Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Genetic diversity of hepatitis E virus (HEV) in imported and domestic camels in Saudi Arabia

Abstract

Camels gained attention since the discovery of MERS-CoV as intermediary hosts for potentially epidemic zoonotic viruses. DcHEV is a novel zoonotic pathogen associated with camel contact. This study aimed to genetically characterize DcHEV in domestic and imported camels in Saudi Arabia. DcHEV was detected by RT-PCR in serum samples, PCR-positive samples were subjected to sequencing and phylogenetic analyses. DcHEV was detected in 1.77% of samples with higher positivity in domestic DCs. All positive imported dromedaries were from Sudan with age declining prevalence. Domestic DcHEV sequences clustered with sequences from Kenya, Somalia, and UAE while imported sequences clustered with one DcHEV isolate from UAE and both sequences clustered away from isolates reported from Pakistan. Full-genome sequences showed 24 amino acid difference with reference sequences. Our results confirm the detection of DcHEV in domestic and imported DCs. Further investigations are needed in human and camel populations to identify DcHEV potential zoonosis threat.

Introduction

Approximately 60% of all human pathogens and 75% of emerging infectious diseases are zoonotic (of animal origin). Contact with Dromedary camels (DCs) or their products was identified as major risk factor for zoonotic spillover to humans of the novel lethal coronavirus, Middle East Respiratory Syndrome Coronavirus (MERS-CoV)1,2,3,4. MERS-CoV remains in the WHO Blueprint list of priority pathogens. Since the first discovery of MERS-CoV, increasing attention is being focused on dromedary camels (DCs) as intermediary hosts for novel zoonotic viruses with epidemic potential.

Several recent reports of possible transmission of Hepatitis E Virus (HEV) to humans through consumption of animal products and/or frequent contact with animals have led to the acknowledgement of HEV as an important emerging zoonotic pathogen of humans of global public health significance5. HEV is a member of the family Hepeviridae, genus Orthohepevirus A. The virus is a common cause of acute viral hepatitis in humans, causing up to 20 million human infections annually. HEV is one of the leading causes of illness in the developing world, is endemic in Central Asia, with outbreaks reported from the Middle East and Central America. HEV has relatively high mortality rates among pregnant women and young children6,7. Chronic HEV infection can cause more severe disease in immunocompromised individuals, such as people living with HIV, organ transplants and other immunosuppressivestates8,9.

There are four main genotypes, HEV1, HEV2, HEV3 and HEV410. HEV1 and HEV2 infect only humans. HEV is shed in the stools of infected persons and is transmitted in areas with poor sanitation through contaminated water supplies. In areas with good sanitation and pure water supplies, animals are a major source of HEV infection to humans, human to human transmission is also reported through blood transfusion11. HEV has been identified in a wide range of mammals including pigs, boar, deer, rodents, ferrets, rabbits, mongoose, bats, cattle, sheep, foxes, minks, and horses12,13,14,15. HEV3 and HEV4 circulate in several animals such as pigs, wild boar, deer, other mammals and infect humans through consumption of contaminated raw or undercooked pork or game meat16. Several studies have reported serological evidence of HEV in blood donors, hemodialysis patients and blood transfusion recipients17,18,19,20. A novel HEV genotype, named Dromedary camel hepatitis E virus (DcHEV), was initially detected in dromedary camels (DCs) in the Middle East in 201421. DcHEV was first reported to cause chronic hepatitis in a transplant patient in UAE who regularly consumed camel milk and meat22. Recent studies from UAE have confirmed the presence of DcHEV-specific viral genomes in DCs23.

