One-Year Investigation of Hepatitis A Virus and Rotavirus in Two Waste Water Treatment Plants in Egypt

Sahar Abd Al-Daim*

Sahar Abd Al-Daim*

Volume5-Issue2
Dates: Received: 2023-12-26 | Accepted: 2024-02-01 | Published: 2024-02-03
Pages: 106-116

Abstract

Background: Waterborne enteric viruses are evolving source of disease outbreaks and represent a major threat to global public health. The repetitive assessment of water environments is necessary to manage enteric virus-mediated fecal infection and the probable emergence of different variants.

Methods: Here, we detected human rotavirus and hepatitis A virus circulating in two wastewater treatment plants, for one year in sewage and sludge samples from two largest wastewater treatment plant (El-Gabal El-Asfar and Zenin) located in Egypt. For this purpose, we examine predefined viruses' prevalence in 72 samples (24 raw sewage samples, 24 treated effluent samples, and 24 sludge) collected from August 2022 to July 2023. Viral RNA was extracted and detected by nested Reverse Transcriptase-Polymerase Chain Reaction (RT-PCR) in case of HAV and by multiplex semi nested RT-PCR In case of rotavirus with the

Results: Percentage of detection rate 58.3%, 25% 41.6%, 50%, 16.6%58.6%, 41.6%, 8.3%, 41.6%41.6%, 8.3% and 41.6% for inlet, outlet, sludge in WWTP zenin and WWTP El-Gabal El-Asfar for HAV, RV respectively. Using generic primer result indicated G1P8 was the most common although G2P [4], G1, G2, G3P? G9P [8], G9P [11], G1 P [4] were detected with different percentage.

Conclusion: These results demonstrated that HAV and RV still remains in the environment after sewage treatment and could play an important role in maintaining the endemicity of HAV and RV infection. Routine and continuous monitoring of waterborne viruses are most useful approach to understand disease occurrence in communities.

FullText HTML FullText PDF DOI: 10.37871/jbres1877

Certificate of Publication

Copyright

How to cite this article

Al-Daim SA. One-Year Investigation of Hepatitis A Virus and Rotavirus in Two Waste Water Treatment Plants in Egypt. J Biomed Res Environ Sci. 2024 Feb 03; 5(2): 106-116. doi: 10.37871/jbres1877, Article ID: JBRES1877, Available at: https://www. jelsciences.com/articles/jbres1877.pdf

Subject area(s)

