Evaluation of hepatitis E virus RNA persistence in experimentally contaminated cured pork liver sausages

Submitted: 15 January 2024
Accepted: 11 March 2024
Published: 2 April 2024
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Hepatitis E is a disease sustained by RNA viruses, which have four different genotypes, all of which are responsible for acute forms of hepatitis. Genotypes 1 and 2 infect only humans, causing epidemics mainly transmitted by contaminated water, while genotypes 3 and 4 are zoonotic, and the infection is linked to the consumption of raw or undercooked meat or meat products. Hepatitis E virus (HEV) genotypes 3 and 4 have been detected in domestic Suidae, considered the asymptomatic reservoir of HEV, and in wild animals such as wild boar and deer. Despite scientific studies that have highlighted the presence of HEV in cured meat products, such as pork liver sausages, the viral persistence in the different production steps of curing has not been evaluated. Therefore, this study aimed to evaluate the persistence of HEV genotype 3 during the different curing and storage times of experimentally contaminated pork liver sausages using biomolecular methods. The sausages tested positive at all curing and storage times. This study confirms the potential risk attributed to pork liver sausages in HEV transmission. However, to guarantee an efficient risk assessment, future studies will be performed to correlate the presence of HEV RNA with infectious viral particles.

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Barnaud E, Rogée S, Garry P, Rose N, Pavio N, 2012. Thermal inactivation of infectious hepatitis E virus in experimentally contaminated food. Appl Environ Microbiol 78:5153-9. DOI: https://doi.org/10.1128/AEM.00436-12
Bosch A, Gkogka E, Le Guyader FS, Loisy-Hamon F, Lee A, van Lieshout L, Marthi B, Myrmel M, Sansom A, Schultz AC, Winkler A, Zuber S, Phister T, 2018. Foodborne viruses: detection, risk assessment, and control options in food processing. Int J Food Microbiol 285:110-28. DOI: https://doi.org/10.1016/j.ijfoodmicro.2018.06.001
Boxman ILA, Jansen CCC, Hägele G, Zwartkruis-Nahuis A, Tijsma ASL, Vennema H, 2019. Monitoring of pork liver and meat products on the Dutch market for the presence of HEV RNA. Int J Food Microbiol 296:58-64. DOI: https://doi.org/10.1016/j.ijfoodmicro.2019.02.018
Colavita G, 2023. Igiene e tecnologie degli alimenti. Point Veterinaire Italie, Milan, Italia.
Colson P, Borentain P, Queyriaux B, Kaba M, Moal V, Gallian P, Heyries L, Raoult D, Gerolami R, 2010. Pig liver sausage as a source of hepatitis E virus transmission to humans. J Infect Dis 202: 825-34. DOI: https://doi.org/10.1086/655898
Deest G, Zehner L, Nicand E, Gaudy-Graffin C, Goudeau A, Bacq Y, 2007. Autochthonous hepatitis E in France and consumption of raw pig meat. Gastroenterol Clin Biol 31:1095-7. DOI: https://doi.org/10.1016/S0399-8320(07)78342-2
Di Bartolo I, Angeloni G, Ponterio E, Ostanello F, Ruggeri FM, 2015. Detection of hepatitis E virus in pork liver sausages. Int J Food Microbiol 193:29-33. DOI: https://doi.org/10.1016/j.ijfoodmicro.2014.10.005
Di Pasquale S, De Santis P, La Rosa G, Di Domenico K, Iaconelli M, Micarelli G, Martini E, Bilei S, De Medici D, Suffredini E, 2019. Quantification and genetic diversity of Hepatitis E virus in wild boar (Sus scrofa) hunted for domestic consumption in Central Italy. Food Microbiol 82: 194-201. DOI: https://doi.org/10.1016/j.fm.2019.02.005
Drexler JF, Seelen A, Corman VM, Fumie Tateno A, Cottontail V, Melim Zerbinati R, Gloza-Rausch F, Klose SM, Adu-Sarkodie Y, Oppong SK, Kalko EKV, Osterman A, Rasche A, Adam A, Müller MA, Ulrich RG, Leroy EM, Lukashev AN, Drosten C, 2012. Bats worldwide carry hepatitis E virus-related viruses that form a putative novel genus within the family Hepeviridae. J Virol 86. DOI: https://doi.org/10.1128/JVI.00800-12
Garbuglia AR, Bruni R, Villano U, Vairo F, Lapa D, Madonna E, Picchi G, Binda B, Mariani R, De Paulis F, D’amato S, Grimaldi A, Scognamiglio P, Capobianchi MR, Ciccaglione AR, 2021. Hepatitis E outbreak in the central part of Italy sustained by multiple HEV genotype 3 strains, June-December 2019. Viruses 13:1159. DOI: https://doi.org/10.3390/v13061159
Garbuglia AR, Scognamiglio P, Petrosillo N, Mastroianni CM, Sordillo P, Gentile D, La Scala P, Girardi E, Capobianchi MR, 2013. Hepatitis E virus genotype 4 outbreak, Italy, 2011. Emerg Infect Dis 19:110-4. DOI: https://doi.org/10.3201/eid1901.120983
Giannini P, Jermini M, Leggeri L, Nüesch-Inderbinen M, Stephan R, 2018. Detection of hepatitis E virus RNA in raw cured sausages and raw cured sausages containing pig liver at retail stores in Switzerland. J Food Prot 81:43-5. DOI: https://doi.org/10.4315/0362-028X.JFP-17-270
Hakim MS, Wang W, Bramer WM, Geng J, Huang F, de Man RA, Peppelenbosch MP, Pan Q, 2017. The global burden of hepatitis E outbreaks: a systematic review. Liver Int 37:19-31. DOI: https://doi.org/10.1111/liv.13237
International Committee on Taxonomy of Viruses, n.d. Subfamily: Orthohepevirinae Genus: Paslahepevirus. Available from: https://ictv.global/report/chapter/hepeviridae/hepeviridae/orthohepevirinae/paslahepevirus. Accessed on: 27/12/2023.