In Saudi Arabia and other Middle Eastern communities, camels serve considerable social and economic roles since they are used as domestic pets, reared for their milk and meat, racing and beauty contests. Saudi Arabia is the world’s largest importer of DCs from African countries, while countries of the horn of Africa are the main exporter of camels to the Arabian Peninsula2,24. In Saudi Arabia, we recently showed that the prevalence of DcHEV antibodies in domestic camels is slightly higher than in camels imported from Africa25. Identifying DcHEV genotypes and performing detailed molecular and phylogenetic characterization of the virus in DCs is critical for surveillance, understanding the evolution of human infections and designing appropriate control and preventive measures. Therefore, we performed this molecular and phylogenetic analyses of DcHEV in domestic and imported camels in Saudi Arabia.

Materials and methods

Ethical statement

Ethical permission to conduct this study was obtained from the Directorate of Agriculture, Ministry of Environment, Water and Agriculture, Jeddah, Saudi Arabia. The study was approved by the Unit of Biomedical Ethics, King Abdulaziz University Hospital, (Approval number 16-121). All methods and procedures in this study were carried out in accordance with ARRIVE guidelines and regulations.

Dromedary camels

Two cohorts of DCs were enrolled in this study. The first cohort comprised DCs imported into Saudi Arabia on incoming ships from Sudan or Djibouti at the Sea Port of Jeddah. Samples were collected over a period of 2 years from 2017 to 2019. The second cohort comprised local DCs in Jeddah, Saudi Arabia and were collected from three camel farms and from an abattoir in the city before camels were slaughtered.

All methods were carried out in accordance with relevant guidelines and regulations.

Sample collection

Jugular blood samples were collected from both cohorts of DCs. The blood samples were left to clot and then centrifuged, serum obtained and stored at − 80 °C till testing.

RNA extraction and HEV RT-PCR

Serum samples were pooled in 9 samples per pool. RNA was extracted from serum pools using the Qiaquick viral RNA extraction kit (Qiagen, Germany) according to manufacturer recommendation. Extracted RNA was subjected to real time RT-PCR using the LightMix® Modular Hepatitis E Virus (HEV) (TIB MOLBIOL, Germany). Samples in positive serum pools were tested separately to identify the positive individual sample using the same protocol.

Sequencing and phylogenetic analysis

Positive individual samples were subjected to nested RT-PCR reaction as described earlier26,27. In brief, a ~ 341 bp fragment of the HEV RNA dependent RNA polymerase (RdRp) gene was amplified and the resulting PCR product was purified using the agarose gel purification kit (Qiagen, Germany) and subjected to direct sequencing using the BigDye dideoxy termination kit on the ABI 3500 sequence analyzer (Applied Biosystems, Germany). The full genome sequencing was performed on two positive cases one imported and one domestic case. The full genome sequence was performed according to Lee et al.22. The full HEV genome was amplified in 19 fragments and the PCR products were purified from agarose gel and sequenced using the same protocol as for the RdRp fragments. The fragments were assembled using the assembly tool of the Geneious prime software (version 2021.12.2)28. The generated sequences were multiple aligned using Geneious software and phylogenetic trees were produced using the maximum likelihood method with 1000 bootstrap replicates. Sequences were deposited in Genbank and were assigned the accession numbers MZ027568–MZ027584 for the RdRp gene sequences and MW835252–MW835253 for the two full genome sequences.

Results

Camels and blood sample collection

Blood samples were collected from 1189 DCs: 893 (75.1%) were from DCs imported from Africa (724, from Sudan and 169 from Djibouti). Two hundred and ninety-six were domestic Saudi DCs from local farms and slaughterhouses in and around Jeddah. 1085 out of 1189 DCs were male (91.3%) and 104/1,189 (8.7%) were female. Nine hundred and fifty two out of 1189 (80.1%) DCs were 3–5 years old. 229 (19.2%) were between 1 and 3 years of age and 8 (0.7%) were < 1-year-old.