Infectious Diseases

Virology

References

Nicole SU, Garry AL, Caroline K. Occurrence of Human Enteric Viruses in Water Sources and Shellfish: A Focus on Africa, Food and Environmental Virology. 2021;13:1-31. doi: 10.1007/s12560-020-09456-8.
Kitajima M, Gerba CP. Aichi virus 1: environmental occurrence and behavior. Pathogens. 2015 May 19;4(2):256-68. doi: 10.3390/pathogens4020256. PMID: 25996404; PMCID: PMC4493473.
Global Hepatitis Report Geneva. WHO. 2017.
Lemon SM, Ott JJ, Van Damme P, Shouval D. Type A viral hepatitis: A summary and update on the molecular virology, epidemiology, pathogenesis and prevention. J Hepatol. 2017 Sep 5:S0168-8278(17)32278-X. doi: 10.1016/j.jhep.2017.08.034. Epub ahead of print. PMID: 28887164.
Aboubakr H, Goyal S. Involvement of Egyptian Foods in Foodborne Viral Illnesses: The Burden on Public Health and Related Environmental Risk Factors: An Overview. Food Environ Virol. 2019 Dec;11(4):315-339. doi: 10.1007/s12560-019-09406-z. Epub 2019 Sep 27. PMID: 31560123.
Progress on Household Drinking Water, Sanitation and Hygiene 2000-2017. Special Focus on Inequalities. United Nations Children’s Fund (UNICEF) and World Health Organization. New York. 2019.
Taylor MB, Cox N, Vrey MA, Grabow WO. The occurrence of hepatitis A and astroviruses in selected river and dam waters in South Africa. Water Res. 2001 Aug;35(11):2653-60. doi: 10.1016/s0043-1354(00)00551-0. PMID: 11456164.
Bivins A, North D, Ahmad A, Ahmed W, Alm E, Been F, Bhattacharya P, Bijlsma L, Boehm AB, Brown J, Buttiglieri G, Calabro V, Carducci A, Castiglioni S, Cetecioglu Gurol Z, Chakraborty S, Costa F, Curcio S, de Los Reyes FL 3rd, Delgado Vela J, Farkas K, Fernandez-Casi X, Gerba C, Gerrity D, Girones R, Gonzalez R, Haramoto E, Harris A, Holden PA, Islam MT, Jones DL, Kasprzyk-Hordern B, Kitajima M, Kotlarz N, Kumar M, Kuroda K, La Rosa G, Malpei F, Mautus M, McLellan SL, Medema G, Meschke JS, Mueller J, Newton RJ, Nilsson D, Noble RT, van Nuijs A, Peccia J, Perkins TA, Pickering AJ, Rose J, Sanchez G, Smith A, Stadler L, Stauber C, Thomas K, van der Voorn T, Wigginton K, Zhu K, Bibby K. Wastewater-Based Epidemiology: Global Collaborative to Maximize Contributions in the Fight Against COVID-19. Environ Sci Technol. 2020 Jul 7;54(13):7754-7757. doi: 10.1021/acs.est.0c02388. Epub 2020 Jun 12. PMID: 32530639.
Kamel AH, Ali MA, El-Nady HG, Deraz A, Aho S, Pothier P, Belliot G. Presence of enteric hepatitis viruses in the sewage and population of Greater Cairo. Clin Microbiol Infect. 2011 Aug;17(8):1182-5. doi: 10.1111/j.1469-0691.2011.03461.x. Epub 2011 Mar 7. PMID: 21375654.
Rodrígue, RA, Pepper ILA, Gerba CP. Application of PCR-based methods to assess the infectivity of enteric viruses in environmental samples. Applied and Environmental Microbiology. 2009;75(2):297-307. doi: 10.1128/AEM.01150-08.
Petrignani M, Verhoef L, de Graaf M, Richardus JH, Koopmans M. Chronic sequelae and severe complications of norovirus infection: A systematic review of literature. J Clin Virol. 2018 Aug;105:1-10. doi: 10.1016/j.jcv.2018.05.004. Epub 2018 May 24. PMID: 29804008.
Pintó RM, Alegre D, Domínguez A, El-Senousy WM, Sánchez G, Villena C, Costafreda MI, Aragonès L, Bosch A. Hepatitis A virus in urban sewage from two Mediterranean countries. Epidemiol Infect. 2007 Feb;135(2):270-3. doi: 10.1017/S0950268806006753. Epub 2006 Jul 3. PMID: 16817987; PMCID: PMC2870566.
Rachida S, Matsapola PN, Wolfaardt M, Taylor MB. Genetic characterization of a novel hepatitis a virus strain in irrigation water in South Africa. J Med Virol. 2016 Apr;88(4):734-7. doi: 10.1002/jmv.24370. Epub 2015 Sep 21. PMID: 26331799.
Ouardani I, Manso CF, Aouni M, Romalde JL. Efficiency of hepatitis A virus removal in six sewage treatment plants from central Tunisia. Appl Microbiol Biotechnol. 2015 Dec;99(24):10759-69. doi: 10.1007/s00253-015-6902-9. Epub 2015 Aug 19. PMID: 26286509.