Istituto Superiore di Sanità, n.d. Epatite virale. Available from: https://www.epicentro.iss.it/epatite/dati-seieva. Accessed on: 27/12/23. [Material in Italian].
Johne R, Reetz J, Ulrich RG, Machnowska P, Sachsenröder J, Nickel P, Hofmann J, 2014. An ORF1-rearranged hepatitis E virus derived from a chronically infected patient efficiently replicates in cell culture. J Viral Hepatitis 21:447-56. DOI: https://doi.org/10.1111/jvh.12157
Johne R, Trojnar E, Filter M, Hofmann J, 2016. Thermal stability of hepatitis E virus as estimated by a cell culture method. Appl Environ Microbiol 82:4225-31. DOI: https://doi.org/10.1128/AEM.00951-16
Kamar N, Dalton HR, Abravanel F, Izopet J, 2014. Hepatitis E virus infection. Clin Microbiol Rev 27:116-38. DOI: https://doi.org/10.1128/CMR.00057-13
Lenti R, 2022. Rapporto Annuale 2022. Available from: https://www.assica.it/news/#rapporto-annuale.
Lorusso P, Bonerba E, Pandiscia A, Mottola A, Di Pinto A, Piredda R, Terio V, 2022. Occurrence of hepatitis E virus (HEV) in Calabrian wild boars. Int J Food Microbiology 371:109671. DOI: https://doi.org/10.1016/j.ijfoodmicro.2022.109671
Martínez-Martínez M, Diez-Valcarce M, Cook N, Hernández M, Rodríguez-Lázaro D, 2011. Evaluation of extraction methods for efficient detection of enteric viruses in pork meat products. Food Anal Method 4:13-22. DOI: https://doi.org/10.1007/s12161-010-9165-1
Masuda JI, Yano K, Tamada Y, Takii Y, Ito M, Omagari K, Kohno S, 2005. Acute hepatitis E of a man who consumed wild boar meat prior to the onset of illness in Nagasaki, Japan. Hepatol Res 31:178-83. DOI: https://doi.org/10.1016/j.hepres.2005.01.008
Montone AMI, De Sabato L, Suffredini E, Alise M, Zaccherini A, Volzone P, Di Maro O, Neola B, Capuano F, Di Bartolo I, 2019. Occurrence of HEV-RNA in Italian regional pork and wild boar food products. Food Environ Virol 11:420-6. DOI: https://doi.org/10.1007/s12560-019-09403-2
Pallerla SR, Harms D, Johne R, Todt D, Steinmann E, Schemmerer M, Wenzel JJ, Hofmann J, Kuo Shih JW, Wedemeyer H, Bock CT, Velavan TP, 2020. Hepatitis E virus infection: circulation, molecular epidemiology, and impact on global health. Pathogens 9:856. DOI: https://doi.org/10.3390/pathogens9100856
Ricci A, Allende A, Bolton D, Chemaly M, Davies R, Fernandez Escamez PS, Herman L, Koutsoumanis K, Lindqvist R, Nørrung B, Robertson L, Ru G, Sanaa M, Simmons M, Skandamis P, Snary E, Speybroeck N, Ter Kuile B, Threlfall J, Wahlström H, Di Bartolo I, Johne R, Pavio N, Rutjes S, van der Poel W, Vasickova P, Hempen M, Messens W, Rizzi V, Latronico F, Girones R, 2017. Public health risks associated with hepatitis E virus (HEV) as a food-borne pathogen. EFSA J 15:e04664. DOI: https://doi.org/10.2903/j.efsa.2017.4886
Said B, Ijaz S, Kafatos G, Booth L, Thomas HL, Walsh A, Ramsay M, Morgan D, 2009. Hepatitis E outbreak on cruise ship. Emerg Infect Dis 15:1738-44. DOI: https://doi.org/10.3201/eid1511.091094
Sair AI, D’Souza DH, Moe CL, Jaykus LA, 2002. Improved detection of human enteric viruses in foods by RT-PCR. J Virol Methods 100:57-69. DOI: https://doi.org/10.1016/S0166-0934(01)00397-4