RT-PCR DcHEV RNA testing

RT-PCR testing of the samples showed DcHEV RNA in 21/1189 camels (1.77%) with a higher prevalence of DcHEV RNA in domestic dromedaries (12/296, 4.1%) as compared to the imported dromedaries (9/893, 1.0%), Ct values from the real time RT-PCR assay are shown in Supplementary Table 1. All positive cases were male dromedaries and all the positive imported dromedaries were imported from Sudan. The highest prevalence was found in the juvenile dromedaries < 1 year (1/8, 12.5%), followed by the age group 1–3 years (9/229, 3.9%), while the lowest prevalence was found in the age group 3–5 years (11/952, 1.2%).

Sequencing and phylogenetic analyses

Positive PCR samples were subjected to direct sequencing, and we were able to sequence 19 out of 21 (90.5%) positive samples in the RdRp gene. Phylogenetic analysis of the generated sequences showed that all sequences belong to HEV genotype 7. They clustered with sequences reported earlier mainly from UAE and Kenya. The RdRp sequences showed mutations at 95 nucleotide positions with 6 non-synonymous mutations leading to amino acid changes (Supplementary Table 2) with more frequency in domestic compared to imported dromedaries. The RdRp showed higher similarities among imported dromedary sequences compared to domestic sequences (Supplementary Fig. 1).

The full genome sequences showed clustering with the two available full genome sequences in the Genbank. They showed 242 nucleotide mutations including 24 nonsynonymous mutations that led to amino acid changes (Supplementary Table 3) along the viral genome when compared to the reference sequence KJ496143-HEV-7a.

Figure 1 shows the grouping of all sequencing with the reference sequences of HEV genotype 7 (KJ496143 and KJ496144) together with the previously reported GT-7 sequences by Rasche et al.26. Phylogenetic tree also shows the clustering of the sequences mainly with the African sequences and sequences from UAE but not with sequences from Pakistan.

Figure 1
figure 1

Phylogenetic tree for the RdRp gene of DcHEV Red-colored sequences represent domestic camels while blue colored sequences represent imported sequences. Phylogenetic tree was constructed using Maximum Likelihood method with 1000 bootstrap replicates using Geneious prime software (version 2021.2.2).

Figure 2 shows the clustering of the two full genomes generated from this study with the two available genotype 7 from Genbank.

Figure 2
figure 2

Phylogenetic tree for the two full genome sequences generated in the study. Blue-colored labels represent the new sequences from this study, while the blue-colored labels represent the two full genome reference sequences available in the Genbank. Phylogenetic tree was constructed using Maximum Likelihood method with 1000 bootstrap replicates using Geneious prime software (version 2021.2.2).

Discussion

Our data add further to the growing knowledge on the role of HEV as a possible camel associated zoonotic pathogen with epidemic potential. There are several notable findings from our study.

First, our study of DcHEV in domestic and imported DCs from Africa in Saudi Arabia is the largest published to date and provides evidence for the presence of DcHEV in both domestic and imported camels from Africa with evolving genomic changes.

Second, phylogenetic analysis of the RdRp sequences identified infection with HEV genotype 7. When comparing with HEV genotype 7 sequence KJ496144, the two full genome sequences from our study showed 242 nucleotide variations including 24 nonsynonymous mutations leading to the amino acid changes.

Third, sequences from domestic camels formed a separate cluster together with published sequences from Kenya, Somalia, and UAE.

Fourth, RdRp sequences of imported camels clustered with one DcHEV isolate previously reported from UAE. Both domestic and imported sequences clustered away from isolates reported from Pakistan. The higher number of mutations in the RdRp sequences of domestic dromedaries compared to imported dromedaries indicate a potential multiple sources of infection but this needs more studies on larger sample numbers to be confirmed. To have solid evidence of the source of HEV infection in dromedary camels in Saudi Arabia a larger number of full genome sequences need to be generated from both domestic and imported dromedaries and phylogenetically analyzed. The low volume of our serum samples did not allow for the generation of more than two full genome sequences.

Fifth, full-genome sequences generated from this study were added to the only two full-genome sequences of genotype 7 in GenBank. The analysis showed a 24 amino acid difference between our sequences and the GenBank sequences while the other 218 nucleotide mutations were synonymous mutations and did not result in amino acid changes.