Goel AK, Chawla S, Dhingra A, Thiyagarajan V, Nair NP. Rotavirus Diarrhea and its Determinants Among Under-Five Children Admitted in a Tertiary Care Hospital of Southern Haryana, India. Indian J Pediatr. 2021 Mar;88(Suppl 1):16-21. doi: 10.1007/s12098-020-03616-1. Epub 2021 Jan 27. PMID: 33501607.
Greenberg HB, Estes MK. Rotaviruses: from pathogenesis to vaccination. Gastroenterology. 2009 May;136(6):1939-51. doi: 10.1053/j.gastro.2009.02.076. Epub 2009 May 7. PMID: 19457420; PMCID: PMC3690811.
Pinon A, Vialette M. Survival of Viruses in Water. Intervirology. 2018;61(5):214-222. doi: 10.1159/000484899. Epub 2018 Jan 10. PMID: 29316545.
Meng ZD, Birch C, Heath R, Gust I. Physicochemical stability and inactivation of human and simian rotaviruses. Appl Environ Microbiol. 1987 Apr;53(4):727-30. doi: 10.1128/aem.53.4.727-730.1987. PMID: 3034154; PMCID: PMC203745.
Dbaibo G, Rajab M, Inati A, Mikhael R, Choueiry E, Al-Tannir M, Salam O, Ramakrishnan G, DeAntonio R. Hospital-based surveillance study of rotavirus gastroenteritis in children under 5 years of age in Lebanon. Trials Vaccinol. 2013;2:25-30. doi: 10.1016/j.trivac.2013.08.002.
Bányai K, Estes MK, Martella V, Parashar UD. Viral gastroenteritis. Lancet. 2018 Jul 14;392(10142):175-186. doi: 10.1016/S0140-6736(18)31128-0. Epub 2018 Jun 29. PMID: 30025810; PMCID: PMC8883799.
Ahmed W, Payyappat S, Cassidy M, Harrison N, Besley C. Sewage-associated marker genes illustrate the impact of wet weather overflows and dry weather leakage in urban estuarine waters of Sydney, Australia. Sci Total Environ. 2020 Feb 25;705:135390. doi: 10.1016/j.scitotenv.2019.135390. Epub 2019 Nov 23. PMID: 31838427.
Hassard F, Gwyther CL, Farkas K, Andrews A, Jones V, Cox B, Brett H, Jones DL, McDonald JE, Malham SK. Abundance and Distribution of Enteric Bacteria and Viruses in Coastal and Estuarine Sediments-a Review. Front Microbiol. 2016 Nov 1;7:1692. doi: 10.3389/fmicb.2016.01692. PMID: 27847499; PMCID: PMC5088438.
Chigor VN, Sibanda T, Okoh AI. Assessment of the risks for human health of adenoviruses, hepatitis A virus, rotaviruses and enteroviruses in the Buffalo River and three source water dams in the Eastern Cape. Food Environ Virol. 2014 Jun;6(2):87-98. doi: 10.1007/s12560-014-9138-4. Epub 2014 Mar 28. PMID: 24676673.
Iritani N, Kaida A, Abe N, Kubo H, Sekiguchi J, Yamamoto SP, Goto K, Tanaka T, Noda M. Detection and genetic characterization of human enteric viruses in oyster-associated gastroenteritis outbreaks between 2001 and 2012 in Osaka City, Japan. J Med Virol. 2014 Dec;86(12):2019-25. doi: 10.1002/jmv.23883. Epub 2014 Jan 10. PMID: 24415518.
Latif EF. Applying novel methods in conventional activated sludge plants to treat low-strength wastewater. Environmental Monitoring and Assessment. 2022;194:323. doi: 10.1007/s10661-022-09968-9.
Rose JB, Singh SN, Gerba CP, Kelley LM. Comparison of microporous filters for concentration of viruses from wastewater. Appl Environ Microbiol. 1984 May;47(5):989-92. doi: 10.1128/aem.47.5.989-992.1984. PMID: 6742838; PMCID: PMC240036.
Katzenelson E, Fattal B, Hostovesky T. Organic flocculation: an efficient second-step concentration method for the detection of viruses in tap water. Appl Environ Microbiol. 1976 Oct;32(4):638-9. doi: 10.1128/aem.32.4.638-639.1976. PMID: 10841; PMCID: PMC170320.
Villar LM, Morais LM, Aloise R, Melo MM, Calado IA, Lampe E, Gaspar AM. Co-circulation of genotypes IA and IB of hepatitis A virus in Northeast Brazil. Braz J Med Biol Res. 2006 Jul;39(7):873-81. doi: 10.1590/s0100-879x2006000700004. PMID: 16862277.
