an infectious threat to blood safety. Infection 2016, 44, 11–22. [Google Scholar] [CrossRef] [PubMed]
- Corwin, A.L.; Tien, N.T.; Bounlu, K.; Winarno, J.; Putri, M.P.; Laras, K.; Larasati, R.P.; Sukri, N.; Endy, T.; Sulaiman, H.A.; et al. The unique riverine ecology of hepatitis E virus transmission in South-East Asia. Trans. R. Soc. Trop. Med. Hyg. 1999, 93, 255–260. [Google Scholar] [CrossRef]
- Pisano, M.B.; Martinez-Wassaf, M.G.; Mirazo, S.; Fantilli, A.; Arbiza, J.; Debes, J.D.; Re, V.E. Hepatitis E virus in South America: The current scenario. Liver Int. 2018, 38, 1536–1546. [Google Scholar] [CrossRef] [PubMed]
- Ghabrah, T.M.; Stickland, G.T.; Tsarev, S.; Yarbough, P.; Farci, P.; Engle, R.; Emerson, S.; Purcell, R. Acute viral hepatitis in Saudi Arabia: Seroepidemiological analysis, risk factors, clinical manifestations, and evidence for a sixth hepatitis agent. Clin. Infect. Dis. 1995, 21, 621–627. [Google Scholar] [CrossRef]
- Amer, A.F.; Zaki, S.A.; Nagati, A.M.; Darwish, M.A. Hepatitis E antibodies in Egyptian adolescent females: Their prevalence and possible relevance. J. Egypt. Public Health Assoc. 1996, 71, 273–284. [Google Scholar]
- Darwish, M.A.; Faris, R.; Clemens, J.D.; Rao, M.R.; Edelman, R. High seroprevalence of hepatitis A, B, C, and E viruses in residents in an Egyptian village in The Nile Delta: A pilot study. Am. J. Trop. Med. Hyg. 1996, 54, 554–558. [Google Scholar] [CrossRef]
- Meng, X.J.; Purcell, R.H.; Halbur, P.G.; Lehman, J.R.; Webb, D.M.; Tsareva, T.S.; Haynes, J.S.; Thacker, B.J.; Emerson, S.U. A novel virus in swine is closely related to the human hepatitis E virus. Proc. Natl. Acad. Sci. USA 1997, 94, 9860–9865. [Google Scholar] [CrossRef]
- Meng, X.-J. From barnyard to food table: The omnipresence of hepatitis E virus and risk for zoonotic infection and food safety. Virus Res. 2011, 161, 23–30. [Google Scholar] [CrossRef]
- Pavio, N.; Meng, X.-J.; Renou, C. Zoonotic hepatitis E: Animal reservoirs and emerging risks. Vet. Res. 2010, 41, 46. [Google Scholar] [CrossRef]
- Li, T.C.; Zhou, X.; Yoshizaki, S.; Ami, Y.; Suzaki, Y.; Nakamura, T.; Takeda, N.; Wakita, T. Production of infectious dromedary camel hepatitis E virus by a reverse genetic system: Potential for zoonotic infection. J. Hepatol. 2016, 65, 1104–1111. [Google Scholar] [CrossRef]
- Zhou, X.; Kataoka, M.; Liu, Z.; Takeda, N.; Wakita, T.; Li, T.C. Characterization of self-assembled virus-like particles of dromedary camel hepatitis e virus generated by recombinant baculoviruses. Virus Res. 2015, 210, 8–17. [Google Scholar] [CrossRef] [PubMed]
- Li, T.C.; Yoshizaki, S.; Zhou, X.; Sentsui, H.; Shirato, K.; Matsuyama, S.; Melaku, S.K.; Bazartseren, B.; Takeda, N.; Wakita, T. Serological evidence of hepatitis E virus infection in dromedary camels in Ethiopia. J. Virol. Methods 2017, 246, 34–37. [Google Scholar] [CrossRef] [PubMed]
- Abdelaal, M.; Zawawi, T.H.; al Sobhi, E.; Jeje, O.; Gilpin, C.; Kinsara, A.; Osoba, A.; Oni, G.A. Epidemiology of hepatitis E virus in male blood donors in Jeddah, Saudi Arabia. Ir. J. Med. Sci. 1998, 167, 94–96. [Google Scholar] [CrossRef] [PubMed]
- al-Fawaz, I.; al-Rasheed, S.; al-Mugeiren, M.; al-Salloum, A.; al-Sohaibani, M.; Ramia, S. Hepatitis E virus infection in patients from Saudi Arabia with sickle cell anaemia and beta-thalassemia major: Possible transmission by blood transfusion. J. Viral. Hepat. 1996, 3, 203–205. [Google Scholar] [CrossRef] [PubMed]
- Ayoola, E.A.; Want, M.A.; Gadour, M.O.; Al-Hazmi, M.H.; H amza, M.K. Hepatitis E virus infection in haemodialysis patients: A case-control study in Saudi Arabia. J. Med. Virol. 2002, 66, 329–334. [Google Scholar] [CrossRef] [PubMed]
