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Effectiveness of Cold Smoking on Inactivating Murine Norovirus in Salami-Like Pork Sausages (Mettwurst), and Hepatitis E Virus and Murine Norovirus in Solution

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FOOD AND ENVIRONMENTAL VIROLOGY 2025年第1期17卷 1-14页

作者： Loikkanen, Emil Mikkela, Antti Joutsen, Suvi Tuominen, Pirkko maunula, leena Univ Helsinki Fac Vet Med Dept Food Hyg & Environm Hlth Helsinki Finland Finnish Food Author Risk Assessment Unit Lab & Res Dept Helsinki Finland

Hepatitis E virus (HEV) is a zoonotic virus that infects humans when virus-containing pork products are consumed. This study aimed to explore MNV (murine norovirus) and HEV inactivation during cold smoking and ripening/fermentation treatments used for salami-like sausages (mettwurst). MNV inactivation was monitored in culture medium solution and in sausage while being subjected to a salami-like sausage manufacturing process. The inactivation of MNV in the solution was also monitored at room temperature (RT) for four weeks. HEV inactivation was monitored in solution during the cold smoking process and at RT. A TCID50 assay was used to calculate the infectious MNV and HEV titres. MNV survival was modelled using Bayesian inference. MNV load in solution decreased by as much as 4.7 (SD 0.9) log(10) TCID50/ml when it was subjected to the cold smoking process. Modelling revealed that 99.999% MNV might be inactivated during the treatment when observed at a level of 95% CI (Bayesian Confidence Interval). On the contrary, MNV load decreased by only 1.8 (0.2) log(10) when stored at RT. The low-titre HEV in solution was inactivated (> 1.1 (0.2) log(10)) when treated, and at RT. However, MNV was resistant in the sausage matrix during the cold smoking process (log(10) reduction of 1.9 (0.5) TCID50/ml). Based on modelling, a substantial amount of virus would remain in the product, even when the uncertainty was considered. Hence, viruses, here exemplified by MNV, may not be inactivated from salami-like pork sausages during manufacturing, which poses a risk for consumers in real-life situations.

关键词： Murine norovirus Hepatitis E virus Cold smoking Long-term virus inactivation Salami-like sausage Weibull model

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Detection of Porcine Norovirus GII.18 Strains in Pigs Using Broadly Reactive RT-qPCR Assay for Genogroup II Noroviruses

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FOOD AND ENVIRONMENTAL VIROLOGY 2025年第1期17卷 1-8页

作者： Gupta, Ankita K. Heinonen, Mari Konig, Emilia Mikkonen, Venla maunula, leena Univ Helsinki Fac Vet Med Dept Food Hyg & Environm Hlth Helsinki Finland Univ Helsinki Fac Vet Med Dept Prod Anim Med Helsinki Finland

Noroviruses, belonging to the family Caliciviridae, are classified into at least ten genogroups (G) based on their major capsid protein (VP1). The common genogroup to be identified in both humans and pigs is GII, although porcine noroviruses (PoNoVs) belong to genotypes of their own (GII.11, GII.18, and GII.19). So far, PoNoVs have not been studied much in Finland, possibly due to their rather symptomless nature in pigs. In the present study, we enrolled a total of 189 fecal samples collected from pigs from Finnish farms. Samples were taken from 12 farms in 2010, 2019 and 2020. We analyzed feces from growing pigs ranging from 2.1 to 6 months of age. RNA was extracted from fecal suspensions using a commercial viral RNA extraction kit, followed by RT (reverse transcription)-qPCR. The genotypes were determined by Sanger sequencing of the PCR fragments amplified by conventional PCR. Of the 12 farms, 6 (50%) had at least one PoNoV-infected pig. Altogether 18 (9.5%) of the 189 pigs tested positive for PoNoVs. Pigs mostly aged over 4 months were infected with PoNoVs. Eventually, 12 positive samples were determined as genotype GII.18. We could demonstrate the presence of PoNoVs in Finnish pigs. In future, more studies in which longer sequences from PoNoV genome can be obtained, are required.

关键词： Caliciviridae Human norovirus Porcine norovirus RT-qPCR Genotyping

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Waterborne norovirus outbreaks

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FUTURE VIROLOGY 2007年第1期2卷 101-112页

作者： maunula, leena Univ Helsinki Fac Vet Med Dept Food & Environm Hyg FIN-00014 Helsinki Finland

Noroviruses (NoVs) are the most common nonbacterial causative agents of waterborne outbreaks. Due to the mild and short-lived disease of gastroenteritis, even large epidemics may go unnoticed, since patients do not necessarily visit a doctor. NoVs have several means by which to survive both in the environment and in a population. The nonenveloped small virus retains its infectivity in the environment, and particularly in cold water, for a long time. Unlike most enteric viruses, it causes disease both in children and adults. A large number of genotypes combined with a small infective dose and short-term immunity guarantee efficient circulation of these viruses. The world of NoVs has been revealed to us predominantly by molecular methods. Having learned to detect these viruses first in patients, the emphasis is now in searching for methods sensitive enough to find them in environmental samples. In this review, the latest methods and their use in monitoring of these viruses are discussed.