Iturriza-Gómara M, Isherwood B, Desselberger U, Gray J. Reassortment in vivo: driving force for diversity of human rotavirus strains isolated in the United Kingdom between 1995 and 1999. J Virol. 2001 Apr;75(8):3696-705. doi: 10.1128/JVI.75.8.3696-3705.2001. PMID: 11264359; PMCID: PMC114861.
Iturriza-Gómara M, Kang G, Gray J. Rotavirus genotyping: keeping up with an evolving population of human rotaviruses. J Clin Virol. 2004 Dec;31(4):259-65. doi: 10.1016/j.jcv.2004.04.009. PMID: 15494266.
Gouvea V, Glass RI, Woods P, Taniguchi K, Clark HF, Forrester B, Fang ZY. Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol. 1990 Feb;28(2):276-82. doi: 10.1128/jcm.28.2.276-282.1990. PMID: 2155916; PMCID: PMC269590.
Gentsch JR, Glass RI, Woods P, Gouvea V, Gorziglia M, Flores J, Das BK, Bhan MK. Identification of group A rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol. 1992 Jun;30(6):1365-73. doi: 10.1128/jcm.30.6.1365-1373.1992. PMID: 1320625; PMCID: PMC265294.
Gómara MI, Cubitt D, Desselberger U, Gray J. Amino acid substitution within the VP7 protein of G2 rotavirus strains associated with failure to serotype. J Clin Microbiol. 2001 Oct;39(10):3796-8. doi: 10.1128/JCM.39.10.3796-3798.2001. PMID: 11574622; PMCID: PMC88438.
Malik A, Yasar A, Tabinda A, Abubakar M. Water-borne diseases, cost of illness and willingness to pay for diseases interventions in rural communities of developing countries. Iran J Public Health. 2012;41(6):39-49. Epub 2012 Jun 30. PMID: 23113192; PMCID: PMC3469006.
Ruggeri FM, Bonomo P, Ianiro G, Battistone A, Delogu R, Germinario C, Chironna M, Triassi M, Campagnuolo R, Cicala A, Giammanco GM, Castiglia P, Serra C, Gaggioli A, Fiore L. Rotavirus genotypes in sewage treatment plants and in children hospitalized with acute diarrhea in Italy in 2010 and 2011. Appl Environ Microbiol. 2015 Jan;81(1):241-9. doi: 10.1128/AEM.02695-14. Epub 2014 Oct 24. PMID: 25344240; PMCID: PMC4272723.
World health statistics: monitoring health for the SDGs. Geneva: WHO. 2018.
La Rosa G, Fratini M, della Libera S, Iaconelli M, Muscillo M. Emerging and potentially emerging viruses in water environments. Ann Ist Super Sanita. 2012;48(4):397-406. doi: 10.4415/ANN_12_04_07. PMID: 23247136.
Allen WE, Altae-Tran H, Briggs J, Jin X, McGee G, Shi A, Raghavan R, Kamariza M, Nova N, Pereta A, Danford C, Kamel A, Gothe P, Milam E, Aurambault J, Primke T, Li W, Inkenbrandt J, Huynh T, Chen E, Lee C, Croatto M, Bentley H, Lu W, Murray R, Travassos M, Coull BA, Openshaw J, Greene CS, Shalem O, King G, Probasco R, Cheng DR, Silbermann B, Zhang F, Lin X. Population-scale longitudinal mapping of COVID-19 symptoms, behaviour and testing. Nat Hum Behav. 2020 Sep;4(9):972-982. doi: 10.1038/s41562-020-00944-2. Epub 2020 Aug 26. PMID: 32848231; PMCID: PMC7501153.
Beetz C, Skrahina V, Förster TM, Gaber H, Paul JJ, Curado F, Rolfs A, Bauer P, Schäfer S, Weckesser V, Lieu V, Radefeldt M, Pöppel C, Krake S, Kandaswamy KK, Bruesehafer K, Vogel F.Rapid Large-Scale COVID-19 Testing during Shortages. Diagnostics. 2020;10(7). doi: 10.3390/diagnostics10070464.
Boehm AB, Hughes B, Duong D, Chan-Herur V, Buchman A, Wolfe MK, White BJ. Wastewater concentrations of human influenza, metapneumovirus, parainfluenza, respiratory syncytial virus, rhinovirus, and seasonal coronavirus nucleic-acids during the COVID-19 pandemic: a surveillance study. Lancet Microbe. 2023 May;4(5):e340-e348. doi: 10.1016/S2666-5247(22)00386-X. Epub 2023 Mar 22. PMID: 36965504; PMCID: PMC10032662.
Bidawid S, Farber JM, Sattar SA. Contamination of foods by food handlers: experiments on hepatitis A virus transfer to food and its interruption. Appl Environ Microbiol. 2000 Jul;66(7):2759-63. doi: 10.1128/AEM.66.7.2759-2763.2000. PMID: 10877765; PMCID: PMC92070.