Sixth, we found that domestic DCs from Saudi Arabia had higher prevalence of DcHEV RNA than imported camels from Africa.

HEV is a cause of morbidity in several regions around the world, where it is endemic in some developing countries with poor sanitation/hygiene and frequent water contamination, which are the most common risk factors29. While in developed countries like the US, Japan and Europe, the most common risk factor is the consumption of infected meat and animal products30. The zoonosis of HEV was established by the identification and characterization of HEV isolated from pigs that have close genetic relationship to human HEV31. Several other reports on the transmission of HEV to human through consumption of animal products or frequent contact with animals have led to the acknowledgement of HEV as an important human zoonosis5. HEV studies from Saudi Arabia have been scanty. One seroprevalence study in 2002 reported HEV seroprevalence ranging from (7.2% vs. 10.8%) in dialysis patients from Jeddah as compared to 16.9% and 18% HEV seroprevalence in blood donors in Jeddah (West)19 and sickle cell anemia in children from Jizan (South)17,18, respectively.

The importance of investigating HEV infection in camels in Saudi Arabia comes from the social and economic role that dromedaries play in the Arabian Peninsula. Dromedaries constitute a source of income through camel trade, camel races and camel shows and consumption of meat and milk. Camel herds frequently move across the Arabian Peninsula and might cross the borders of many Gulf countries for many reasons such as grazing, participation in camel races and camel shows. Camels’ frequent movement might increase the risk of transmitting the infection to different populations of these countries. However, there is no official national identification procedures nor obligatory vaccination campaigns focused on camels; it is difficult to quantify the extent of these movements. Camels from both UAE and Qatar travel every year during the winter seasons (November–February) for grazing, shows and racing in the Eastern region of Saudi Arabia.

The main source of dromedary camels to the Arabian Peninsula is the importation of life camels from the Horn of Africa (Sudan, Djibouti, Somalia, Ethiopia and Kenya) to the Arabian Peninsula. The importance of performing this study in Jeddah comes from the geographical location of the seaport in Jeddah as the main port of entry of dromedaries from Africa32. In 2013, official records in Saudi Arabia reported the import of 131,932 camels representing more than 70% of the animals slaughtered in the country33. Detailed spatiotemporal studies of camel movement patterns are lacking and are urgently needed to try and understand the role of camel movement in spreading the infection.

Recent studies from UAE have also identified the presence of DcHEV-specific viral genomes in DCs where calves became infected during the first 6 months of life and cleared the virus with time23. In this study, the prevalence of HEV RNA was higher in domestic camels (4.1%) compared to imported camels (0.9%). The difference might be due to the younger age of domestic camels (the majority are 1–3 years old) where they acquire the infection early in life compared to the imported camels (all are 4–5 years old) where they have most probably acquired and cleared the DcHEV infection. Alternatively, this higher prevalence might indicate a possible risk factor for the infection in domestic camels responsible for this higher prevalence. In a recent study on the same subset of samples25, we showed that the seroprevalence of DcHEV in domestic camels is slightly higher than those of imported camels (25.4% vs. 22.4%, p value = 0.3). Observations from both studies warrant the need for further investigations to identify the possible risk factor that is causing this higher prevalence.

Both domestic and imported sequences clustered away from isolates reported from Pakistan. This indicates the presence of a genetic difference between sequences from this study and those from Pakistan. Further investigation is needed to clarify the significance of these differences. Phylogenetic analysis of the RdRp sequences in this study shows that they belong to HEV genotype 7. Sequences from domestic camels formed a separate cluster with reported sequences from Kenya, Somalia, and UAE (except for three samples) while imported sequences clustered with one isolate from UAE indicating a possible common source of infection. Previous studies have demonstrated the HEV seropositive DCs in Africa and the Middle East21,25,34,35,36,37. A recent study37 showed a higher seroprevalence in dromedaries in Israel where they found a seroprevalence of 68.6%. Further investigation is needed to identify the clinical role of these amino acid changes in the course of the disease. The duration seropositivity and the protective immune mechanisms also need to be defined.