关键词： gastroenteritis molecular epidemiology norovirus waterborne outbreak

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Hepatitis E virus: zoonotic and foodborne transmission in developed countries

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FUTURE VIROLOGY 2018年第9期13卷 657-670页

作者： Kantala, Tuija maunula, leena Univ Helsinki Fac Vet Med Dept Food Hyg & Environm Hlth POB 66 FI-00014 Helsinki Finland Finnish Food Safety Author Evira Mustialankatu 3 FI-00790 Helsinki Finland

Hepatitis E virus (HEV), together with hepatitis A virus, transmits via the fecal-oral route. The number of domestic hepatitis E cases among Europeans has grown alarmingly during the past 5 years. Surveillance studies suggest that the number of foodborne HEV infections is increasing most rapidly. Zoonotic HEV genotype HEV-3 is prevalent among pigs and wild boars in Europe and many developed countries, whereas zoonotic genotype HEV-4 is more common in pigs in some Asian countries. This review presents the most recent data about possible foodborne transmission of HEV via pigs and other production animals and about the presence of HEV in high-risk foods, such as ready-to-eat meat products. Possible solutions about how to tackle this problem are discussed here.

关键词： foodborne hepatitis E zoonotic

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Noroviruses on surfaces: detection, persistence, disinfection and role in environmental transmission

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FUTURE VIROLOGY 2016年第3期11卷 207-217页

作者： Ronnqvist, Maria maunula, leena Univ Helsinki Fac Vet Med Dept Food Hyg & Environm Hlth POB 66 FIN-00014 Helsinki Finland Finnish Food Safety Author Evira Mustialankatu 3 FI-00790 Helsinki Finland

Human noroviruses (HuNoVs), the most common cause of infectious nonbacterial gastroenteritis and the cause of numerous foodborne and hospital outbreaks, are easily transmitted from person-to-person. HuNoVs may persist on surfaces for long periods of time and may be transferred via hands, foods, fomites and air. In this review, studies on methods for detecting HuNoVs on environmental surfaces, such as swabbing, are presented. The review also focuses on recent studies on the efficiency of disinfectants for inactivating HuNoV or its surrogates, such as murine norovirus, on environmental surfaces and hands. Although HuNoV is probably more resistant than MuNoV, this study data adds to the understanding of HuNoV transmission routes and selection of tools for the prevention of HuNoV gastroenteritis outbreaks.

关键词： environmental swabbing norovirus norovirus inactivation

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Rapid Detection of Human Norovirus in Frozen Raspberries

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FOOD AND ENVIRONMENTAL VIROLOGY 2018年第1期10卷 51-60页

作者： Summa, Maija maunula, leena Univ Helsinki Fac Vet Med Dept Food Hyg & Environm Hlth POB 66 FIN-00014 Helsinki Finland

Raspberries have lately caused several human norovirus (HuNoV) outbreaks in Europe. In this study, we developed and evaluated for HuNoV reverse transcription (RT)-PCR detection in frozen raspberries extraction methods that have equal sensitivity but are less time-consuming than widely used methods based on polyethylene glycol (PEG) precipitation and chloroform-butanol purification. One method was applied to stored frozen raspberries linked to previous HuNoV outbreaks and berries on sale. In the virus elution-based Method 1, sparkling water eluted viruses most efficiently from the berries. Method 2, based on direct nucleic acid extraction with minor PEG supplement, yielded the highest number of positive findings (4 out of 9) at low virus concentration level of 100 genome copies HuNoV genogroup II per 25 g raspberries. Both methods showed approximately equal sensitivity to a method including PEG precipitation and chloroform-butanol purification. Two naturally contaminated berry samples linked to HuNoV outbreaks in 2006 and 2009 were still positive for HuNoV genogroup I, but all berry products purchased from a local store remained negative for HuNoV. In conclusion, this study presents two efficient and rapid methods which can be used in urgent HuNoV outbreak investigations, since the results of the virus analysis are available in a few hours.