Forés E, Rusiñol M, Itarte M, Martínez-Puchol S, Calvo M, Bofill-Mas S. Evaluation of a virus concentration method based on ultrafiltration and wet foam elution for studying viruses from large-volume water samples. Sci Total Environ. 2022 Jul 10;829:154431. doi: 10.1016/j.scitotenv.2022.154431. Epub 2022 Mar 9. PMID: 35278558.
Abd El-Daim SE, Mohamed Shaheen NF, Hosseney EN, Elhosainy AM, Nehal IA, Elmahdy ME, Ali MA. Molecular detection and genotyping of group a rotavirus by multiplex semi-nested rt-pcr in sewage water and sludge. Journal of Microbiology & Biotechnology. 2019;4(1):2576-7771. doi: 10.23880/oajmb-16000141.
Hassine-Zaafrane M, Kaplon J, Ben Salem I, Sdiri-Loulizi K, Sakly N, Pothier P, Aouni M, Ambert-Balay K. Detection and genotyping of group A rotaviruses isolated from sewage samples in Monastir, Tunisia between April 2007 and April 2010. J Appl Microbiol. 2015 Nov;119(5):1443-53. doi: 10.1111/jam.12920. Epub 2015 Sep 24. PMID: 26248601.
Dubois E, Le Guyader F, Haugarreau L, Kopecka H, Cormier M, Pommepuy M. Molecular epidemiological survey of rotaviruses in sewage by reverse transcriptase seminested PCR and restriction fragment length polymorphism assay. Appl Environ Microbiol. 1997 May;63(5):1794-800. doi: 10.1128/aem.63.5.1794-1800.1997. PMID: 9143113; PMCID: PMC168473.
Shaheen MNF, Abd El-Daim SA, Ahmed NI, Elmahdy EM. Molecular detection of three gastroenteritis viruses in urban sewage treatment plant and river water in Egypt. Egypt. J. Aquat. Biol. Fish. 2018;22(5):615-627. doi: 10.21608/EJABF.2018.60278.
Frank C, Walter J, Muehlen M, Jansen A, van Treeck U, Hauri AM, Zoellner I, Rakha M, Hoehne M, Hamouda O, Schreier E, Stark K. Major outbreak of hepatitis A associated with orange juice among tourists, Egypt, 2004. Emerg Infect Dis. 2007 Jan;13(1):156-8. doi: 10.3201/eid1301.060487. PMID: 17370535; PMCID: PMC2725821.
MacDonald E, Steens A, Stene-Johansen K, Gillesberg Lassen S, Midgley S, Lawrence J, Crofts J, Ngui SL, Balogun K, Frank C, Faber M, Gertler M, Verhoef L, Koopmans M, Sane J, van Pelt W, Sundqvist L, Vold L. Increase in hepatitis A in tourists from Denmark, England, Germany, the Netherlands, Norway and Sweden returning from Egypt, November 2012 to March 2013. Euro Surveill. 2013 Apr 25;18(17):20468. Erratum in: Euro Surveill. 2013;18(18). pii: 20473. PMID: 23647624.
Divizia M, Gabrieli R, Stefanoni ML, Renganathan E, El Ghazzawi E, Kader OA, Gamil F, El Sawaf G, El Sherbini E, Saleh E, Degener AM, Noce A, Zaratti L, Modesti A, Panà A. HAV and HEV infection in hospitalised hepatitis patients in Alexandria, Egypt. Eur J Epidemiol. 1999 Aug;15(7):603-9. doi: 10.1023/a:1007514030062. PMID: 10543349.
Hamza H, Abd-Elshafy DN, Fayed SA, Bahgat MM, El-Esnawy NA, Abdel-Mobdy E. Detection and characterization of hepatitis A virus circulating in Egypt. Arch Virol. 2017 Jul;162(7):1921-1931. doi: 10.1007/s00705-017-3294-4. Epub 2017 Mar 16. PMID: 28303345.
Miagostovich MP, Ferreira FF, Guimarães FR, Fumian TM, Diniz-Mendes L, Luz SL, Silva LA, Leite JP. Molecular detection and characterization of gastroenteritis viruses occurring naturally in the stream waters of Manaus, central Amazonia, Brazil. Appl Environ Microbiol. 2008 Jan;74(2):375-82. doi: 10.1128/AEM.00944-07. Epub 2007 Dec 7. PMID: 18065620; PMCID: PMC2223260.
Villena C, El-Senousy WM, Abad FX, Pintó RM, Bosch A. Group A rotavirus in sewage samples from Barcelona and Cairo: emergence of unusual genotypes. Appl Environ Microbiol. 2003 Jul;69(7):3919-23. doi: 10.1128/AEM.69.7.3919-3923.2003. PMID: 12839761; PMCID: PMC165171.
Rodríguez-Díaz J, Querales L, Caraballo L, Vizzi E, Liprandi F, Takiff H, Betancourt WQ. Detection and characterization of waterborne gastroenteritis viruses in urban sewage and sewage-polluted river waters in Caracas, Venezuela. Appl Environ Microbiol. 2009 Jan;75(2):387-94. doi: 10.1128/AEM.02045-08. Epub 2008 Nov 21. PMID: 19028907; PMCID: PMC2620703.