Sankaranarayanan A, Amaresan N, Dhanasekaran D, 2019. Fermented food products. CRC Press, Boca Raton, FL, USA. DOI: https://doi.org/10.1201/9780429274787
Schrader C, Schielke A, Ellerbroek L, Johne R, 2012. PCR inhibitors - occurrence, properties and removal. J Appl Microbiol 113:1014-26. DOI: https://doi.org/10.1111/j.1365-2672.2012.05384.x
Smith DB, Izopet J, Nicot F, Simmonds P, Jameel S, Meng XJ, Norder H, Okamoto H, van der Poel WHM, Reuter G, Purdy MA, 2020. Update: proposed reference sequences for subtypes of hepatitis E virus (species Orthohepevirus A). J Gen Virol 101:692-8. DOI: https://doi.org/10.1099/jgv.0.001435
Spada E, Simeoni M, Martina A, Pati I, Villano U, Adriani D, D’Angiò A, Tritarelli E, Taffon S, Bellino S, Boros S, Urciuoli R, Masiello F, Marano G, Bruni R, Pezzotti P, Ciccaglione AR, Pupella S, De Angelis V, Pisani G, 2022. Prevalence and risk factors for hepatitis E virus infection in blood donors: a nationwide survey in Italy, 2017 to 2019. Euro Surveill 27:2100516. DOI: https://doi.org/10.2807/1560-7917.ES.2022.27.22.2100516
Straube J, Albert T, Manteufel J, Heinze J, Fehlhaber K, Truyen U, 2011. In vitro influence of D/L-lactic acid, sodium chloride and sodium nitrite on the infectivity of feline calicivirus and of ECHO virus as potential surrogates for foodborne viruses. Int J Food Microbiol 151:93-7. DOI: https://doi.org/10.1016/j.ijfoodmicro.2011.08.010
Szabo K, Trojnar E, Anheyer-Behmenburg H, Binder A, Schotte U, Ellerbroek L, Klein G, Johne R, 2015. Detection of hepatitis E virus RNA in raw sausages and liver sausages from retail in Germany using an optimized method. Int J Food Microbiol 215:149-56. DOI: https://doi.org/10.1016/j.ijfoodmicro.2015.09.013
Tei S, Kitajima N, Takahashi K, Mishiro S, 2003. Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet 362:371-3. DOI: https://doi.org/10.1016/S0140-6736(03)14025-1
Tsarev SA, Tsareva TS, Emerson SU, Govindarajan S, Shapiro M, Gerin JL, Purcell RH, 1994. Successful passive and active immunization of cynomolgus monkeys against hepatitis E. Proc Natl Acad Sci U S A 91:10198-202. DOI: https://doi.org/10.1073/pnas.91.21.10198
Wolff A, Günther T, Albert T, Schilling-Loeffler K, Gadicherla AK, Johne R, 2020. Stability of hepatitis E virus at different pH values. Int J Food Microbiol 325:108625. DOI: https://doi.org/10.1016/j.ijfoodmicro.2020.108625
Wolff A, Günther T, Johne R, 2022. Stability of hepatitis E virus after drying on different surfaces. Food Environ Virol 14:138-48. DOI: https://doi.org/10.1007/s12560-022-09510-7
Yazaki Y, Mizuo H, Takahashi M, Nishizawa T, Sasaki N, Gotanda Y, Okamoto H, 2003. Sporadic acute or fulminant hepatitis E in Hokkaido, Japan, may be food-borne, as suggested by the presence of hepatitis E virus in pig liver as food. J Gen Virol 84:2351-7. DOI: https://doi.org/10.1099/vir.0.19242-0

How to Cite

1.
Lorusso P, Pandiscia A, Manfredi A, Tantillo GM, Terio V. Evaluation of hepatitis E virus RNA persistence in experimentally contaminated cured pork liver sausages. Ital J Food Safety [Internet]. 2024 Apr. 2 [cited 2024 Nov. 21];13(2). Available from: https://www.pagepressjournals.org/ijfs/article/view/12286