关键词： Human norovirus Reverse transcription PCR Rapid method Frozen raspberry Foodborne virus

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Reduction of Norovirus in Foods by Nonthermal Treatments: A Review

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JOURNAL OF FOOD PROTECTION 2020年第12期83卷 2053-2073页

作者： Ahmed, Hany maunula, leena Korhonen, Jenni Univ Eastern Finland Inst Publ Hlth & Clin Nutr Kuopio 70211 Finland Univ Helsinki Fac Vet Med Dept Food Hyg & Environm Hlth Helsinki 00014 Finland

Human noroviruses are enteric pathogens that cause a substantial proportion of acute gastroenteritis cases worldwide regardless of background variables such as age, ethnicity, and gender. Although person-to-person contact is the general route of transmission, foodborne infections are also common. Thorough cooking eliminates noroviruses, but several food products such as berries, leafy vegetables, and mollusks undergo only limited heat treatment, if any, before consumption. Novel applications of nonthermal processing technologies are currently being vigorously researched because they can be used to inactivate pathogens and extend product shelf life with limited effects on nutrient content and perceived quality. These technologies, adopted from several industrial fields, include some methods already approved for food processing that have been applied in the food industry for years. However, a majority of the research has been conducted with bacteria and simple matrixes or surfaces. This review focuses on elimination of norovirus in food matrixes by use of nonthermal technologies in four categories: high hydrostatic pressure, light, irradiation, and cold atmospheric plasma. We discuss the properties of noroviruses, principles and inactivation mechanisms of select technologies, and main findings of relevant studies. We also provide an overview of the current status of the research and propose future directions for related work.

关键词： Food safety High pressure processing Irradiation Nonthermal processing Norovirus UV light

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Human norovirus infection: surveillance and source tracking

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FUTURE VIROLOGY 2011年第4期6卷 431-438页

作者： maunula, leena von Bonsdorff, Carl-Henrik Univ Helsinki Dept Food Hyg & Environm Hlth FI-00014 Helsinki Finland

The clinical importance of noroviruses has increased in recent years. It is challenging to control the annual gastroenteritis and vomiting outbreaks caused by noroviruses in hospital wards and also long-term care facilities. This problem is partly due to the repeated emergence of highly penetrant genotype GII.4 variants that cause global epidemics. Consequently, this has led to an increased awareness of norovirus receptor selection and the population immunity characteristics that drive the evolution of the virus. Noroviruses mainly transmit from person to person by the feco-oral route and also via food, water and environmental fomites. International norovirus surveillance helps in source-tracking and in being able to follow the dissemination of viruses with food products in addition to the early detection of emerging variants.

关键词： genotyping molecular epidemiology norovirus RT-PCR source-tracking surveillance

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Emerging and re- emerging enteric viruses causing multinational foodborne disease outbreaks

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FUTURE VIROLOGY 2014年第3期9卷 301-312页

作者： maunula, leena von Bonsdorff, Carl-Henrik Univ Helsinki Fac Vet Med Dept Food & Environm Hyg FIN-00014 Helsinki Finland

The development of molecular detection methods has led to recognition of viruses as important foodborne pathogens. The most common foodborne virus is norovirus, which together with HAV are transmitted via food consumed raw, such as shellfish, fresh produce and soft fruit. HEV is increasingly being recognized as an emerging foodborne virus in developed countries. The transmission route of HEV includes zoonotic transmission in association with pork products. Ongoing changes in food commerce and production from national to internationally-distributed foodstuffs are leading to widespread infections and multinational outbreaks. Recent large viral outbreaks have been linked to oysters, frozen berries and semidried tomatoes.

关键词： foodborne virus HAV HEV multinational outbreak norovirus

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Applicability of microarray technique for the detection of noro- and astroviruses

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JOURNAL OF VIROLOGICAL METHODS 2006年第1-2期136卷 210-216页

作者： Jaaskelainen, Anne J. maunula, leena Univ Helsinki Haartman Inst Dept Virol FIN-00014 Helsinki Finland Univ Helsinki Dept Food & Environm Hyg FIN-00014 Helsinki Finland Univ Helsinki Cent Hosp HUS Lab FIN-00029 Helsinki Finland

Noroviruses and astroviruses are widespread viral agents causing gastroenteritis. Noroviruses are actually a diverse group of viruses. A new microarray-based detection method is presented for both noro- and astroviruses. This method enables simultaneous identification of genogroups and types of noro- and astroviruses. For pre-amplification, the monoplex- and multiplex-RT-PCR assays were applied to test sensitivity. The 202 specimens were used to determine the specificity, precision, and accuracy of the microarray. Stool samples representing 13 of norovirus GI and GII genotypes were assayed. The microarray detected all but one genotype. In a panel of 74 stool samples, 45 tested positive for norovirus by microarray, against 35 by a conventional PCR-method. In addition, microarray detected some double infections. In a panel of archival samples, astroviruses of genotype 4 frequently emerged in Finland from 1977 to 1997. This study demonstrates that microarray is useful for simultaneous monitoring of several viruses and their subtypes. Microarray provides a convenient tool for the detection of RNA viruses for which frequent changes in the panel of detection primers may be required. (c) 2006 Elsevier B.V. All rights reserved.

关键词： norovirus astrovirus microarray detection genogrouping

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