Our data should be viewed considering several limitations of our study. Whilst our DCs study sample was large, the number of positive DcHEV cases was small. The low number of domestic camels compared to imported camels could not allow for statistical significance in the differences between the two groups of camels. Pooling leads to sample dilution which might have affected prevalence. The prevalence of HEV RNA might be underestimated because lifespan of viraemia in serum is short23. Study of more full genomes would have shown better the virus evolution, and future studies are suggested.

Our results provide evidence for the presence of DcHEV in both domestic and imported camels from Africa with evolving genomic changes. Further surveillance studies are required to identify the role of the identified DcHEV amino acid changes in the course of the disease. Our data highlight the potential role of DcHEV in the burden of HEV in the Saudi population specially in populations who have frequent contact with dromedaries like camel handlers and slaughterhouse workers and those who frequently consume camel meat and milk. Any change in transmissibility and virulence of DcHEV in DCs would affect the risks of spread to humans and its potential impact on national and regional public health security. Further clinical, serological, molecular and epidemiology investigations of DcHEV in human populations in the Middle East and Africa are needed to define and monitor the potential threat of DcHEV to Middle eastern and global public health security in light of 10 million pilgrims who visit Saudi Arabia every year from 182 countries.

Data availabilitiy

Data collected for the study, on camels, and molecular analyses can be made available upon request from the corresponding author.

References

  1. Azhar, E. I. et al. Evidence for camel-to-human transmission of MERS coronavirus. N. Engl. J. Med. 370(26), 2499–2505 (2014).

    CAS  Article  Google Scholar 

  2. El-Kafrawy, S. 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 3(12), e521–e528 (2019).

    Article  Google Scholar 

  3. Memish, Z. A., Perlman, S., Van Kerkhove, M. D. & Zumla, A. Middle East respiratory syndrome. Lancet (London, England) 395(10229), 1063–1077 (2020).

    CAS  Article  Google Scholar 

  4. Abid, F. B. et al. Middle East respiratory syndrome coronavirus infection profile in Qatar: An 8-year experience. IDCases 24, e01161 (2021).

    Article  Google Scholar 

  5. Nan, Y., Wu, C., Zhao, Q. & Zhou, E. M. Zoonotic hepatitis E virus: An ignored risk for public health. Front. Microbiol. 8, 2396 (2017).

    Article  Google Scholar 

  6. Rayis, D. A., Jumaa, A. M., Gasim, G. I., Karsany, M. S. & Adam, I. An outbreak of hepatitis E and high maternal mortality at Port Sudan, Eastern Sudan. Pathog. Glob. Health 107(2), 66–68 (2013).

    Article  Google Scholar 

  7. Chaudhry, S. A., Verma, N. & Koren, G. Hepatitis E infection during pregnancy. Can. Fam. Physician 61(7), 607–608 (2015).

    PubMed  PubMed Central  Google Scholar 

  8. Miyoshi, M. et al. Chronic hepatitis E infection in a persistently immunosuppressed patient unable to be eliminated after ribavirin therapy. Intern. Med. 55(19), 2811–2817 (2016).

    Article  Google Scholar 

  9. Parvez, M. K. Chronic hepatitis E infection: Risks and controls. Intervirology 56(4), 213–216 (2013).

    CAS  Article  Google Scholar 

  10. Zhang, Y., Gong, W., Zeng, H. & Wang, L. Genetic evolution of hepatitis E virus. Adv. Exp. Med. Biol. 948, 73–88 (2016).