- Abdallah, H.R.; Faye, B. Typology of camel farming system in Saudi Arabia. Emir. J. Food Agric. 2013, 25, 250–260. [Google Scholar]
- Younan, M.; Bornstein, S.; Gluecks, I.V. MERS and the dromedary camel trade between Africa and the Middle East. Trop. Anim. Health Prod. 2016, 48, 1277–1282. [Google Scholar] [CrossRef]
- El-Kafrawy, S.A.; Corman, V.M.; Tolah, A.M.; Al Masaudi, S.B.; Hassan, A.M.; Muller, M.A.; Bleicker, T.; Harakeh, S.M.; Alzahrani, A.A.; Alsaaidi, G.A.; et al. Enzootic patterns of Middle East respiratory syndrome coronavirus in imported African and local Arabian dromedary camels: A prospective genomic study. Lancet Planet. Health 2019, 3, e521–e528. [Google Scholar] [CrossRef]
- Himmelsbach, K.; Bender, D.; Hildt, E. Life cycle and morphogenesis of the hepatitis E virus. Emerg. Microb. Infect. 2018, 7, 196. [Google Scholar] [CrossRef]
- Khuroo, M.S.; Khuroo, M.S.; Khuroo, N.S. Hepatitis E: Discovery, global impact, control and cure. World J. Gastroenterol. 2016, 22, 7030–7045. [Google Scholar] [CrossRef]
- Dreier, J.; Knabbe, C.; Vollmer, T. Transfusion-Transmitted Hepatitis E: NAT Screening of Blood Donations and Infectious Dose. Front. Med. 2018, 5, 5. [Google Scholar] [CrossRef] [PubMed]
- Domanović, D.; Tedder, R.; Blümel, J.; Zaaijer, H.; Gallian, P.; Niederhauser, C.; Sauleda Oliveras, S.; O’Riordan, J.; Boland, F.; Harritshøj, L.; et al. Hepatitis E and blood donation safety in selected European countries: A shift to screening? Eurosurveillance 2017, 22, 30514. [Google Scholar] [CrossRef] [PubMed]
- Bassal, R.; Wax, M.; Shirazi, R.; Shohat, T.; Cohen, D.; David, D.; Abu-Mouch, S.; Abu-Ghanem, Y.; Mendelson, E.; Ben-Ari, Z.; et al. Seroprevalence of hepatitis E virus in dromedary camels, Bedouins, Muslim Arabs and Jews in Israel, 2009-2017. Epidemiol. Infect. 2019, 147, e92. [Google Scholar] [CrossRef] [PubMed]
Prevalence % (n) | ||||
---|---|---|---|---|
Total | Imported | Domestic | ||
Gender | Male | 94.81 (256) | 98 (194) | 86.11 (62) |
Female | 5.19 (14) | 2 (4) | 13.89 (10) | |
Age Group | 1–3 yrs | 20.37 (55) | 1.52 (3) | 72.22 (52) |
>3 yrs | 79.63 (215) | 98.48 (195) | 27.78 (20) | |
Collection Year | 2016 | 33.33 (90) | 45.45 (90) | 0 (0) |
2017 | 32.96 (89) | 44.95 (89) | 0 (0) | |
2018 | 33.70 (91) | 9.60 (19) | 100 (72) |
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El-Kafrawy, S.A.; Hassan, A.M.; El-Daly, M.M.; Qadri, I.; Tolah, A.M.; Al-Subhi, T.L.; Alzahrani, A.A.; Alsaaidi, G.A.; Al-Abdullah, N.; Kaki, R.M.; et al. Seroprevalence of Dromedary Camel HEV in Domestic and Imported Camels from Saudi Arabia. Viruses 2020, 12, 553. https://doi.org/10.3390/v12050553
El-Kafrawy SA, Hassan AM, El-Daly MM, Qadri I, Tolah AM, Al-Subhi TL, Alzahrani AA, Alsaaidi GA, Al-Abdullah N, Kaki RM, et al. Seroprevalence of Dromedary Camel HEV in Domestic and Imported Camels from Saudi Arabia. Viruses. 2020; 12(5):553. https://doi.org/10.3390/v12050553
Chicago/Turabian StyleEl-Kafrawy, Sherif Aly, Ahmed Mohamed Hassan, Mai Mohamed El-Daly, Ishtiaq Qadri, Ahmed Majdi Tolah, Tagreed Lafi Al-Subhi, Abdulrahman A. Alzahrani, Ghaleb A. Alsaaidi, Nabeela Al-Abdullah, Reham Mohammed Kaki, and et al. 2020. "Seroprevalence of Dromedary Camel HEV in Domestic and Imported Camels from Saudi Arabia" Viruses 12, no. 5: 553. https://doi.org/10.3390/v12050553
APA StyleEl-Kafrawy, S. A., Hassan, A. M., El-Daly, M. M., Qadri, I., Tolah, A. M., Al-Subhi, T. L., Alzahrani, A. A., Alsaaidi, G. A., Al-Abdullah, N., Kaki, R. M., Li, T.-C., & Azhar, E. I. (2020). Seroprevalence of Dromedary Camel HEV in Domestic and Imported Camels from Saudi Arabia. Viruses, 12(5), 553. https://doi.org/10.3390/v12050553