    Article  Google Scholar 

  11. Kamar, N. et al. Hepatitis E virus infection. Nat. Rev. Dis. Prim. 3, 17086 (2017).

    Article  Google Scholar 

  12. Raj, V. S. et al. Novel hepatitis E virus in ferrets, the Netherlands. Emerg. Infect. Dis. 18(8), 1369–1370 (2012).

    Article  Google Scholar 

  13. Krog, J. S., Breum, S. O., Jensen, T. H. & Larsen, L. E. Hepatitis E virus variant in farmed mink, Denmark. Emerg. Infect. Dis. 19(12), 2028–2030 (2013).

    Article  Google Scholar 

  14. Xia, J. et al. Swine and rabbits are the main reservoirs of hepatitis E virus in China: Detection of HEV RNA in feces of farmed and wild animals. Arch. Virol. 160(11), 2791–2798 (2015).

    CAS  Article  Google Scholar 

  15. Spahr, C., Knauf-Witzens, T., Vahlenkamp, T., Ulrich, R. G. & Johne, R. Hepatitis E virus and related viruses in wild, domestic and zoo animals: A review. Zoonoses Public Health 65(1), 11–29 (2018).

    CAS  Article  Google Scholar 

  16. Matsuda, H., Okada, K., Takahashi, K. & Mishiro, S. Severe hepatitis E virus infection after ingestion of uncooked liver from a wild boar. J. Infect. Dis. 188(6), 944 (2003).

    Article  Google Scholar 

  17. Al-Fawaz, I. et al. Hepatitis E virus infection in patients from Saudi Arabia with sickle cell anaemia and β-thalassemia major: Possible transmission by blood transfusion. J. Viral Hepat. 3(4), 203–205 (1996).

    CAS  Article  Google Scholar 

  18. Abdelaal, M. et al. Epidemiology of hepatitis E virus in male blood donors in Jeddah, Saudi Arabia. Ir. J. Med. Sci. 167(2), 94–96 (1998).

    CAS  Article  Google Scholar 

  19. Ayoola, E. A., Want, M. A., Gadour, M. O., Al-Hazmi, M. H. & Hamza, M. K. Hepatitis E virus infection in haemodialysis patients: A case-control study in Saudi Arabia. J. Med. Virol. 66(3), 329–334 (2002).

    CAS  Article  Google Scholar 

  20. Johargy, A. K., Mahomed, M. F., Khan, M. M. & Kabrah, S. Anti hepatitis E virus seropositivity in a group of male blood donors in Makkah, Saudi Arabia. J. Pak. Med. Assoc 63(2), 185–189 (2013).

    PubMed  Google Scholar 

  21. Woo, P. C. et al. New hepatitis E virus genotype in camels, the Middle East. Emerg. Infect. Dis. 20(6), 1044–1048 (2014).

    Article  Google Scholar 

  22. Lee, G. H. et al. Chronic infection with camelid hepatitis E virus in a liver transplant recipient who regularly consumes camel meat and milk. Gastroenterology 150(2), 355–7.e3 (2016).

    Article  Google Scholar 

  23. Corman, V. M. et al. Hepatitis E virus genotype 7 RNA and antibody kinetics in naturally infected dromedary calves, United Arab Emirates. Emerg. Infect. Dis. 26(9), 2214–2217 (2020).

    CAS  Article  Google Scholar 

  24. Younan, M., Bornstein, S. & Gluecks, I. V. MERS and the dromedary camel trade between Africa and the Middle East. Trop. Anim. Health Prod. 48(6), 1277–1282 (2016).

    CAS  Article  Google Scholar 

  25. El-Kafrawy, S. A. et al. Seroprevalence of dromedary camel HEV in domestic and imported camels from Saudi Arabia. Viruses 12(5), 553 (2020).

    CAS  Article  Google Scholar 

  26. Rasche, A. et al. Hepatitis E virus infection in dromedaries, North and East Africa, United Arab Emirates, and Pakistan, 1983–2015. Emerg. Infect. Dis. 22(7), 1249–1252 (2016).

    CAS  Article  Google Scholar 

  27. Drexler, J. F. et al. Bats worldwide carry hepatitis E virus-related viruses that form a putative novel genus within the family Hepeviridae. J. Virol. 86(17), 9134–9147 (2012).

    CAS  Article  Google Scholar 

  28. Kearse, M. et al. Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).

    Article  Google Scholar 

  29. Goel, A. & Aggarwal, R. Advances in hepatitis E - II: Epidemiology, clinical manifestations, treatment and prevention. Expert Rev. Gastroenterol. Hepatol. 10(9), 1065–1074 (2016).

    CAS  Article  Google Scholar 

  30. Dalton, H. R., Hunter, J. G. & Bendall, R. Autochthonous hepatitis E in developed countries and HEV/HIV coinfection. Semin. Liver Dis. 33(1), 50–61 (2013).

    CAS  Article  Google Scholar 

  31. Meng, X. J. et al. A novel virus in swine is closely related to the human hepatitis E virus. Proc. Natl. Acad. Sci. U S A 94(18), 9860–9865 (1997).

    CAS  Article  ADS  Google Scholar 

  32. Abdallah, H. R. & Faye, B. Typology of camel farming system in Saudi Arabia. Emir. J. Food Agric. 25(4), 250–260 (2013).

    Article  Google Scholar 

  33. Mackay, I. M. & Arden, K. E. Middle East respiratory syndrome: An emerging coronavirus infection tracked by the crowd. Virus Res. 202, 60–88 (2015).

    CAS  Article  Google Scholar 

  34. Li, T.-C. et al. Serological evidence of hepatitis E virus infection in dromedary camels in Ethiopia. J. Virol. Methods 246, 34–37 (2017).

    CAS  Article  Google Scholar 

  35. Obaidat, M. M. & Roess, A. A. Seroprevalence and risk factors of Hepatitis E infection in Jordan’s population: First report. Int. J. Infect. Dis. 66, 121–125 (2018).

    Article  Google Scholar 

  36. Sayed, I. M., Elkhawaga, A. A. & El-Mokhtar, M. A. Circulation of hepatitis E virus (HEV) and/or HEV-like agent in non-mixed dairy farms could represent a potential source of infection for Egyptian people. Int. J. Food Microbiol. 317, 108479 (2019).

    Article  Google Scholar 

  37. Bassal, R. et al. Seroprevalence of hepatitis E virus in dromedary camels, Bedouins, Muslim Arabs and Jews in Israel, 2009–2017. Epidemiol. Infect. 147, e92 (2019).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

The work was supported by the King Fahd Medical Research Center. Sir Prof Alimuddin Zumla, is co-Principal Investigator of the (PANDORA-ID-NET), the Pan-African Network for Rapid Research, Response, Relief and Preparedness for Infectious Disease Epidemics, supported by the EDCTP. He is in receipt of a UK National Institutes of Health Research, Senior Investigator Award and is a Mahathir Foundation Science Award laureate.

Funding

King Abdulaziz University, Jeddah, Saudi Arabia.

Author information

Authors and Affiliations

Authors

Contributions

S.A.E., V.M.C., C.D., A.Z. and E.I.A. conceptualization; S.A.E., A.M.H., M.M.E., N.A.O., A.M.T., T.A.A. methodology; S.A.E., M.M.E., A.M.H. and E.I.A. supervised the study; S.A.E., M.A., E.F., F.A.E., A.K., Z.A.M., A.Z. and E.I.A. visualization; S.A.E., M.M.E., A.M.H. data analysis; E.I.A. Fund Acquisition; S.A.E., A.Z. and E.I.A. writing the first draft; E.I.A., Facilities; All authors reviewed the manuscript.

Corresponding author

Correspondence to Esam I. Azhar.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

El-Kafrawy, S.A., Hassan, A.M., El-Daly, M.M. et al. Genetic diversity of hepatitis E virus (HEV) in imported and domestic camels in Saudi Arabia. Sci Rep 12, 7005 (2022). https://doi.org/10.1038/s41598-022-11208-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41598-022-11208-6

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing